Modern Foraminifera

Modern Foraminifera

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Modern Foraminifera

edited byBarun K. Sen Gupta

Louisiana State University

KLUWER ACADEMIC PUBLISHERSNEW YORK, BOSTON, DORDRECHT, LONDON, MOSCOW

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Nous disons qu’elle est à la portée de tout le monde, en ce sens que, placén’importe où, sur les côtes des diverses portions du globe terrestre ou sur lesparties des continents recouvertes par des terrains tertiares, crétacés ouoolithiques, partout disons-nous, l’observateur trouve sous ses pieds, et dans uneseule pincée de sable, une grande quantité de Foraminifères qu’il peut étudieravec le seul secours d’une loupe. Pour l’importance réelle de leur étude, nouscroyons qu’il n’est pas de série animale offrant plus de facilités et d’avantagesau géologue et au zoologiste: au premier, pour déterminer la température deslieux où vivaent les espéces perdues, par la comparaison avec ce que nousvoyons maintenant dans les mers, et pour expliquer la formation des couches(questions de la plus haute importance dans l’histoire de notre planète); ausecond, par leur admirable diversité, par l’élégance de leurs formes, par lasingularité de leur organisation, et enfin en ce qu’ils constituent une classe desplus nombreuses du règne animal, et jouent, malgré leur petitesse, un rôleimmense dans la nature.

Alcide d’Orbigny, 1839, in Ramon de la Sagra, Histoire Physique, Politique etNaturelle de l’Ile de Cuba

Love the organisms for themselves first, then strain for general explanations,and, with good fortune, discoveries will follow. If they don’t, the love andpleasure will have been enough.

Edward O. Wilson, 1994, Naturalist.


Contents

Contributors

Preface and Acknowledgments

PART I: BASIC CONSIDERATIONS

Introduction to Modern ForaminiferaBarun K. Sen Gupta

Systematics of Modern ForaminiferaBarun K. Sen Gupta

Foraminifera: A Biological OverviewSusan T. Goldstein

3

7

37

57

71

Shell Construction in Modern Calcareous ForaminiferaHans Jørgen Hansen

Quantitative Methods of Data Analysis in Foraminiferal EcologyWilliam C. Parker and Anthony J. Arnold

PART II: FEATURES OF DISTRIBUTION

Biogeography of Neritic Benthic ForaminiferaStephen J. Culver and Martin A. Buzas

Biogeography of Planktonic ForaminiferaAnthony J. Arnold and William C. Parker

Symbiont-Bearing ForaminiferaPamela Hallock

93

103

123

1

2

3

4

5

6

7

8

ix

xi

Contentsviii

9

10

11

12

13

Foraminifera in Marginal Marine EnvironmentsBarun K. Sen Gupta

Benthic Foraminiferal Microhabitats below the Sediment-Water InterfaceFrans Jorissen

Benthic Foraminifera and the Flux of Organic Carbon to the SeabedPaul Loubere and Mohammad Fariduddin

Foraminifera of Oxygen-Depleted EnvironmentsJoan M. Bernhard and Barun K. Sen Gupta

Effects of Marine Pollution on Benthic ForaminiferaValentina Yanko, Anthony J. Arnold, and William C. Parker

PART III: GEOCHEMISTRY OF SHELLS

Stable Oxygen and Carbon Isotopes in Foraminiferal Carbonate ShellsEelco J. Rohling and Steve Cooke

Trace Elements in Foraminiferal CalciteDavid W. Lea

14

15

PART IV: PRESERVATION OF RECORD

Taphonomy and Temporal Resolution of Foraminiferal AssemblagesRonald E. Martin

References

General Index

Taxonomic Index

141

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181

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239

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281

299

353

361

16

Contributors

Anthony J. ArnoldDepartment of GeologyFlorida State UniversityTallahassee, FL 32306U.S.A.

Stephen J. CulverDepartment of GeologyEast Carolina UniversityGreenville, NC 27858U.S.A.

Mohammad FariduddinDepartment of Earth SciencesNortheastern Illinois Universi ty5500 North St. Louis AvenueChicago, IL 60625U.S.A.

Susan T. GoldsteinDepartment of GeologyUniversity of GeorgiaAthens, GA 30602U.S.A.

Joan M. BernhardDepartment of Environmental Health Sciences

and Marine Science ProgramUniversity of South CarolinaColumbia, SC 29208U.S.A.

Martin A. BuzasDepartment of PaleobiologyNational Museum of Natural HistorySmithsonian InstitutionWashington, DC 20560U.S.A.

Pamela HallockDepartment of Marine ScienceUniversity of South Florida140 7th Ave. SSt. Petersburg, FL 33701U.S.A.

Steve CookeSchool of Ocean and Earth ScienceUniversity of SouthamptonSouthampton Oceanography CentreSouthampton SO 14 3ZHU.K.

Hans Jørgen HansenGeological Ins t i tu teOster Voldgade 101350 CopenhagenDenmark

Frans JorissenLaboratoire de GéologieUniversité d’Angers2 Boulevard Lavoisier49045 Angers CedexFrance

William C. ParkerDepartment of GeologyFlorida State UniversityTallahassee, FL 32306U.S.A.

David W. LeaDepartment of Geological SciencesUniversity of California, Santa BarbaraSanta Barbara, CA 93106U.S.A.

Eelco J. RohlingSchool of Ocean and Earth ScienceUniversity of SouthamptonSouthampton Oceanography CentreSouthampton SO 14 3ZHU.K.

Paul LoubereDepartment of Geology and Environmental

GeosciencesNorthern Illinois UniversityDe Kalb, IL 60115U.S.A.

Barun K. Sen GuptaDepartment of Geology and GeophysicsLouisiana State UniversityBaton Rouge, LA 70803U.S.A.

Ronald E. MartinDepartment of GeologyUniversity of DelawareNewark, DE 19716U.S.A.

Valentina YankoAvalon In s t i t u t e of Applied ScienceCharleston Technology Centre3227 Roblin BoulevardWinnipeg, MB R3R OC2Canada

Prefaceand Acknowledgments

Modern Foraminifera started wi th a simple idea:to write an advanced text for un ivers i ty studentsthat would also serve as a reference book forprofessionals. Being keenly aware of the bound-aries of my competence, I invited fourteen col-leagues to write most of the chapters. Thechapters were designed to be balanced reviews,but, with the lone exception of chapter two, theyhad to be wri t ten under a rather stringent spacelimitation. Thus, al though the list of referencesis long, it surely does not include every singlesignificant article on every topic covered in thebook. Both the subject matters of the chaptersand the selection of authors were ent i rely myresponsibity, and no other author can beaccused of a personal bias in the s t ructure ofthe book. I have assumed that the reader willhave an elementary knowledge of foraminiferalshell morphology, as found in undergraduatepaleontology texts.

I am deeply indebted to the reviewers whohelped shape the chapters into their final form.They are: Paul Aharon, Elisabeth Alve, LaurieAnderson, Anthony Arnold, Wil l iam Berggren,Joan Bernhard, Samuel Bowser, Kevin Carman,Robert Carney, Lui-Heung Chan, Bruce Corliss,Robert Douglas, Thomas Gibson, Susan

Goldstein, Andrew Gooday, Pamela Hallock,Jeffrey Hanor, John Haynes, Johann Hoheneg-ger, Scott Ishman, Frans Jorissen, Susan Kid-well, Martin Langer, David Lea, Richard Norris,Wil l iam Parker, Nancy Rabalais, CharlesRamcharan, Charles Schafer, Scott Snyder, Ken-neth Towe, Bert v a n der Zwaan, and two otherswho chose to remain anonymous. JessicaSchreyer assisted in editorial tasks. In the f inalstages of p u t t i n g the book together, my burdenwas lightened by the cheerful cooperation ofPetra van Steenbergen, our publishing editor atKluwer . In addit ion, I was helped by Ian Francisat the p lanning stage of the book.

Two people deserve special acknowledgment.I am grateful to Mary Lee Eggart for the art onthe cover and in several chapters, and to PoreeSen Gupta, my wife, for her tolerance of myobsessive preoccupation with the book for thepast two years.

Final ly, I t hank the Cushman Foundation fori ts very special role in publ ishing and promotingforaminiferal research. In appreciation of thisservice, the roya l ty for the book has been trans-ferred to this organization.

Baton RougeDecember, 1998

Barun K. Sen Gupta


PART I:BASIC

CONSIDERATIONS


1Introduction to modern

ForaminiferaBarun K. Sen Gupta

‘These minute a n i m a l s are interesting objects of study, geologically and biologically aswell as esthetically. As objects of beauty they arrest the attention of even the casualobserver by the del icacy of their structure as well as the symmetry and variety of theirforms. Geologically they are of interest because they are among the most ancient andabundant of fossils and also the most efficient of rock builders. Biologically they areinstructive examples of the powers and possibilities of an individualized bit of protoplasm.’

Foraminifers are better known for their spectac-ular fossil record than for their variety or abun-dance in modern marine environments . They,however, consti tute the most diverse group ofshelled microorganisms in modern oceans. In1846, Alcide d’Orbigny counted 68 modern fora-miniferal genera, and estimated tha t there are1,000 modern species. In the latest taxonomicmagnum opus on the class, Alfred R. Loeblichand Helen Tappan ( 1 9 8 7 ) described 878 moderngenera. The number of extant foraminiferalspecies is now estimated to be about 10,000(Vickerman, 1992), that is, about one-eighth ofthe estimated number of modern species withinthe Kingdom Protoctista (Hammond et al.,

1995). The overwhelming majori ty of modernForaminifera are benthic; there are only about40–50 planktonic species. In addition to theirmuch greater divers i ty , the benthic species havea much longer geological record. Their oldestfossils are Cambrian in age, whereas those ofthe p lankton ic species are Jurassic.

Shells (usua l ly called ‘tests’) of extant Fora-minifera have been noticed in shore sands sincethe 17th century (see Cifelli , 1990). An unusua learly find was by the great microscopist Antonievan Leeuwenhoek, who, in 1700, wrote aboutforaminifer shells ‘no bigger than a coarse sandgrain’ in stomachs of shrimps, and described thespecimens as ‘very l i t t l e snai l shells, which

Barun K. Sen Gupta (ed), Modern Foraminifera, 3–6© 1999 Kluwer Academic Publishers. Printed in Great Britain.

James M. Flint, 1899, Recent Foraminifera: A Descriptive Catalogue of Specimens Dredgedby the U.S. Fish Commission Steamer Albatross.

4 Introduction to modern Foraminifera

because of their roundness, I called l i t t l e cockles’(Dobell, 1932). Leeuwenhoek’s drawing of oneof these shells (Fig. 1.1) is detailed enough to berecognized as that of an Elphidium. It is aninteresting but not a surprising coincidence thatafter foraminifers were identified as shelled pro-tists (chapters 2, 3), the early studies of their lifecycle were focused on E l p h i d i u m (e.g. Lister,1895; chapter 3). This genus is easily collectedfrom nearshore environments, where large pop-ulations are common (chapter 9). Overall, a rela-t ive ease of collection is reflected in the muchgreater body of literature that exists on conti-nental-shelf foraminifers, compared to tha t ondeeper-water species.

The biology of foraminifers has not beenexamined as intensively as that of some protoc-tistan cousins (e.g. ciliates); apparently, the shellhas been somewhat of a problem in cellularstudies. The biological feature that has drawnthe most attention is the alternation between asexual and an asexual generation (and the varia-tions of this cycle; chapter 3), because thisexplains the distinct morphological dimorphismthat is seen in the shells of many species, includ-ing, especially, some relatively large fossil forms.In addition, from the very beginning of biologi-cal studies of foraminifers in the 19th century,the reticulate pseudopodia (‘reticulopodia’) have

been regarded as a special feature of this group,and recent studies have shed l igh t on the i rdiverse functions (chapter 3) . To most s tudentsand researchers, however, the most s i g n i f i c a n taspect of foraminiferal biology is the productionof an amazing var ie ty of shells (chapter 2) ,matched in no other class of organisms. On thebasis of the morphology of these shells, one canrecognize 15 extant foraminiferal orders. Inseven orders, the shell is made of secreted calcite;in others, the species secrete aragonite or opalinesilica, or make the i r shells w i t h organic mat te ror foreign particles (chapter 2). The mechanicsof chamber formation in some calcareous specieshas been studied in great detai l (chapters 3, 4) ,and used in the recognition of suprageneric taxa(chapter 2 ) . Genetic research on Foraminifera isa new and sparsely populated f i e ld , but judg ingby the effect of th is research on species-leveltaxonomy (e.g. Pawlowski et al., 1995), a majorimpact on foraminiferal systematics is expectedin the future.

The ecology of Foraminifera became a majorarea of study in the second half of the 20thcentury, and the first text on this subject was byFred B Phleger ( 1960a). In the the past 30 years,research in th i s field has increased grea t ly ,main ly because of the real izat ion that modernforaminiferal d is t r ibu t ions are l ike ly to providereliable clues (‘analogs’) for the unders tandingof marine env i ronmenta l changes in the geologi-cal (and, in some cases, historical) past. Theadvantage of using foraminifers in paleoecologylies in the i r s ign i f i can t numerical densi ty indiverse marine sediments and in the excellentpreservation of the i r shells. Both of these factorsare part ly related to their small size. Somespecies, however, are better preserved thanothers, causing a taphonomic bias even in rela-tively recent sedimentary records (chapter 16).

Traditionally, the focus of foraminiferal distri-but ion studies has been on water depth ( re levan tto paleodepth research on sedimentary rocks),except for marginal marine species, which arestrongly influenced by sa l in i ty changes (chap-ter 9). In waters of normal marine sa l in i ty , plac-ing a foraminifera l zone boundary at the shelf-slope break is common practice. Furthermore,

Introduction to modern Foraminifera 5

numerous investigators have followed Phleger(e.g. 1964a) in recognizing distinctive foramini-feral assemblages on the ‘inner continental shelf,outer continental shelf, upper continental slope,lower continental slope and deep sea.’ Applica-tion of numerical techniques of data analysis(chapter 5) to relative abundances of species hasled to finer groupings in many areas. With adifferent perspective, latitudinally extensive bio-geographic provinces of benthic Foraminiferahave been recognized on various continentalshelves and slopes. In many of these provinces,the proportion of endemic species in the fora-miniferal community is very high (chapter 6).

Recognition of patterns (and their causes)in the distribution of deep-sea benthic Foramini-fera has remained a problem since the Chal-lenger report of 1884, because many species ofthis ‘cold-water sphere’ are ubiquitous. They,however, are not equally abundant everywhere,and the dominance of certain species seems tobe connected with particular deep-bathyal orabyssal water masses, although invariant associ-ations are hard to establish. Two associationsthat have been verified in multiple deep basinsrelate to well-oxygenated waters: Cibicides wuel-lerstorfi is a dominant species in North AtlanticDeep Water (or its remnant in Caribbeanbasins), and Nuttallides umbonifera in AntarcticBottom Water (e.g. Streeter, 1973; Schnitker,1974b; Douglas and Woodruff, 1981; Sen Gupta,1988). In many correlations between a benthicforaminiferal species or assemblage and a watermass (defined by the combination of temper-ature and salinity), causality is elusive. On theother hand, there is compelling evidence thatthe variable input of labile organic matter (areflection of surface-ocean productivity) affectsabundances of deep-sea foraminiferal species(chapter 11 ) . Thus, Epistominella exigua, oncethought to be a foraminiferal marker of somedeep-water masses, is now known to be a specieswhose population density is dependent on phy-todetritus falls (e.g. Gooday, 1993). In bathyaldepths, the correlation between a benthic fora-miniferal association and the oxygen-minimumwater has been clearly demonstrated (e.g. Her-melin and Shimmield, 1990; Denne and Sen

Gupta, 1993), but the controlling factor may bethe organic-rich sediment on the seafloor (Her-melin and Shimmield, 1990). This book doesnot include a chapter on the connection betweenwater masses and foraminiferal assemblages onthe deep-sea floor, but the point of view thatthere is a connection is expressed succinctly bySchnitker (1994): ‘Benthic foraminifers areunequivocal indicators of productivity in areaswhere productivity is high. In areas of low orvery uniform productivity the composition ofthe benthic fauna clearly carries the imprint ofdeep water mass structure as the dominant fea-ture.’ An additional difficulty is posed by theprobability that all species in the same deep-seaassemblage may not be equally dependent onfood falls. A recent study in eastern South Atlan-tic Ocean provides an i l lustration. Schmiedl andMackensen (1997 ) studied the variations in theQuaternary benthic foraminiferal record of twocores taken from the same depth (about3,000 m), but under surface waters of sharplydifferent productivities. They concluded thatfluctuations in the abundances of Cibicides wuel-lerstorfi and Bulimina alazanensis are related totemporal changes in the advection of NorthAtlantic Deep Water, whereas those of Cassidul-ina laevigata, Melonis barleeanus, and M. zaan-dami are linked to shifts in productivity.

At the sediment-water interface, many Fora-minifera are neither obligate epibenthos ( l iv ingon the sediment) nor obligate endobenthos(living within the sediment), because they canmove up or down the sediment column in searchof food, and thus have variable microhabitats(L inke and Lutze, 1993). Some truly epibenthicspecies (free or attached) live on substrates abovethe sediment surface, whereas some t ru ly endo-benthic species live several centimeters down inthe sediment (chapter 10). Such deep endoben-thic species may have to cope with a severeshortage of oxygen in the sediment pore water,but as recent research has shown, many fora-miniferal species can live in extremely oxygen-poor water in varying depths of the sea (chap-ter 12). Because of the paucity of observationson the preferred depths of l iv ing individualswi th in the substrate, microhabitats of most sedi-

Introduction to modern Foraminifcra6

ment-dwelling species are unknown. Someresearchers use the shell shape (‘morphotype’)to infer the microhabitat, but this practice hasan inherent uncertainty (chapter 10).

In many coastal areas, especially in industrial-ized countries, pollution has severely affectedforaminiferal microhabitats. Studies on theeffects of various forms of pollution on Fora-minifera show that many species can serve asindicators in pollution monitoring programs(chapter 13). Many foraminiferal species haveadapted to extreme natural environments, suchas habitats of very high salinity (chapter 9),areas near hydrothermal vents (e.g. Jonassonet al., 1995), bacterial mats at hydrocarbon vents(e.g. Sen Gupta et al., 1997) or in silled basins(e.g. Bernhard et al., 1997), and pack ice (plank-tonic species, chapter 7). These are not exoticspecies, however; they are recruited from thesurrounding areas where the environment is‘normal’ for the water depth and distance fromthe shore.

Modern planktonic Foraminifera, because oftheir enormous population sizes, produce a sig-nificant amount of oceanic carbonate. There isa much larger proportion of taxa with algalsymbionts within this group than within thebenthic group (chapter 8). The environmentalcontrols on planktonic species are much betterunderstood than those on benthic species,because the only major variables are the temper-ature, salinity, and productivity of the surfacelayer of seawater (mainly in the upper 100 m).The species are distributed in a few large latitu-

dinal provinces, with some showing bipolar dis-tributions; many species can be used as tracersof ocean currents (e.g. Oberhänsli, 1992). Thepresent-day temperature limits of the biogeo-graphic provinces have been of great use inestimating Quaternary sea-surface paleo-temperatures from the fossil record of extantspecies (chapter 7).

The extraordinary progress of foraminiferalshell geochemistry in recent years has been inthe context of major questions of paleoceanog-raphy that relate to the nature and movementof past water masses, at the sea surface and inthe water column. The principles behind theseinquiries have to be established by analyses ofmodern foraminiferal shells – both planktonicand benthic. Culturing studies have becomeespecially significant in this research, because ofthe necessity of understanding the species-specific ‘vital effect’ in the incorporation of traceelements and the acquiring of the oxygen andcarbon isotope signatures in the shell (chapters14 and 15).

In summary, much of this book is about pat-terns of foraminiferal distr ibut ion in seafloorsediments and in seawater, and about the pro-cesses that govern this distribution. In spite ofprolific research since Phleger’s days, manyquestions about processes remain unresolved.On matters of speculative interpretation, theremay be disagreement even among authors ofthis book. We hope such issues will generatethought and discussion, not frustration.

Acknowledgment. I thank Anthony Arnoldand Joan Bernhard for reviewing this chapter.

2Systematics of modern

ForaminiferaBarun K. Sen Gupta

2.1 INTRODUCTION: THE EARLYPHASE OF SUPRAGENERIC TAXONOMY

As J.J. Lister wrote, ‘the Foraminifera receivedtheir name before their nature was understood’(Lister, 1903). In fact, numerous foraminiferalspecies had been described under a linnaeanbinomial before this understanding. In the la t terhalf of the 18th century, most foraminifers weredescribed as cephalopods, particularly as Nauti-lus. The original descriptions of about 140 suchfalse nautiluses named between 1758 and 1819are given in the Catalogue of Foraminifera ( Ellisand Messina, 1940 and later). Many of thespecies and varieties were well i l lustrated bytheir authors, and it is possible to place themunder currently accepted generic labels. The bestknown example of this phase of foraminiferaltaxonomy is the Testacea Microscopica of Fich-tel and Moll (1798) in which 47 extant and fossiltaxa (putat ively, distinct species or varieties)were given linnaean names under the singlegeneric heading of Nautilus ; 18 separate genera(Fig. 2.1) , all extant, are now recognized wi th inthis group ( R ö g l and Hansen, 1984).

The identification and separation of foramini-feral species, genera, and higher taxa solely by

aspects of test morphology, especially chamberarrangement, did not change with the recogni-tion by Felix Dujardin (1835a–c; spelt‘Desjardins’ in 1835a) that the foraminiferalbody was simply a je l ly- l ike mass (‘sarcode’) wi thpseudopodia (Fig . 2.2; see also chapter 3). Theclassification in vogue at this time (d’Orbigny,1826) underwent only minor modifications afterd’Orbigny’s acceptance of Dujardin’s conclusionthat foraminifers were unice l lu lar organisms,and not cephalopods. In d’Orbigny’s 1826 classi-fication, the Foraminifera, as a foramina-bearing(as opposed to siphon-bearing) class of cephalo-pods, was split into five orders; his 1852 classifi-cation of the Foraminifera (as sarcodines),included all of these orders, plus an order forsingle-chambered forms ( Monostègues) and onein which chambers were arranged in annu l i(Cyclostègues; Fig. 2.3). At th is stage, d’Orbignyhad recognized a total of 72 foraminiferalgenera. Al though wall characters were consid-ered a significant criterion in generic taxonomy ,d’Orbigny ( 1 8 5 2 ) placed both calcareous andagglutinated genera in the same family, becauseof some s imi la r i ty in chamber arrangement. Forexample, the agglutinated form Clavulina andthe calcareous forms Bulimina and Globigerina

Barun K. Sen Gupta (ed.), Modern Foraminifera, 7–36© 1999 Kluwer Academic Publishers. Printed in Great Britain.

Systematics of modern Foraminifera8

Introduction: The early phase of suprageneric taxonomy 9

10 Systematics of modern Foraminifera

were all placed under Tubinoidaea (Order Heli-costègues). This practice of placing agglutinatedand calcareous genera (especially those withserial chamber arrangements) within one familycontinued well into the 20th century. At thehighest level of taxonomic discrimination, how-ever, the shift in the primary emphasis fromchamber arrangement to wall characters is clearin many schemes of foraminiferal classificationdeveloped in Europe and the U.S. (see, e.g. Gal-loway, 1933; Glaessner, 1945; Loeblich andTappan, 1964a, b). The most significant trans-itions are discussed below. An elegant summaryof all major classifications from d’Orbigny(1826) to Galloway (1933), their philosophicalbases, and their relevance in an evolutionarycontext are given in Cifelli (1990).

The hierarchical base of d’Orbigny’s classifi-cation was severely criticized by a number ofresearchers in Great Britain in the 1850s and1860s (W.K. Parker, T.R. Jones, W.C. William-son, W.B. Carpenter, and H.B. Brady; see Cifelli,1990), because they concluded that these unicel-lular organisms are so variable that clear distinc-tions, whether among species or among orders,are unattainable (Carpenter et al., 1862). Never-theless, attempts at classification, by these criticsand others, continued, culminating in two hier-archical schemes of great significance (Reuss,1861; Carpenter et al., 1862). Although theywere considerably different in details, wall struc-ture was used as the feature of primary impor-tance in both of these schemes, and two majordivisions were recognized, one with perforatefamilies, the other with imperforate families. Thescheme was significantly modified by Jones(1876) when he separated the porcelaneousgroup from the arenaceous, thus recognizingthree major divisions.

One of the greatest works on modern Fora-minifera was H.B. Brady’s magnificent mono-graph (1884) on the material collected duringthe Challenger expedition of 1873–1876. Brady’sillustrations are still used extensively for speciesidentifications; names may have changedbecause of questions of priority, but by andlarge, the internal consistency of nomenclatureis impressive (see Barker, 1960; Jones, 1994).

Brady’s views on foraminiferal systematics,forcefully expressed in the Challenger mono-graph, strongly influenced researchers in thenext five decades. Brady included both modernand ancient ( including Paleozoic) genera in his10 families and 29 subfamilies, but placed noimportance on stratigraphic distributions, occa-sionally grouping Paleozoic genera togetherwith very different Cenozoic ones. In Brady’sview, even the largest taxa wi th in the Foramini-fera (to him, an order) had to be recognized onthe basis of mult iple characters, and no singlecharacter (e.g. wall composition or texture)could be used as the sole basis for the separationof these taxa. Thus, he kept all known generawith serially arranged chambers within a singlefamily, the Textularidae (Textulariidae of laterworkers), because he considered the wall com-position to span the range between agglutinatedor calcareous, warranting no more than arecognition of two subfamilies, Textularinae(Textulariinae of later workers) for the former,and Bulimininae for the latter. On the whole,however, the value of wall structure is reflectedin Brady’s classification. Of the other nine fami-lies, the largest taxonomic groups in his scheme,one (Gromidae) is characterized by organicwalls, two (Astrorhizidae and Lituolidae) byagglutinated walls, one (Mil iol idae) by calcare-ous imperforate walls, and five (Chilostomelli-dae, Lagenidae, Globigerinidae, Rotaliidae,Nummulinidae) by calcareous perforate walls.Furthermore, the practice of placing all plank-tonic foraminifers into a distinct major taxonwas firmly established with Brady’s classifica-tion, although current ly this group has the statusof an order (Globigerinida as in Loeblich andTappan, 1992) rather than that of a family(Globigerinidae as in Brady, 1884). About twodecades later, Lister (1903), while keeping thebasic hierarchy of Brady, elevated his 10 fora-miniferal families to superfamilies (with a suff ixchange from -idae to -idea), and the order Fora-minifera to a class. Lister categorically rejectedCarpenter’s extreme view (Carpenter et al., 1862)that morphological variabi l i ty and intergrada-tion among foraminifers are so strong that theseparation of species is impossible. He clarified

The age of Cushman 11

the issue by stating that the question ‘appearsto be not whether all intermediate forms do ordo not exist between dissimilar forms, butwhether the whole body of forms, as they occurin nature, tend to group themselves or are aggre-gated about certain centres. ... In a very largenumber of cases, ... such centres do exist amongthe Foraminifera, as among other organisedbeings, and the characters of the middle individ-uals of them are those of the species’ (Lister,1903).

2.2 THE AGE OF CUSHMAN

Joseph A. Cushman, the most notable foramini-feral taxonomist in the first half of the 20thcentury, was strongly influenced by Brady’s viewof suprageneric groupings. Cushman’s f irst clas-sification (1925) was simply an adaptation ofBrady’s 10 families with some changes in thenaming of subfamilies. Although he arguedagainst keeping genera with the same chamberarrangement but different wall structures (e.g.the coiled-tubular Ammodiscus, Cornuspira, andSpirillina) within one family, he retained Brady’sconcept of the Textulariidae, with both aggluti-nated and calcareous genera. The big expansioncame with his 1927 and 1928 classifications, inwhich he increased the number of families to 45,without proposing superfamilies or orders.Apart from test morphology, Cushman’s newclassification was ‘based upon the known geol-ogical history of the genera, upon the phylo-genetic characters through a study of very muchfossil material from all the continents, and f inal lyby a study of the ontogeny in very many micro-spheric specimens, which show the relationshipsmuch more definitely than do megalosphericspecimens of the same species’ (Cushman, 1933;see Fig. 2.4). In the final version of this classifi-cation (Cushman, 1948), the number of families(without any suprafamilial groupings) was 50.Galloway’s classification, apparently ready in1927, and the cause of a private and publicdispute between Galloway and Cushmanregarding claims to priority (see Cifelli, 1990),was published in 1933. As in Cushman (1927) ,

( 1 ) the number of families was greatly expanded(to 35, from Brady’s 10), without the recognitionof superfamilies or suborders, and ( 2 ) the agglu-tinated textular i ids were separated from the cal-careous-hyaline buliminids, but the phylogeneticconcepts of Cushman and Galloway and theirfamily and subfamily groupings were substan-tially different. With Cushman’s expanded clas-sification of 1927, the role of wall s tructure wasfirmly established as the primary basis for first-level splitting. Although Cushman did not pro-pose any suprafamilial taxon wi th in the OrderForaminifera, he arranged the families in a wall-structure sequence, beginning wi th membranousand single-chambered agglutinated families,which he considererd the most primitive, andending with calcareous, perforate, trochospiralfamilies, which he considered the mostadvanced. The morphological separation of fam-ilies and genera was unambiguous, permit t ingCushman to produce identification keys (1928,1933, 1940, 1948). An abbreviated version of hislast identification key to foraminiferal families(1948) is given below (Table 2 . 1 ) . Cushman didnot identify any suprafamilial , subordinal taxa,but the identities of several of the morphologicalgroups in his key match the orders proposed inthe most widely accepted classification of laterdecades ( Loeblich and Tappan, 1964a).

Wi th in about twenty years after its publica-tion, Cushman’s 1927 classification became thestandard classification, ‘adopted by workerson the Foraminifera throughout the world’(Cushman, 1948). A contr ibut ing factor wasCushman’s reputation as the foremost specialistin the use of fossil Foraminifera in petroleumexploration. Biological research on the Fora-minifera, however, had not progressed muchbeyond what it was at the beginning of the 20thcentury. Thus, according to a distinguished pro-tozoologist, not enough information was avail-able on l iv ing organisms to war ran t a completerevision of the classification, and Cushman’smonumental work was subject to some derisionbecause it was ‘plain that some of Cushman’sspli t t ing of groups’ was not ‘biologically sound.’An allowance was made that such a classifica-tion, based purely on shell morphology, ‘may


serve the commercial purpose for which it wasin fact designed,’ but zoologists were admon-ished to ‘adhere to Brady’s simpler classification’(Jepps, 1956). A reticence s t i l l exists amongsome biologists in accepting shell morphology ,

especially wall s t ructure , as a basis for elaborate,hierarchical, foramini fera l classifications (e.g.Cavalier-Smith , 1993, discussed la te r ) .

Several classif icat ions developed in the twodecades fol lowing Cushman’s last major taxo-

The age of Cushman 13


nomic work (1948) introduced a suprafamilialhierarchy within the order Foraminifera, butother than a scheme developed in the SovietUnion (Rauzer-Chernousova and Fursenko,1959, 1962; Grigelis, 1978; see later), nonereceived a wide acceptance. This scene changedwith the appearance of Loeblich and Tappan’sfirst book on foraminiferal systematics (1964a).Meanwhile, a landmark paper on foraminiferalwall structure (Wood, 1949) focused attentionon optical characters of calcitic foraminiferalwalls that had been more or less ignored untilthis time.

2.3 CRYSTAL ORIENTATION INCALCAREOUS WALLS

As already explained, the wall structure hadbeen considered as a basis for foraminiferal tax-onomy since its early days. However, little atten-tion had been paid to the details of the wallcharacters of calcareous taxa, other than thesimple distinction between perforate and imper-forate groups, and the related hyaline and porce-laneous surface textures observed in reflectedlight under the microscope. Although severalstudies of the optical phenomena observed incalcareous walls of Foraminifera had been pub-lished in late 19th and early 20th centuries, andthe presence of an extinction cross had beenreported in polarized-light studies of certainspecies (e.g. Ehrenberg, 1854; Sollas, 1921), thecareful documentation by Wood (1949) demon-strated clearly the difference between two inter-ference patterns produced by polarized lightwhen viewed between crossed nicols: ( 1 ) a‘radial’ pattern, in which a black cross and con-centric color bands are observed in single cham-bers or fragments of chambers (Fig. 2.5, 2.6a)and (2) a ‘granular’ pattern, characterized byrandomly distributed flecks of color (Fig. 2.6b).The radial pattern, a mimic of the uniaxial nega-tive interference figure, is caused by the perpen-dicular orientation of the c-axis of calcitecrystals in relation to the curvature of the testwall. The granular pattern reflects the lack ofany such preferred orientation. The extensive

documentation of the optical characters ofnumerous calcareous hyaline genera by Woodmade it possible for Loeblich and Tappan(1964a) to place a new emphasis on crystal ori-entation in their first suprageneric classification(see next section). Electron-microscopic studiesof crystal orientation (e.g. Towe and Cifelli, 1967;Stapleton, 1973; Bellemo, 1974a, 1976) latershowed that calcite crystals in optically granularwalls are not randomly put together butarranged in oblique orientation or in bundles ofseveral preferred orientations, but the optical

Earlier classifications of Loeblich and Tappan 15

distinction between radial and granular wallshas been retained as a taxonomic guide at somelevel, especially in the schemes proposed byAlfred R. Loeblich and Helen Tappan.

2.4 EARLIER CLASSIFICATIONS OFLOEBLICH AND TAPPAN

New suprafamilial taxonomic entities were pro-posed within the Foraminifera by severalworkers in the 1950s (see Loeblich and Tappan,1964a), including one in which the nature oflamellae in the foraminiferal wall was used asthe basis for the recognition of superfamilies(Reiss, 1958). The most elaborate of these post-Cushman classifications was organized by ateam of Soviet paleontologists (Rauzer-Chernousova and Fursenko, 1959; 1962). Itcontained 13 orders (wi thin the subclass Fora-minifera), 14 superfamilies, and 72 families. Incontrast, Loeblich and Tappan’s 1964 classifica-tion, which soon became the most widely usedtaxonomic guide to the Foraminifera, included5 suborders (within the order Foraminiferida),17 superfamilies, and 94 families (see Grigelis,1978, for a comparison of the two systems).Loeblich and Tappan (1964a) recognized about1200 extant and extinct genera as valid, abouta three-fold increase since the last revision ofCushman’s taxonomy (1948), but still the out-come of a conservative approach (Berggren,1965).

Following Galloway (1933) and Cushman(1945), Loeblich and Tappan (1964a) arguedthat ‘the same chamber arrangement and formof test may have developed in independent lin-eages by parallel evolution, without indicatinginterrelationship of the similarly shaped shells.’Thus, in the descending hierarchy of classifica-tion, the starting point was the nature of thetest wall. The wall composition and textureformed the basis for the separation of the livesuborders: ( 1 ) organic wall for the Allogromiina,(2 ) agglutinated wall for the Textulariina,( 3 ) calcareous microgranular wall for the extinctFusulinina, ( 4 ) calcareous, porcelaneous wall for

the Miliolina, and ( 5 ) calcareous, hyaline wallfor the Rotaliina.

Within the Rotaliina, the suborder with themost variety (10 superfamilies), eight superfami-lies were par t ia l ly or completely segregated onthe basis of various combinations of wall layer-ing (monolamellar, bilamellar with primarilydoubled septa, and bilamellar with secondarilydoubled septa; see chapter 4) and optical orien-tation of crystals (single crystal, radial arrange-ment, and granular crystal arrangement). Thesedistinctions sufficed for the Discorbacea, Spirilli-nacea, Rotaliacea, and Cassidulinacea. Addi-tional features were needed for distinguishingsuperfamilies that could not be segregated onthe basis of the observed wall characters:(a) apertural characteristics (terminal radiate vs.loop-shaped aperture with internal toothplate)for Nodosariacea and Buliminacea; and ( b ) envi-ronmental adaptation (benthic vs. planktonic)for Orbitoidacea and Globigerinacea. Appa-rently, the optical properties were consideredmore significant in superfamily distinctions thanthe wall layering. Cassidulinacea, the only super-family with granular test wall, included bothmonolamellar and bilamellar taxa. Single prop-erties were used to dist inguish Carterinacea andRobertinacea: a wall with secreted calcite spic-ules for the former, an aragonitic wall for thelatter. Within the suborders Textulariina andFusulinina (‘lower groups’), the number ofchambers was used for the separation of super-families. Thus, in the Textulariina, an essentiallynon-septate test was considered typical of theAmmodiscacea, whereas multiple-chamberedforms were placed within the Lituolacea.

Several modifications to thei r 1964 classifica-tion were proposed by Loeblich and Tappan inlater years (e.g. Loeblich and Tappan, 1974,1984; Tappan and Loeblich, 1982), culminatingin a large compendium (Loeblich and Tappan,1987; not 1988, as in some citations in the litera-ture; see Loeblich and Tappan, 1989) wi thdescriptions of 2,446 genera ( H a m a n , 1988),including 878 extant genera (Tappan andLoeblich, 1988). A brief, but significant , revisionof the taxonomic hierarchy (orders to subfamil-ies) was published in 1992. The 1987 classifica-


tion included 12 suborders (Fig. 2.7). In the 1992revision, 10 of these were changed to orders, 4new orders were recognized, and the taxon Fora-minifera (labeled ‘Foraminiferea’ after Lee,1990a) was raised to the rank of class.

2.5 PRESENT CLASSIFICATION

2.5.1

The classification adapted in this chapter is amodified version of Loeblich and Tappan(1992) , with morphological criteria taken fromLoeblich and Tappan (1987) , and, for one order(Globigerinida), also from Simmons et al.(1997) . The 1987 monograph of Loeblich andTappan does not include a hierarchical sum-mary of the classification, but outlines are givenin Ross and Haman (1989) and Decrouez(1989) . At infraordinal levels, there are manyinconsistencies and inadequate explanations;these have been noted and discussed in an i l lu -minating review by Haynes (1990). Loeblich andTappan (1992) includes some discussion of thewall structure, as used in that f inal revision ofthe 1964 classification, but not all new taxo-nomic groups are defined. Perhaps the mostserious lag is in the non-definit ion of the neworder, Bul iminida ( Fursenko, 1958). In the mod-ified version of Loeblich and Tappan’s 1992classification proposed in this chapter, thedist inction between Rotaliida and Bul iminida(split from Rotal i ina of Loeblich and Tappan,1987) is partly taken from Grigelis ( 1 9 7 8 ) and

Haynes ( 1981), but since the inclusion of infraor-dinal taxa in either Buliminida or Rotaliida fol-lows the practice in Loeblich and Tappan(1992), the dis t inct ion is equivocal. The separa-t ion, based on m u l t i p l e characters, is easy intypical cases, for instance between a high-trochospiral test w i th a loop-shaped aper turethat projects in te rna l ly as a toothplate ( Bu l imin -ida) and a low-trochospiral test w i th a s l i t - l ikeaperture and no toothplate ( Rota l i ida) , bu t thereare many taxa whose placement in one of thesetwo orders (us ing the 1992 scheme for supragen-eric taxa, and the 1987 scheme for genera)appears to be h igh ly subjective. The term ‘tooth-plate’ has been used by var ious authors for sev-eral in ternal structures that differ in detail(Revets , 1993); a restricted d e f i n i t i o n (aninternal s t ructure descending from an aper tura ll ip and ‘composed of a single piece of innerlining,’ Revets, 1993) would apply to theBul imin ida . In Loeblich and Tappan (1992) .however, th i s order includes taxa such as Loxo-stomatacea tha t possess no toothplate. Clearly,a major taxonomic and phylogenetic s tudyis needed to resolve the ambigui t ies and contra-dictions in th i s part of the foraminiferalclassification.

Table 2.2 gives a comparison of the orders inthe present classif ication wi th those in two rela-t ively recent classif ications in which the Fora-minifera are considered a class (Haynes, 1981;Lee, 1990a). The total number of orders in thepresent classification is 16, and it differs fromLoeblich and Tappan ( 1 9 9 2 ) in the s tatus oftwo orders.

( 1 ) Order Silicoloculinida. The primarycharacter for the separation of the orders in the1992 classification is the shell composition,inc luding mineralogy. However, Sil icoloculi-nina, separated from Miliol ina in 1987, wasmade part of the Mil io l ida , the new porcelane-ous order. Loeblich and Tappan ( 1992) did notclearly explain th i s shif t , except to say tha t ‘min-eralized particles of the wall in the abyssal-dwell-ing suborder Sil icoloculinina also are randomlyoriented rodlike crystals, a l though consisting ofsilica rather than calcite’ (as is the case withtypical Miliolida). Although not articulated, the

Present classification 17

milioline chamber arrangement of Miliammellus,the single genus within the silicic group, wasprobably a factor in this taxonomic placement.In the present adaptation, the Silicoloculinida(silicic wal l ) is retained as a distinct entity andnot placed under the Miliolida (calcitic wal l ) .The available information on the wall structure(Resig et al., 1980) shows that the opaline silicais secreted, not agglutinated. Furthermore, theinterpretable phylogeny of Miliolida isunaffected by the recognition of silicic foramini-fers as a separate suborder or a separate order.Thus, in spite of test isomorphism with miliolids,the placement of silicic foraminifers in a separatemajor taxon, the order Silicoloculinida (as inLee, 1990a), is justified.

( 2 ) Order Involutinida. In Loeblich andTappan (1992), the calcite-aragonite distinctionwas not used as an invariant basis for ordinalseparation among calcareous Foraminifera. Thearagonitic Involutinina was placed under theotherwise calcitic Spirillinida, whereas the ara-gonitic Robertinina of the 1987 classificationwas given the status of a separate order, Rober-tinida, and thus separated from the calcitic Buli-minida and Rotaliida. The present adaptation

reverts to the hierarchy in Loeblich and Tappan(1987), with a rank elevation, thus retainingboth the Involut inida and Spir i l l inida as orders.The family Planispirill inidae (aragonitic w a l l ) isretained within the Involu t in ida as the onlyextant family within this order, and not transfer-red to Spirillinida (calcitic wal l ) .

There are many ambiguities in the superfam-ily and family designations in Loeblich andTappan (1987) . The problems are mainly of twokinds: ( 1 ) the defining characters of a largertaxon being inadequate for the inclusion of allsubordinate taxa listed under it, and ( 2 ) thedefining characters of two taxa of the same rankbeing inadequate for their separation. An exam-ple of the first problem is the inclusion of theNotodendrodidae (bulbous central region andtubular arms) wi thin the Hippocrepinacea (pro-loculus followed by tubular or flaring secondchamber); that of the second problem is thedistinction between the Cornuspiridae andHemigordiopsidae, a streptospiral to planispiralcoiling being the characteristic of both (Haynes,1990). Conflicts of these kinds are not resolvedin Loeblich and Tappan (1992), becausealthough a complete outline classification (down


to the subfamily level) is given there, the infraor-dinal taxa are not defined. Other than theassignment of the Planispirillinidae to the Invo-lutinina, the classification summarized later inthis chapter retains the placement of super-families and families as in Loeblich andTappan (1992), notwithstanding unreconciledcontradictions.

2.5.2 Supraordinal taxa

Kingdom PROTOCTISTA. Foraminifers, aseukaryotic unicellular organisms, belong to theKingdom Protoctista, which includes all suchorganisms and some multicellular ones, i.e. ‘theentire motley and unruly group of non-plant,non-animal, non-fungal organisms representa-tive of lineages of the early descendants ofeukaryotes’ (Margulis, 1990). To avoid confu-sion, the recommended practice is to restrict aninformal designation of Protista to only micro-scopic protoctists (Margulis, 1990). Followingthis usage, all foraminifers are protoctists, butnot all are protists.

A contrary practice, the recognition of a sub-kingdom or phylum of single-celled animals,Protozoa (under Kingdom Animalia), is still invogue. Margulis (1990) takes strong exceptionto this taxonomy: ‘Even today, many scientists(e.g. especially cell biologists, plankton ecolo-gists and geologists) routinely write about Pro-tozoa and Algae as if they were phyla in theAnimal and Plant kingdoms, respectively. Theseorganisms are no more “one-celled animals andone-celled plants” than people are shell-lessmulticellular amoebas.’ To most foraminiferalsystematists, however, Protoctista/Protista vs.Protozoa is not a major controversy. Ever sincethe publication of Loeblich and Tappan (1964a),most of them have placed the foraminifers inthe Protista (in the traditional sense, i.e. sameas the current Protoctista) rather than in theProtozoa (see Hart and Williams, 1993, for arecent exception).

Phylum GRANULORETICULOSA. Thephylum includes heterotrophic protoctists char-acterized by granular reticulopods (pseudo-podial networks) with two-way streaming.

Complex sexual cycles are present in this group(Lee, 1990a).

Class FORAMINIFERA. The taxonomicrank of foraminifers was raised from order toclass by Loeblich and Tappan (1992) because ofthe following characteristics of the organisms:( 1 ) granuloreticulose pseudopodia, ( 2 ) outercover (usually a test), (3) alternation of haploidand diploid generations, and ( 4 ) ‘a test wall insome that is constructed of non-oriented cala-careous or siliceous crystals (Textulariida,Fusulinida, Miliolida, Carterinida), such crystal-line disorder being unknown elsewhere in theanimal kingdom.’ Accompanying this rankchange was a change in nomenclature, from For-aminiferida to Foraminiferea, although theInternational Code of Zoological Nomenclature( In ternat ional Commission of ZoologicalNomenclature, 1985) does not require or suggestsuch a change, being silent on the nomenclatureof orders or classes. Loeblich and Tappan ( 1 9 9 2 )chose ‘Foraminiferea’ because d’Orbigny’s ‘For-aminifères’ (1826) was not a latinized name, andthe ‘earliest formal Latinized citation as a class’they found was the Foraminiferea of Lee(1990a). In fact, however, the usage of the latin-ized class name Foraminifera goes back to 1903(Lister, p. 47), but more importantly, the r ightfulauthor of the class name Foraminifera isd’Orbigny, because the change from Foramini-fères to Foraminifera is simply an emendationthat calls for the retention of the original authorand date. This is fitting. Regardless of later harshopinions on d’Orbigny’s approach to foramini-feral systematics, a consensus exists that in theworld of foraminiferologists ‘one name mustalways be held in an esteem which may bedescribed as affectionate, and that is the nameof Alcide d’Orbigny’ (Heron-Allen, 1917).

2.5.3 Morphologic basis of presentclassification

The overwhelming importance of the chemistry,mineralogy, and structure of the foraminiferaltest wall in the ordinal classification is obviousin Loeblich and Tappan (1992) . In the presentadaptation, the sole use of these features leads


to the following separations: (a) organic wall,Order Allogromiida; ( b ) agglutinated, withproteinaceous or mineralized matrix, OrdersAstrorhizida, Lituolida, Trochamminida;(c) agglutinated, with low-Mg calcitic cement,Order Textulariida, (d) microgranular calcite,Order Fusulinida (extinct); (e) elongate, high-Mgcalcite, Order Miliolida; ( f ) elongate, low-Mgcalcite forming large spicules, Order Carterin-ida; (g) one or a few crystals of elongate, low-Mgcalcite, Order Spirillinida; (h) numerous crystalsof elongate, low-Mg calcite, forming monola-mellar wall, Order Lagenida; ( i ) numerous crys-tals of elongate, low-Mg calcite, formingbilamellar wall, Orders Buliminida, Rotaliida,and Globigerinida (all extant and most extinctgenera); ( j ) aragonite, Orders Involutinida, Rob-ertinida, and Globigerinida (a few extinctgenera); (k) silica, Order Silicoloculinida. A sig-nificant difference between the present classifi-cation and those of Loeblich and Tappan is theplacement of the sole planktonic order, Globi-gerinida, under a calcitic group, as well as underthe aragonitic group. This is because of therecognition by Simmons et al. (1997) thatin the most primitive planktonic superfamily,the Favusellacea (Jurassic and early Cret-aceous), the test wall is aragonitic, in contrastto the calcitic wall in all other planktonicgroups, including the three modern super-families (Heterohelicacea, Globorotaliacea, andGlobigerinacea).

Further distinctions of orders within groups b,i, and j are based on the number (one, two, ormany) and arrangement of chambers, presenceof toothplates, and benthic vs planktonic adap-tations. Subordinal distinctions within mostorders are based on numerous combinations ofdiverse morphological features, including wallpores, wall passages, and principal apertural fea-tures for superfamilies, and free or fixed natureof the test, mode of chamber addition, simple ordivided nature of chamber interior, and aper-tural modifications for families (Loeblich andTappan, 1987; Haman 1988). In one remarkableexception, a non-test character, biflagellate vsamoeboid gametes, has been used to separatetwo families of Allogromiida – Lagynidae andAllogromiidae (Loeblich and Tappan, 1987).

2.5.4 Identification key to orders

The present classification of 16 orders does notlend itself to the construction of a simple ordinalkey, based on just two or three morphologicalfeatures. The system designed by Loeblich andTappan is complex, and takes into account notjust the morphology but the long geologicalhistory and an interpreted phylogeny of theForaminifera. In this context, it is hard to dis-pute that ‘the fundamental purpose of classifica-tion ... is to provide an orderly hierarchicalarray of taxa reflecting the genetic lines ofdescent, not simply to provide a convenientpigeon-holing’ and that a natural classificationmust not be confused with ‘an artificial identifi-cation key or retrieval system’ (Haynes, 1990).On the other hand, even a perfectly naturalclassification (a hypothetical construct for theForaminifera, given the guesswork involved indetermining lines of descent) is useless if we areunable to place major taxa into clearly markedcompartments in that classification. With thispractical aspect of taxonomy in mind, a keyto the identification of foraminiferal orders(Loeblich and Tappan, 1992, modified) is givenbelow. A simplified graphic version of this mor-phological key is given in Fig. 2.8. Representa-tive genera (one per order) are illustrated inFig. 2.9.

Class FORAMINIFERA

Group 1 Test or outer membrane made oforganic material, in some cases with a few par-ticles picked up from the environment: Order 1,ALLOGROMIIDA.

Group 2 Test agglutinated, i.e. made of par-ticles picked up from the environment (‘foreignparticles’), 4 orders.

2.1 Test particles attached to a proteinaceousor mineralized matrix: 3 orders.2.1.1 Test shape irregular; typically single-chambered or branching tubular; septaincomplete in multichambered forms: Order2, ASTRORHIZIDA.




2.1.2 Multichambered, i.e. septa present:2 orders.2.1.2.1 Coiling usually planispiral, but insome cases streptospiral or trochospiral:Order 3, LITUOLIDA.2.1.2.2 Coiling trochospiral: Order 4,TROCHAMMINIDA.2.2 Test particles cemented by low-Mgcalcite: Order 5, TEXTULARIIDA.

Group 3 Test wall made of secreted calciumcarbonate: 9 orders.

3.1 Calcite: 8 orders.3.1.1 Crystals microgranular, i.e. very smalland nearly equidimensional; no preferredcrystal orientation: Order 6, F U S U L I N I D A(Extinct) .3.1.2 Crystals elongate along the c-axis: 7orders.3.1.2.1 High-Mg calcite: Order 7,MILIOLIDA.3.1.2.2 Low-Mg calcite: 6 orders.3.1.2.2.1 Large spicules (unusually large crys-tals) in a matrix of fine spicules: Order 8,CARTERINIDA.3.1.2.2.2 Optically, a single crystal or a fewcrystals (or, rarely, a mosaic of crystals): Order9, SPIRILLINIDA.3.1.2.2.3 Numerous small crystals; lamellarwall: 4 orders.3.1.2.2.3.1 Monolamellar. Single-chamberedor multichambered, but no complexly coiledforms beyond planispiral: Order 10,LAGENIDA.3.1.2.2.3.2 Bilamellar. Multichambered: 3orders.3.1.2.2.3.2.1 Environmental adaptation ben-thic: 2 orders.3.1.2.2.3.2.1.1 Chamber arrangement trocho-spiral (typically, high-trochospiral), triserial,biserial, or uniserial; aperture typicallycomma-shaped ot loop-shaped, typically withtoothplate: Order 11, BULIMINIDA.3.1.2.2.3.2.1.2 Chamber arrangement trocho-spiral (typically, low trochospiral), plani-spiral, annular, or irregular: Order 12,ROTALIIDA.

3.1.2.2.3.2.2 Environmental adaptation plank-tonic: Order 13, G L O B I G E R I N I D A , part(a l l modern and most fossil taxa) .3.2 Aragonite: 3 orders.3.2.1 Two chambers: Order 14,I N V O L U T I N I D A .3.2.2 Many chambers: 2 orders.3.2.1.1 Environmental adaptation benthic:Order 15, ROBERTINIDA.3.2.1.2 Environmental adaptation plank-tonic: Order 13, GLOBIGERINIDA , part(only Favusellacea, extinct).

Group 4 Test wall made of silica: Order 16,SILICOLOCULINIDA.

2.5.5 Superfamilies and families

The characteristic features of Holocene super-families and representative families are brieflysummarized below, with examples of extantgenera. The listing does not include subfamiliesand some minor families. Only essential descrip-tions are given here, summarized from Loeblichand Tappan (1987) and corrected for contradic-tions or ambiguities, especially in cases (e.g. Spir-oplectamminacea) where superfamily characters,as reported by Loeblich and Tappan, do notaccommodate those of all constituent families.Unfortunately, some uncertainties still remainin the distinction between closely related super-families or families, because the present modifi-cation of Loeblich and Tappan (1992) leaves thesubordinal hierarchy untouched. For fu l ldescriptions of the taxa, and for generic descrip-tions, see Loeblich and Tappan (1987) . Only283 genera are mentioned below as examples,out of a total of 878 extant genera described inLoeblich and Tappan (1987) . For a completel ist ing of genera and suprageneric taxa underthe Loeblich and Tappan (1987 ) hierarchy, seeDecrouez (1989), but the status and placementof some subfamilies, families, and superfamiliesare different in Loeblich and Tappan (1992) ,and thus in the present adaptation.

Most morphological terms used in thefollowing brief descriptions are simple, andrequire no fur ther explanation. A few are defined


when they first appear. One frequently usedapertural term, ‘interiomarginal,’ refers to anopening at the basal margin of the final chamber(Loeblich and Tappan, 1964a). The principaltypes of chamber arrangement and aperture aresketched in Figs. 2.10 and 2.11.

Order 1, ALLOGROMIIDA. Organic wall.Includes freshwater forms. No superfamilynamed. Examples of extant families and genera:

Family Lagynidae. Single-chambered or colo-nial; agglutinated matter rare; biflagellategametes. Myxotheca, Ophiotuba.

Family Allogromiidae. Single-chambered;agglutinated matter common; amoeboidgametes. Allogromia (Fig. 2.9), Dendrotuba,Hospi te l la .

Order 2, ASTRORHIZIDA. Agglutinatedwall with particles attached to a proteinaceousor mineralized matrix; single-chambered,branching tubular, or irregularly multicham-bered with incomplete septa.

( 1 ) Superfamily Astrorhizacea. Test of vari-ous shapes, including branching; no septa,although the single chamber may be partiallydivided. Examples of extant families and genera:

Family Astrorhizidae. Branching test,branches diverging from the central part of thetest. Astrorhiza, Pelosina.

Family Bathysiphonidae. Test a straight orslightly curved tube. Bathysiphon.

Family Rhabdamminidae. Test a branchingor twisted tube. Psammatodendron, Rhabdam-mina, Rhizammina.

Family Psammosphaeridae. Test globular orirregular; several may be joined together. Withlarge pores, but no distinct apertures.Psammosphaera.

Family Saccamminidae. Test globular or elon-gate. Single or multiple apertures. Lagenammina,Saccammina (Fig. 2.9), Technitella.

Family Hemisphaeramminidae. Test with sub-globular or discoidal chambers. Crithionina,Iridia.

( 2 ) Superfamily Komokiacea. Test formed ofmultiple branching tubules. With pores, but no

distinct aperture. Examples of extant familiesand genera:

Family Komokiidae. Bushlike or tree-likearrangement of tubules. Komokia, Normanina.

( 3 ) Superfamily Hippocrepinacea. Test tubu-lar with one closed end, or two-chambered, withrounded or irregular first chamber and tubularor flaring second chamber. Examples of extantfamilies and genera:

Family Hippocrepinidae. Test typically tubu-lar; terminal aperture sl ightly constricted. Hip-pocrepina, Hyperammina, Jaculella, Saccorhiza.

Family Notodendrodidae. Test with a bulbouscenter, an arborescent upper part, and abranching lower part serving as anchor. Withsmall pores but no distinct aperture.Notodendrodes.

Order 3, LITUOLIDA. Agglutinated wallwith particles attached to a proteinaceous ormineralized matrix; planispirally (or in somecases, streptospirally or trochospirally) coiledthroughout, or uncoiled in the later stage; also,arranged in series throughout.

( 1 ) Superfamily Ammodiscacea. Two-cham-bered test, with a globular initial chamber anda tubular (coiled or uncoiled) second chamberwith terminal aperture.

Family Ammodiscidae. The only family underAmmodiscacea; defining characters same asthose of the superfamily. Examples: Ammodiscus(Fig. 2.9), Ammolagena, Glomospira.

(2 ) Superfamily Rzehakinacea. Test plani-spiral or with milioline coiling (chambersarranged in various planes); imperforate.

Family Rzehakinidae. The only family underRzehakinacea; defining characters same as thoseof the superfamily. Examples: Ammoflintina,Miliammina.

( 3 ) Superfamily Hormosinacea. Test withuniserial chambers. Examples of extant familiesand genera:

Family Reophacidae. Test wth asymetricalchambers (made of a single layer of agglutinatedmaterial) arranged in a slightly arcuate series;terminal aperture on a neck. Nodulina, Reophax.

Family Hormosinidae. Thick-walled test withsymmetrical chambers arranged in a rectilinear




series; terminal aperture on a neck. Hormosina,Pseudonodosinella.

(4) Superfamily Lituolacea. Imperforate testwith multiple chambers; planispirally coiledthroughout or in early stage. Examples of extantfamilies and genera:

Family Haplophragmoididae. Chambers in afully or partially involute coil. Aperture singleor multiple, interiomarginal or areal. Cribrosto-moides, Haplophragmoides.

Family Lituotubidae. Initial chamber fol-lowed by a coiled, tubular second chamber, andthen by a series of coiled or uncoiled adult cham-bers with interiomarginal or terminal aperture.Lituotuba, Trochamminoides.

Family Lituolidae. Coiled throughout, or laterchambers in a linear series, with terminal aper-ture. Ammoastuta, Ammobaculites, Ammomargi-nulina, Ammotium, Lituola.

Family Placopsilinidae. Attached test, withcoiled, curved, or biserial early portion, anduncoiled later portion with terminal aperture.Ammocibicides, Placopsilina.

(5) Superfamily Haplophragmiacea. Teststreptospirally coiled throughout or in the ini t ialpart, with interiomarginal or areal aperture.Examples of extant families and genera:

Family Ammosphaeroidinidae. Streptospiral,with a small number of chambers. Adercotryma,Recurvoides.

(6) Superfamily Coscinophragmatacea. Testattached, uniserial or branching, but initial partmay be coiled; coarsely perforate. Examples ofextant families and genera:

Family Coscinophragmatidae. Test with alve-olar wall, aperture terminal. Bdelloidina.

( 7 ) Superfamily Loftusiacea. Test with plani-spiral, Streptospiral, or trochospiral coil; wallwith an imperforate outer layer and an alveolarinner layer. Examples of extant families andgenera:

Family Cyclamminidae. Test planispiral invo-lute, with interiomarginal or areal aperture.Alveophragmium, Cyclammina.

(8) Superfamily Spiroplectamminacea. Cham-ber arrangement variable: (a) planispiral orStreptospiral in early part, and biserial oruniserial in later part, ( b ) biserial to uniserial,

(c) high spiral. Examples of extant families andgenera:

Family Spiroplectamminidae. Planispiral orStreptospiral in early part, and biserial or uniser-ial in later part. Spiroplectammina, Vulvulina.

Family Nouriidae. Chambers arranged biseri-ally or in a high spiral, wi th terminal aperture.Nouria.

( 9 ) Superfamily Verneuilinacea. Test trocho-spiral, triserial, or biserial; last part may be unis-erial. Examples of extant families and genera:

Family Verneuilinidae. Triserial throughoutor in the early part, wi th biserial or uniseriallater part. Gaudryina.

( 1 0 ) Superfamily Ataxophragmiacea. Trocho-spiral throughout or in the early part, with trise-rial, biserial, or uniserial later part. Examples ofextant families and genera:

Family Globotextulariidae. Test hightrochospiral throughout or wi th triserial or bise-rial later part; aperture interiomarginal or areal.Globotextularia, Liebusella.

Family Textulariellidae. Test trochospiral inearly part, later triserial, biserial, or uniserial;wall alveolar. Guppyella, Textulariella.

Order 4, T R O C H A M M I N I D A . Agglutinatedwall with particles attached to a proteinaceousor mineralized matrix; trochospirally coiledthroughout or uncoiled in later part.

( 1 ) Superfamily Trochamminacea. Trocho-spirally coiled throughout or uncoiled in laterpart. Examples of extant families and genera:

Family Trochamminidae. Test wi th lowtrochospiral coil; with interiomarginally or are-ally located single or mul t ip le apertures.Ammoglobigerina, Arenoparrella, Jadammina,Tipotrocha, Tritaxis, Trochammina (Fig. 2.9).

( 2 ) Superfamily Remaneicacea. Test with lowtrochospiral coil; chambers subdivided bysecondary partitions.

Family Remaneicidae. The only family underRemaneicacea; defining characters same as thoseof the superfamily. Example: Remaneica.

Order 5, T E X T U L A R I I D A . Agglutinatedwall, with particles cemented by low-Mg calcite.

Superfamily Textulariacea. Test trochospiral ,


triserial, or biserial throughout, or with biserialor uniserial later part; wall with canals. Exam-ples of extant families and genera:

Family Eggerellidae. Test trochospiral or tri-serial throughout, or wi th biserial or uniseriallater part, with interiomarginally or areallylocated single or multiple apertures. Eggerella,Karreriella, Martinottiella.

Family Textulariidae. Test biserial throughoutor uniserial in later part, with interiomarginallyor areally located single or multiple apertures.Bigenerina, Cribrobigenerina, Siphotextularia(Fig. 2.9), Tawitawia, Textularia.

Family Pseudogaudryinidae. Test triserial inearly part, later biserial or uniserial, with interio-marginal aperture. Pseudogaudryina.

Family Valvulinidae. Test trochospiral, trise-rial, or biserial throughout, or with uniseriallater part; aperture single (with tooth) ormultiple. Clavulina, Goesella.

Order 6, FUSULINIDA. Extinct. Microgran-ular, calcitic test wall. Example: Triticites(Fig. 2.9).

Order 7, MILIOLIDA. Test of high-Mgcalcite; surface texture porcelaneous; adultchambers imperforate, except in a few fossilgenera; surface pitted in some genera.

(1 ) Superfamily Squamulinacea. Test imper-forate, single-chambered.

Family Squamulinidae. The only family underSquamulinacea; defining characters same asthose of the superfamily. Example: Squamulina.

(2 ) Superfamily Cornuspiracea. Test imperfo-rate, two-chambered. Initial chamber rounded;second chamber tubular, and planispirally,streptospirally, or irregularly coiled, or uncoiledin later part.

Family Cornuspiridae. The only family underCornuspiracea; defining characters same asthose of the superfamily. Examples: Cornuspira,Meandrospira.

(3 ) Superfamily Hemigordiopsacea. Testimperforate, two-chambered. Init ial chamberrounded; second chamber streptospiral through-out or planispiral in later part.

Family Hemigordiopsidae. The only family

under Hemigordiopsacea; defining characterssame as those of the superfamily. Example:Gordiospira.

(4 ) Superfamily Nubeculariacea. Test imper-forate, multichambered, coiled planispirally,streptospirally, trochospirally, or irregularly.Examples of extant families and genera:

Family Fischerinidae. Test coiled planispir-ally; initial chamber rounded, second chambercoiled tubular, succeeding chambers arranged ina spiral. Fischerina, Nodobaculariella. Planispir-ina, Vertebralina. Wiesnerella.

Family Nubeculariidae. Test planispiral,trochospiral, or irregularly coiled throughout,or uncoiled in later part. Calcituba, Nodophthal-midium, Nubecularia.

Family Ophthalmidiidae. Chambers arrangedplanispirally or in various planes. Initial cham-ber and coiled tubular second chamber suc-ceeded by chambers one-half to one coil inlength. Cornuloculina, Edentostomina.

( 5 ) Superfamily Discospirinacea. Test imper-forate, multichambered, planispiral, discoid; firstchamber rounded, second chamber coiled tubu-lar, later chambers one-half coil in extent orannular.

Family Discospirinidae. The only familyunder Discospirinacea; defining characters sameas those of the superfamily. Example:Discospirina.

(6) Superfamily Miliolacea. Test imperforate,multichambered; chambers arranged in variousplanes. Examples of extant families and genera:

Family Spiroloculinidae. Ini t ia l chamberrounded, second chamber coiled tubular , adultchambers one-half coil in extent; aperture termi-nal, toothed or partly covered. Spiroloculina,Cribrospiroloculina.

Family Hauerinidae. Ini t ia l chamber rounded,succeeding chambers arranged in one or severalplanes, each chamber covering one-half coil orless; later part of test may be uncoiled; apertureterminal, toothed or partly covered. The testmay have an outer agglutinated layer. Ammo-massilina, Biloculinella, Cruciloculina, Hauerina,Massilina, Miliolinella (Fig. 2.9), Pyrgo, Quin-queloculina. Siphonaperta, Sigmoilina, Sigmoi-lopsis, Triloculina.


Family Tubinellidae. Test coiled in early part,with chambers arranged in one or several planes,but uncoiled in later part. Articulina, Tubinella.

Family Miliolidae. Test with pitted surface,coiled in one or several planes; aperture termi-nal, open or partly blocked. Rupertianella.

(7) Superfamily Alveolinacea. Test imperfo-rate, wall thickened, with passages and pillars;chambers (with chamberlets in some genera)arranged planispirally, streptospirally, or in var-ious planes; aperture multiple. Examples ofextant families and genera:

Family Alveolinidae. Test coiled around thelong axis; initial chamber rounded, secondchamber coiled tubular, adult chambers in aplanispiral coil and divided into chamberlets.Borelis, Alveolinella.

Family Keramosphaeridae. Globular test withconcentric chambers and chamberlets. Kera-mosphaera.

(8) Superfamily Soritacea. Adult chambersimperforate, except in a few fossil genera. Earlychambers pitted or perforate; chamber arrange-ment planispiral, multispiral, annular, or serial.Examples of extant families and genera:

Family Peneroplidae. Chamber arrangementplanispiral in early part, multispiral, serial, orannular in later part; chambers undivided. Den-dritina, Monalysidium, Peneroplis.

Family Soritidae. Chamber arrangementplanispiral throughout, or multispiral, annular,or serial in later part; chambers subdivided intochamberlets. Amphisorus, Archaias, Cyclorbicul-ina, Marginopora, Parasorites, Sorites.

Order 8, CARTERINIDA. Wall of secretedlow-Mg calcite, with large spicules in a matrixof small spicules; imperforate. No Superfamilydesignated.

Family Carterinidae. Test trochospiral,attached; later chambers may be subdivided byseptula. Carterina (Fig. 2.9).

Order 9, SPIRILLINIDA. Test with wall oflow-Mg calcite, optically a single crystal, a fewcrystals, or a mosaic of crystals; imperforate orperforate; coiling planispiral or trochospiral. Nosuperfamily designated. Examples of extant fam-ilies and genera:

Family Spirillinidae. Test coiled, with twochambers; first chamber globular, second cham-ber tubular. Spirillina (Fig. 2.9).

Family Patellinidae. Test conical, multicham-bered; first chamber globular, second chamberspiral tubular, two chambers in each later whorl.Patellina.

Order 10. LAGENIDA. Test of low-Mgcalcite; wall monolamellar; perforate; single-chambered or multichambered with serial orplanispiral chamber arrangement.

( 1 ) Superfamily Nodosariacea. Test single-chambered or multichambered, with serial orspiral chamber arrangement; aperture terminal.Examples of extant families and genera:

Family Nodosariidae. Test (a) multichamb-ered with uniserial or biserial chamber arrange-ment, or (b) single-chambered, with a longslitlike aperture. Dentalina (Fig. 2.9), Frondicu-laria, Lingulina, Nodosaria, Rimulina.

Family Vaginulinidae. Test coiled throughoutor in early stage. Amphicoryna, Astacolus, Lenti-culina, Marginulina, Saracenaria, Vaginulina.

Family Lagenidae. Test single-chambered;aperture round or radiate. Lagena.

(2) Superfamily Polymorphinacea. Testsingle-chambered or multichambered with serialor elongate spiral chamber arrangement; aper-tural modifications include the presence of aninternal tube (entosolenian tube). Examples ofextant families and genera:

Family Polymorphinidae. Test multicham-bered; chamber arrangement serial or elongatespiral, with round, radiate, or slitlike terminalaperture. Globulina, Guttulina, Polymorphina,Ramulina, Sigmomorphina, Webbinella.

Family Ellipsolagenidae. Test single-cham-bered, aperture with an internal tubular exten-sion. Oolina, Fissurina.

Family Glandulinidae. Test multichambered,uniserial, biserial, or elongate spiral; aper-ture terminal, with an internal tubular exten-sion. Glandulina, Laryngosigma, Seabrookia,Tappanella.

Order 1 1 , B U L I M I N I D A . Test of low-Mgcalcite; wall bilamellar, perforate, multicham-bered, with high trochospiral, triserial, biserial.


or uniserial chamber arangement; aperture inmany advanced forms with internal toothplate.

( 1 ) Superfamily Bolivinacea. Test biserialthroughout, or uniserial in later part; apertureelongate, with a toothplate. Wall opticallyradial. Examples of extant families and genera:

Family Bolivinidae. Aperture loop-shaped,interiomarginal or areal. Bolivina (Fig. 2.9).

( 2 ) Superfamily Loxostomatacea. Apertureinteriomarginal or terminal , wi thout toothplate.Wall optically radial or granular. Examples ofextant families and genera:

Family Bolivinellidae. Test biserial, palmate;aperture cribrate. Bolivinella.

( 3 ) Superfamily Bolivinitacea. Test biserial:aperture interiomarginal. rounded, with tooth-plate. Wall optically radial.

Family Bolivinitidae. The only family underBolivinitacea; defining characters same as thoseof the Superfamily. Example: Bolivinita.

(4) Superfamily Cassidulinacea. Test biserial,coiled planispirally or trochospirally throughoutor in early part; aperture interiomarginal or ter-minal, with or without toothplate: wall opticallyradial or granular. Examples of extant familiesand genera:

Family Cassidulinidae. Coiling planispiral.Cassidulina, Cassidulinoides, Ehrenbergina, Glo-bocassidulina, Is landiel la.

( 5 ) Superfamily Turrilinacea. Test hightrochospiral, triserial, or biserial throughout, orchanging to biserial or uniserial in later part;aperture with or without toothplate; wall opti-cally radial or granular. Examples of extant fam-ilies and genera:

Family Stainforthiidae. Test ( a ) triserial inearly part and twisted biserial in later part, or(b) twisted biserial throughout; aperture large,elongate; rimmed or lipped apertural margin,partly infolded and linked with internal tooth-plate. Hopkinsina, Stainforthia.

(6) Superfamily Buliminacea. Test hightrochospiral throughout, or modified to biserialor uniserial in later part. Aperture interiomargi-nal, loop-shaped, with internal toothplate; walloptically radial. Examples of extant familiesand genera:

Family Siphogenerinoididae. Test triserial or

biserial in early part, biserial or uniserial in laterpart. Rectobolivina, Rectuvigerina, Sagrina.Siphogenerina.

Family Buliminidae. Test triserial. Bulimina,Globobulimina.

Family Buliminell idae. Test high trochospiral.wi th numerous chambers in a whorl. Buliminella.

Family Uvigerinidae. Test triserial throughoutor in early stages; aperture terminal , extendedinto a neck, with internal toothplate. Anguloger-ina, Trifarina, Uvigerina.

Family Reussellidae. Test triserial throughout ,or changing to biserial or uniserial in later part:periphery angular; aperture inter iomarginal orterminal, s l i t l ike or cribrate. Reussel la.

Family Pavoninidae. Test biserial in earlypart, uniser ial later: fan-shaped. Pavonina.

( 7 ) Superfamily Fursenkoinacea. Test twistedor flat biserial. or tr iserial . Aperture loop-shaped, w i th in ternal toothplate. wall opticallygranular. Examples of extant families andgenera:

Family Fursenkoinidae. Test twisted biserialthroughout , or uniserial in later part. Fursen-koina. Sigmavirgulina.

Family Virgulinel l idae. Test triserial or bise-rial, with partly covered su tu ra l apertures.Virgulinella.

( 8 ) Superfamily Delosinacea. Test trocho-spiral or triserial th roughout , or biserial in laterpart. Aperture areal, elongate, or in the form ofsutural pores. Wall optically granular . Examplesof extant families and genera:

Family Delosinidae. Test high triserial; wi thsutural pores, but no primary aperture. Delosina.

( 9 ) Superfamily Pleurostomellacea. Test trise-rial or biserial, changing to uniserial, or uniserialthroughout; aperture areal, slitlike (and partlycovered) or cribrate; aperture and foramina con-nected by internal siphon; wall opticallygranular.

Family Pleurostomellidae. The only familyunder Pleurostomellacea; defining characterssame as those of the superfamily. Examples:Ellipsoglandulina, Pleurostomella.

( 1 0 ) Superfamily Stilostomellacea. Test unis-erial; aperture terminal , w i t h ph ia l ine l ip andsmall tooth.


Family Stilostomellidae. The only familyunder Stilostomellacea; defining characters sameas those of the superfamily. Examples: Nodogen-erina, Siphonodosaria, Stilostomella.

(11) Superfamily Annulopatellinacea. Testlow conical; round initial chamber enclosed bysecond chamber; succeeding uniserial chambersarranged in annul i on the convex side, but over-lapping on concave or flat side, and subdividedby small tubules (internal extensions of surfacepores); no aperture, but conspicuous pores.

Family Annulopatellinidae. The only familyunder Annulopatellinacea; defining characterssame as those of the superfamily. Example:Annulopatellina.

Order 12, ROTALIIDA. Test of low-Mgcalcite; wall bilamellar, perforate; chamberarrangement low or (rarely) high trochospiral,planispiral, annular, or irregular.

( 1 ) Superfamily Discorbacea. Chamberarrangement low trochospiral; aperture umbili-cal, interiomarginal, with or without supplemen-tary apertures; wall structure optically radial.Examples of extant families and genera:

Family Bagginidae. Test wall finely perforateoverall, but imperforate in a part of ventral side.Baggina, Cancris.

Family Eponididae. Aperture interiomarginaland slitlike (or a narrow arch) or areal andcribrate. Eponides, Ioanella, Paumotua, Poro-eponides.

Family Heleninidae. Primary aperture interio-marginal; secondary apertures sutural. Helenina.

Family Mississippinidae. With distinct,translucent or opaque bands near periphery onone or both sides. Mississippina, Stomatorbina.

Family Pegidiidae. Coiling modified trocho-spiral, with resorbed early chambers; aperturesopen ends of tubes on ventral side. Pegidia.

Family Discorbidae. Umbilical area partlycovered by chamber extensions; each chamberpartly divided by an imperforate wall. Discorbis,Neoeponides.

Family Rosalinidae. Aperture a low interio-marginal arch; chamber interiors simple; umbili-cus partly covered by chamber extensions orclosed. Gavelinopsis, Neoconorbina, Rosalina.

Family Sphaeroidinidae. Chambers stronglyoverlapping, arranged trochospirally or indifferent planes; aperture areal and sl i t l ike orsutural and multiple. Sphaeroidina.

(2) Superfamily Glabratellacea. Apertureumbilical, interiomarginal. Umbilicus depressed,surrounded by radial sutures or ornamentation;wall structure optically radial. Examples ofextant families and genera:

Family Glabratellidae. Test low trochospiral;radially aligned striations or granules aroundumbilicus. Glabratella.

Family Heronallenidae. Test low trochospiral,planoconvex; aperture closed by a plate; radialstriations around umbilicus. Heronallenia.

( 3 ) Superfamily Siphoninacea. Test lowtrochospiral throughout or in early part; aper-ture interiomarginal or areal. with a lip (usual lyon a short neck); wall structure optically radialor granular.

Family Siphoninidae. The only family underSiphoninacea; defining characters same as thoseof the superfamily. Example: Siphonina.

(4 ) Superfamily Discorbinellacea. Test lowtrochospiral or nearly planispiral; aperturewholly or partly interiomarginal, arch-like orslitlike; wall structure optically radial. Examplesof extant families and genera:

Family Pseudoparrellidae. Test low trocho-spiral; aperture partly interiomarginal andpartly an almost vertical slit on the terminalchamber face. Eilohedra, Epistominella,Stetsonia.

Family Discorbinellidae. Test flat trochospiralor nearly planispiral; primary aperture interio-marginal, with or without secondary aperturesunder umbilical flaps. Laticarinina, Discor-binella.

(5 ) Superfamily Planorbulinacea. Test lowtrochospiral throughout or in the early part,with planispiral , uniserial, biserial, or irregulararrangement in the later part; coarsely perforate;primary aperture interiomarginal in coiledforms, with or without secondary apertures; wal lstructure optically radial or intermediate. Exam-ples of extant families and genera:

Family Planulinidae. Test evolute or partlyevolute on both sides; chamber arrangement


trochospiral throughout or planispiral in thelater part. Hyalinea, Planulina.

Family Cibicididae. Test attached; chamberarrangement (a) low trochospiral throughout, oruniserial or biserial in the later part, or (b) plani-spiral or annular. Aperture interiomarginal introchospiral forms, usually extending fromventral to dorsal side. Cibicides, Cibicidoides,Cyclocibicides, Dyocibicides.

Family Planorbulinidae. Chamber arrange-ment trochospiral throughout, or planispiral.annular, or irregularly multispiral in the laterpart. Aperture in adult forms peripheral andmultiple. Caribeanella, Planorbulina.

Family Cymbaloporidae. Chamber arrange-ment trochospiral in early part, annular in laterpart; numerous apertures, usually as large pores.Cymbaloparetta.

(6) Superfamily Acervulinacea. Earliestchambers may be coiled; adult chambers numer-ous and irregularly arranged, producing diversetest forms; aperture present only as mural pores;test coarsely perforate; wall structure opticallyradial. Examples of extant families and genera:

Family Acervulinidae. Chambers spirallyarranged in early part, and spreading irregularlyin layers in later part. Test attached or free.Acervulina, Gypsina.

Family Homotrematidae. Chambers arrangedspirally in early part, and forming a massive orbranching structure in the later part. Testattached. Homotrema, Miniacina.

(7 ) Superfamily Asterigerinacea. Chamberarrangement trochospiral to nearly planispiral;chambers fully or partly subdivided by internalpartitions; primary aperture interiomarginal orareal; secondary apertures sutural or areal; wallstructure optically radial. Examples of extantfamilies and genera:

Family Epistomariidae. Test trochospiral;chambers with complete or incomplete cham-berlets. Nuttallides, Palmerinella.

Family Asterigerinidae. Test trochospiral;alternating larger and smaller chamberlets in astellate arrangement on the ventral side.Asterigerina.

Family Amphisteginidae. Test trochospiral;numerous chambers and chamberlets wi th sinu-ous sutures. Amphistegina.

( 8 ) Superfamily Nonionacea. Test fully ornearly planispiral; aperture distinct or pore-like,with interiomarginal, areal, sutural , or peri-pheral location; wall structure optically granularor radial. Examples of extant families andgenera:

Family Nonionidae. Test fully planispiralthroughout or in early part; aperture slitlike ora series of pores. Astrononion, Haynesina. Mel-onis, Nonion, Nonionella, Nonionellina, Pullenia.

(9 ) Superfamily Chilostomellacea. Testtrochospiral to planispiral throughout, or in theearly part, with uncoiled later part; apertureinteriomarginal in coiled forms, terminal inuncoiled forms; wall structure optically granu-lar. Examples of extant families and genera:

Family Chilostomellidae. Test low trocho-spiral to planispiral; later chambers envelopingearlier ones; chambers wi thout internal parti-tions. Allomorphina, Chilostomella.

Family Quadrimorphinidae. Test lowtrochospiral; chambers not enveloping, withinternal partitions. Quadrimorphina.

Family Osangulariidae. Test low trochospiral;aperture (a) partly interiomarginal, partly arealoblique, or ( b ) wholly areal. Osangularia.

Family Oridorsalidae. Test low trochospiral;primary aperture interiomarginal; secondaryapertures sutural, on both sides of test.Oridorsalis.

Family Gavelinellidae. Test low to hightrochospiral; aperture interiomarginal, usuallybordered by a narrow or wide extension ofchamber wall. Gyroidina, Gyroidinoides, Han-senisca, Hanzawaia.

Family Karreriidae. Test attached. Chamberarrangement low trochospiral in early part,serial later. Karreria.

(10) Superfamily Rotaliacea. Test typicallylow trochospiral or planispiral, with numerouschambers; intercameral septa doubled by theaddition of a lamina during new chamber forma-tion, usually with various internal passages;aperture interiomarginal or areal, single ormultiple; wall structure optically radial, with afew granular exceptions. Examples of extantfamilies and genera:

Family Rotaliidae. Test low trochospiral


throughout, usually with radial, intraseptal, orsutural canals or fissures. Ammonia (Fig. 2.9),Asterorotalia, Pararotalia.

Family Calcarinidae. Test low trochospiral toplanispiral; symmetrical or nearly so; usual lyspinose. Baculogypsina, Calcarina.

Family Elphidiidae. Test planispiral to lowtrochospiral; with sutural canal system andpores. Cribroelphidium, Elphidium, Elphidiella,Ozawaia, Parrellina.

( 1 1 ) Superfamily Nummulitacea. Chamberarrangement planispiral or annular; numerouschambers, with or without chamberlets; spiralor interseptal canals present. Examples of extantfamilies and genera:

Family Nummulitidae. Test form lenticular,discoidal, or stellate; numerous chambers on theequatorial plane; with or without lateral cham-bers; with a complex canal system. Cycloclypeus,Operculina, Heterostegina.

Order 13, GLOBIGERINIDA. The onlyplanktonic order of the Foraminifera. Test oflow-Mg calcite in all extant and most extincttaxa, but aragonitic in the Favusellacea (Jurassicto early Cretaceous); wall bilamellar, perforate;chamber arrangement trochospiral, planispiral,or serial; wall structure optically radial.

( 1 ) Superfamily Heterohelicacea. Chamberarrangement biserial or triserial throughout, orin the early part (with fewer or more series inthe later part). Examples of extant familiesand genera:

Family Guembelitriidae. Test triserialthroughout or in the early part. Gallitellia.

Family Chiloguembelinidae. Test biserial;aperture with a rim. Laterostomella.

(2 ) Superfamily Globorotaliacea. Chamberarrangement trochospiral or streptospiral; sur-face nonspinose; primary aperture interiomargi-nal. Examples of extant families and genera:

Family Globorotaliidae. Chamber arrange-ment low trochospiral; wall smooth or pustu-lose; aperture with rim. Berggrenia, Clavatorella,Globorotalia, Neogloboquadrina, Turborotalia.

Family Pulleniatinidae. Chamber arrange-ment streptospiral in the adult stage; chambersinflated. Pulleniatina.

Family Candeinidae. Chamber arrangementtrochospiral; primary aperture interiomarginaland single, or sutura l and multiple, in someforms covered by bullae. Candeina. Tenuitella.Tinophodella.

( 3 ) Superfamily Globigerinacea. Chamberarrangement trochospiral to planispiral: test sur-face characteristically spinose; primary apertureusual ly interiomarginal, secondary aperturessutural; aperture may be replaced by surfacepores. Examples of extant families and genera:

Family Globigerinidae. Chamber arrange-ment trochospiral throughout or changing toplanispiral in later part; test partially or com-pletely enclosed by the final chamber in somegenera. Spines loosely attached. Beella, Bolliella,Globigerina Globigerinella, Globigerinoides(Fig. 2.9), Orbulina, Sphaeroidinella.

Family Hastigerinidae. Chamber arrange-ment trochospiral in early part, planispiral orstreptospiral in later part. Spines growing fromcollar-like projections. Hastigerina, Hastigeri-nopsis, Orcadia.

Order 14, I N V O L U T I N I D A . Test made ofaragonite. Two chambered test; in i t ia l chamberenclosed by coiled, tubu la r second chamber. Nodesignated superfamily.

Family Planispirillinidae. The only extantfamily in this suborder. Asymmetrical test, coil-ing planispiral or trochospiral; umbilical area,at least on one side, filled by lamellar growth;aperture terminal. Examples: Alanwoodia,Conicospirillinoides, Planispirillina (Fig. 2.9).Trocholinopsis.

Order 15, ROBERTINIDA. Test made of ara-gonite, perforate, multichambered.

( 1 ) Superfamily Ceratobuliminacea. Cham-bers with internal partitions and arranged in atrochospiral coil; aperture areal or interiomargi-nal. Examples of extant families and genera:

Family Ceratobuliminidae. Primary apertureentirely interiomarginal or with areal extension.Ceratobulimina.

Family Epistominidae. Primary aperture a sl i ton the test margin. Hoeglundina.

( 2 ) Superfamily Robertinacea. Chambers

Concluding remarks 33

with double internal part i t ions; secondarychambers clearly distinguishable from primarychambers.

Family Robertinidae. The only family underRobertinacea; def ining characters same as thoseof the superfamily. Examples: Al l iat ina. Cush-manella, Robertina, Robertinoides (Fig. 2.9).Sidebottomina.

Order 16, S ILICOLOCULINIDA. Test madeof opaline silica; imperforate. No superfamilydesignated.

Family Silicoloculinidae. Mult ichamberedcoiled test; chambers arranged in various planes:aperture terminal, part ly blocked. Example:Miliammellus (Fig. 2.9).

2.6 GEOLOGICAL RECORD OF EXTANTFORAMINIFERAL TAXA

Many foraminiferal species and genera werefi rs t reported as fossils ra ther than as l iv ingorganisms. Any massive compilation of geolo-gical ranges of such taxa is likely to miss afew later reports of their occurrence in modernsediments. Thus, some genera cont inu ing intothe Holocene (e.g. Loxostomum, Suggrunda)are listed as extinct in Loeblich and Tappan(1987) . On the other hand, about half of thenearly 900 extant foraminiferal genera men-tioned in Loeblich and Tappan ( 1 9 8 7 ) haveno pre-Holocene record (Tappan andLoeblich, 1988). This does not necessarilymean that the earliest species of all thesegenera actually evolved in the last 10,000years; the earlier history may be lost, becauseof taphonomic processes (see chapter 16) anddiagenesis, and by the destruction of the sedi-mentary record by diverse geological pro-cesses. Organic-walled tests (Al logromi ida) arepreserved only under exceptionally favorableconditions; they have a very poor and erraticfossil record. Agglut inated tests w i t h looselyattached grains or wi th organic cement fre-quent ly disintegrate in many sedimentary envi-ronments, and dur ing diagenesis. Aragonitictests (Robert inida and Invo lu t in ida ) are

destroyed in diagenesis more readily thancalcitic tests. Compared to low-Mg calcit ictests, both aragonitic and high-Mg calcitictests ( M i l i o l i d a ) are preferent ia l ly dissolved inthe deep sea. Apparent ly , tests made of calcitespicules (Car te r in ida ) are also poorly pre-served: they are known from the Eocene andHolocene. but not from the interveningepochs.

The geological record of ex tan t families isgiven in Table 2.3. About three-four ths of these164 families have a pre-Holocene record.Eleven can be traced as far back as earlyPaleozoic (Cambrian and Ordovician); all ofthese taxa are organic-walled or agglutinated

(orders Allogromiida. Astrorhizida, and Lituo-lida). The most specialized calcareous order ofthe Paleozoic ( F u s u l i n i d a ) is ext inct . Amongmodern famil ies wi th secreted calcareous tests,only two can be traced to the Paleozoic (earlyCarboniferous); both of these are characterizedby imperforate walls ( M i l i o l i d a ) . A few extanthyal ine families (calcareous perforate tests)extend back to the Triassic. but for the t w omost diverse groups of Holocene calcareousForaminifera, the record of modern famil iesbegins in the Cretaceous; 27% of extant fami-lies of the Bul imin ida and 37% of extantfamilies of the Rotal i ida started in th is 78-my-long period. The effect of the mass ext inct ionat the Cretaceous-Paleogene boundary wasmuch more severe on p lank ton ic Foraminifera.All seven extant families of the Globigerinidawere present in the Miocene, but only onefamily, Guembeli t r i idae ( w i t h a single Holo-cene genus, Gallitellia), can be traced back tothe Cretaceous. Overall, the s t ra t igraphicrecord shows tha t 62 benthic families origi-nated in the Cretaceous, of which 22 areext inct . For p lanktonic families, the numbersare 10 and 9, respectively.

2.7 CONCLUDING REMARKS

The Loeblich and Tappan classif ication of 1987.emended by them in 1992. and fu r the r modifiedfor ordinal taxa in this chapter, is the most


Concluding remarks 35

elaborate hierarchical classification of the Fora-minifera ever produced. Although the 1987 clas-sification was not as well-received as theirsimpler 1964 classification (Haman, 1988), it isthe current standard, at least for the placementof genera into families and superfamilies. Hierar-chical biological classifications are inherentlysubjective, especially where a large part of thedata is derived from the fossil record. There isdisagreement between Loeblich and Tappan(1987, 1992) and other taxonomists even onsome well-known foraminiferal taxa, e.g.(a) about the recognition of superfamilies, fami-lies, subfamilies, and their constituent generawithin the Buliminida (Revets, 1996), (b) aboutthe inclusion of Discorbis, Rosalina, Eponides,and Gavelinopsis in the Discorbacea, rather thanin the Rotaliacea or Eponidacea, a superfamilynot recognized by Loeblich and Tappan(Hansen and Revets, 1992), and (c) about theplacement of the Elphidiidae in the Rotaliacea,rather than in the Nonionacea (Haynes, 1990).In the context of the entire classification, how-ever, these problems are not overwhelming.

On the positive side, the major improvementover the 1964 version is the de-emphasizing ofthe optical property of hyaline walls in the1987 expansion. The use of the radial andgranular wall structures (as seen in polarizedl ight ) for superfamily distinctions has beenconsidered an ‘unnecessarily rigid constraint’for a long time (e.g. Cifelli, 1976). This con-straint was removed by Loeblich and Tappanin 1987. For example, Cassidulina and Islan-diella, two similar genera, were placed in twodifferent superfamilies (Cassidulinacea andBuliminacea) in Loeblich and Tappan (1964a);they are now in the same family (Cassidulini-dae). The problem is not fully resolved, how-ever. In view of the fact that both radial andgranular structures have been observed withina single genus (Elphidium), the usefulness ofthis optical property at any level of taxonomichierarchy needs reexamination. At the ordinallevel, the status of the Silicoloculinida and theplacement of the extant members of the Invo-lutinida are uncertain; the decisions inLoeblich and Tappan (1992) are different fromthose in Loeblich and Tappan (1987).

Foraminiferal classifications are largely theoutcome of paleontological research. Thosereported in relatively recent protozoological lit-erature (e.g. Levine et al., 1980; Lee, 1990a) gen-erally agree in concept and overall structure, ifnot in the ranks of taxa, with one of the Loeblichand Tappan schemes. However, a startlingregression to chamber count as the chosen pri-mary criterion is observed in one classification(Cavalier-Smith, 1993). In this, the Foraminifera(as a subphylum within the Kingdom Protozoa)is split into two classes, one with single-cham-bered forms (Monothalamea), the other withmultichambered forms (Polythalamea). TheMonothalamea, reminiscent of d’Orbigny’sMonostègues, is not split fur ther into lowersuprageneric categories. The included genera arenot named, but by defintion, this group wouldinclude Myxotheca (organic-walled), Saccam-mina (agglutinated), Squamulina (calcareousimperforate), and Lagena (calcareous perforate),i.e. genera representing four separate orders(three of them with numerous multichamberedgenera) in the schemes of Haynes ( 1 9 8 1 ) , Lee(1990a), and Loeblich and Tappan (1992). Suchtaxonomy is a denial of the enormous body ofextant information on foraminiferal wall com-positions, stratigraphic distributions, and prob-able phylogenies.

On the other hand, it is almost axiomatic thatscientific classification of the Foraminifera mustnot be based on skeletal morphology alone. Thegeological record of fossils and the DNA signa-tures of living species, both providing significantclues to phylogenetic connections, must supportany logical scheme of classification. The geologi-cal history of the Foraminifera has been takeninto consideration by most systematists, startingwith Cushman, but the genetic study is still inits infancy (see, e.g. Pawlowski et al., 1994a, b,1996; Wray et al., 1995; Holzmann and Pawlow-ski, 1997), and has not yet become a cause forrestructuring the suprageneric classification. Inany case, the half-century old statement of AlanWood is still true: ‘If classifications of the futureare to be “natural,” reflecting the evolutionaryhistory of the group, they will be not less butmore complicated than those at present infavour’ (Wood, 1949).


2.8 ACKNOWLEDGMENTS

I thank Laurie Anderson, Anthony Arnold, Wil-liam Berggren, and John Haynes for their help-ful suggestions regarding the manuscript,Johanna Resig for sharing her current thoughtson the Silicoloculinida, and Samuel Bowser,

Leanne French, Susan Goldstein, Megan Jones,Manfred Kage, and Emil Platon for contribut-ing i l lus t ra t ions to this chapter. I am indebtedto Mary Lee Eggart for art work and to EmilPlaton for scanning electron micrography of myforaminiferal specimens.

3Foraminifera:

A biological overviewSusan T. Goldstein

3.1 INTRODUCTION: FORAMINIFERAAS LIVING ORGANISMS

The Foraminifera are an enormously successfulgroup of amoeboid protists. Branching verydeeply wi th in the eukaryotic evolutionary tree(Pawlowski et al., 1998b), they f i r s t appeared inthe Cambrian, and, over the course of thePhanerozoic, invaded most marginal to ful lymarine environments and diversified to exploita wide variety of modes of life. Foraminifera areabundant and diverse in modern oceans wherethey occur from coastal settings to both plank-tonic and benthic habitats of the deep sea. Theyoccupy tiered epibenthic to deep infaunal micro-habitats and util ize a diversity of trophicmechanisms.

Some representatives have attained giganticproportions. The extinct Lepidocyclina ele-phantina, for example, at over 14cm is amongthe largest reported (Grell. 1973). The Foramini-fera, al though exclusively unicellular, accom-plish nearly all of the fundamental funct ions oflife performed by the myriad of mul t icel lu laranimals. Foraminifera eat, defecate, move, grow,reproduce, and respond to a variety of environ-mental stimuli. Whereas metazoans evolved

organs and other specialized features throughmulticellularity, Foraminifera and other protistsspecialized by diversifying subcellular compo-nents or organelles to perform these variousfunctions.

Two broad morphological features dis t in-guish the Foraminifera from other protists. First,all Foraminifera possess granuloreticulopodia(Figs. 3.1, 3.2), which are fine, thread-like, pseu-dopodia that anastomose (spl i t and rejoin) andhave a granular texture when viewed with thelight microscope. Second, nearly all Foramini-fera possess a test or shell tha t encompasses theorganism and separates it from the surroundingmilieu. The test may be organic (not mineral-ized), agglutinated (constructed of foreign par-ticles cemented together by the foraminifer) ,composed of calcium carbonate or, in rare cases,silica (see chapter 2). In addition, the Foramini-fera are united by a l ife cycle characterized bya fundamental alternation of sexual and asexualgenerations tha t has become secondarily modi-fied in some groups. Having made these general-izations, it is interesting to note that thefreshwater rhizopod Reticulomyxa has pseudo-podia that are s t r ik ingly similar to those of theForaminifera (Orokos et al., 1997). though it

Barun K.Sen Gupta (ed.), Modern Foraminifera, 37–55© 1999 Kluwer Academic Publishers. Printed in Great Britain.

Foraminifera: A biological overview38

lacks a shell. Genetically, this protist is a fora-miniferan (Pawlowski et al.. 1998a).

Our understanding of the Foraminifera asliving, amoeboid protists dates to Dujardin’s(1835a,b,d) observations on several l iv ing shal-low-water Foraminifera (Triloculina, Elphidium,Ammonia, Peneroplis) which he obtained bywashing fucoid and coralline algae collectedfrom the Mediterranean into glass vessels. Healso observed Gromia oviformis, a protistan rela-tive of the Foraminifera that superficially resem-bles the foraminifer Allogromia (Gromia’spseudopodia and life cycle differ from thosecharacteristic of the Foraminifera; see Arnold,1972). Watching live milioline Foraminiferaclimb the walls of his vessels, Dujardin (1835b)described granule-filled, anastomosing ‘fila-ments’ (pseudopodia) which slowly extendedand retracted as the Foraminifera adhered tothe vessel walls and slowly moved. Dujardincoined the term ‘sarcode’ to describe amoeboi-dal cytoplasm, and established the ‘Rhizopodes’,suggesting a relationship between the Foramini-fera and other amoebae.

3.2 PSEUDOPODIA

The key to Dujardin’s (1835a,b,d) correct identi-fication of the Foraminifera as amoeboid organ-isms, thus removing them from the cephalopodswhere d’Orbigny (1826) had previously placedthem (see Cole, 1926; Lipps, 1981), were hisobservations on the undifferentiated body (‘sar-code’) of the Foraminifera and on the anasto-mosing, granular pseudopodia which allForaminifera possess (see Fig. 2.2). We nowknow that pseudopodia accomplish many essen-tial life functions for the Foraminifera and are.therefore, of fundamental importance (Travisand Bowser, 1991). Pseudopodia are essentialnot only for moti l i ty and attachment, as recog-nized by Dujardin (1835a,b,d), but also for feed-ing, building and structur ing tests, protection,and some aspects of respiration and repro-duction. Pseudopodia provide the mechanismby which Foraminifera interact wi th theirsurroundings.

Foraminifera extrude pseudopodia throughone or more apertural openings in the test. Thefirst pseudopodia extruded commonly are finefi laments or ‘filopodia’ t ha t are often stra ight .As this process continues, the pseudopodialt runk or ‘peduncle’ thickens and vi r tua l ly fi l lsthe apertural opening(s) , branching into numer-ous finer pseudopodia tha t often anastomose.The result, if the foraminifer is provided a hardsmooth surface, is an intricate, st icky pseudopo-dial network of ‘reticulopodia’ tha t r iva l s thecomplexity of a spider’s web (Carpenter et al.,1862; Leidy, 1879). U n l i k e a spider’s web, how-ever, reticulopodia are continuously remodeledand transport a variety of materials. Particlemovement, as many early observers remarked,is bidirectional, even w i t h i n a single pseudopo-dial strand (Allen , 1964).

The intr icacy and funct ion of reticulopodiacaptivated many of the early foraminiferal biolo-gists who provided detailed and sometimespoetic accounts of thei r observations ( Dujardin,1835a,b,d; Carpenter et al., 1862; Leidy, 1879[though his descriptions were based largely onfreshwater protists included in ‘Gromia’]: Lister,1903; Winter, 1907; Sandon, 1934; Jepps. 1942).Contemporary cell biologists have found fora-miniferal pseudopodia excellent experimentalsystems for a number of processes including cellmotility and the assembly and disassembly ofmicrotubules (e.g. Jahn and Rinaldi , 1959; Allen ,1964; Travis and Allen, 1981; Bowser andReider, 1985; Bowser et al., 1986; Travis andBowser, 1986a,b; Bowser et al., 1988; Travis andBowser, 1988; Welnhofer and Travis. 1996).

Though some benthic Foraminifera do indeedlive attached to hard or f i r m surfaces such asseagrasses, macroscopic algae, shells, sponges, orrocks (Lu tze and Altenbach, 1988; Lutze andThiel, 1989; Langer, 1993), and probably extendreticulopodial nets in the field much as they doon glass slides, most l ive associated with f i n e -grained sediments through which they activelymigrate (Severin and Erskian, 1981; Severin.1987b; Wetmore, 1988; Weinburg. 1991; Hem-leben and Kitazato, 1995; Bornmalm et al., 1997).When offered abundant fine-grained sediment,most Foraminifera use thei r pseudopodia to col-

Trophic mechanisms 39

lect a variety of materials, including sediment,algal cells, bacteria, and organic detritus (seeGoldstein and Corliss, 1994). Such collections areformed into mounds that may be large enoughto completely encompass the test and are riddledwith a three-dimensional reticulopodial array.Though commonly associated with feeding,many benthic Foraminifera construct somewhatsimilar mounds or cysts during the formation ofa new chamber or prior to reproduction.

Structurally, foraminiferal pseudopodia areencased by a cell membrane and contain acytoskeletal core of microtubules which mayoccur singly, but more typically as loosely orga-nized bundles (Fig. 3.3) (reviewed in Travis andBowser, 1991). These loosely arranged microtu-bules in the Foraminifera lack the intricate micro-tubular patterns found in cross sections of the‘axopodia’ of such amoeboid protists as the helio-zoans (Kitching, 1964; Smith and Patterson,1986) and radiolarians (Cachon and Cachon,1971, 1972; Anderson, 1983). However, perhapsnot unlike the heliozoans, the Foraminifera havedeveloped specialized mechanisms for rapidassembly and disassembly of microtubules, whichallow rapid retraction of reticulopodia and theirredeployment when needed (Welnhofer andTravis, 1996. and references therein).

Ultrastructural studies show that the charac-teristic granular appearance of foraminiferalpseudopodia is due to the presence of severalorganelles or structures that include mito-chondria, ‘dense bodies’, phagosomes, defeca-tion vacuoles, and a variety of other smallerstructures (Fig. 3.3) (reviewed in Travis andBowser, 1991). Mitochondria are the mostprominent pseudopodial granules. They movebidirectionally, are essential for aerobic respira-tion, and are probably responsible for trans-porting metabolic energy (ATP) wi th in thereticulopodial network. ‘Dense bodies’ are mem-brane-bound vesicles that appear refractileunder the light microscope and opaque withTEM (transmission electron microscopy). Theirfunction has not yet been determined, thoughTravis and Bowser ( 1 9 9 1 ) suggest that they mayserve as storage vesicles for phospholipids(building blocks of membranes). Phagosomes

are vacuoles that contain materials captured foringestion, and their content varies widely,depending on the diet of the foraminifer. Xan-thosomes, packets of undigested materials alongwi th metabolic wastes, are transported out andaway from the foraminifer along pseudopodiain defecation vacuoles ( i l lustrated in Bowseret al., 1985). For more information on pseudo-podial structure and function, see Travis andBowser ( 1 9 9 1 ) .

3.3 TROPHIC MECHANISMS

As a group, the Foraminifera utilize a broadrange of feeding mechanisms and nutr i t ionalresources, including grazing, suspension feeding,deposit feeding, carnivory, parasitism, the directuptake of DOC, and symbiosis. Many smallerForaminifera that l ive wi th in the photic zonecommonly feed on selected species of algae(Fig. 3.4) (see reviews by Arnold, 1974, andAnderson et al., 1991). but are also known toingest bacteria, yeasts, fungi, and in some cases,small animals (Lee et al., 1966; Lipps. 1983; Lee.1980; Bernhard and Bowser, 1992). Bacteriaappear to play an indispensable role in the nutr i-tion of many Foraminifera (Lee, 1980). Thoughthe diet of most Foraminifera may be quitevaried, feeding experiments have shown thatmany species feed selectively (Lee et al., 1966;Lee, 1980). Pseudopodia play an indispensablerole in feeding in that they funct ion to gatherfood (e.g. Jepps, 1942), subdue prey (Bowseret al., 1992), and, in at least some species,may also function in extrathalamous digestion(Jepps, 1942; Meyer-Reil and Köster, 1991; Leeet al., 1991b; Faber and Lee, 1991b).

Foraminifera that live below the photic zonecannot rely on l iving algal cells as a food source.However, the influx of phytodetritus to the sea-floor from the plankton provides important pri-mary and secondary food resources for Fora-minifera and other members of the benthos.Gooday (1988) documented the selective exploi-tation of phytodetri tus by several small speciesthat appear to reproduce very rapidly, thus colo-nizing fresh phytodetritus as it arrives on the

40 Foraminifera: A biological overview

seafloor. A number of subsequent investigationssupport these findings (Thie l et al., 1989;Gooday and Lambshead, 1989; Lambshead andGooday, 1990; Gooday and Turley, 1990;Gooday, 1993). More degraded forms of organicdetritus, and, especially, the microbiotas ( largelybacteria) associated with this material provideimportant food resources for shallow (Heeger,1990) to deeper infaunal taxa (Goldstein andCorliss, 1994).

Grazing, found in some shallow-water Fora-minifera, is accomplished by feeding largely onalgal cells while moving over a surface such asa seagrass blade, kelp, or coralline algae. Thisprocess can be observed easily in culture. Jepps(1942), for example, described individuals of‘Polystomella’ ( = Elphidium) crispum feeding onlawns of cultured diatoms. The foraminiferswould use their pseudopodia to collect moundsof diatoms so extensive that they completelycovered the test. After feeding w i t h i n one moundfor some time (usual ly hours), the foraminiferwould discard it, move on, then construct a freshmound. Discarded mounds, or ‘feeding cysts’contained small orange xanthosomes (wasteparticles) that were shed by the foraminifer.

Suspension feeding Foraminifera make use ofthe small organisms and detritus that are sus-pended in the water column. This mode of feed-ing occurs in Foraminifera that occupy elevatedepibenthic substrates as well as some of thosethat live in association with soft sediments.

Lipps ( 1 9 8 3 ) suggested tha t suspension feedingis widespread in Foraminifera tha t elevate the i raperture(s) above the sediment–water interfaceand extrude their pseudopodia directly into thewater column. Because Foraminifera lack amechanism for creating water currents as domany suspension-feeding invertebrates and cil i-ated protists, the suspension-feeding Foramini-fera are most likely ‘passive’ suspension feeders(Lipps , 1983).

Suspension feeding occurs in both aggluti-nated and calcareous taxa. Astrorhiza limicola,for example, is a biconvex, agglutinated, mono-thalamous foraminifer with mult iple apertures,each positioned at the end of a tube. In l ifeposition, th is foraminifer rises up on i ts edge,posit ioning some apertures in to the sedimentand others into the overlying water column.Pseudopodia extend from all apertures. Thoseprotruding in to the sediment serve to anchorthe foraminifer while those protruding from ele-vated apertures extend in to the water column,and trap food particles (Cedhagen, 1988). Pelo-sina arborescens, another monothalamousagglutinated foraminifer t h a t lives in soft sedi-ments, s imilarly u t i l izes suspension feeding as atrophic mechanism (Fig. 3.5, 3.6) (Cedhagen,1993). Suspension feeding also occurs in severalcalcareous species that occupy elevated habitats:Rupertina stabilis, Cibicides wuellerstorfi, andPlanulina ariminensis (Lu tze and Altenbach ,1988; Lutze and Thiel, 1989) as well as the agglu-



tinated Saccorhiza ramosa (Al tenbach et al.,1988). Epizoic Foraminifera that reside on theshells of living brachiopods may also ut i l ize sus-pension feeding and benefit from brachiopodfeeding currents (Zumwalt and DeLaca, 1980).

The construction of feeding cysts, as in Elphi-dium crispum, is not limited to grazing, but is alsoan integral part of deposit feeding. Many benthicForaminifera that live in muddy sediments, bothwi th in and below the photic zone, use their pseu-dopodia to construct feeding cysts (Hofker , 1927;Nyholm, 1957; Goldstein and Corliss. 1994) withsediment, algal cells (or their remains in the formof phytodetritus), bacteria, and organic detritus(Goldstein and Corliss, 1994). Some of the mate-rial gathered by the pseudopodia is partitionedinto small parcels which the foraminifer ingestsby phagotrophy wi th in the terminal chamber(Fig 3.7). Deposit feeding Foraminifera, such asthe deep-sea dwellers Globobulimina pacifica andUvigerina peregrina and the shallow-water Ammo-nia beccarii, ingest a surprisingly large amount ofsediment as well as algal cells, bacteria, andorganic detritus. Bacteria appear to constitute animportant element in the diet of deposit-feedingForaminifera (Goldstein and Corliss, 1994).

Carnivory is utilized by some Foraminifera,including both benthic and planktonic speciesand both symbiont-bearing and non-symbiont-bearing forms. The large symbiont-bearing fora-minifer Peneroplis pertusus, for example, feedson copepods, but ingests only portions of theprey, leaving the empty carapace behind(Winter , 1907). The large non-symbiont-bearingagglutinated foraminifer Astrorhiza limicola is atleast partly carnivorous, and captures prey aslarge as 2–3 cm, including several types of smallcrustaceans (cumaceans, caprellids), and echi-noid larvae ( Buchanan and Hedley, 1960). Somecarnivorous Foraminifera are quite small. Hal-lock and Talge (1994) described a small preda-tory foraminifer (Floresina amphiphaga) thatattacks the larger foraminifer , Amphistegina gib-bosa. F. amphiphaga attaches to the test of itsprey and dri l ls up to 10 holes per at tachmentsite, often k i l l ing i ts prey. Carnivory has beenreported in several additional benthic species(see Boltovskoy and Wright, 1976).

Carnivory also occurs in some p l a n k t o n i cForaminifera. Anderson and Bé ( 1 9 7 6 ) and Béet al. (1977a) found the remains of copepodsand other small crustaceans w i t h i n the bubblecapsule of Hastigerina pelagica and among thespines and pseudopodia of Globigerinella aequi-lateralis. These and several other p lank ton ictaxa (Orbulina universa, Globigerinoides ruber.Globorotalia menardii, and Pulleniatina obliqui-loculata) would prey on copepods and naupliiof the brine shrimp, Artemia, in laboratorycultures.

The pseudopodia of carnivorous Foraminiferamay be specially adapted for captur ing prey. Inthe large agglutinated foraminifer Astramminarara, pseudopodia secrete an extracellularmat r ix material tha t funct ions to strengthenpseudopodia and m a i n t a i n their i n t eg r i t y asprey resist capture. Non-carnivorous Foramini-fera lack t h i s mater ia l and have pseudopodiatha t are many times weaker than those fromcarnivorous Foraminifera (Bowser et al., 1992).In addition, some carnivorous Foraminiferamay have the ability to secrete an adhesive mate-r ia l in the area where prey contact pseudopodia

(Anderson and Bé. 1976; Bowser et al., 1992).Many carnivorous Foraminifera , however, are

not s t r ic t ly carnivorous, but u t i l i z e carn ivory inaddition to at least one other t rophic mecha-nism. Cedhagen (1988) , for example, reportedsuspension feeding in Astrorhiza limicola, aforaminifer better known for its carnivory(Buchanan and Hedley, 1960). Astrammina raraingests bacteria and diatoms in addition tometazoan prey (Bowser et al., 1992), and somecarnivorous p lank ton ic Foraminifera also ingestdiatoms (Bé et al., 1977a). Some species, bothbenthic and p lank ton ic , u t i l i z e carnivory in con-junct ion wi th algal endosymbiosis.

Though the vast majority of Foraminifera arefree-living, a few species show parasitism, pri-mar i ly infes t ing other foraminifers , b ivalve mol-luscs, sponges, or stone corals. Le Calvez ( 1947)first documented parasitism in the Foraminiferaby reporting the ectoparasitic existence of theuni locu la r ‘Entosolenia’ ( = Fissurina) marginataon the fo ramin i f e r Discorbis vilardeboanus.F. marginata attaches to the spiral side of the


host and uses its pseudopodia to capture gran-ules from the host’s extrathalamous cytoplasm.This species could be cultured only in associa-tion with D. vilardeboanus and not when offeredalternative foods such as algae or other speciesof Foraminifera. The small foraminifer Metaro-taliella tuvaluensis may potentially parasitizeseveral miliolid species (Collen, 1998). M. tuva-luensis attaches to the surface of juveni le milio-lids, and causes deformations of the host test asthe host overgrows this small foraminifer; livingmaterial, however, was not observed. The fora-minifer Cibicides refulgens parasitizes the Ant-arctic scallop Adamussium colbecki by erodingthrough the scallop’s shell and feeding on thenutrient-rich fluids in the extrapallial cavity; thisspecies also feeds by grazing and suspensionfeeding (Alexander and DeLaca, 1987). Unlikeother parasitic Foraminifera, Hyrrokkin sarco-phaga infests multiple hosts (selected bivalves,sponges, and stone corals). This foraminifer pen-etrates the body wall of the hosts and feeds onsoft tissues (Cedhagen, 1994).

Pawlowski (1989) and Pawlowski and Lee(1992) described an unusual association betweenthe small foraminifer Rotaliella elatiana and themacrophytic alga Enteromorpha. The foramini-fer lives inside the filaments of the alga and wil lnot grow in culture unless the alga is present.Pawlowski (1989), therefore, suggests that thisforaminifer is nutr i t ionally dependent on thealga.

The large arborescent foraminifer Notoden-drodes antarctikos is capable of utilizing dis-solved organic carbon (DOC) (DeLaca et al.,1981; DeLaca, 1982). Labeled amino acids andglucose introduced into sterile seawater weretaken up by the foraminifer and rapidly metabo-lized. Given the opportunity, however, this fora-minifer also ingests bacteria and paniculateorganic matter, and thus, does not rely exclu-sively on the uptake of DOC. Reservoirs ofDOC present in sediments may provide animportant nutritional resource during particu-larly oligotrophic seasons in the Antarctic(DeLaca, 1982). This potentially widespreadtrophic mechanism, however, has received l i t t leattention.

Symbiotic relationships, discussed in detail inchapter 8, are quite varied in the Foraminifera,and include algal endosymbiosis (Lee andAnderson, 199 la ) , chloroplast husbandry(Lopez, 1979; Lee et al., 1988; Bernhard, 1996),and bacterial endosymbiosis (Bernhard, 1996).Of these, algal endosymbiosis, which occurs inlarger calcareous benthic Foraminifera (Fig. 3.8)and many planktonic species, is the best known.Chloroplast husbandry, the process by whichForaminifera sequester and house chloroplastsbut not the entire algal cell, occurs in somebenthic Foraminifera from both shallow-waterhabitats (Lopez, 1979; Leutenegger, 1984; Leeet al., 1988; Lee and Anderson, 199la) and low-oxygen microhabitats located well below thephotic zone (Bernhard, 1996). In addition, bac-terial endosymbionts have been identified insome benthic Foraminifera that live in anoxicor very low-oxygen microhabitats, though theactual mechanisms involved in this relationshiphave not yet been determined (Bernhard, 1996).

Algal endosymbiosis occurs in some represen-tatives from three Foraminiferal orders: Milio-lida, Rotaliida, and Globigerinida. Symbiont-bearing Foraminifera include most, though notall, large shallow-water dwellers from oligotro-phic tropical and subtropical environments.Symbionts in the Miliolida are the most diverse,and include chlorophytes (Soritidae), rhodo-phytes (Perneoplidae), dinoflagellates (Soriti-dae), and diatoms (Alveolinidae). Only diatoms,however, are found in the algal symbiont-bear-ing members of the Rotaliida (Amphisteginidae,Calcarinidae, Nummuli t idae) . Planktonic Fora-minifera (Globigerinida) may host either dino-flagellate or chrysophyte symbionts (seechapter 8, and reviews by Leutenegger, 1984,and Lee and Anderson. 1991a).

This broad array of potential algal endosym-bionts allows different foraminiferal hosts tothrive at different depths within the photic zone(Leutenegger, 1984; Hallock. 1988a, 1988b; seechapter 8). The shallowest-water habitats arehome to benthic Foraminifera with all types ofsymbionts. Those bearing chlorophytes, how-ever, are limited to the shallowest depths(~30 m), whereas those with rhodophytes or


dinoflagellates extend to deeper habitats(60–70 m). Those with diatoms are found asdeep as The photosynthetic pigmentsof different algal groups are activated by lightof different wavelengths. Diatoms utilize light inthe blue to green range, allowing them to exploitthe deepest habitats (Leutenegger, 1984).Though diatom-bearing Foraminifera occur atall depths, those in shallow-water habitats mayprotect themselves behaviorally by avoidingdirect sunlight (Heterostegina depressa) or pos-sessing a test that morphologically preventsoverexposure (calcarinids) (Leutenegger, 1984;Hallock et al., 1991b; Lee and Anderson, 1991a).

Relationships between Foraminifera and theiralgal endosymbionts are often not specific. Asingle foraminiferal species may host differentspecies of symbionts, particularly if they are dia-toms (Lee et al., 1989, 1992; Lee and Anderson,199la). In addition, the same species of sym-biont may occur in more than one species ofForaminifera. The dinoflagellate Gymnodiniumbéii, for example, has been reported from fourdifferent species of planktonic Foraminifera (seereview by Lee and Anderson, 199la). Relation-ships between the foraminiferal host and sym-biont are varied and complex. In general, how-ever, symbionts release exudates to the host, and

can in some cases supply the foraminifer with allthe organic carbon it requires (Jørgensen et al.,1985). Algal symbionts also promote calcifica-tion in some planktonic and benthic hosts (Béet al., 1982; Duguay, 1983). The foraminifer, inreturn, provides the symbiont with a fairly stablemicroenvironment in addition to dissolvednitrogen, phosphorus, and potentially other nu t -ritional requirements (see Lee and Anderson,199la). Carnivory plays an important dietaryrole in some symbiont-bearing Foraminifera byproviding a source for nitrogen and phosphorusfor the host-algal system (Jørgensen et al., 1985).

Foraminifera that host algal symbionts arequite dependent on their presence and wellbeing. Hosts do not grow well in the dark orwhere the symbionts have been experimentallyremoved. Most symbionts, however, can begrown in culture quite readily without their fora-miniferal host, and this is perhaps an essentialfeature of the relationship. Though symbiontsare transmitted to offspring during asexualreproduction (multiple fission), gametes and(presumably) zygotes are symbiont-free. Howand when the developing zygotes acquire symbi-onts in not known.

Some benthic Foraminifera belonging to thefamilies Nonionidae, Elphidiidae, and Rotalielli-

Growth and test morphogenesis 45

dae sequester and house chloroplasts obtainedfrom algal food sources (Lopez, 1979; Lee andAnderson, 199la). Such chloroplasts retain the i rability to photosynthesize in some hosts tha treside within the photic zone. Over time, how-ever, the foraminiferal host digests its chloro-plasts, suggesting that the foraminifer mustconstantly replenish its supply (Lee and Ander-son, 1991a). Interestingly, Bernhard (1996) iden-tified a similar relationship in a nonionid tha tlives well below the photic zone in low-oxygen,benthic microenvironments of the Santa Bar-bara Basin.

3.4 GROWTH AND TESTMORPHOGENESIS

Growth in the Foraminifera is accomplished byeither increasing the size of a single chamber(unilocular forms) or, more commonly, byintermit tently adding a new chamber. Details ofthe former process are sketchy for agglutinatedtaxa and unknown in uni locular calcareousones; the latter is better known in both calcare-ous and agglutinated representatives.

In allogromiid Foraminifera, new shell mate-rial appears to be added near the aperture(Angell, 1980), and this may also be the case formany members of the Astrorhizida. In addit ion,however, single-chambered agglutinated Fora-minifera, such as Cribrothalammina alba, addmaterial to the inner organic l in ing of the testat sites distant from the aperture (Goldstein andBarker, 1988). Figure 3.9. for example, i l lus t ra testhe addition of vesicles (probably conta in ingglycosaminoglycans; see Langer, 1992) to thebase of the inner organic lining of Myxotheca sp.

Astrammina rara is a large single-chambered,coarsely agglutinated foraminifer that occursabundantly in shallow-water habitats of theAntarctic. This astrorhizid is perhaps unusua lin that it frequently sheds its test, and after abrief shell-less existence, stops and builds a newone (Bowser et al., 1995). The inter ior of thetest is characterized by a f ibrous inner organicl ining that is continuous wi th cables of bioadhe-sive (organic cement of other authors) that

anchor sediment grains in place. Finer sedimentgrains f i l l the spaces between larger grains alongthe distal surface of the test and are also boundwith bioadhesive ( Bowser and Bernhard, 1993).As the foraminifer rebuilds its test, it i n i t i a l l ygathers sediment of a v a r i e t y of sizes, thenappears to separate it by size by extending andretracting i ts pseudopodia. This concentrates thelarger sediment grains to the interior of theforming test ( K i n o s h i t a et al., 1996).

Many pioneers of foraminiferal biologyobserved and described the process of chamberformation in calcareous Foraminifera at thelevel of the light microscope (see comments in:Bé et al., 1979; Hemleben et al., 1986; 1989).Angell ( 1967b), however, provided the first u l t ra -s t ruc tura l account of chamber formation in acalcareous perforate fo r amin i f e r , Rosalina flori-dana (Order Rotaliida). This benthic speciesbegins the process by forming a t ranslucent algalcyst tha t is cemented to the substrate andextends over the entire spiral surface of the test.Next, pseudopodia coalesce within the cyst toform a template or anlage in the shape of thenew chamber. This anlage is highly vesicular ,and contains mitochondria , f i b r i l l a r material,electron-dense vesicles, and vesicles that appearto be empty. The inner organic l i n ing ( I O L ) ofthe new chamber forms by the act ivi t ies of pseu-dopodia over the surface of the anlage. Oncethe IOL is complete, cytoplasm from w i t h i n thetest floods the inter ior of the forming chamberand forces the vesicular mater ia l of the anlageout through the new aperture, thus forming asheath over the entire test surface. A layer ofcalcite is then deposited over both the newchamber and the entire test. The sheath breaksup as the foraminifer frees itself from its cystand resumes feeding. This process produces a‘monolamellar’ test ( t e rmina l chamber is onelayer th ick) which, overall , is mult i layered (seechapter 4 ) . Figure 3.10 i l l u s t r a t e s a very s imilarsequence of events du r ing chamber formation inthe calcareous perforate foramini fer Ammoniatepida (Order Ro taliida). Older chambers of thetest consist of layers of calcite separated byorganic l in ings tha t are cont inuous w i t h theorganic materials that fill the pores (Fig. 3.11and 3 .12) (Angell , 1967a).


In subsequent tracer studies using Ca45 andC14, Angell (1979) showed that R. f loridana (cal-careous perforate species) does not pool eithercalcium or carbonate ions in the cytoplasm, butrather extracts them from the su r round ing sea-water during calcification. This, however, is notuniversal among calcareous perforate Foramini-fera. The symbiont-bearing, calcareous perforateforaminifer Amphistegina lobifera indeed poolsfairly large reserves of carbonate in the cyto-plasm for use during calcification. The symbi-ont-bearing, calcareous imperforate Amphisorushemprichii, however, does not pool carbonate,but obtains it directly from seawater dur ingcalcification (ter Kuile and Erez, 1987; terKuile, 1991) .

Chamber formation in planktonic Foramini-fera, also calcareous and perforate, shows broadsimilarities to the process in R. floridana, as wellas significant differences. In the non-spinoseGloborotalia truncatulinoides, G. hirsuta, andG. menardii, a protective organic envelope isformed (Hemleben et al., 1977, 1986), compar-able to the translucent cyst described by Angell(1967b). A cytoplasmic bulge ul t imately f i l l s theenvelope and forms a ‘primary organic l ining’( P O M ) between the envelope and the cyto-plasmic bulge. The POM and the envelope col-lectively comprise the anlage for the newchamber (a s l ight ly different usage than tha t ofAngell, 1967b), and calcification occurs aspatches of calcite are deposited on both sides ofthe POM, thus forming a bilamellar shell (Hem-leben et al., 1977; Bé et al., 1979; Hemleben et al.,

1989). Chamber formation is generally similarin spinose and non-spinose taxa wi th spinesbeing added once the chamber is otherwise com-plete (Hemleben et al.. 1986).

In the plank tonic, non-spinose taxa, the newlyformed chamber undergoes subsequent modif i -cation. Pores form secondarily by pseudopodiatha t pass through the wall and form rudimen-tary pores. Further, additional calcite is addedto the surface of the chamber, t hus th ickeningthe test (Hemleben et al., 1977, 1986). Thisdiffers s ign i f i can t ly from the formation of amonolamellar, mul t i layered shell in Rosalinaf l o r i d a n a .

Among the Miliol ida (calcareous imperforateForaminifera), chamber formation at the u l t ra-s t ruc tura l level has been described in Calcitubapolymorpha (Berthold, 1976a; Hemleben et al.,1986) and in Spiroloculina hyalina (Angel l ,1980). C. polymorpha is an unusual miliolid inthat its shell is cemented to a substrate andconsists of somewhat randomly arranged, b i fur -cating calcareous tubes that are partially subdi-vided by constrictions. Occasionally, theseind iv idua l s reproduce by what appears to bemult iple f iss ion, forming numerous young w i t hmi l io l ine coiling that grow by forming longbranching tubes (Arno ld , 1967). C. polymorphaadds a new tube or chamber by forming an‘outer organic lining,’ then t ranspor t ing vesiclesof preformed calcite needles to the site of calcifi-cation where they are released to form the shel l .An inner organic l in ing is the last element added

Growth and test morphogenesis 47

to the shell (Berthold, 1976a; Hemleben et al.,1986).

Chamber formation in Spiroloculina hyalina,reported by Angell (1980), begins with the con-struction of a cyst that surrounds the entire testand is composed of algal cells and detritusbound by a transparent membrane, similar tothe process in Rosalina floridana. Fine pseudo-podia anchor the foraminifer wi thin the cyst andremain active throughout the process. Cyto-plasm begins to flow from the test, and star t ingnear the aperture, forms the shape of the newchamber which is being simultaneously secretedand calcified. Calcification occurs beneath acytoplasmic sheath (probably comparable to theouter organic lining in C. polymorpha), begin-ning near the aperture of the last chamber andprogressing from the base to the new apertureof the forming chamber. The interior of thechamber is formed and calcified by pseudo-podia. The aperture and apertural tooth are thelast to form. The resulting new chamber wall inmiliolids consists of calcite needles randomlyoriented in an organic matrix (Fig. 3.13), bothof which are preformed within the cytoplasmand transported in vesicles to the developing

wall where they are released. Older chambersare thicker than younger ones, but are ‘nonlam-ellar.’ Angell (1980) suggests that additionalcalcite is added to older portions of the testduring chamber formation.

Chamber formation in the miliolid Spirolocul-ina hyalina differs from that in the rotaliid Rosal-ina floridana and globigerinids in two importantregards. First, S. hyalina does not form an anlageof membranes or organic linings as does R.floridana and the planktonic Foraminifera, andcalcification does not occur on the template ofan organic lining. Rather, calcite needles andtheir associated organic matr ix are preformedwithin the cytoplasm and transported to theforming chamber where they are released intothe wall. Second, calcification occurs as cyto-plasm is being extruded from the last completechamber, proceeding from the base of the newchamber to the aperture and tooth. That is,extruded cytoplasm does not first form the shapeof the new chamber and then the wall.

The agglutinated foraminifer Textularia can-deina utilizes both organic and calcitic cementsin the construction of its test (Bender, 1992).Chamber formation begins with the foraminifer


gathering sediment grains into a mound nearthe aperture. Once a cavity is formed wi th in thismound of sediment, the foraminifer begins con-structing a chamber by first coating grains witha thin organic envelope, and then cementingthem together with a small amount of organiccement, beginning on the surface of thepenultimate chamber and working outwardtoward the aperture. Calcite is then added pri-marily to the external surface of the chamber inthe form of calcite bundles that fill in the openspaces in the test and further cement the aggluti-nated materials together. Pores, characteristic ofthe test of T. candeiana, appear during calcifica-tion, with their position depending on the orien-tation of the agglutinated grains and theposition of the calcite bundles (Bender, 1992).

It should also be noted that many Foramini-fera are capable of repairing their shells. Angell(1967c) showed that Rosalina floridana, decalci-fied with HCl, recalcified their shells, though thelaminated wall structure was not restored. Theplanktonic foraminifer Globigerinoides sacculifercan reconstruct its shell after major in jury ,though extensive shell repair often results in veryaberrant morphologies (Bé and Spero, 1981).The large nummuli t id Cycloclypeus carpenterican also repair a damaged shell (Song et al.,1994) within about four months (Krüger et al.,1996). Shell repair has also been reported inHeterostegina depressa (Röttger, 1978; Röttgerand Hallock, 1982), the miliolid Triloculina bar-nardi (Collen, 1998), and a number of fusulinids(e.g. Kahler, 1942; Wilde, 1965). The ability torepair damaged shells appears to have evolvedin the Paleozoic and is widespread among Fora-minifera. It imparts obvious advantages toindividuals subjected to attacks by predators orto mechanical damage.

and asexual generations (Fig. 3.14). Though‘species pairs’ (now recognized as dimorphictests) had been identified as early as themid-1800s (Lister , 1895), the fundamenta l out-line of the life cycle was first presented by Lister( 1 8 9 5 ) , wi th additional comments supplied bySchaudinn (1895) . The foraminifer Polystomella( = Elphidium) crispum, a fairly large, regionallyabundant , shallow-water dweller, was the sub-ject of both studies.

The life cycle of Elphidium crispum includes anumber of features that are shared by numerousother taxa, and it is perhaps for tui tous tha tLister and Schaudinn selected this foraminiferas the subject of their observations. Had theystudied any of a number of other species (e.g.Allogromia laticollaris. Spirillum vivipara, Patel-lina corrugata, or any of the ‘microforaminifera’studied by Grell; see Grell, 1979), these earlyaccounts of the life cycle might have taken avery different form.

Elphidium crispum is a dimorphic foraminifer(Lis ter , 1895, 1903; Schaudinn, 1895; Jepps,1942). The adul t gamont, which producesgametes, has a single nucleus and a megalosph-eric test characterized by a relat ively large pro-loculus but a relat ively small overall diameter.The adult agamont, which produces numerousyoung by mul t ip le fission, is multinucleate andhas a microspheric test characterized by a t inyproloculus but a relatively large overall testdiameter. The terms megalospheric and micro-spheric, therefore, refer to the size of the prolocu-lus, not the size of the entire test.

E. crispum produces biflagellated gametes andis gametogamous (gametes liberated directlyinto the surrounding seawater; see below), whichis the case for most species of Foraminifera (seeGoldstein, 1997). Fertilization then takes placeby the fusion of two gametes, generally fromdifferent parents. Flagellated foraminiferalgametes typically are quite small (~1–4 µm),and the resulting zygote is also small. In gameto-gamous species, the zygote may spend a briefphase as a naked (shell-less) amoeba dur ingwhich it feeds and grows before it calcifies, form-ing the microspheric proloculus.

In higher animals, meiosis typically occurs as

3.5 REPRODUCTION AND THEFORAMINIFERAL LIFE CYCLE

3.5.1

The typical foraminiferal life cycle is charac-terized by a heterophasic alternation of sexual

Reproduction and the foraminiferal life cycle 49

an integral part of gametogenesis. Meiosis is areduction division in t ha t i t halves the diploidnumber of chromosomes and produces haploiddaughter cells. In the Foraminifera. howeve r ,meiosis occupies an intermediate position in thelife cycle, occurring in the agamont as an in tegralpart of mult iple fission. The resul t ing young arehaploid individuals that typically grow tobecome adul t , uninucleate gamonts. Gameto-genesis then occurs in haploid i n d i v i d u a l s andinvolves only mi to t ic nuclear divisions.

Perhaps l imited by technology or the smallsize of nuclei in E. crispum, none of these pio-neers in foramini fera l biology ( J . J . Lister,F. Schaudinn, M.W. Jepps) were able to docu-ment the correct position of meiosis. This ele-ment of the life cycle was f i rs t documented byLe Calvez (1946, 1950) who reexamined the life

cycles of Patellina corrugata and Discorbis vilar-deboanus and recognized meiotic division figurestha t preceded m u l t i p l e fission in the agamont.Grell (1954) and Arnold (1955) soon verified LeCalvez’s f indings by document ing the in termedi-ate position of meiosis in Rotaliella heterocary-otica and Allogromia laticollaris, respect ive ly .

3.5.2 Variations on the general theme

Today, reasonably complete life cycles areknown for fewer than 30 of the > 10,000 extantspecies of Foraminifera . In spite of t h i s l i m i t a -tion, these r e l a t i v e l y few well -documented l i fecycles illustrate a significant range of variationin the l ife cycle and in the corresponding mor-phological v a r i a t i o n impar ted to the test(Table 3.1). These variations relate to the



sequence of ‘alternating’ generations, trimor-phism, apogamic and possibly gamic life cycles,binary fission and various forms of budding,type of gametes, mode of fertilization, occur-rence of nuclear dimorphism, and test dimor-phism. Overall, the life cycle is more varied inthe Foraminifera than in vir tual ly any othergroup of protists.

The alternation of generations in the Fora-minifera may be obligatory in some species, andfacultative in others. In the obligatory alterna-tion of generations, reproduction in the agamontalways includes meiosis as a precedent tomultiple fission. The resulting young are alwayshaploid and uninucleate, and they grow to formmature gamonts. With the possible exception ofIridia lucida in which both gamonts and aga-monts are uninucleate ( Le Calvez, 1936a, 1938),the uninucleate forms are gamonts that producegametes which ultimately form zygotes andmature into agamonts. This type of life cycledoes not deviate from this regular alternationof generations. Examples include Elphidium cris-pum (Lister, 1895, 1903; Jepps, 1942), Glabratellasulcata (Grell, 1958b), Rotaliella heterocaryotica(Grell, 1954), and Patellina corrugata (Myers,1935; Grell, 1958c).

Alternatively, the life cycle may be charac-terized by a facultative alternation of genera-tions. In some species, the life cycle includessuccessive asexual cycles that include repro-duction by multiple fission (e.g. Ammonia tepida– Bradshaw, 1957; Schnitker, 1974a; Goldstein

and Moodley, 1993). In this case, the agamont( B ) begins as a zygote, and is diploid. The aga-mont may undergo meiosis and mult iple fissionto produce haploid young that mature into uni-nucleate gamonts (A 2 ) . Alternatively, the aga-mont ( B ) may produce, by multiple fission, asecond asexual generation, the schizont ( A 1 ) ,which in tu rn may produce a number of succes-sive asexual generations. The type of nucleardivisions that occurs in schizonts, however, hasnot been documented.

This facultative alternation of generations isreferred to as biological trimorphism, and hasbeen documented in the living nummul i t id Het-erostegina depressa by Röttger et al. (1990) andin the amphisteginid Amphistegina gibbosa byHarney et al. (1998) and Dettmering et al.(1998). This type of life cycle includes one micro-spheric generation ( B ) and two megalosphericgenerations, the gamont ( A 2 ) and the schizont( A 1 ) . A number of foraminiferologists have

Foraminifera: A biological overview52

reported biological trimorphism, particularly inregard to the larger, algal symbiont-bearingForaminifera (see Röttger et al., 1986, 1990;Harney et al., 1998; Dettmering et al., 1998).

Does biological trimorphism extend to tri-morphism of the test? The validity of thishypothesis requires two observations: (a) thepresence of three morphologically distinct typesof tests based on the diameter of the proloculus,and (b) the correlation of each of these distinctmorphologies to a specific phase of the life cycle(gamont, agamont, schizont) (Röttger et al.,1986, 1990). Most studies on test trimorphism,however, have relied almost exclusively on mor-phological observations.

Rather than adding alternative cycles to thelife cycle as in biological trimorphism, some taxaare apogamic and appear to have reduced thecomplexity of the life cycle by omitting one ofthe generations. At least two species, Fissurinamarginata and Spiroloculina hyalina, have appa-rently lost the sexual phase of the life cycle ( thegamont and gametogenesis) (Le Calvez, 1947;Arnold, 1964). Only successive asexual genera-tions were observed in these species, and in S.hyalina, asexual reproduction occurs in un inu-cleate individuals (Arnold, 1964).

Only sexual reproduction has been observedin planktonic Foraminifera, in spite of numerousinvestigations. As a result, Hemleben et al.(1989) proposed a possible ‘gamic’ life cycle forplanktonic Foraminifera in which the agamontand multiple fission have been lost. Gamonts,which are uninucleate, undergo gametogenesis,producing thousands of free-swimming, biflag-ellated gametes that are released directly intothe surrounding seawater. Zygotes presumablyform as gametes from separate parents fuse. Itis possible then that zygotes mature to adultgamonts and that meiosis occurs in the zygote,immature gamont, or adult gamont, though thishas yet to be demonstrated.

The life cycle of some allogromiids andastrorhizids appears to be more plastic or vari-able than in other Foraminifera. In addition tomultiple fission, several other forms of asexualreproduction have been observed, including:binary fission in Allogromia laticollaris (McEn-

ery and Lee, 1976); budding in Saccamminasphaerica (Rhumbler, 1894), S. alba (Goldstein,1988a), Allogromia laticollaris (Arnold, 1954,1955), Halyphysema tumanowiczii (Hedley,1958), Technitella legumen (Haman, 1971) ,Astrammina ram (DeLaca, 1986a), Ovamminaopaca (Goldstein, unpublished observations),and Psammophaga simplora (Goldstein, unpub-lished observations); serial budding in Nemogull-mia longevariabilis (Nyholm, 1956) andCylindrogullmia alba (Nyholm, 1974); and plas-motomy or multiple budding in Allogromia lati-collaris (Arnold, 1955) and Saccammina alba(Goldstein, 1988a). In addition, fragmentationoccurs in the miliolid Calcituba polymorpha(Arnold, 1967), and Spiroloculina hyalina andFloresina amphiphaga are capable of producingmult iple broods (Arnold, 1964; Hallock andTalge, 1994).

Gametes in the Foraminifera may be biflagel-lated, triflagellated, or amoeboid. Of these,biflagellated gametes (Fig. 3.15) are by far themost common, and occur in many extan tgroups, including planktonic taxa and the mostdiverse benthic suborders. The sequence ofevents by which biflagellated gametes are pro-duced is remarkably similar, even in dis tant lyrelated taxa, suggesting that this mode ofgametogenesis is probably primit ive within theForaminifera (Goldstein, 1997). The other typesof gametes and the processes that produce them,therefore, are most l ikely derived from the moreprimitive biflagellated type (Grell, 1967;Goldstein, 1997).

Triflagellated and amoeboid gametes haveevolved on more than one occasion and inde-pendently in different groups of Foraminifera.Triflagellated gametes are best known in a fewplastogamic (forms in which the gamonts fusebefore gamete release, see below) discorbids andglabratellids (e.g. Discorbis patelliformis. D. med-iterranensis, Glabratella sulcata – Myers, 1940;Le Calvez, 1950; Grell, 1958b). However, theyalso occur in at least one (Nummulites venosus– Röttger et al., 1998), but not all of the fewextant nummuli t ids . It is noteworthy that N.venosus is gametogamous (see below) and notplastogamic. Amoeboid gametes occur in the


allogromiid Allogromia laticollaris (Arnold,1955), but are also known in several of the smallrotaliellids (e.g. Rotaliella heterocaryotica, R.roscoffensis, Metarotaliella simplex, M. parva,Rubratella intermedia – Grell, 1973, 1979) andin the spirillinids Patellina corrugata (Myers,1935) and Spirillina vivipara (Myers, 1936).Amoeboid gametes may also occur in the sac-camminid Psammophaga simplora. However,although Arnold (1984) reported the formationof amoeboid structures during gametogenesis,he also reported that they may become flagel-lated before their release from the shell. Trifla-gellated and amoeboid gametes generally arelarger than biflagellated ones and are producedin fewer numbers.

Fertilization in the Foraminifera may begametogamous, gamontogamous, or autoga-mous (Grell, 1973). Gametogamy is the mostcommon mode found in the Foraminifera andinvolves the release of numerous gametesdirectly into the surrounding seawater where

fertilization occurs. Gametogamy is generallyassociated with the production of numerous(often thousands), small ( ~ 1–4 µm), biflagel-lated gametes. However, although rare, gameto-gamy may also occur in Foraminifera withtriflagellated gametes, as in the nummul i t idNummulites venosus (Röttger et al., 1998).

Alternatively, rather than simply broadcast-ing gametes, gamonts can associate in pairs orgroups (e.g. Spirillina vivipara, Patellina corru-gata. Metarotaliella parva, M. simplex) prior tothe release of gametes. This mode of fertilizationis referred to as gamontogamy, and mostgamontogamous Foraminifera produce eithertriflagellated or amoeboid gametes. Plastogamyis a specific type of gamontogamy in which twogamonts attach to each other along the umbili-cal margins of the tests. Gametes are thenreleased wi th in the shared space of the joinedtests (internal septa are generally removedduring gametogenesis). Examples of plastogamicForaminifera include: Discorbis patelliformis, D.


pulvinata, D. ornatissima (Myers, 1940), D. medit-erranensis (Le Calvez, 1950), and Glabratellasulcata (Grell, 1958b).

The gamonts of some gamontogamousspecies are differentiated into ‘sexes’ or mat ingtypes. No morphological features distinguishconspecific gametes or gamonts. However,gamonts of Discorbis mediterranensis from onemating type wi l l pair only with those fromanother (Le Calvez, 1950). In species that associ-ate in groups (e.g. Patellina corrugata), bothmating types must be present for reproductionto occur (Grell, 1958c). It is not known whetheror not mating types occur in gametogamousspecies as well.

Autogamy (self fertilization) is known in sometaxa. Amoeboid gametes are produced, but arenot released from the parental test. Rather, fert i l -ization occurs w i th in the parental test fromwhich the resulting young then escape. Autog-amy occurs in Allogromia laticollaris (Arnold,1955), Rotaliella heterocaryotica (Grell, 1954),and R. roscoffensis (Grell, 1957). In culture, thismode of fertilization can be very difficult todist inguish from multiple fission (asexual repro-duction), al though the size of offspring may pro-vide a clue for some species. Arnold (1955)reported that sexually produced young are gen-erally smaller than those produced by mul t ip lefission in Allogromia laticollaris.

Nuclear dimorphism is perhaps best known inciliated protozoans, but also occurs in somesmall calcareous perforate Foraminifera, partic-ularly Glabratella sulcata and members of theFamily Rotaliell idae (see Grell, 1973, 1979). InForaminifera with nuclear dimorphism, differenttypes of nuclei occur simultaneously in the aga-mont. Generally, there is one somatic nucleusand one to live generative nuclei. The generativenuclei remain in the proloculus u n t i l the aga-mont reproduces, at which time all undergomeiosis. The somatic nucleus resides in an inter-mediate chamber, is generally larger, and con-tains more DNA than the generative nuclei; itis involved in the cell’s metabolic functions. Thesomatic nucleus, however, degenerates at theonset of meiosis in the generative nuclei (Grel l ,1973). Zech (1964) showed that nuclear dimor-

phism does not occur in the foraminifer Patellinacorrugata. Whether t h i s phenomenon occurselsewhere in the Foraminifera, however, remainsto be demonstrated.

The classical form of test dimorphism inwhich the gamont (and schizont if it occurs) isrelat ively small and megalospheric, and the aga-mont is relat ively large and microspheric, hasbeen identified in numerous modern and fossiltaxa. However, not all Foraminifera that showan al ternat ion of generations also display classi-cal test dimorphism. Patellina corrugata andSpirillina vivipara, for example, have reversedtest d imorphism (Myers , 1935, 1936). The aga-monts are smaller and ‘megalospheric,’ whereasthe gamonts are larger and ‘microspheric.’ Thisforamin i fe r produces fa i r ly large amoeboidgametes, and the resul t ing zygotes are generallylarger than the young produced by m u l t i p l efission.

Test d imorphism in Glabratella sulcata alsodeviates from the norm. In this species, thegamont typ ica l ly is larger than the agamont,and no significant differences in size i d e n t i f y theproloculus as either megalo- or microspheric. Inmany of the t iny Foraminifera studied by Grell(see Grell, 1973, 1979), the gamonts and aga-monts are morphologically indist inguishable.

Some Foraminifera are characterized by awide range of morphological va r i ab i l i ty whichmay extend to the size of the proloculus.Gamonts of Ammonia tepida, for example, havea wide range of prolocular diameters (Goldsteinand Moodley, 1993), mak ing it d i f f icul t to d is t in-guish gamonts from agamonts by the morphol-ogy of empty shells.

What causes test dimorphism? Early workerson the foraminiferal life cycle explained testdimorphism as the result of the small size of theproloculus formed by amoeba-form zygotes t ha thad resulted from the fus ion of two very smallbiflagellated gametes, and observations onElphidium crispum seemed to support this view(Myers, 1935). Myers ( 1935), however, proposedtha t the control l ing factor more l ike ly was thesize of the nucleus, and not the size of the zygote.This, he believed, better explained why in somespecies, the shape and form of the proloculus

Acknowledgments 55

were similar in tests of both generations ( thoughnot in Patellina corrugata, the subject of his 1935paper). Similarly, Le Calvez (1938) proposedthat the number of nuclei in the young agamontdetermined the size of the proloculus. This mayalso provide a reasonable explanation for thesize of proloculi in the small heterocaryotic fora-minifer Rotaliella elatiana (Lee et al., 1991a).

Test dimorphism was defined wi th regard tomultilocular taxa, and application of this termshould therefore be restricted to these forms.However, morphological differences may alsooccur in unilocular taxa for which Grell (1988)coined the term heterothalamy. In some casesthe distinction occurs only with regard to size.Gamonts of Heterotheca lobata (Grell, 1988)and Saccammina alba (Goldstein, 1988a) aresignificantly larger than the correspondingagamonts. In S. sphaerica (Føyn, 1954) andMyxotheca arenilega (Grell, 1958c), however, theagamonts are larger. Because all four of thesespecies liberate numerous, small, biflagellated,free-swimming gametes, the size of gametes doesnot explain this form of heterothalamy.

Ovammina opaca and Cribrothalammina albaexhibit another variation. The gamonts of both

species form secondary pores dur ing gametogen-esis that serve as the sole avenue for the releaseof numerous biflagellated gametes (Fig. 3.16). InO. opaca, pores form in a ring just behind theaperture (Dahlgren, 1962, 1964), whereas in thelarger C. alba, pores are distributed over theentire test, with the exception of the abaperturaltip (Goldstein and Barker, 1988, 1990).

3.6 ACKNOWLEDGMENTS

I thank Pamela Hallock, Rudolf Röttger, andSamuel Bowser for their formal and informalcomments on this paper. Samuel Bowser pro-vided the TEM micrograph of a pseudopodiumfrom Spiroloculina hyalina (Fig. 3.3), and TomasCedhagen provided the micrographs of Pelosinaarborescens (Figs. 3.5 and 3.6). Beth Richardsoncollaborated on the TEM micrograph, preparedby high pressure freezing and freeze substitution,of Myxotheca sp. (Fig. 3.9). I also thank Eliza-beth Gardiner and Daniel Hunter , graduate stu-dents at the University of Georgia, for providingthe results of their 1998 micropaleontology classproject on shell morphogenesis in Ammoniatepida (Fig. 3.10).


4Shell construction in

modern calcareousForaminifera

Hans Jørgen Hansen

4.1 INTRODUCTION

The majority of foraminiferal species build theirshells (or ‘tests’) wi th Such calcareousspecies constitute 11 out the 15 extant orders ofthe class Foraminifera (see chapter 2). The pre-sent chapter is focused on the modes in whichvarious types of walls are built by modern cal-careous taxa.

4.2 WALL OF SECRETED CALCITESPICULES (CARTERINIDA)

The order Carterinida is represented by a singlegenus, Carterina, which constructs its shell withconcentrically laminated, ovoid spicules (Figs. 2.9,4.1) that are held in place by organic material(Hansen and Grønlund, 1977). To test the possi-bility that the shell may be agglutinated, Deutschand Lipps (1976) searched for loose spicules inthe sediments of Eniwetok atoll, from where theyhad collected specimens of C. spiculotesta, but didnot find any. In addition, adult specimens werefound attached to hard substrate where sedi-

mentary particles do not accumulate. Such evi-dence led to the suggestion that the spicules inthe test of Carterina were secreted. The spiculesare made of calcite (with c-axis parallel to elonga-

Barun K. Sen Gupta (ed.), Modern, Foraminifera, 57–70© 1999 Kluwer Academic Publishers. Printed in Great Britain.

Shell construction in modern calcareous Foraminifera

tion) which contains blebs of organic matter. Theycome in two size groups, with the smaller spiculespacked tightly between the larger ones (Fig. 2.9),and reported as a ‘ground mass’ by earlier observ-ers (e.g. Brady, 1884; Loeblich and Tappan,1964a). The rounded shapes of the spicules andthe lack of connections between adacent spiculesshow that they are not formed in situ in the shell(Hansen and Grønlund, 1977).

4.3 PORCELANEOUS, IMPERFORATEWALLS (MILIOLIDA)

The non-lamellar porcelaneous wall is con-structed of rods/laths of high magnesium calcite(Blackmon and Todd, 1959). The calcite units ofthe wall are arranged in a disorderly manner inthe embedding organic material. On the basis ofultrastructural studies, Berthold (1976a) reportedthat in Calcituba polymorpha, calcite rods are pre-sent in cytoplasmatic vesicles formed duringchamber construction. Similar observations weremade by Angell (1980) in a study of chamberformation in Spiroloculina hyalina. Some porcela-neous forms possess a smoothly finished outer-most layer of well crystallized calcite, withrhombohedral crystal faces arranged parallel tothe surface (‘tile roof pattern’). It is diff icult toimagine how these crystallites could have formedaway from their position, since many show aninterlocking pattern (see also Debenay et al.,1996). Haake ( 1 9 7 1 ) recorded a ‘cobble pattern’on the surface of porcelaneous forms in whichcalcite crystals are more or less perpendicular tothe shell surface in the outermost layer. It may beconcluded that the porcelaneous wall in this caseis mainly constructed of calcitic units that aresecreted by the foraminifer away from their f ina llocations in the shell; the smoothly finished sur-face layer, however, is most likely formed in situ.

4.4 MONOCRYSTALLINE WALLS(SPIRILLINIDA)

The optically monocrystalline wall of Patellinahas an a-axis-preferred orientation (Towe et al.,

1977). As observed by Berthold (1976c), newchamber material is added by lateral apposition.Growth is initiated in the apertural region ofthe preceding chamber where nearby st ructuressuch as radial septa grow faster than dis tantstructures. Berthold (1976b) also found tha tduring growth of the septa in the spiral (dorsal)wall, small spaces are formed, and they are notclosed in the course of shell development, thusbecoming rounded pores. The reason for thesuppression of calcification in the pore regionsmay be linked to the filling of pores by granularorganic material . The pores and both sides ofthe shell wall are covered by a delicate organiclayer. At the inner entrance to a pore, this cover-ing organic layer is f ine ly perforated by open-ings of about diameter. In contrast,the exterior pore opening apparently remainsuncovered.

4.5 LAMELLAR WALLS

4.5.1

The lamellar shells are constructed of eithercalcite or aragonite. As a new chamber is added,one new layer of shell material is secreted, cover-ing the exposed earlier part of the shell (wh ichdoes not happen in non-lamellar walls). Thisleads to an increase in wall thickness from laterto earlier chambers (Fig. 4.2). In non-lamellarForaminifera the addition of a new chamberdoes not lead to the deposition of a layer ofshell material onto the earlier exposed part ofthe shell.

4.5.2 Optical orientation of the wall material

Following the pioneering work of Wood ( 1949)on the optical orientation of the carbonate mate-rial of foraminiferal shells, Loeblich and Tappan(1964a) introduced the radial-granular distinc-tion in foraminiferal c lassif icat ion (see chapter 2and Figs. 2.5, 2.6). This was a very a t t rac t ivefeature of this classification, because major taxo-nomic groups could be distinguished by a simpleoptical character. The crystallographic orienta-

58

Lamellar walls 59

tion of optically radial and granular walls hasbeen studied by several authors (e.g. Towe andCifelli, 1967; Hansen, 1968), and the terms ‘radi-ate’ and ‘granulate’ have also been used for thetwo optical properties. Their determination,however, is not necessarily easy under a polariz-ing microscope. For example, the presence ofvery narrow pores may give the impression of aradial optical structure in thin sections.

Both radial and granular optical propertieshave been observed within the same genus.Hansen (1972a) demonstrated a granular wallstructure in an Eocene species of Turrilina, anda radial structure in an Oligocene species.Within the 26 species of elphidiids studied byHansen and Lykke-Andersen (1976), 19 wereradial and 7 were granular, thereby corroborat-ing an earlier report of a granular elphidiid(Buzas, 1966). Thus, the optical orientation ofshell material is not an infallible character fortaxonomic distinctions above the species level.Ultrastructures of both radial and granularwalls show considerable variability; severalstructural types have been identified (Bellemo,1974a, b; 1976).

4.5.3 Monolamellar, hyaline, perforate walls(Lagenida)

In this group of hyaline Foraminifera, the latestadded chamber is constructed of a single layerof shell material (Grønlund and Hansen, 1976).

When this new chamber is added, the layer thatforms that chamber also covers the exposedexterior walls of earlier chambers. Thus, the ulti-mate chamber wall consists of one layer, thepenultimate chamber of two layers, and so on(Fig. 4.2). Partial deviations from this modeof wall construction exist within the group.Secondary lamellae may cover only the two pre-vious chambers or only part of the penultimatechamber, or as in Lingulina, the final chambermay be composed of one to six lamellae, all ofwhich extend over the exposed earlier part ofthe shell (Fig. 4.2). Where one curved chambermeets another, the columnar morphology ofcalcite in the wall leads to a somewhat irregularstructural arrangement. The pores in mono-lamellar walls (and those in aragonitic bilamel-lar walls) are all of small diameter. Present datashow that monolamellar walls in modern speciesare constructed with only optically radial calcite.

4.5.4 Bilamellar, hyaline, perforate walls(Buliminida, Rotaliida, Globigerinida)

In the bilamellar group, the wall of the finalchamber consists of two carbonate layers sepa-rated by an organic ‘median layer.’ Tradition-ally, the outside calcareous layer is termed the‘outer lamella,’ while the inside calcareous layeris termed the ‘inner lining’ (Fig. 4.3); the latteris not to be confused with the inner organiclining of the calcareous wall. In some taxa, the

60 Shell construction in modern calcareous Foraminifera

median layer is thin and well defined; in others,it may not be sharply delineated between thetwo carbonate lamellae. In Cibicides and Stoma-torbina, the median layer contains particles (f inesedimentary grains, e.g. quartz) that are notsecreted by the foraminifer. In Stomatorbina,these particles are absent in porous regions ofthe shell, but are clearly seen through the shellin non-porous areas. In Cibicides, they appearto be distributed randomly in the median layer.It is unclear if these particles in the median layershould be regarded as being truly agglutinatedor as contaminations, but their distribution inStomatorbina points to some degree of organiza-tion. The median layer apparently plays a sig-nificant role in the chamber forming process andcalcification. In thin section under the lightmicroscope, it may be seen as a dark line or adark diffuse band that is usually most conspicu-ous in the septal part closest to the aperture andforamina. Sometimes the median layer and theboundaries between secondary lamellae aredifficult to observe, but a parallel alignment ofthe two polarizers in the microscope improvesthe visibility of the lamellar boundaries, theirplanar orientation being at right angles to theplane of polarization. The thickness of eachlamella may be only a few microns, or even lessthan a micron. In such cases, observations witha light microscope may not be adequate, and

scanning electron microscope (SEM) studies ofembedded, sectioned, polished, and etched speci-mens may be necessary.

The basic bilamellar mode of wall construc-tion was first explained by Reiss (1957) as amodification of the mode suggested by Smout(1954). The inner lining stops at the junctionwith the previous chamber, while the outerlamella continues over the exposed parts of theearlier chambers to form a secondary lamella.The septum of the previous chamber becomesisolated from the surface, and does not receivethe secondary laminaton, thus becoming theshell interior (Fig. 4.3). The result is a shellwhere all septa (including the ultimate one) havetwo calcareous layers. In a variant of this con-structional design, the inner l ining does not stopat the junction with the previous apertural facebut continues as a calcareous layer depositedonto the penultimate septum (former aperturalface), leading to a three-layered septum(Fig. 4.4). In this model, the ultimate septum istwo-layered while the penultimate and earliersepta are three-layered. The calcareous layercovering the penultimate septum is termed a‘septal flap.’ Septal flaps have not been found inmonolamellar forms and appear to be confinedto the bilamellar group.

Lamellar walls 61

4.5.5 Interlocular spaces and subsutural canals

The presence of a septal flap is often, but notalways, connected with interlocular spaces, i.e.spaces between adjacent chambers. Melonispompilioides has a septal flap, but no interlocularspace (Fig. 4.5). It does, however, possess anumbilical spiral canal system (Fig. 4.6). Nonionlabradoricum has septal flaps, but no interlocularspaces or umbilical canal system (Hansen andLykke-Andersen, 1976). When an interlocularspace is present, the attachment of one chamberto another is very fragile, and the weak shellarchitecture leads to breakage of the last cham-ber(s). In Pseudorotalia, interlocular spaces arepresent, but secondary lamellae build protru-sions in both anterior and posterior directionsfrom the sutures; after the addition of two orthree chambers, pillars bridge the interlocularspaces, and thereby prevent breakage (Fig 4.7).The interlocular walls receive secondary lamina-

tion, showing that these walls are functionalshell surfaces.

An alternative constructional design is seenin the presence of posterior extensions (retralprocesses) of the chamber lumen and surround-ing walls (ponticuli); these are attached to theexterior-most part of the preceding aperturalface when a new chamber is added (e.g. in Elphi-dium, Fig. 4.8). This leads to the formation of awell-anchored final chamber with little chanceof mechanical damage, in spite of the presenceof a deep interlocular space. Thus, both Pseudo-rotalia and Elphidium have deep interlocularspaces crossed by small bridges, but ofdifferent origin.

In Asterigerina, the addition of a new chamberproduces a chamber lumen that is primarilydivided into two sub-chambers. The peripheralpart is termed the ‘main chamber,’ while thepart with a rhombohedral outline found closest


to the umbilicus is the ‘chamberlet.’ These twounits are separated from each other by a two-lay-ered partition which bridges the previous aperturewith an arch. Their development represents an‘instar,’ i.e. a single episode in the formation of

the shell (see next section). When the two-layeredpartition is followed to the outer chamber wall, itis seen to be constructed by a doubled inner lining(Fig 4.9). In this case, the construction of the innerlining does not involve a simultaneous construc-

Lamellar walls 63

tion of an outer lamella (Hansen and Reiss, 1972).Exactly the same plan of lamellar constructionis found in Elphidiella, where the space betweenthe ultimate and the penultimate chamber isdelimited by the double inner lining of the ulti-mate chamber against the penultimate septum.(Fig. 4.10). Several openings in the roof (Fig. 4.11)connect the chamber interior with shell surface,thereby becoming true multiple apertures of theultimate chamber (Hansen and Lykke-Andersen,1976). Such openings in the sutures are sometimesmisleadingly called ‘sutural pores.’

4.5.6 Umbilical cover plates and foraminalplates

The concept of instars in shell formation wasintroduced by Smout (1954) who regarded the

formation of a chamber and the associateddeposition of a secondary lamella as one instar.This concept is useful in explaining the develop-ment of several shell structures. A chamber-forming instar in Ammonia also involves thedeposition of structural elements in thepenultimate chamber (Hansen and Reiss, 1971).The umbilical part of the final chamber inAmmonia is open to the umbilicus. However, themain umbilical opening in the penultimatechamber is closed by the deposition of a coverplate that is continuous with a folded, almostvertical, foraminal plate protruding in the proxi-mal direction. In section, the folded plate is seenas a two-layered hook extending from the umbil-ical cover plate of the preceding chamber. Theseumbilical cover plates and the exposed parts ofthe hooks are secondarily laminated. The foldedplate represents the site of attachment of thesucceeding cover plate. These structures showup in a shell section as a continuous series ofhooks and plates (Figs. 4.12. 4.13). This con-structional pattern is characteristic of manytrochospirally and planispirally coiled forms.Even in apparently simple forms such asAstrononion in which hooks (foraminal plates)are absent, the deposition of a cover plate in thepenultimate chamber is easy to recognize in shellmolds (Fig. 4.14).

The deposition of umbilical cover plates inthe earlier chambers leads to the formation ofthe so-called umbilical spiral canal systems(shown by Carpenter et al., 1862, in a naturalmold of Elphidium craticulatum) . The origin ofthis conspicuous canal system is in parts of theshell that are closest to the umbilicus. In Elphi-dium, the single umbilical chamber tip embracesthe previous chamber tip and covers its proxi-mal umbilical part, allowing the presence of apassage (aperture) into the final chamber. Alongwith this, a plate is deposited in such a way thatit seals off the communication between the mainpart of the preceding chamber lumen and thepart closest to the umbilicus (Figs. 4.15, 4.16).The plate, deposited through one of the multipleinteriomarginal apertures ( the one closest to theumbilicus) of the preceding chamber, is a two-layered structure consisting of an outer lamella


and an inner lining. The inner lining faces thechamber lumen and is covered by the outerlamella in the umbilical direction. In betweenchambers, the umbilical part of the interlocular

space retains an opening into the small space(closest to the umbilicus) now isolated by theumbilical cover plate. With the addition of newchambers, openings between adjacent chambertips gradually form a spiral canal system in theumbilical region. When the umbilical chambertip is not attached to the umbilicus (e.g. inAmmonia), the umbilical spiral canal remainsopen, demonstrating that the spiral canal is afunctional surface, since it receives secondarylamination.

The cytoplasm leaves the chamber lumen inElphidium through the interiomarginal multipleapertures or, posteriorly, through the openingconstituted by a former aperture (closest to theumbilicus) of the penultimate chamber. Thus, itmoves inside the umbilical spiral canal system,which is a functional surface, and then into inter-locular spaces through openings in the spiral

Lamellar walls 65

canal. This allows the cytoplasm to emergeeverywhere on the foraminiferal shell, betweenthe ponticuli that bridge the interlocular spaces,as well as into interlocular spaces of previouswhorls.

The nummulitids, in addition to possessingan umbilical spiral canal system, have developeda so-called marginal cord. This is a system ofelongate ‘islands’ or ridges in the peripheral partof the final chamber, which, with the additionof secondary lamination, is gradually convertedinto a multi-pipe marginal channel. This channelcommunicates with all interlocular spaces,which are formed between the primary ridges ofthe septa and the septal flaps.

‘Toothplates’ are a special feature of somecalcareous bilamellar Foraminifera. True tooth-plates are found within the Buliminida, andseem confined to that group. A buliminid tooth-

plate is constructed of a single inner l ining(Revets, 1993). Following the construction prin-ciples outlined above, the toothplate, if it werea functional surface, would have receivedsecondary lamination. That has never beenobserved.

All planktonic Foraminifera are known orassumed to construct bilamellar shells. Althougha monolamellar structure was reported in Has-tigerina pelagica (Hemleben et al., 1989), thescanning electron micrograph of a wall sectionshows it to be bilamellar (Fig. 4.17). This wallis only about thick, rendering observationof the lamellarity difficult.

4.5.7 Aragonitic walls (Robertinida)

The study of several taxa belonging to the arago-nitic order Robertinida shows that the shell con-


struction is bilamellar, although there is noobvious difference between the median layer andthe boundary between the secondary lamellae.For example, the ult imate chamber wall inHoeglundina is bilamellar, but in contrast tocalcitic bilamellar walls, the aperture is not con-verted into a foramen with the addition of anew chamber. The aperture in Hoeglundina ispositioned in the peripheral region of the f ina lchamber; as a new chamber is added, this peri-pheral aperture is closed in the penult imatechamber by the deposition of a two-layeredplate, while an opening is resorbed in thepenultimate septal face, thereby creating asecondary foramen. Along wi th the formationof the outer chamber wall, Hoeglundina depositsa folded two-layered plate as a prolongation ofthe wall on the spiral side. This structure is oftenreferred to as a toothplate, but it is not a t ruetoothplate, which is a single-layered feature so

far found only in the buliminids (see earlier).The two-layered plate ends in a folded extension,and is attached to the previous septum wherethe inner lining continues as a septal flap. Theplate extends in the anterior direction for abouthalf the length of the chamber. The entry of thecytoplasm into a chamber interior and earlierchambers of Hoeglundina takes place over thefree folded part and through a foramen on thespiral side of the plate, and then from one fora-men into the next (see i l lus t ra t ions in Hansen,1979). A Jurassic Epistomina has exactly thesame construction pattern. Ceratobuliminidshells have identical two-layered plates wi th afolded edge, and show the resorption of a fora-men in the penul t imate chamber. Cushmanellaand related genera are extremely delicate, andtheir inner structures are more complicated thanthose of Hoeglundina and Ceratobulimina, andsome species have several apertures associated

Lamellar walls 67

with partially closed inner pipes. The more com-plicated aragonitic shells appear to have evolvedin the Jurassic, but the study of fossil aragoniticforms is hampered by the frequent recrystalliza-tion of their wall material. The record of simpleraragonitic forms goes back to the Permian(Loeblich and Tappan, 1987), but early involu-tinids may be unrelated to the structurallyadvanced forms of the Jurassic and later times(Piller, 1983).

4.5.8 The carbonate units of bilamellar forms

The shells of bilamellar forms are oftendescribed as being constructed of platelets ofcalcite. The platelets thick) arearranged in stacks with identical orientation,but are apparently separated from each otherby very thin organic layers. These organic layersare much thinner than those separating adjacent

secondary lamellae, which, in turn, are thinnerthan the median layer.

There has been much speculation on the calci-fication process in bilamellar walls, but fewdirect observations have been made; such obser-vations are hampered by the limited resolutionof the light microscope. Angell (1979) made astudy of shell formation in Rosalina floridana,but he had to clean various parts of the shellwith chlorine; the effect of this procedure isuncertain, and some of the observed structuresmay be artifacts. Some speculative models ofcalcification are in poor agreement with theavailable ultrastructural evidence. In essence,explanations are needed for (a) the formation ofstacks of platelets with the same orientationacross spongy organic layers that separate adja-cent secondary lamellae, and (b) the presence ofpairs of euhedral calcite rhombohedrons thatsandwich the median layer.


The difference between secondary lamellarboundaries and the median layer was noted byHansen and Reiss (1971). In forms such asAmmonia and Pseudorotalia, the median layerwas found to be composed of an organic sponge-like mat, sandwiched between calcite rhombohe-drons whose obtuse angles protrude in the direc-tion of the shell surface and the shell interior.Thus, from pure morphology, the optical axis isoriented perpendicular to the shell surface ofthis base pair of calcite crystallites. The rhombo-hedrons appear almost perfect, indicating thatthey formed without interference. The stacks ofoverlying platelets continue the orientation ofthe base-pair crystal faces. On etched shell sec-tions, such stacks are separated by concen-trations of organic material, which wereregarded by Hansen (1970) as delimiters of ‘crys-tal units.’

Debenay et al. (1996) illustrated two impor-

tant features from the surface of a natura l lycorroded specimen of Helenina anderseni. Thefirst concerns the nature of crystal units. Theplatelets around a pore are steep, indicating thatplatelets in H. anderseni may be oriented accord-ing to a more acute crystallographic form than

with the pore oriented along the c-axis.The other observation is on the detail of theboundary between crystal units, which shows analmost whisker-like pattern, and points to unin-hibited growth, with neighboring crystal uni tsin identical crystallographical orientation.

Debenay et al. (1996) suggested a calcificationmodel for calcareous Foraminifera in which theprimary elements are globular crystallites. Theexistence of such globular units, however, hasnot been satisfactorily documented. The possi-bility exists that they are artifacts, because sim-ilar globules can be produced in the laboratoryby etching a foraminiferal wall, from which they

Lamellar walls 69

can be completely or partially removed byextraction peels. Angell (1979) illustrated globu-lar units of about 600 Å diameter on the surfaceof a Rosalina floridana, and there is a hint of alayered arrangement in these globules. However,Angell had removed organic material from theshell surface with sodium hypochlorite, andtherefore there is a possibilty that these globulestoo may be etching artifacts.

4.6 THE PORES

Details of pore structures have been studied injust a few calcareous species. The pores in themonocrystalline Patellina were described byBerthold (1976b), who found an organic tubuleand granular organic material fi l l ing the interiorof the tubule, and demonstrated the uptake of

the neutral red dye through the pores. The con-struction of the pores in the bilamellar Amphi-stegina was described by Leutenegger (1977b).These pores have an organic tubule that is sub-divided by organic plates; each plate corres-ponds to a boundary between secondarylamellae. The median layer also crosses the poretubule, and carries calcite crystallites that mayrepresent the crystal base pairs of the medianlayer, indicating a late time of formation of thepores. In contrast to the pores of Amphistegina,those in genera such as Heterostegina, Cyclo-clypeus, and Operculina are not lined withorganic tubules (Leutenegger, 1977b). Leuteneg-ger and Hansen (1979) demonstrated the uptakeof radioactive through the pores of symbi-ont-bearing Amphistegina, but neither

glucose nor the neutral red dye passedin appreciable amounts. This is not surprising,


because it has been known for a long time thatthe Rose Bengal dye used for s taining l i v i n gForaminifera generally produces coloration inonly the youngest two or three chambers, whi lethe remaining shell, in spite of the presence ofcytoplasm, does not take up any dye, showingthe impermeability of the pores for larger fluidmolecules. Hemleben et al. (1989) found thatthe pores in some p lanktonic species originatethrough resorption in the late state of chamberformation. The pore tubules in p lank ton ic Fora-minifera apparently cross the median layer, butthe boundary layers between secondary lamellaedo not correspond to any structures crossingthe pores.

So far, the presence of pore plates has beendemonstrated only in lamellar forms. It appearsthat the so-called sieve plates of the pores inAmphistegina are nothing but a cont inuat ion ofthe organic material tha t separates adjacentlamellae (Hansen, 1972b). The extremely com-plicated pore-plate pattern i l lus t ra ted by Jahn(1953) has not been found by other workers,and unfortunately, the species studied has neverbeen identified.

A concentration of mitochondria in cyto-plasmic material at the inner end of pores hasbeen observed by Leutenegger and Hansen(1979) in some shells collected from low-oxygen

environments . They interpreted th i s as an ind i -cation t h a t pores serve as conduits for the pas-sage of dissolved oxygen and carbon dioxide.This in te rp re ta t ion , however, is cont rovers ia l ,because of later observation t h a t mitochondriaare also concentrated in aper tura l cytoplasm(Bernhard and Alve , 1996) and tha t they movethrough pseudopodia (see chapter 12) . Thin,thread- l ike s t ructures emerging from pore platesin Amphistegina have been interpreted as extru-sions of pseudopodial material (Hansen , 1972b).This has been challeged by Berthold ( 1976b)and Leutenegger (1977b) , because the passageof cytoplasm could not be confirmed by TEMstudies of pores. According to Berthold, thestrands were most l i ke ly produced by fungi t h a tinvaded the pores in the laboratory cu l tu re .

Pore-like pits (‘pseudopores’ of authors) occurin some porcelaneous forms. They do not havean organic pore t ubu le , and a t h i n calcareouswa l l (about 10 t h i c k ) separates the bottomof the pits from the shell in ter ior . In radio-tracerexperiments, Hansen and Dalberg ( 1979) founduptake of labeled direct ly th rough the t h i nlateral walls of l iv ing symbiont-bear ing Amphi-sorus. They explained the up take as being causedby diffusion direct ly through the organicmater ial of the shell wall , and considered thepits (pseudopores) as an adaptat ion to obligatealgal symbiosis.

5Quantitative methods of

data analysis inforaminiferal ecology

5.1 INTRODUCTION

Undeniably, the Foraminifera offer a wealth ofecological information. Rarely, the data aresufficiently uncomplicated that knowledgeableobservation is all that is required to reveal thecritical ecological relationships. The desiredinformation is most often camouflaged byaspects of the data involving undesired syneco-logic and autecologic factors, historical factors,sampling effects, etc. This is where quanti tat iveanalytical methods become necessary. Theappropriate method can enhance the desiredecological signal in the data while suppressingthe unwanted noise; it may simplify or condensethe complicated structure of the data, making iteasier to explore relationships; and it can facili-tate testing an apparent relationship against thestandard of chance occurrence. Additionally, theresults of commonly used analytical techniquesmay be more convincing and more easilyexplained than an intui t ive understanding of thedata. Even when the relationship seems obvious,confirmatory analyses are a good idea.

With the proliferation in the 1980s and 1990s

Barun K. Sen Gupta (ed..), Modern Foraminifera, 71–89© 1999 Kluwer Academic Publishers, Printed in Great Britain.

of desktop microcomputers and packaged analyt-ical software, most foraminiferal researchers nowuse some form of quantitative analysis, rangingfrom simple spreadsheet or database operationsto complex multivariate statistical techniques.However, most workers have a limited back-ground in statistics and, when faced with the pros-pect of choosing an analytical method, can makeinappropriate choices. When using the techniquesdescribed here as exploratory devices to increaseunderstanding of a complex and confusing arrayof data, there are no right or wrong techniques.Some are certainly more efficient or appropriate‘signal-enhancing’ filters, depending on the natureof the data and the questions of the researcher.For most of these methods, evaluation of success

or failure of the analysis depends on whether theresults offer a meaningful view of the data in thecontext of the research focus. The purpose of thischapter is to explore the variety of available andcommonly used techniques, and to comment ontheir characteristics and applicability, so as to( 1 ) aid in understanding the choice, application,and interpretation of methods employed by otherresearchers, and ( 2 ) provide an introduction to

William C. Parker and Anthony J. Arnold

72 Quantitative methods of data analysis in foraminiferal ecology

the selection of techniques for the reader’sresearch. We will assume an understanding ofsimple statistical concepts (mean, standard devia-tion, etc.) and wi l l focus on the more complicatedmultivariate techniques. The interested reader isreferred to sources such as Shi (1993), Davis(1986), and Dillion and Goldstein (1984) for moregeneral coverage of the methods discussed.

As an explanatory aid we will include analysesof a set of benthic foraminiferal assemblagescollected from the Georgia–South Carolina con-tinental slope. This data set includes counts of183 species present in 38 samples of bottomsediment. The data and some analyses are dis-cussed in Arnold (1977, 1983), Arnold and SenGupta (1981), and Sen Gupta and Hayes (1979).The data are available in Arnold ( 1 9 7 7 ) or fromthe chapter authors at http://quartz.gly.fsu.edu/~ parker/data.html.

5.2 DATA

Stevens’ classic paper (1946) on scales of meas-urement provides valuable insights in to types ofmeasurements and the operations tha t can beperformed on them. Foraminiferal data can be( 1 ) nominal (using numbers as labels, e.g. 0 =smooth, 1 = spined, etc.), ( 2 ) ordinal (numericalvalues record monotonically increasing states,but not necessarily with equivalent intervals,e.g. 0 = absent, 1 = rare, 2 = common, etc.),( 3 ) interval (numbers indicating equal measure-ment intervals, but with no true zero, e.g. dis-tance from a geographic point or dep th / t imefrom a stratigraphic marker), and (4) ratio ( l i k einterval, but wi th a fixed zero, e.g. counts ofspecimens in a sample). Note that calculation ofmeans, standard deviations, and correlations aretechnically valid only with in terva l and ratiodata. Calculations involving alteration of vari-ance (e.g. log calculations or standardizations)are only appropriate for true rat io data.

Some foraminiferal studies may include typesof data that require special coding. For example,angular data, such as angular morphometric orlat i tudinal/ longitudinal measures can presentproblems due to the apparent numerical disconti-

nuity at the limits of the scale (e.g. 360°). Thisproblem is best handled by orienting the meas-urement scale (in most senses an interval scale)such that the recorded observations fal l only inthe cont inuous portion. Quant i ta t ive chemicalmeasurements, often used wi th environmenta lstudies, present problems at the low end of thescale. A chemical const i tuent can rarely be saidto be t r u l y absent from a sample, even when theanalytical technique fails to detect i t . Such ‘falsezeroes’ are more appropriately recorded as‘below detection limit,’ reflecting a possible con-centrat ion somewhere between the analyt icallower l im i t and t rue zero. Under these circum-stances, a recorded value of some fraction of thedetection limit (e.g. 1/2) is more appropriate.Finally, most data have a few samples for whichall desired measurements are not possible. Whilein some cases it may be most desirable to s implydiscard the samples (or variables) concerned, th ismay also result in serious reduction in the study’scoverage. Although the missing values can beestimated using a variety of techniques (e.g.regression, kriging. etc.), the resul t ing analysisu t i l iz ing the estimated values may be biased bythe estimation process. A better approach is tocode the missing values wi th some label or valuedesignated as ‘missing.’ Most packaged analyticalprograms include the option of using missingvalue codes, and wil l provide options for dealingwith such values that are most appropriate forthe techniques available in the package.

Since many numerical techniques are sensitiveto the relat ive sizes of the recorded values (e.g.variables recorded wi th ‘big numbers’ maydominate an analysis) or to the way in whichthe values are d is t r ibuted (e.g. a normal d is t r ibu-t ion), it is often desirable to transform the datato make it numerically more suitable (see Davis.1986, for a discussion, and Table 5.1 for the mostcommon data t ransformat ion types). However,these recalculations can hide or distort some ofthe informat ion originally present. For example,recalculation of species abundance as a percentof the sample is a common practice, but maydisguise the presence of very depauperatesamples, and hide major differences in variance.Some measurements, l ike species abundance in

Data 73

a pool of samples, may be dist inct ly ‘non-normal’ (e.g. skewed) and benefit from a vari-ance-altering transformation (e.g. log transformor power transform). Additionally, species pre-sent as no more than a minor faunul elementmay have little impact on the analysis, unlessspecies numbers or proportions are standard-ized (for each variable, recalculating the valueby subtracting its mean and dividing by its stan-dard deviation).

Because many foraminiferal data sets aresparse (e.g. having many species present in lowabundances in a few samples), researchers ofteneliminate rare species from the analysis toimprove the analytical response. Traditionally,species present at abundances of less than 1 or2% (sometimes only when low in more than50% of the samples) are eliminated. Keep inmind that the analytical results will then say-nothing about the eliminated taxa, or the por-tion of the fauna they represent.

Outliers are data elements which, for one ormore reasons, seem at odds with the rest of the

data (i.e. they do not l i t the expected t rend) .Outliers exist for a variety of reasons: ( 1 ) errorsin sampling, measuring, and recording of data,( 2 ) greater than expected v a r i a b i l i t y in asampled value, ( 3 ) inclusion of one or moremembers of a ‘different population,’ and(4) incorrect expectations of relationships withinthe data. It is principally because they differfrom the majority of the data that out l iers areso often viewed as troublesome hindrances.Their variance from the data mean often givesthe outliers unexpected influence in the outcomeof analytical techniques. While the researchermay be inclined (and sometimes justified) in dis-carding such distracting elements, this is apotentially dangerous course. The outliers, byvirtue of their difference, contain more ‘informa-tion’ than thei r counterparts, and to eliminatethem is to discard this information. If a goodcase can be made that the outliers are differentbecause of some a priori condition, then theymay be discarded, along with all other entitiesthat meet the same criteria. Otherwise, they


should remain in the analysis (with attemptsmade to minimize the i r distracting effects), orthe analysis should be continued w i t h o u t themand their relationship to the final results stated.

One potential ly confusing aspect of m u l t i v a r i -ate analytical techniques is the use of the terms‘sample’ and ‘variable’. As used here, ‘samples’refer to enti t ies which are conceptually com-posed of or described by other entities, the ‘vari-ables.’ Thus, for a biogeographic study offoraminiferal assemblages, a sample might bethe collection of recorded abundances of variousspecies at a given location, and the variableswould be the species. For a morphometric s tudyof a single species, the sample might be a singlespecimen (or a population of specimens), andthe variables would be the morphometric meas-urements. In our example data set, we have 38foraminiferal assemblages from splits of washed,sieved, and floated sediment (containing at least300 ind iv idua l foraminiferal specimens, wherepossible) as samples. The 138 species present inthese samples are the variables, and the i r valuesare recorded as counts of individual specimensfor each species in each sample (rat io data). Dueto the large and unwieldy nature of a138-element variable l is t (many packaged pro-grams have restrictions on the number of vari-ables used in some analyses), and theobservation that many of the species occursparsely and have l i t t l e correlation w i th anyother species, we have reduced the variable l istto the 77 species which show significant associa-tions wi th at least one other species ( fo l lowingArnold, 1983). Log transformation of data waschosen because species abundances are generallylog-normal and because, philosophically, thedifference between 0 and 1 individuals shouldbe more s ignif icant than the difference between100 and 101. Note that since the data set con-tained 0 values (for which the log transform isundefined), a constant, small value (smaller thanthe minimum positive value, e.g. 0.5) was addedto each entry in the data set prior to log trans-formation. Thus a 0.0 value becomes –0.69. Inaddition to species abundances, we also havedata on the depth, location, and sediment typeat each sampling locality. These la t ter variables

will be used to interpret the results of m u l t i v a r i -ate analyses of the species assemblages.

5.3 CLUSTER ANALYSIS

Cluster analysis (CA) is one of the most widelyused and commonly understood m u l t i v a r i a t eanaly t ica l techniques in the foraminifera l l i tera-ture. It segregates entities (samples, species,measurements) into ‘naturally occurring’ groupsand q u a n t i f i e s the between-group relat ionships.It is diff icult to peruse a copy of Journal ofForaminiferal Research or Marine Micropaleon-tology w i thou t seeing at least one example ofthe characteristic dendrogram (see Fig. 5.1 ) gen-erated by most packaged cluster ana lys i s pro-grams. The spindles of the dendrogram trackthe entities in the clusters, while the linkage barsreflect the s imi la r i ty of the clustered ent i t ies .Cluster analysis has been used to delineate bio-facies (e.g. I shman , 1996), species associations(e.g. Ishman and Domack. 1994), and morpho-metric associations (e.g. Saraswati, 1995). Onecaveat which must be remembered is that clusteranalysis always produces clusters, whether ornot any na tu ra l ly distinct groupings occur inthe data. It is most often used as an explora torytechnique, to see what groupings might be pre-sent. To conf i rm the presence of any clustersobserved, researchers resort to the quantifica-tion techniques discussed at the end of th is sec-t ion, or a comparison (‘mapping’) of the clusteranalysis results with results of other multivariatetechniques (e.g. factor analysis, principal compo-nents analysis, correspondence analysis, m u l t i -dimensional scaling).

Almost exclusively, the varieties of cluster ingused with foraminiferal data fall under the head-ing of ‘hierarchical agglomerative’ clustering,meaning that they start w i t h all ent i t ies in sepa-rate groups and proceed to cluster i t e r a t i v e l y ,by merging pairs of groups from previous i tera-tions, unt i l all entities are grouped into a singlecluster. Analyses are referred to as Q-mode forc lus ter ing of samples ( i .e . ent i t ies composed ofseveral measurable parameters), or R-mode forclustering of variables (the measurable parame-

Cluster analysis 75


ters). The choice of R- or Q-mode is a logicalresult of the kind of question being ‘asked’ ofthe data. If your interest is in similarity/dis-similarity among samples, then a Q-modeclustering of samples is indicated. Most imple-mentations begin with conversion of the data toa matrix of similarities (or dissimilarities) amongthe entities to be clustered, and end with theproduction of the descriptive dendrogram. Vari-ations on the basic format arise from differencesin ( 1 ) the similarity (or dissimilarity) calculationused, (2 ) the means of choosing which entit iesto cluster at each step, and ( 3 ) the means ofcalculating similarities of entities to newlyfused clusters.

Commonly chosen similarity measuresinclude the Pearson’s correlation coefficient(0-1.0) and euclidean distance (0- inf ini ty) . Thischoice can be important due to interactionbetween the nature of the data and the waysimilarity is calculated. Some indices of sim-ilarity, such as Pearson’s correlation, are rela-tively immune to differences in the ‘numericalsize’ of the entities being clustered, (i.e. whetherthe values are numerically larger or smaller thanfor other entities). Others, such as euclidean dis-tance, change similarity values with changes inscale of measurement. Additionally, some datasets may produce similarity values between enti-ties that have such small numerical ranges thatinterpretation of the dendrogram becomesdifficult. Unless the worker is interested inexploring the numerical nuances of the varioussimilarity measures, it is advisable to run severalanalyses with different indices, and discard, orat least distrust, any result that is fundamentallydifferent from the others. Davis (1986), Sneathand Sokal (1973), and Sepkoski (1974) discussvarious similarity measures available.

Most of the common clustering methodssimply join the two entities with the highestmutual similarity at each iteration. One popularvariant is Ward’s minimum variance clusteringmethod, which does not involve a similaritymeasure as such, but uses the data to calculatea sums-of-squares index E for all entities. Ateach step, a potential new cluster that yields thelowest total E value (for all the entities present

at that step) is formed. This continues unt i l asingle cluster remains. Ward’s method is oftenpreferred because the dendrogram, when scaledto E, produces what appears to be exceptionallywell defined clusters. This is primarily becauseE is a function of squared differences andis, therefore, nonlinear. A dendrogram scaledaginst the square root of E would be more com-parable to the other methods. Note that Ward’smethod, because it uses no similari ty measure(other than E, surrogate for variance), is suscep-tible to scale and measurement changes.

Among the variety of methods for calculatingsimilari t ies for newly fused clusters, two meth-ods, Unweighted Pair Group Method w i t hArithmetic averaging ( U P G M A ) and singlelinkage ( S L I N K ) , appear most popular. Theformer averages similarities of entities to newclusters (adjusting for the number of enti t ies ineach cluster), while the other takes the maximumsimilarity between the en t i ty and any memberof the new cluster. As expected, these differentmethods can produce dramatically different den-drograms, especially with regard to the levels oflinkage between clusters.

Recognition of ‘significant’ clusters wi th in adendrogram is largely a subjective process. Prac-titioners most commonly attempt to define clus-ters based on relative spacing of linkages in thedendrogram. Clusters can be graphically desig-nated by shading or by construction, on thedendrogram, of a ‘phenon line,’ marking a levelof similarity (or dissimilarity) at which the clus-ters are presumed to represent meaningfulaggregations.

If the aim of clustering is to explore orillustrate group s t ructure in the data, then theappropriateness of the specific choice of methodcan be judged subjectively (i.e. do you see whatyou were looking for?). However, if the goal isto objectively quant i fy the ‘success’ of a givenanalysis, we require more rigor. Two quant i f ica-tion techniques are available. The copheneticcorrelation value compares the between-entitysimilarity values in the original matr ix wi th asimilar set derived from the clustered results(described in detail in Davis, 1986). Valuesapproaching 1.0 indicate less distortion of the

Eigenvector techniques 77

original similarities by the clustering process.More involved techniques use a Monte Carloprocess (described in Milligan, 1996) to generateartificial, random data sets from the originaldata. Analysis of the artificial data provides abasis for quantitative comparison of the resultsof a given cluster analysis. Comparisons of vari-ous techniques (Milligan, 1996; Milligan andCooper, 1986; Hubert and Arabie, 1985) suggestthat the correlation coefficient generally outper-forms euclidean distance and that Ward’smethod may show some superiority toUPGMA. SLINK methods, in general, farepoorly.

Recent examples of CA include delineation ofspecies assemblages (Ishman and Domack,1994; Chang and Yoon, 1995) and environmen-tally related biofacies (Whitehead and McMinn,1997). A dendrogram for Q-mode CA (SPSS forWindows 7.5.1) of the example data set is shownin Fig. 5.1 with the clusters (shaded for identifi-cation) chosen on the basis of relative separa-tion. Arnold (1983) presents both R- andQ-mode clusters of this data, using the data inpresence/absence (1 or 0) form, and demon-strates that the Q-mode clusters thus formed arestrongly related to sample depth. The analysisshown here uses fully quantitative data (countsrather than presence/absence) converted to nat-ural logs and subsequently standardized. Samplesimilarites were calculated using Pearson’scoefficient and the clusters formed using theUWPGA method. As you can see, the clustersdisplay a relationship, albeit an imperfect one,with sample depth. The selection of the optionspresented here is based on approximately 15different runs with a variety of data treatments,similarity coefficients, and clustering strategies,with varying success in producing depth-relatedclusters. While the results shown illustrate thatthe assemblages are related by their depths, themanipulation of the methodology necessary toachieve even moderately strong depth-relatedclusters suggests that depth is not the only factorinfluencing groupings in the data. For example,note that the clusters also tend to separategroups related by sediment type. We also notethat those techniques which tend to minimize

the range of the variables, and make themnumerically comparable, produce results mostsimilar to that of Arnold (1983), perhapsbecause the presence or absence of a speciesindicates the environment better than itsabundance.

5.4 EIGENVECTOR TECHNIQUES

5.4.1

Eigenvector techniques embrace a variety ofanalytical methods, including Principal Compo-nents Analysis, Factor Analysis, and Correspon-dence Analysis. All of these techniques attemptto portray/resolve the similarities or differencesbetween entities (samples, species, etc.) in termsof placement in a multidimensional space. Thedimensions of this new space are determined byconverting the original or transformed data intosome measurement of similarity between enti-ties, and factoring the matrix of similarities intoeigenvectors (mutua l ly perpendicular axesdefining the coordinate system of the new space)and eigenvalues (a measure of how ‘important’each new axis is to the data). This factoringprocess is used to reduce the dimensionality ofa multivariate data set, without losing importantinformation, to the point that researchers caneasily work with it. Although some of the tech-niques are most often used with species, andothers with samples, all of these methods can beused in both R- and Q-modes (see discussion inDavid et al., 1974; Klovan and Imbrie, 1971);the choice is less restrictive than for CA. Withthe calculation of loadings and scores, it is pos-sible to derive information from the analyticalresults about the roles of samples and variablesin the reduced dimensional space. Keep in mindthat loadings address the relationships betweenthe entities being factored and the new axes (e.g.for R-mode, loadings variables; for Q-mode,loadings samples), while scores represent the‘alternate entities’ (R-mode, scores samples;Q-mode, scores variables). The differencesbetween the various techniques discussed hereare primarily due to the different assumptions


about the data and the different ways of datatreatment.

5.4.2 Principal Components Analysis

Principal Components Analysis (PCA) is thesimplest of the eigenvector analytical techniques.In PCA a variance/covariance matr ix or a corre-lation matrix is factored, thus making this tech-nique most suitable for R-mode investigations(note that calculation of an R-mode correlationmatrix involves standardization of the vari-ables). The process ideally will extract as manynew dimensions as there were original entitiesin the data (e.g. factoring a matrix wi th 10 enti-ties, you get 10 principal coordinates or factors).These new dimensions are mutual ly independentand each accounts for a decreasing share of theinformation in the original data (reflected bymonotonically decreasing eigenvalues).

Most commonly, researchers are not inter-ested in all of the new dimensions. The decisionabout how many dimensions to consider can bemade in many ways. A common method is toplot the eigenvalue (or its log) versus its order(see Fig. 5.2 for an example, also known as a‘scree plot’) and look for a ‘natural break’ in thedecrease in eigenvalues wi th increasing rank.

Others choose to retain only those eigenvaluesaccounting for more variance than any originalen t i ty would have, if variance were dis t r ibutedevenly (e.g. when factoring 20 species, only keepdimensions wi th 5% or more of the total vari-ance). Keep in mind that as you reduce dimen-sionali ty, you lose informat ion . Communali tyvalues (square root of sums of squares of load-ings for retained dimensions) wi l l help indicatewhen reducing dimensionali ty has e f f ec t i ve lyeliminated an ent i ty from the analysis.

The new axes can be rotated in mul t id imen-sional space to increase their explanatory value.Rota t ions can be either orthogonal (main ta in ingthe axes as independent) or obl ique (a l lowingfor inter-correlation). The only commonly usedrotation is V A R I M A X , an orthogonal rota t ionwhich maximizes the variance in factor loadings,thus having the effect of leaving each factorcharacterized by a few enti t ies w i th highloadings.

There are a variety of ways in which PCAresults can be interpreted. The principal compo-nents or factors can be viewed as new, ‘synthetic’variables ( R-mode), or new, ‘endmember’ associ-ations of variables (Q-mode). Sometimes sig-n i f icant members of the original variables orsamples have sufficiently strong loadings on acertain factor that the factor can be ‘named’ (e.g.the f i r s t factor in morphometric analyses oftencontains strong loadings from size-dependentvariables, and is called the growth or size axis) .One advantage of the new synthet ic variables istheir orthogonali ty; they are independent ( i .e.uncorrelaled) to each other. Thus, if one axisdescribes size, the other axes are size-indepen-dent. The loadings can be used to characterizethe original entit ies, or to explore relationshipsbetween subsets of entities. Natural ly occurringgroups of ent i t ies can be picked out on plots ofloadings or scores. Lines or arcs of ent i t ies onloading or score plots reveal gradients of change.Often, plots of PCA loadings may display ahighly curved or horseshoe-shaped arc. This is‘Kendall’s horseshoe,’ an artifact in the ana ly t i -cal process tha t can distort a simple (e.g. one-d imens iona l ) gradient of change into a higherdimensional curve.


Recent examples of PCA in foraminiferalresearch include Mackensen et al. (1993b) andHarloff and Mackensen (1997); these useQ-mode PCA to differentiate ecologically sig-nificant benthic foraminiferal associations.Loubere (1996) uses PCA of benthic speciesabundance data to il lustrate the differencesbetween factoring correlation versus variance/covariance matrices (correlation equally weightsall taxa, variance/covariance favors abundanttaxa). Speijer et al. (1996) present results of bothan R-mode CA and a PCA of Egyptian Paleo-gene benthic foraminiferal assemblages, giving acomparative view of the two techniques andshowing how to incorporate the results of onein the other. Fig. 5.3 (after Speijer et al., 1996)shows the stratigraphic distribution of samplescores, using the scores as synthetic sampledescriptors which the authors have related toenvironmental variables.

An R-mode PCA carried out on the exampledata set (using log transformed variables)yielded eigenvalues (and associated percentagesof the total variance each accounts for) shownin Table 5.2. A scree plot of these eigenvalues(Fig. 5.2) shows a distinct drop after the firstthree components, suggesting that these threehave substantial ly more explanatory power thanthe rest. A condensed table of V A R I M A Xrotated loadings (containing only those vari-ables wi th high loadings on one of these firstthree components) is shown in Table 5.3. Notethat many species, especially Textularia conica(TXT_CONI), Textularia agglutinans (TXT_AGGL), Siphonaperta sabulosa (SIPHON_S),Reophax curtus (REOPX_CU) , Eponidesantillarum (EPON_ANT), and Calcituba decor-ata (CATLUB_D) have high loadings on com-ponent one, the species Amphistegina lessonii(AMPHIS), Cassidulina laevigata (CASS_LAE),Cibicides floridanus (CIB_PSEU), Glabratellalauriei ( G L A B _ L A U ) , Quinqueloculina jugosa(Q_JUGOS), and Rosalina bertheloti (ROSA_


BRT), on component two, and especially, Cib-cides sp. cf. C. refulgens (CIB_RFLG), Rosalinafloridana (ROSA_FLD), Stilostomella antillea(STILOSTO), and Martinottiella communis(MARTNOT) on component three (a negativesign on the loading indicates that the speciesdecreases as the component increases). A plotof sample scores in Fig. 5.4 shows a gradationof samples along PC1 with a separate group-ing of points high on PC2. PC3 primarilyaccounts for two samples ( 1 1 1 2 and 1113) . A

plot of PC1 versus depth, shown in Fig. 5.5shows a positive correlation, so that PC1 maybe thought of as a depth component. The circlesin Fig. 5.4a surround the clusters defined pre-viously, demonstrating that the clusters A andC break up a cont inuum, while cluster B repre-sents something different. Referral to a map ofsample locations (Arnold, 1983) reveals that thesamples scoring high on PC2 are subs tan t i a l lyfarther northeast along the slope than othersamples at similar depths, and are typified byfiner grained sediments. Thus, the analysis haspicked up differences due to a variety of causes.

5.4.3 Factor analysis

Factor analysis (FA) , sensu stricto, differs fromPCA primarily in conceptualization of the data.In contrast to PCA, FA assumes that the infor-mation in the data is composed of a few factorscommon to all entities, mixed with factorsunique to ind iv idua l entities. The underlyingcommon factors are not directly observable butare reflected in the observable entities. Oneimplication of the factor analytic approach isthat the number of underlying common factorsmay be known a priori, rather than approxi-mated by looking at scree plots, loadings, orcommunalities.

A variety of methods exist for extraction offactors: principal components, principal factor,maximum likelihood, alpha, etc. Dillon andGoldstein (1984) conclude that ( 1 ) with commu-nalities ~ = 1.0, all methods produce nearlyidentical results, and ( 2 ) with more variables,method choice is less important. Various studies(cited in Dillon and Goldstein, 1984) have sug-gested that the maximum likelihood methodmay be superior for very large numbers ofsamples (> 1500), while the alpha and imagemethods may be better for small data sets.

Like PCA, FA can be done in Q- or R-mode,the factors can be rotated either orthogonallyor obliquely, and the results interpreted as dis-cussed for PCA above. Recent examples of FAinclude an R-mode analysis of biometric databy Saraswati (1995), analyses of benthic speciesdistribution data in relation to environment by



Nigam (1987) and Jayaraju and ReddeppaReddi (1996a), and an R-mode factor analysisof benthic foraminiferal assemblages in thenorthwestern Gulf of Mexico by Denne and SenGupta (1993).

5.4.4 Correspondence analysis

Correspondence Analysis, described by Davis(1986) and David et al. (1974), is similar to FAexcept that the data matrix is transformed intoa matrix of conditional probabilities. This pro-cess allows for the use of data that are not ratioor interval type (e.g. enumerative data such asthe counts of specimens in various species). Thetransformation is such that relationshipsbetween rows and columns in the transformedmatrix are the same as in the original data; thusR- and Q-mode solutions are equivalent and areobtained simultaneously. Published results ofcorrespondence analysis often show samples andvariables plotted on the same set of axes, thus

enhancing interpretat ion of the results (providedthe plots remain comprehensible) and reducingthe number of figures necessary to i l lus t ra te theanalysis. Recent examples of correspondenceanalysis include Widmark (1995) and Hermelinand Shimmield (1990).

5.5 MULTIDIMENSIONAL SCALING

Multidimensional scaling (MDS) is another datareduction technique that attempts to uncover‘hidden structure’ in data. It requires a matr ix ofsimilarities (or dissimilarities), and can be used ineither Q- or R-mode. Unl ike eigenvalue tech-niques. MDS attempts to ‘map’ entities into alimited dimensional space such that the proximit-ies between entities reflect their similarities. Theprocess is iterative, i nvo lv ing changing themapped locations of entities, and checking a cal-culated value of mismatch (between distances inthe map and similarities) called ‘stress.’ Most

Discriminant function analysis 83

packaged varieties of MDS require specificationof the number of dimensions for the map and astarting configuration. MDS can be either metric(assuming ratio or interval data and a precisefunction relating similarities to mapped distances)or nonmetric (assuming nominal or ordinal dataand an unspecifiable monotonic relationshipbetween similarity and mapped distance). Non-metric MDS can be superior to eigenvector tech-niques when relationships between entities are notlinear, because nonmetric MDS does not assumelinearity. Interpretation of the results is superfi-cially similar to that for PCA, with mapped coor-dinates for the entities in each requesteddimension ( ~ loadings) and correlations betweenmap axes and entity characteristics ( ~ scores).

A good general description of MDS can befound in Dillon and Goldstein (1984), while dis-cussions of applicability to paleontological dataare in Shi (1993), Hazel (1977) , and Millendorfet al. (1978). Despite its many advantages for fora-miniferal research, MDS has seen less use thaneigenvector techniques. Ishman (1996) uses aQ-mode MDS, CA, and PCA to analyze fora-miniferal assemblages as indicators of NorthAtlantic deep water circulation patterns.

Application of Q-mode MDS to the sampledata (log transformed) yields the two dimensionalmap shown in Fig. 5.6. The routine used wasALSCAL (SPSS for Windows 7.5.1). and thematrix of scaled distances was calculated from thedata by the program using euclidean distance. Atwo dimensional solution was chosen for compar-ison to the results from PCA. Note that thepattern of sample locations is very similar to thatfrom the PCA scores. The envelopes drawn arethe clusters generated from CA. Again, MDS axisone seems highly correlated with depth while axistwo separates geographically distinct groups ofsamples.

5.6 DISCRIMINANT FUNCTIONANALYSIS

Discriminant function analysis (DFA) is a tech-nique for classifying entities into mutually exclu-sive a priori groups based on a set of

independent variables. The technique operatesby deriving linear combinations (discriminantfunctions) of the variables such that misclassifi-

cation of the entities into the groups is mini-mized. Entities of unknown group aff ini ty canthen be classified using the discriminant functionand a probability calculated for membership ineach of the groups. This technique works bestwhen the groups are well known and at leastsome of their members can be identified une-quivocally. DFA shares many similarities w i t hmultiple linear regression, and it should beremembered that if the variables are highlyintercorrelated, the list of ‘discriminator’ vari-ables used in the discriminant function manynot include all those expected.

Recent examples of DFA include Jenningsand Nelson (1992) , in which the technique isused to discriminate foraminiferal assemblage

zones in Oregon tidal marshes. Mart in et al.(1995) use DFA, along with CA and FA, todistinguish species assemblages in Gulf of Cali-fornia tidal flats. Ishman and Domack (1994)use DFA, CA, and PCA to identify benthic fora-miniferal assemblages from the Antarctic Penin-sula. For the sample data set, we have used DFAto distinguish between samples associated withcoarse sandy sediment and those from finergrained sediments. Fifteen samples with obviouscoarse sandy sediment were coded 1.0, and thir-teen obviously fine-grained samples were coded2.0. The remaining samples were left uncodedand were classified by the analysis. As shown inTable 5.4 the DFA achieved 100% correct classi-fication of the coded samples wi th a functionusing only six of the species abundances(Melonis zaandami [MELON_ZA], Quinquelo-culina jugosa [Q._JUGOS], Rosalina berth-eloti [ROSA_BRT], Rosalina floridensis[ROSA_FLE], Spiroloculina atlantica [SPIR-OL_A], and Martinottiella communis [MART-NOT]). Figure 5.7 illustrates the dis t r ibut ion ofall the samples on a plot comparing the samplediscriminant scores with their depths. Note thatthe discriminant axis divided the samples intotwo groups, sand to the left, fine-grained to theright, and both groups falling in the 0–200 mrange (possibly explaining w h y attempts to sep-


arate these samples by depth alone were notsuccessful). The deeper samples (not originallycoded), although primarily classified by theDFA as sandy, do include one intermediate andone fine-grained sample.

5.7 REGRESSION ANALYSIS

Regression analysis is principally concernedwith predicting the mean expected value of onevariable (‘dependent variable’) from one or moreexplanatory variables (‘independent variables’).The model for the predictive relationship is alinear function of the independent variables asshown below:

where Y = dependent variable, X = independentvariable, b = regression coefficient isintercept), e = error or residual.

Note that although the form of the regressionmodel is linear, the relationship between the

Regression analysis 85

independent and dependent variables may benonlinear. For example, any independent vari-able can be replaced with or Thevalues of independent variables are assumed tobe known precisely and the dependent variableis assumed to be normally distributed for anyset of independent variables. In the commonOrdinary Least Squares (OLS) approach, thecoefficients (b’s) are chosen so as to minimizethe sums of squares of the error terms (e’s).Packaged regression analysis routines not onlyestimate the coefficient terms (b’s) but also thestandard errors of the coefficients. Coefficientswith large standard errors may be insignificantlydifferent from 0.0 (checked with a t-test), andtherefore contribute l i t t le to the prediction. Inaddition, an analysis of variance (ANOVA) forthe entire regression wi l l indicate whether thepredictive equation represents a significant par-tit ioning of variance in the dependent variable.The residuals (differences between the predictedand observed values of the dependent variable)should be inspected for heteroscedasticity (a

pattern in their variance) which would suggestan inappropriate choice in the form of theregression model. Because all of the coefficientshave standard errors, the confidence limits forthe equation as a predictor of the dependentvariable are notably ‘vase-shaped,’ with ‘tightest’confidence limits near the mean of each indepen-dent and larger limits near the extremes (i.e. thepredicted values will be most precise near themeans of the predictors).

If the independent variables are highly corre-lated (multicollinearity), then fewer than theexpected number of independents is needed foran efficient prediction equation. Calculation ofa regression equation with correlated indepen-dents can lead to instability in the coefficients(e.g. coefficients may change radically with theaddition or subtraction of a single datum). Step-wise regression, a process that sequentially addsor deletes independents to produce the mostefficient regression equation, solves the dilemmaof selecting the most efficient subset of indepen-dent predictors.


Interpretation of regression results can takemany forms. For example, the regression can beused to specify a trend, which can then be ana-lyzed separately from the deviations (residuals).In foraminiferal research, mult iple regressionanalysis is commonly used to predict physicaland chemical environmental parameters fromsample loadings in Q-mode PCA or FA (e.g.Giraudeau and Rogers, 1994; Mudie et al.,1984), the regression equations then becomingtransfer functions. This use of the procedurebenefits from the orthogonal nature of the PC’ssuch that no multicollinearity should occur.Other possible uses include trend surface analy-sis, where the independent variables recorddimensions of a ‘space’ (e.g. map coordinatesand/or depth and/or time), in which the depen-dent variable records the values of a presumablycontinuous function (e.g. an environmental vari-able or species density). The regression equationspecifies a multidimensional ‘surface’ describingthe regional trend in the dependent variable,while the residuals indicate local deviations fromthe trend. Both the regional trend and thepattern of local deviations may be of interest.

Table 5.5 shows the results of regression

(SPSS for Windows 7.5.1 ) of sample scores forthe previous sample data PCA against naturallog of depth (regression against linear depth wasalso significant, but wi th substant ia l ly smallerR2). The adjusted R2 values show that almost80% of the variance in depth can be predictedor explained using a ‘transfer function’ con-sisting of PC1 and PC3. The form of the transferfunction is

A comparison of true and predicted depth isshown in Fig. 5.8. Samples plot t ing above andto the left of a diagonal through the graph havepositive residuals and have predicted depthshigher than real, those to the lower right havenegative residuals and under-predicted depths.Table 5.6 shows the results of a stepwise regres-sion of the species abundance data against logdepth. Here six independent variables (species)are included, yielding an adjusted R2 of 0.939,almost 94% of depth variance explained. Fig. 5.9shows a comparison of true versus predicteddepths with much smaller residuals. Note tha t

Roads less traveled 87

although only six species’ abundances weredeemed sufficient for prediction of depth, otherspecies may also be strongly depth-dependent.

5.8 ROADS LESS TRAVELED

There are a number of techniques in use in otherareas of earth and life sciences which have poten-tial for application to foraminiferal studies, buthave yet to be commonly employed by research-ers. Some of these methods suffer from a lack ofinclusion in software packages, others fromobscure backgrounds. Since they are not incommon use, we will mention them only briefly,but the interested researcher may find value insome of these techniques.

Polar ordination is a data reduction techniquedeveloped by plant ecologists (Orloci, 1978;applied to fossil assemblages by Cisne and Rabe,1978) which places entities in a limited dimen-sional space, the axes of which are defined by

select enti t ies from the original data. It can beoperated in either Q- or R-mode, and interpre-ted much like PCA or MDS. It has the advan-tage of being less perturbed by out l ier entities(those wi th l i t t l e in common with the rest of thedata), but is handicapped by a limited numberof non-orthogonal axes. However, it has pro-duced excellent results w i t h ecological data, andhas the distinct advantage that the endpoints ofthe axes are represented by ‘real’ entities, ratherthan by calculated associations.

Recurrent group analysis (Sen Gupta andHayes, 1979) attempts to define groups ofspecies which co-occur in a statistically signifi-cant number of samples. Working with presence/absence, it is somewhat s imi la r to cluster analy-sis. Unavai lab le in common stat is t ical packages,it has seen limited usage. Sen Gupta and Hayes( 1 9 7 9 ) used it for groups of species on the Geor-gia shelf and Grand Banks, and compared it tocluster analysis, f inding tha t recurrent groupanalysis gave a better fit to species diversity


gradients and identified patterns of group distri-bution that correlated with water depth andsediment type.

Kriging, developed in geology, is a methodof analyzing regionalized data (data sampledat discrete locations, but wi th a con t inuousdis t r ibut ion over a spatial region). It can beused to estimate values of regionalized variatesat unsampled locations, or to analyze thepattern of increase in variance between twoobservations wi th increasing separation dis-tance. Having many of the same appl ica t ionsas regression (specifically, trend surface analy-sis), it differs in that the regionalized variateneed not be modeled as a specific l inear func-t ion. In addi t ion, confidence l imi t s are not assensitive to the position wi th in the region.Described in Isaaks and Srivastava (1989) ,kr ig ing has seen l i t t l e application in paleonto-logical research.

5.9 CONCLUSION

For a researcher approaching q u a n t i t a t i v eanalysis for the first time, or for one con-sidering the expansion of a l imi ted repertoireof techniques, the var ie ty of d i f fe ren t tech-niques and options ava i lab le may i n i t i a l l yseem overwhelming and undecipherable. Ingeneral, if the researcher believes tha t the dataset contains natural groupings, and wishes todef ine these numer ica l ly , then cluster analys isor recurrent group analysis are recommended.If some or a l l of the members of the groupsare k n o w n a priori, and the researcher wishesto classify u n k n o w n s or q u a n t i f y the d i f f e r -ences between the groups, then DFA is recom-mended. If the researcher is invest igat ingunderlying structure independent of groupings,then PCA, FA, correspondence analysis, MDS,or polar o rd ina t ion are recommended. If the

Roads less traveled 89

researcher wishes to use underlying relation-ships to predict values or compare predictionmodels with observed values, then regressionanalysis or kriging is recommended.

This chapter has provided only the briefestintroduction to what techniques are availableand in use in the field of foraminiferal research.The references cited, along with the software

packages available, wi l l give more detaileddescriptions of specific methods. In closing, weleave the reader with a single caveat: Rememberthat no statistical technique or software routine,no matter how complex or expensive, can takethe place of a deep understanding of the dataand the processes being studied.


PART II:FEATURES OF

DISTRIBUTION


6Biogeography of neritic

benthic ForaminiferaStephen J. Culver and Martin A. Buzas

6.1 INTRODUCTION

Biogeographical studies ( the distribution oforganisms, present and past, and the historicaland ecological processes that cause these distribu-tions) are a natural extension of systematics. Atthe highest level of the systematic hierarchy, King-dom, we recognize a ubiquitous geographic distri-bution of organisms. As we proceed downwardto the lower members of the systematic hierarchy,discrete geographic distributions emerge. Recog-nizing patterns of distribution and attempting toexplain them is the domain of the biogeographer.However, the recognition of pattern dependsupon our definition of what constitutes pattern(s),what systematic level we are examining, and atwhat geographic scale. Likewise, explanationrequires a historical as well as an ecological per-spective. These considerations, coupled with thevast variety and numbers of organisms plus thediverse interests of the investigators, insure a lackof simplicity or unification of the subject.

At the species level, differences in distributionwith depth and latitude are readily apparent formost benthic marine organisms, including theForaminifera. If we were to list desirable attributesfor an organism at the Class or Order level that

would ideally suit it for biogeographic studies atthe species level, we might list: 1, ubiquitous distri-bution; 2, easily sampled: 3, high density; 4, manyspecies; 5, good preservation providing an excel-lent fossil record; 6, large number of researchers;and 7, many years of study. Curiously, the benthicForaminifera have all of these attributes and yetthey have received very l i t t le attention for biogeo-graphic studies. North America is the exceptionin that Culver and Buzas (1980, 1981a, 1982a,1985, 1986, 1987) compiled and taxonomicallystandardized all the existing data on the distribu-tion of benthic Foraminifera around the marginsof the North American continent. We will use thisdata set to gain some understanding of the bioge-ography of neritic benthic Foraminifera, but firstwe will briefly review two worldwide provincialschemes.

6.2 GLOBAL BIOGEOGRAPHY

6.2.1 Cushman’s faunas

Joseph Cushman’s knowledge and experiencewith Foraminifera led him to recognize generaldistribution patterns for different groups (Cush-

Barun K.Gupta (ed.), Modern Foraminifera, 93–102© 1999 Kluwer Academic Publishers. Printed in Great Britain.

94 Biogeography of neritic benthic Foraminifera

6.2.2 Boltovskoy and Wright’s provinces

6.3 BIOGEOGRAPHY OF NORTH ANDCENTRAL AMERICA

6.3.1 Background

man, 1948). For example, he noted that lagenidscharacterize continental shelves, miliolids (withsome deep water exceptions such as Pyrgo) aremost abundant in shallow warm-water, coralreef regions, while larger benthic foraminfera areessentially restricted to tropical waters less than60 m deep. Cushman considered that temper-ature is the predominant controlling factor ofbenthic foraminiferal distributions. This led himto a global subdivision into cold-water andwarm-water faunas (Fig. 6.1a, b: Cushman,1948, map dated 1921).

The distribution of cold-water faunas is obvi-ously relatable to cold oceanic currents (e.g.southern extension of cold faunas on the westernsides of the North Atlantic and North Pacific;Fig. 6.1a). Cushman noted that although theAntarctic region has its own characteristicspecies, faunas there are very similar to those inthe Arctic (species lists given in Murray, 1991b,suggest this is an over-simplification). Cushmanalso recognized the extension of cold-waterfaunas into the ocean basins, most of the infor-mation for this conclusion deriving from Brady’s(1884) Challenger Report.

Warm-water faunas were recognized by Cush-man (1948) to be less cosmopolitan; he drew foursubdivisions but noted that there could be more(Fig. 6.1b). These are essentially shallow-waterfaunas as indicated by the extension of the WestIndian fauna from Florida to Bermuda and acrossthe Atlantic to the coast of Ireland. The Mediter-ranean fauna extends into the shallow margins ofthe Red Sea, and the Atlantic and Indian Oceanmargins of Africa. Warm-water faunas around theislands of the Indian Ocean (East African fauna)were distinguished by Cushman from the gen-erally more diverse East Indian fauna of thePacific Ocean (Fig. 6.1b).

Cushman (1948) believed that although tem-perature controls benthic foraminiferal distri-butions, historical factors, such as Tertiarymigrations, are of great importance in explainingmodern distribution patterns. Cushman notedthat the faunas of the Caribbean region are muchmore like those of Australia than of other tropicalregions. Similarly, he pointed out that the cold-water fauna of the west coast of South America

is more like that of northern Europe than of themuch closer Pacific island groups. These patternswere attributed to earlier migrations rather thanmodern oceanographic conditions.

Boltovskoy and Wright (1976) concurred withCushman’s ideas concerning the importance oftemperature and migrations in explaining thebiogeography of neritic benthic foraminfera.They refined Cushman’s map using the datapublished in many papers during the 1950s to1970s and recognized 17 provinces, seven char-acterized by warm-water species, two by cold-water species, and eight by temperate-waterspecies (Fig. 6.2). Boltovskoy and Wright (1976)noted that where enough data were available,division into subprovinces was possible but asubprovincial scheme was given only for SouthAmerica (subsequently elaborated upon in Bol-tovskoy et al., 1980).

There is great similarity between Cushman’sand Boltovskoy and Wright’s provincialschemes. West Indian, Mediterranean, East Afri-can, and Indo-Pacific provinces are recognizedin both, but Boltovskoy and Wright distin-guished Lusitanian and West African faunasfrom those of the Mediterranean. Similarly, theydistinguished Panamanian and West Indianprovinces. Cushman and Boltovskoy andWright also recognized Arctic and Antarctic-provinces but the greatest difference between thetwo schemes is in the temperate regions whereBoltovskoy and Wright (1976) recognized eightdistinct provinces. The pattern of shading onCushman’s map (Fig. 6.1a) suggests that he con-sidered these temperate regions to be transi-tional between cold- and warm-water provinces(Cushman, 1948).

Like Cushman (1948), Boltovskoy and Wright(1976) did not indicate in detail the criteria used

Biogeography of North and Central America 95

Biogeography of neritic benthic Foraminifera96

to distinguish provinces and subprovinces or todefine the location of provincial and subprovin-cial boundaries. However, thei r provincialscheme is very similar to that produced byHedgpeth (1957b) for macroorganisms of thelittoral zones of the world. Boltovskoy andWright (1976) did not consider this to be sur-prising, given the fact that similar controll ingfactors were involved. They did note, however,that differences could be best explained bydifferences in regional geological history.

Hedgpeth (1957b) was following the leadgiven by famous predecessors in the field ofmarine macrofaunal biogeography (e.g. Milne-Edwards, 1838; Dana, 1853; Woodward, 1856;Ekman, 1953). These workers classified the shal-low seas of the world into realms and provincesbased on the degree of endemism w i t h i n thespecies inhabit ing a province. But the amountof endemism necessary to recognize a provincehas varied greatly. Woodward (1856) considered

a province to be characterized by greater than50% endemic species. Later workers (e.g.Kauffman and Scott, 1976) reduced this figureto 25 to 50% endemism (as low as 20% inpractice), while Briggs (1974) considered 10%endemism to be sufficient .

When Culver and Buzas embarked on a pro-ject in 1978 to study the biogeography ofmodern benthic Foraminifera from the conti-nental margins of North and Central America,they chose to ident i fy provinces using the moreflexible definition of provinces proposed by Val-ent ine (1968, p. 257) namely, ‘... collections ofcommunities associated in space and time.’ Theyalso chose to recognize provinces using thenumerical technique of cluster analysis ratherthan relying on experience and/ or visual exami-nation of distributional data.

The amount of in fo rmat ion on the dis t r ibu-tion of modern benthic Foraminifera aroundNor th America is vast. Several hundred publica-

Biogeography of North and Central America 97

tions (Culver, 1980) contain relevant material,and the database has continued to grow. Themajority of these data were compiled during the1950s and 1960s in response to the pressure tolocate oil and gas. It was realized that a knowl-edge of the distribution of modern Foraminiferawould help interpretation of foraminiferalassemblages recovered from well-cuttings.Studies such as those by Phleger and Parker( 1 9 5 1 ) , Parker (1954), and many others fulfil ledthis need.

Culver and Buzas constructed databases con-taining all of the published distr ibutional datafor all benthic foraminiferal species names everrecorded from the continental margins of NorthAmerica. These data were published in volumesfor the Atlantic continental margin (Culver andBuzas, 1980), the Gulf of Mexico (Culver andBuzas, 198la), the Caribbean (Culver and Buzas,1982a), and the Pacific continental margin fromAlaska to Panama (Culver and Buzas, 1985,1986, 1987). Data were also compiled for theArctic margin of North America but remainunpublished.

Because the methodologies employed byauthors over the years were quite variable (e.g.sampling equipment, sieve size, live or dead,absolute abundances or percent or presence-absence data, etc.), Culver and Buzas’ compila-tions utilized presence-absence data. No infor-mation points were deleted. Some geographiclocations were represented by only one specieswhereas others had scores of species. Wheresmall areas had been intensively sampled, thedata were combined so that a single localityrepresented all of those stations.

The problem with compilations is the incon-sistency of the incorporated data. Util izing apresence-absence approach ameliorates thisproblem but, without doubt, the most significantproblem is taxonomic inconsistency. To addressthis problem, Culver and Buzas conducted anexhaustive process of taxonomic standardiza-tion. For example, by using the literature andextensive collections in the Smithsonian Inst i tu-tion, Washington, D.C., The Natural HistoryMuseum, London, and several other ins t i tu-tions, the 1303 species names used by authors

for species found on the Atlantic continentalmargin were reduced to 876. Similar reductionswere made on the other continental margins. Itis likely that no other foraminiferologist wouldagree with all of the taxonomic decisions thatwere made (all taxonomic changes were docu-mented in the publications), but the resultingdata set was standardized and, indeed, if errorswere included (and they undoubtedly were), thescale of the data set meant that it, and thepatterns that were subsequently recognized,were robust.

In addition to distributional data, Culver andBuzas (1980, 1981a, 1982a, 1985, 1986, 1987)provided maps showing the geographic andbathymetric distribution of the most commonlyoccurring species on the various continentalmargins. Cluster analysis (more elegant statisti-cal procedures were not appropriate for such aheterogeneous database) resulted in the recogni-tion of several provinces on each continentalmargin (Buzas and Culver 1980, 1990; Culverand Buzas, 1981b,c, 1982b, 1983).

Shallow-water provinces were similar to thoserecognized for other organisms, but depth-related provinces were also evident (e.g. Culverand Buzas, 1982b). Indeed, the faunal differencesbetween shallow (<200 m) and deep ( >200 m)provinces at the same latitude were greater thanbetween adjacent shallow-water provinces(Culver and Buzas, 1981b, 1982b).

This succession of provinces with increasingdepth was most evident on the passive continen-tal margins of the Atlantic and the Gulf ofMexico. A similar pattern was present on theactive Pacific margin but was less well devel-oped, probably due to the relative narrownessof the continental margin and the more patchydistribution of data points. Culver and Buzas(1981b, 1983) related the depth-related provin-cial boundaries to water-mass boundaries andspeculated (Buzas and Culver, 1982) that theremay be as many provinces in the marine worldas there are water masses impinging on theseafloor.

The next section will deal only with provinceson the continental shelves around North andCentral America and will compare their config-


urations with those of provinces defined formacrofaunal data (see Sen Gupta 1972, for anearlier comparison).

6.3.2 Neritic provinces

Figure 6.3 diagrammatically indicates the elevenprovinces that Culver and Buzas recognized inthe shelf waters of North and Central America.Clear boundaries are evident along the generallynorth-south Pacific and Atlantic margins butthe boundaries between the Arctic Province( 1 ) and the Aleutian ( 2 ) and Atlantic NorthernInner Shelf Province (10) are not clearly defined.The southern extensions of the PanamanianProvince (5) and Caribbean Province ( = WestIndian Province, 6) are detailed in Boltovskoyand Wright (1976). The entire width of the opencontinental shelf is the site of a single provincearound most of the continental margins, butouter shelf or upper slope provinces are presenton the broad shelves of the Gulf of Mexico, andon the Atlantic margin north of Cape Hatteras,where slope waters impinge on the outer shelf(Culver and Buzas, 1981b, 1983).

The characteristic faunas of the eleven prov-inces are given in the various Culver and Buzaspapers and, for the Arctic, in Vilks (1989), andneed not be repeated here. However, it is interes-ting to compare the benthic foraminiferal prov-inces with those recognized for the benthicmacrofauna around North and Central Amer-ica. Valentine (1966) summarized the provincialschemes proposed by various mollusc workersfor the Pacific shelf of North and Central Amer-ica. Despite differences, all workers, includingValentine, recognized important provincialboundaries at the Strait of Juan de Fuca, PointConception, and Cabo San Lucas (Fig. 6.3). Intheir study of isopods, Brusca and Wallerstein(1979) noted the same important boundaries,but also recognized a Cortez Province (in theGulf of California and a Mexican Province fromTangola Tangola to Cabo San Lucas (Fig. 6.3).They also recognized a transitional zonebetween Cabo San Lucas and Punta Eugenio,a region recognized as the Surian Province byValentine (1976) in a study of ostracod biogeog-

raphy. Valentine (1976) also recognized Orego-nian, Californian, and Panamanian provincesand subprovinces wi thin them. Major changesin foraminiferal faunas also occur at the Straitof Juan de Fuca, Point Conception and CaboSan Lucas (Fig. 6.3), but subprovinces recog-nized by Valentine (1976) and Brusca andWallerstein (1979) are not evident in the fora-miniferal data (Lankford and Phleger, 1973;Crouch and Poag, 1987; Buzas and Culver,1990).

The Caribbean and Gulf of Mexico regionshave also been subject to various provincial clas-sifications based on macrofaunal data. Hall(1964), working with molluscs, included bothareas in a single Caribbean Province, whereasother mollusc workers (Rehder, 1954; Warmkeand Abbott, 1961) included the southern tip ofFlorida and the southern half of the Gulf ofMexico together with the Caribbean region ina Caribbean Province. The benthic Foraminiferaof the shallow waters around the Caribbeanislands and along the northern coast of southand Central America cannot be subdivided atthis scale (Culver and Buzas, 1982a). Togetherwith the carbonate substrate faunas of the Yuca-tan, southern Florida, and the Bahamas, theyconstitute a Caribbean Province. This is distinctin foraminiferal composition from the Gulf ofMexico Inner Shelf Province (Culver and Buzas,1982b; Buzas and Culver, 1982).

Some macrofaunal workers have distin-guished northern and southern shelf areas in theGulf of Mexico and have assigned them to Caro-linian and Caribbean provinces, respectively,with a boundary at Cabo Rojo ( Fig. 6.3) (Hedg-peth, 1953). Foraminiferal distribution patternsin the Gulf of Mexico are largely concentric(Culver and Buzas, 1981c; Poag, 1981) and thefaunas of the Gulf of Mexico Inner Shelf Prov-ince are as distinct from faunas south of CapeHatteras (Fig. 6.3) (the macrofaunal CarolinianProvince) as they are from those of the Carib-bean Province (Culver and Buzas, 1982b; Buzasand Culver 1982).

The foraminiferal data agree with those formacrofauna in placing the carbonate substratesouthern tip of Florida, between Cape Romano

Biogeography of North and Central America

and south of Cape Canaveral (Fig. 6.3), in aCaribbean Province. Between Cape Canaveraland Cape Hatteras, the distinctive foraminiferalassemblage comprises the Atlantic Southern

99

Shelf Province (Fig. 6.3), equivalent to theAtlant ic portion of the macrofaunal CarolinianProvince ( Hedgpeth, 1953). The shelf macrofau-nas nor th of Cape Hatteras have been subdi-


vided into Virginian and Acadian ( = NovaScotian) Provinces with the boundary at CapeCod (e.g. Dana, 1953; Hall, 1964; Maturo, 1968).Several foraminiferal workers followed thisscheme (e.g. Cushman, 1948; Parker, 1948;Murray, 1973), but Culver and Buzas ( 1 9 8 l b )did not make this distinction and recognized asingle Atlantic Northern Inner Shelf Provincestretching from Cape Hatteras to the GrandBanks off Newfoundland (Fig. 6.3). Several mol-lusc workers concur wi th this provincial classi-fication (Coomans, 1962; Franz and Merr i l l ,1980).

The neritic environments of the CanadianArctic Archipelago and northern Alaska areplaced within the Arct ic Province (Fig. 6.3). Inreview papers, Lagoe (1979) and Vilks (1989)noted that the foraminiferal faunas from waterdepths of less than 200 m were generally domi-nated by agglutinated Foraminifera, thus dist in-guishing them from faunas of the Aleut ianProvince and the Atlantic Northern Shelf Prov-ince. This pattern is not ubiquitous, however,and some regions, e.g. the Beaufort shelf(Fig. 6.3; Vilks, 1989) and the Axel Heiberg shelf(Schröder-Adams et al., 1990) are dominated bycalcareous species, and may exhibi t qui te highdiversity.

At the beginning of this chapter, we describedCushman’s (1948) and Boltovskoy and Wright’s(1976) global provincial schemes for shelf Fora-minifera which indicated temperature as themajor controlling factor for species distribu-tions, an opinion shared by Hedgpeth (1957b)and Murray (I991b). While acknowledging theimportant role of temperature as an environ-mental variable, it is worth noting that manyprovincial boundaries are located at headlands(Fig. 6.3) associated with oceanographic bound-aries. Thus, many workers have related thelarge-scale dis tr ibut ion of shelf Foraminifera towater-mass d is t r ibut ions (e.g. Lank ford andPhleger, 1973; Buzas and Culver, 1980, 1990;Culver and Buzas, 1981c; Crouch and Poag,1987).

Figure 6.4 illustrates the relationship betweenwater masses and benthic foraminferal provincesfrom shelf to abyssal depths in the Gulf of

Mexico and on the Atlantic continental margin.The Gulf of Mexico I n n e r Shelf Province(Fig. 6.4) is associated w i t h the surface mixedlayer whose transit ional boundary wi th theunder ly ing Subtropical Underwater lies at 100to 200 m, the depth limit of seasonal effects onwater-mass characteristics ( Phleger and Parker,1954; Nowlin and Parker, 1974). The Gulfof Mexico Outer Shelf and Slope Provinceis related to several layered water masses(Fig. 6.4). Where these impinge upon the outershelf and upper slope, changes in foraminifera lassemblages occur (Culver, 1988), but these areconsidered to represent biofacies v a r i a t i o n swithin a province (Culver and Buzas, 1983).

On the At lan t ic cont inental margin, theAtlantic Southern Shelf Province is related toSouthern Shelf Water ( Fig. 6.4). Nor th of CapeHatteras, the shelf is overlain by the much coolerNor thern Shelf Water, and th i s is reflected inthe significant change to the neri t ic foramini fe ra lassemblages of the At lan t ic Nor thern Inne rShelf Province. Slope water overlies the slopebut impinges on the outer shelf, and this overliesthe At l an t i c Northern Outer Shelf and SlopeProvince (Culver and Buzas, 1981b).

6.4 CENTERS OF ORIGIN ANDDISPERSAL OF BENTHICFORAMINIFERA

The concept of centers of origin for species hasbeen extensively discussed in the l i t e ra ture ofbiogeography and evolution (e.g. McCoy andHeck, 1983). Al though the Arct ic ( H i c k e y et al.,1983) and the Antarctic (Zinsmeister and Feld-mann, 1984) have been proposed as possiblecenters of origin, the tropics usually have th i scharacteristic attributed to them (e.g. Durazziand Stehli, 1972; Briggs, 1974; Pielou, 1979),wi th newly evolved species dispersing to thehigher latitudes. Thus, on the Atlantic continen-tal margin of North America one could hypo-thesise enhanced or iginat ion of benthicforaminiferal species in the Caribbean Province.Buzas and Culver (1986; 1989) examined th i shypothesis by documenting the worldwide dis-

Centers of origin and dispersal of benthic Foraminifera 101


6.5 SUMMARY

6.6 ACKNOWLEDGMENTS

tribution of first reliable stratigraphic occur-rences of all modern species recorded on theNorth American Atlantic continental margin.They found that modern species of benthic Fora-minifera have originated in all parts of theworld’s oceans from the Cretaceous to the Pleis-tocene (Buzas and Culver, 1989). Possible con-centrations of first occurrences in the Mioceneof the Caribbean region were considered to bemonographic effects. The Pleistocene was char-acterized by many more high-latitude occur-rences but this, again, was considered to be dueto one significant paper. Further, the apparenttrend of more high latitude originations as cli-matic cooling occurred during the Neogene wasbelieved to be the result of the distribution ofoutcrops of that age. Buzas and Culver (1989)concluded that the available data do not supporta simple concept of a center of origin for modernbenthic foraminiferal species from the NorthAmerican Atlantic continental margin.

The data used to investigate centers of originshowed that first occurrences were oftenrecorded in more than one place. This could beexplained by poor stratigraphic control, but inthe Pleistocene, where greater resolution is pos-sible, several species were first recorded inAlaska and Maine in deposits of the same age.Buzas and Culver (1989) considered this to bethe result of rapid dispersal, instantaneous interms of our powers of resolution. Thus, thisdispersal ability means that vicariance events,although important in some instances, such asthe formation of the Isthmus of Panama, areprobably factors of little importance to benthicforaminiferal biogeography.

The dispersal ability of continental marginbenthic Foraminifera was further investigatedby Buzas and Culver (1991) . They showed that53 of 878 species that currently occur on theNorth American Atlantic continental margin areubiquitous around North and Central Americaeven though they have no fossil record. Most ofthese are abundant and would have been foundin the well-documented Cenozoic deposits

around the North American margins if they hadexisted in the past. Buzas and Culver ( 1 9 9 1 )concluded that these taxa must have evolvedrecently and dispersed rapidly.

Large-scale biogeographic distributions of ben-thic Foraminifera of the world’s shelves exhibi ta pattern that indicates a major controlling rolefor temperature at this scale. Cold-, temperate-,and warm-water groupings of provinces havebeen recognized around the world, with agreater number of provinces delineated inwarmer regions. Modern provincial patterns,however, have also been influenced by differ-ences in regional geological histories.

The continental margins of North and CentralAmerica have been subject to the most intensivebiogeographic investigations, and eleven benthicforaminiferal provinces have been recognized inthe neritic zone. Their dis t r ibut ion and bound-aries can be closely related to the distr ibut ionand boundaries of major water masses. Thus,the provincial scheme for modern benthic Fora-minifera is similar to that for modern shallowmarine macroorganisms. The differences suggestthat benthic Foraminifera may be somewhat lesssensitive to the changes in the marine climatethan other benthic organisms of the neritic zone.

No center or centers of origin can be identifiedfor the modern benthic Foraminifera of theNorth American Atlant ic continental margin.First stratigraphic occurrences are both tempo-rally and geographically widespread, and sug-gest rapid dispersal.

We thank J. Jett, J. Swallow, and P. Christopherfor their help. This paper is a contr ibut ion fromthe Natura l History Museum-University Col-lege London research program in ‘GlobalChange in the Biosphere.’

7Biogeography of

planktonic ForaminiferaAnthony J. Arnold and William C. Parker

7.1 INTRODUCTION

7.1.1 A historical perspective

It is often said that nothing makes sense in biologyexcept in the light of evolution (Dobzhansky,1973). It could equally well be said that l i t t lemakes sense in biogeography except in the contextof its historical development, since modern bioge-ography reflects both organismal habitat prefer-ences and the historical processes that haveculminated in modern distribution patterns.

Research on most modern plankton groupshas resulted in broad agreement among manyplankton biogeographers as to the dispositionof large scale provinces (e.g. Backus 1986;McGowan, 1986). The frontal systems thatsometimes separate these provinces often showsteep environmental gradients that can corre-spond to faunal transitions. However, even thesemost conspicuous biogeographic provinces donot always show a clearly-defined relationshipto physicochemical variables, and the search forthe factor(s) that explain the distribution of aspecies or a group of species is rarely successful(Backus, 1986). Such difficulties of finding con-nections are usually attributed to the complexity

of interaction between controlling factors, buthistorical considerations can also play a signifi-cant role. Work on the planktonic Foraminiferahas made it increasingly clear that large scalebiogeographic features such as the global diver-sity gradient and the la t i tudinal ly arrayed majorprovinces owe their existence at least par t ly todifferential rates of speciation and extinction – processes that are inherent ly historical in thesense that they involve adaptation to antecedentrather than present-day conditions. It is in pre-cisely this sense that modern biogeographycannot be separated from its evolutionary past.

Nonetheless, with rare exceptions, research onplankton biogeography has focused primarilyon the relationship between species distr ibutionpatterns and the physicochemical environmentthey inhabit . Usually, delineating a modernbiogeographic province involves quantifyingspecies dis tr ibut ions along plankton tow tran-sects, then using physicochemical properties ofthe environment to extrapolate over largerareas. However, when readily fossilized organ-isms such as the planktonic Foraminifera areinvolved, their stratigraphic record adds bothhistorical dimension and complexity to theanalysis; as a consequence, it becomes even more


104 Biogeography of planktonic Foraminifera

essential to develop an understanding of theissue of scale – both spatial and temporal.

For example, it is often smaller-scale factorsthat mediate the evolutionary origins of species,even though larger-scale considerations mayconstrain their dis t r ibut ion. To the extent thatallopatry and peripheral isolation play a role inthe origin of p lanktonic species, the present-dayprovincial-scale geographic range of a givenspecies is likely to be much larger than its rangeat its t ime of origin – and yet the adaptivecircumstances of tha t species’ time and place oforigin may well dictate (and explain) its presentd i s t r ibu t ion . Fur ther , if the conditions for speci-ation arise only rarely – say, on a geological(rather than ecological) time scale – then the fulldiversi ty potential of a given province may notyet have been reached, and the question of equil-ibration time arises. For reasons l ike these,temporal and spatial scale are central issuesand fundamental organizing principles in thischapter.

Before beginning any discussion of biogeogra-phy, it is important to be aware of the tapho-nomic and methodological factors that caninfluence basic data.

Foraminifera trapped in the mesh, and provideda methodology for correcting samples to a nomi-nal mesh size. The fact tha t reported abundancescan vary by eight orders of magnitude, depend-ing largely on the sampling gear used, indicatestha t care must be taken when mak ing biogeo-graphic abundance comparisons between plank-ton tow studies. In addi t ion to absoluteabundances, re la t ive abundances and seasonalabundance variability also show a strong sizedependency in p l ank ton tows, which is reflectedin divers i ty indices, m u l t i v a r i a t e s t a t i s t i ca ltreatments, and even presence absence data(Ottens, 1991) .

In general, the cold water aspect of a l i v i n gfauna tends to be enhanced in the underlyingsediments for two reasons. The first is an ar t i fac tof the d i s s imi la r mesh sizes used in p lank tontows versus the smaller size ranges commonly)included when examining coretop samples, sincethe smaller size fractions tend to have a cooleraspect (Berger, 1971) . The second reason stemsfrom differential dissolution susceptibilitiesbetween species and the resu l t ing biases therebyintroduced in to our perceptions of fossil bioge-ography (useful summaries can be found in R u d -i m a n n , 1977, and Vincent and Berger, 1981) .Many tropical species (as well as those that areenriched in the sediments due to spring upwell -ing) are relatively susceptible to dissolution; thed i f fe ren t ia l removal of these species increases thecold water aspect of sediment-surface assem-blages (Rudimann, 1977). The effects of differ-ent ia l dissolut ion are fu r the r complicated byvariat ions in bottom topography in relation tothe position of the lysocline.

Vertical mixing, current winnowing and sort-ing, and displacement by turbidites, amongother taphonomic effects, can int roduce addi-tional bias into the biogeographic record; theseare discussed in more detail by Bé (1977). Rud i -mann ( 1 9 7 7 ) , Orr and Jenkins ( 1 9 7 7 ) and inchapter 16 of th i s book.

The relationship between abundance in thesediments and s tanding abundance in the w a t e rcolumn is distorted s ign i f i can t ly by a number offactors, not all of them taphonomic. Species w i t hshorter generat ion t imes have propor t ional ly

7.1.2 Taphonomy and methodology

7.1.2.1

Our perceptions of foraminiferal d is t r ibut ionand diversity are necessarily dependent on taxo-nomic philosophy, which can vary considerably.There are cur ren t ly approximately forty-fourrecognized species of Recent planktonic Fora-minifera, of which twenty-one are common inthe world’s oceans (Hemleben et al., 1989),although some specialists recognize up to sixty-four for the total number (e.g. Saito et al., 1981).Data on the patterns of d i s t r ibu t ion of l iv ingplanktonic Foraminifera come from three mainsources: p lankton tows, sediment traps, andsediment-surface samples. Data derived fromplankton tows are vulnerable to methodologicaldiff icul t ies relating to the mesh size used inplankton nets. Berger (1969) showed tha t thereis an inverse relationship between the cube ofthe mesh size and the number of p lank ton ic

Introduction 105

One of the most powerful tools used in theinvestigation of biogeographic and paleobiogeo-graphic patterns is the transfer function. Thesefunctions relate species abundances to their lifehabitats (usually abundances in sediments arerelated to habitat conditions in the overlyingwaters), and the functions are normally appliedto the problem of estimating environmentalcharacteristics from species abundance data.Subject to several assumptions, any environ-mental parameter, say, temperature, can be pre-dicted. Perhaps the simplest and most directpredictive equation was proposed by Berger(1969):

where the optimum temperature preferenceof the ith species, is weighted by the species’proportional representation, yielding anaverage optimum temperature for the assem-blage. This equation has been further refined(see Berger and Gardner, 1975; Vincent andBerger, 1981), but even in its simplest form itcan yield surprisingly accurate results when usedto predict average sea surface temperatures.However, this approach alone cannot accountfor complex interaction between temperatureand other parameters that influence distribution,and requires an a priori understanding of theoptimum temperature preferences of species.

A more widely used transfer function is basedon empirically derived relationships between aspectrum of environmental parameters andspecies abundance data: it takes the form:

parameter, say, temperature, and A,B,C, etc. arevariables, which may be actual species propor-tions, synthetic variables consisting of groupedproportions (e.g. characteristic polar, tropical,etc. species), or variables derived from mult ivar i -ate analysis of species proportions. In this case,knowledge of the optimum environmental con-ditions for the species is replaced by a relation-ship usually derived from statistical regression.

Imbrie and Kipp’s (1971) classic work on Car-ibbean temperature f luctuat ion, for example,used factor analysis to extract synthetic vari-ables consisting of tropical, subtropical, subpo-lar, and ‘gyre margin’ assemblages, which showa partial correspondence to the large-scale lati-tudinal provinces discussed below. It is possibleto apply these synthetic variables to the deriva-tion of any environmental variable associatedwith the samples; they can also be used to esti-mate past environmental conditions (Imbrie andKipp, 1971; CLIMAP 1976, 1981; Thunell et al.,1994, among others). Useful reviews of the tech-nique can be found in Hutson (1977) , Sachset al. (1977) , and Vincent and Berger ( 1 9 8 1 ) .

Although the use of transfer functions hasyielded excellent results, the technique must beused with caution. The predictive value oftransfer functions based on recent sediment sur-face samples in a particular area is high whenapplied to recent environments in the sameregion, but complications arise when the func-tion is applied to spatially or temporally distantsamples. Relevant considerations include thefollowing:

( 1 ) The environmental preferences of extantspecies may not be the same wherever and when-ever they occur. For example, some bipolarspecies can show different environmental prefer-ences in different hemispheres. This could bebecause different l imit ing factors may act to con-trol abundance in different settings. Addition-ally, species habitat preferences may haveevolved through time, thereby diminishing thepredictive power of transfer functions used tocalculate past conditions based on present-daydistributions.

( 2 ) Present-day distr ibutions may not haveequilibrated. If they are still in a state of recovery

7.1.2.2 Transfer functions

greater representation in underlying sediments(Berger and Soutar, 1967; Berger, 1970a, Berger,1971). Current transport can displace livingadult individuals outside the limits of theirnormal reproductive range (McGowran et al.,1997).

where the are predictive coefficients (usuallyregression coefficients), P is an environmental

106

from recent environmental changes (e.g. a recentglacial phase or other shorter-term climaticpulse), then modern foraminiferal distributions(and their derived transfer functions) may notfully reflect either their historical habitat prefer-ences, or their modern preferences. For example,the limiting factor in recovery time may be thepresence of geographic barriers to repopulationrather than the ecological responsiveness of thespecies. Thus, continental positions (see below)can exclude species from occupying areas towhich they would otherwise be adapted.

( 3 ) Since these functions tend to be based onsea surface measurements and sediment samplesrecovered from depth, factors like changing sea-sonality and vertical depth distributions are nottaken into account.

( 4 ) Taphonomic effects such as preferentialdissolution, winnowing, and diagenesis must beassumed to be negligible. To whatever extentthese effects show temporal and spatial varia-tion, it is not accounted for in transfer functionsbased on the distribution of modern faunas insurficial sediments (Vincent and Berger, 1981).

( 5 ) In principle, there is nothing in the transfermethodology that prevents the prediction of anunlimited number of environmental variablesfrom a limited amount of paleontological infor-mation (‘transfer dilemma’ of Vincent andBerger, 1981). This is partly due to covariationbetween environmental variables. Transfer func-tion predictions may not be based on directcausal relationship between species distributionsand the environmental variable being predicted.If the causal relationship is secondary or indi-rect, then that indirect linkage may change geo-graphically or temporally even when the species’actual habitat preference is unchanged. Thisdilemma is a direct result of the methodologyand is ultimately a reflection of the fact thatcorrelation does not demonstrate causality.

(6) There may be some ancient environmentsfor which there are no modern analogs, andwhich are therefore not predicted by transferfunctions based on modern faunas (‘transfer par-adox’ of Vincent and Berger, 1981). In particu-lar, it is not valid to extrapolate beyond thelimits of the parameters used to in i t ia l ly estab-lish the transfer function.

( 7 ) The modern species upon which thetransfer function is based may not have sufficienthistorical range to allow application of the func-tion to older samples, part icularly samples thatpredate the first appearance of the mostrecently-evolved modern species tha t contributeto the transfer function.

Despite these problems, transfer functionsremain a valuable tool in environmental recon-struction. However, it should not be forgottenthat they are formulated to predict environmen-tal characteristics from biogeographic distribu-tion patterns rather than to address the reverseproblem of explaining biogeographic d is t r ibu-tions in terms of environmental parameters.

7.2 ECOLOGICAL FACTORSCONTROLLING THE DISTRIBUTION OFPLANKTONIC FORAMINIFERA

7.2.1

The tolerance l imits of most species are notsharply defined. Instead, departure from optimalconditions causes a gradational reduction oforganismal functionality, resulting in inhibitionof reproduction, nutr ient uptake, and growth,eventually leading to death. These effects can beboth interdependent and nonlinear; for example,an organism may require optimal temperaturesin order to tolerate extremes of hypersalini ty(Odum, 1971; Hedgpeth, 1957a). For a generaldiscussion of models dealing with the couplingbetween plankton and their physical environ-ment, see Eckman (1994) and references therein.For specific correlations of modern speciesabundances with C L I M A P data on specificenvironmental factors, see Hilbrecht (1996).

7.2.2 Temperature

7.2.2.1 Direct control

As a result of the general observation that themost conspicuous planktonic foraminiferal dis-tribution patterns are latitudinal, more researcheffort has focused on the influence of temper-ature than on any other single variable.

Biogeography of planktonic Foraminifera

Ecological factors controlling the distribution of planktonic Foraminifera 107

Some species show a change in the dominanceof coiling direction that appears to be temper-ature-dependent, although there is no knownkinetic reason that one handedness should bepreferred over another. Work on coiling direc-tion has touched on such interrelated topics asstratigraphic applications (Cosijn, 1938; Vasicec,1953; Nagappa, 1957; Bandy 1960), biogeogra-phy (Gandolfi, 1942; Ericson et al., 1954; Bandy,1959, 1960; Ericson, 1959), correlation (Ericsonand Wollin, 1968; Robinson, 1969; Olsson, 1970;Hofker, 1972), evolution (Bolli, 1950, 1951,1971), ecology and paleoecology (Vasicec, 1953;Ericson, 1959; Bandy, 1959, 1960; Loeblich andTappan, 1964a; Bé, 1977; Boltovskoy, 1966b,1969), and life history (Vella, 1974; Lipps, 1976,1979) without explaining the nature of the rela-tionship between temperature and coiling direc-tion. The history of this literature is summarizedin Bolli (1950, 1951), Loeblich and Tappan(1964a), Thiede ( 1 9 7 1 ) , Malmgren (1974) , Ken-nett (1976), Boltovskoy and Wright (1976), Srin-ivasan and Azmi (1978), Lipps (1979), Vincentand Berger (1981) , and Hemleben et al. (1989).

Recent work by Lohmann and Schweitzer(1990) provided concrete evidence that Lipps’(1976, 1979) focus on reproductive strategymight be appropriate, at least in the case ofGloborotalia truncatulinoides. They discussedhandedness-correlated variation with twofactors in G. truncatulinoides: (1) the timing ofdescent from surface waters, and ( 2 ) the conse-

quent depth (especially in relation to thethermocline) at the time of gametogenetic calci-fication and reproduction. Specifically, a shallowthermocline seems to have a negative effect onthe reproductive success of G. truncatulinoides,possibly due to interference from a correlatedhydrographic gradient such as the pycnocline.Since sinistral individuals descend from the sur-face waters earlier in their life cycle, they arelikely to descend to greater depths and, if thethermocline is too shallow, may find themselvesbelow the depth at which seasonal overturn willreturn juveniles to the surface for another repro-ductive cycle. This selects against sinistralindividuals, leaving an increase in the relativefrequency of dextral individuals. Lohmann andSchweitzer point out that this is not a full expla-nation of the relationship between temperatureand handedness, since the effect shows size-dependence even wi th in samples (Thiede, 1971).Schweitzer and Lohmann ( 1 9 9 1 ) showed a sim-ilar relationship between reproductive successand the depth of the pycnocline in menardiiformgloborotaliids.

Lohmann (1992 ) suggested that the apparentbiogeographic relationship between coilingdirection and sea surface temperature may bean indirect result of the fact that the deepestmixing generally happens in late winter in mostparts of the ocean, and is intensified at higherlatitudes where temperatures are lower. He sup-ports this hypothesis with the observation thathandedness dependency persists in the Mediter-ranean where temperature and deep mixing aredecoupled.

7.2.2.2 Temperature and the biogeography ofcoiling directions

Some of the most convincing evidence fordirect control of temperature over distributioncomes from the experimental work of Bijmaet al. (1990). Their results showed a correspon-dence between in vitro temperature tolerancelimits and the known natural limits of theirexperimental species. Vital functions like foodacceptance, growth, and reproduction wereinhibited when natural temperature limits wereexceeded, providing compelling evidence thattemperature may be an important factor in con-trolling individual species distributions.

7.2.2.3 Temperature and the biogeography ofpore size

Bé (1968) reported that porosity was highest intropical and surface-dwelling species (Fig. 7 .1) .Scott (1972) suggests tha t this might imply ahydromechanical funct ion for pores, since thereduced density and increased buoyancy thataccompany increased porosity would retardsettling rates in high-temperature low-densityhabitats; this inference is supported by experi-mental results of Bijma et al. (1990); also see

108

Planktonic Foraminifera are intolerant of brack-ish water. The lowest salinity in which livingspecimens have been captured is about 30‰(Bol tovskoy, 1976). The species most tolerantof hyposaline conditions in na tu re are reportedto be Globigerina bulloides, G. quinqueloba, Globa-

boquadrina pachyderma (f. superficiaria), andOrbulina universal these species have been reco-vered from waters having salinities of 30.5 to31‰ (Bé and Tolderlund, 1971). Neogloboquad-rina dutertrei is also associated wi th re l a t i ve lylow salinities, and shows abundance peaks dur inglate Cenozoic episodes of Mediterranean sapro-pel deposition, which were probably caused bystagnation-induced glacial mel twater sp i l loverfrom the Black Sea (Thunell et al., 1977). Bijmaet al. (1990) studied sa l in i ty tolerances of someplank ton ic species in laboratory cu l tu re andfound that the in vitro salinity tolerance limitsare greater than those found in nature , w i t hGlobigerinoides ruber showing the greatest toler-ance range (22 to 49‰). They concluded thatna tu r a l s a l i n i t y var ia t ion in the open ocean isunlikely to exert signif icant control over thedistribution of modern planktonic Koraminifera.

Kennett ( 1 9 7 6 ) for additional discussion. Fur-bish and Arnold (1997) have investigated thefunctional morphology of hydrodynamicalproperties in spinose planktonic Foraminiferawith specific attention to the determinants ofsett l ing velocity. Since there is a construct ionalconstraint relating pore size and spacing to spinenumber, it follows that these characters mayhave a funct ional or constructional inter-relationship. This possibility has not beeninvestigated.

It is clear that temperature is not the onlyfactor controll ing species d is t r ibu t ions . Forexample, even though temperatures in the deepsea are uniformly low, deep sea benthic taxo-nomic diversity is comparable to diversity levelson tropical shelves. Other factors must beconsidered.

In general, foraminiferal abundance patterns aresimilar to those of other groups that are believedto reflect primary product iv i ty (Bé and Tolder-lund, 1971; McGowan, 1971) . Product ivi ty islargely determined by photic levels and n u t r i e n tsalts, especially phosphate, available to phyto-plankton (Parker, 1960; Ryther, 1963; Berger,1969). A l t h o u g h most research on p l a n k t o n i cforaminiferal abundance has shown correlationswi th phytoplankton product iv i ty and nut r ien tlevels (e.g. Hemleben et al., 1989; Fairbanks andWiebe, 1980; Ravelo and Fairbanks, 1995), thereis evidence tha t the re la t ionship may not be asimple one. For example, Oberhänsli et al.(1990) have shown tha t s tanding stocks can behighest where primary production is intermedi-

7.2.3 Salinity

7.2.4 Nutrients and geographic variation inabundance


igerinita uvula, Globigerinoides ruber, Neoglo-

Ecological factors controlling the distribution of planktonic Foraminifera 109

ate, suggesting the correlation may be nonlinear.Additionally, small-mesh tows correlate withphosphate levels while larger-mesh tows do not(Berger, 1969).

Quanti ta t ive comparisons of absolute abun-dances between studies are often problematicdue to the variation introduced by samplinggear (see section 7.1.2.1). For these reasons, it isbest to discuss abundances in relative terms.Abundances tend to be relatively lower in oligo-trophic high-salinity central basin waters w i t hweak circulation, such as are found in the Northand South Atlantic and Indian Oceans; higherabundances tend, in general, to be found inmajor current gyres, equatorial and West WindDrift, currents, upwellings, and frontal systems.Numerically, planktonic Foraminifera can rangefrom 1.3 to 9.9% of the total zooplankton, rank-ing sixth in winter (after copepods, chaeto-gnaths, tunicates, kril l , and siphonophores,respectively) and third in summer, and some-times achieving local dominance even over cope-pods. However, their small body size means theforaminiferal biomass contr ibution is less sig-nificant than their numerical abundance (Bol-tovskoy and Wright, 1976).

Some of the highest concentrations of Fora-minifera are found in the North Pacific, northof the central water mass (Bradshaw, 1959;Berger, 1969: Bé and Tolderlund, 1971; Spindlerand Dickmann, 1986), where plankton abun-dances are three orders of magnitude greaterthan those in the Sargasso Sea. Indo-Pacificabundances are a factor of two greater thanthose of the Atlantic ocean, although the relat ivepattern of accumulation rates are reversed, sothat there appears to be a negative correlationbetween standing stock and shell depositionrates (Berger, 1969). Berger also noted that con-centration maxima for small-mesh tows arefound in high latitudes, while large-mesh towsshow their concentration maxima at low lati-tudes, and suggested that this may be due toaccelerated reproductive rates in areas of highproductivity, which results in steeper size-fre-quency distributions. Regardless of the steepnessof the size-frequency distribution, its exponentialnature implies that there are many more juve-

niles than adults, and is consistent wi th the gene-ral expectation of high juveni le mortal i ty andconcave-upward survivorship curves.

The highest measured oceanic abundances(greater than specimens per ) occurin major current systems, boundary currents,divergences, and upwellings. Depauperatestanding stocks (less than specimens per

) are found in central waters of oceanicbasins and over continental shelves (Bé, 1977),although slope waters have been reported wi th

specimens per ( C i f e l l i andSmith, 1969). Some of the highest abundancesreported have been ofsmall, juvenile Neogloboquadrina pachyderma,probably living, recovered from melted Antarc-tic annual sea ice (Lipps and Krebs, 1974; Lipps,1979; Spindler and Dickmann. 1986). and byBerger (1969) who reported abundances as highas per for small-mesh tows,although these abundances should not be com-pared due to differences in sampling techniquediscussed by Berger (1969). Berger (op. cit.), andBoltovskoy and Wright (1976) provide usefuldiscussions of abundance var ia t ion .

7.2.5 Water depth and biogeography

Although there is considerable literature on thedepth distr ibut ion of planktonic Foraminifera,the following discussion focuses on those aspectsof depth distr ibut ion that influence biogeogra-phy of the group. L iv ing planktonic Foramini-fera have their maximum abundance in euphoticnear-surface waters between 10 and 50 meters(Fig. 7.2), below which depth they show anapproximately) exponential decline in abundance(Be, 1977). This pattern correlates with theabundance of nutrients, prey, and (for those withphotosymbionts, e.g. Globigerinoides sacculifer)sunlight (Bi jma and Hemleben, 1994). Thedepth habitats of i n d i v i d u a l species can seldombe defined w i t h i n narrow l imits because theyshow diurnal, ontogenetic, seasonal, and long-term var ia t ion that is beyond the scope of moststudies to ful ly document. Bé ( 1 9 7 7 ) consideredthree broad groups on the basis of their depthdis t r ibut ion. The f i rs t consists of shallow-water

104–10

5

110 Biogeography of planktonic Foraminifera

species, primarily spinose forms including allspecies of Globigerinoides and several of Globi-gerina. These species tend to be thinner-walledand smaller than deeper-dwelling forms. Bé’sintermediate water depth assemblage, whosespecies live predominantly in the 50 to 100 meterdepth range, consists of both spinose (Globiger-ina bulloides, Hastigerina pelagica, Orbulinauniversa, Globigerinella aequilateralis, andGlobigerina calida) and non-spinose forms(Pulleniatina obliquiloculata, Neogloboquadrinadutertrei, Candeina nitida, and Globigerinita glu-tinata.) Bé’s deep water assemblage includes thespinose Hastigerinella digitata, which possibly isunique in that it may spend its entire life cyclebelow 1000 m. The remaining 12 species in Bé’sdeep water assemblage all live in the euphoticzone as juveniles but are found mainly below100 meters as adults. These include two addi-tional spinose forms, Globigerinella adamsi andSphaeroidinella dehiscens, the non-spinose Neo-globoquadrina pachyderma and G. conglomerataand all the species of Globorotalia.

Depth often shows a relationship to the distri-bution patterns of living planktonic Foramini-fera, but depth-correlated factors such astemperature, salinity, dissolved oxygen, photicconditions, and nutrient levels are probably thedirect controls over foraminiferal depth habitats.

In nearshore environments, however, the influ-ence of depth can persist even when physico-chemical conditions are equivalent to an openmarine setting. Planktonic Foraminifera areoften undersized, and usually sparsely distrib-uted in shelf waters; this is especially true ofinner shelf environments on broad continentalshelves where they may be entirely absent (Sai-dova, 1957; Lipps and Warme, 1966; Boltov-skoy, 1976; Wang et al. 1985).

Bandy (1956) pointed out that the character-istic depth habitat of some species may precludetheir survival in shallow waters. This could bedue to a relationship between the life cycle andenvironmental gradients like the thermocline(Lohmann and Schweitzer, 1990; Schweitzer andLohmann, 1991), the pycnocline, or the chloro-phyll maximum (Hemleben and Bijma, 1994),rather than to the absolute magnitudes of tem-perature, salinity, and productivity in nearshoreenvironments. In species that depend on sea-sonal overturn above the thermocline for suc-cessful completion of their life cycle, the depthof the thermocline – or even its existence wherebathymetry intervenes in the shelf environment– may play a role in determining vertical andhorizontal abundance and distribution. This issupported by Orr’s (1967) finding that the intra-specific proportion of adult pregametogenicspecimens of some species found in surficial sedi-ments shows a discontinuity at depths that canbe related to the species’ life cycle.

If Orr’s finding is the general case, then inter-specific variations in shoreward distributionmay be understood in terms of the bathymetryof their respective reproductive cycles. As Hem-leben et al. (1989) have pointed out, historicalchanges in biogeographic distribution patternscannot be fully understood until a fuller knowl-edge of foraminiferal depth habitats is devel-oped. Of course, for extinct species, suchknowledge must rely on the indirect evidence ofbathymetry and light isotopes.

Although it is possible in principle to inferthe vertical habitat distribution of planktonicForaminifera from their light isotope composi-tion (Savin and Douglas, 1973; Grazzini, 1976;Fairbanks et al., 1980; Fairbanks, 1982; Deuser,

Large-scale distribution patterns 111

1987; Spero et al., 1991; Sautter and Thunell,1991; Spero and Lea, 1993; Ravelo and Fair-banks, 1992, 1995; Hemleben and Bijma, 1994;van Eijden, 1995), and ranked depth stratifica-tions have been developed on that basis, it isalso clear that ontogenetic changes in depth

tosymbionts and gametogenic calcification)complicate the interpretation of isotopic data –a complication that is compounded whenextrapolated into the fossil record (e.g. Shack-leton et al., 1985; Lohmann and Schweitzer,1990; Corfield and Cartilidge, 1991; D’Hondtet al., 1994; Kelly et al., 1996; see alsochapter 14).

Having enumerated the main factors influ-encing planktonic foraminiferal distributions,we will now discuss the effects they have onbiogeographic patterns. This discussion is(somewhat arbitrarily) divided into large, meso-,and small-scale patterns.

7.3 LARGE-SCALE DISTRIBUTIONPATTERNS

7.3.1 The global diversity gradient andlatitudinal provinciality

7.3.1.1

Perhaps the single most conspicuous aspect ofthe Earth’s biosphere is the global latitudinaldiversity gradient, a gradient that embraces vir-tually all taxonomic levels. Wallace (1878) drewattention to the phenomenon, and Murray(1897) became the first to discuss latitudinalgradients in the planktonic Foraminifera. Sincethat time, eight large-scale biogeographic prov-inces have been identified that are symmetricallydisposed about a ninth tropical province (Figs.7.3, 7.4). Although various authors differ on theexact positions of provincial boundaries, andsome have added details that reflect smaller-scale hydrography (e.g. McGowan, 1974; Hem-leben et al., 1989), the overall picture of latitudi-nal provinces and the diversity gradient thatspans them is consistent with patterns seen inthe remainder of the world’s biota (McGowan,

1971). These large-scale patterns have been thecentral theme in most surveys of planktonicforaminiferal biogeography. The reader isreferred to Bradshaw (1959), Bandy (1964),Belyaeva (1969), Bé and Tolderlund (1971), Bol-tovskoy and Wright (1976), Bé (1977), Bé andHutson (1977), Lipps (1979), Olsson (1982), andHemleben et. al (1989) for useful summaries.Pianka (1966) provides a useful general discus-sion of the phenomenon.

7.3.1.2 General features of latitudinal provinces

These nine large-scale provinces do not mapsystematically onto clearly defined physico-chemical oceanographic properties (Williamset al., 1968; Backus, 1986), or onto planktonicsurface-water distributions (Ottens, 1991), withthe result that provinces are easier to describethan explain. Diversity shows a monotonicdecrease from about 20 species (ten indigenous)in the tropical province to about 5 (one indige-nous) in the polar regions, with few species beingrestricted to a single province (Fig. 7.3). Cold-water faunas are somewhat less diverse in thenorth than in the south, possibly because of therelatively restricted circulation in the Arctic(Bé, 1977).

The high-latitude provinces tend to be longi-tudinally continuous and faunally uniform dueto a relative lack of continental barriers, butlower latitude provinces are interrupted, mostconspicuously by the Americas, with the resultthat faunal differences are most pronouncedbetween the low-latitude provinces of the Atlan-tic and the Eastern Pacific (Fig. 7.4).

Bé (1977) has drawn attention to the fact thatthe ratio of indigenous to total species found inthese nine provinces is lowest in the transitionalzone where only Globorotalia inflata is consid-ered to be indigenous. This observation tendsto characterize the transitional zone as an areaof overlap between higher and lower latitudespecies distributions, and suggests that thenumber of large-scale functional ecosystemsmay be smaller than the number of provincesthat can be delineated on the basis of foramini-feral distribution patterns.

habitat and vital effects (including those of pho-

112

Superimposed on this first-order provincialityis a second-order pattern that correlates moststrongly with currents, frontal systems, andupwellings (e.g. Ottens, 1991), effects that aremost strongly developed in the temperatethrough tropical provinces. Subtropical prov-

most strongly developed along western bound-aries (Gul f Stream, and Kuroshio current in thenorth, Brazil Current, Mozambique-AgulhasCurrent, and East-Australian Current in thesouth) and it is in these areas that provincialdistortion is most apparent (e.g. McGowran

inces, for example, tend to include a significantnumber of species (four of twelve) associatedwith upwellings and boundary currents. Currentgyres also distort the la t i tudinal orientation oflow-latitude faunal provinces by transportingequatorial species poleward in clockwise north-ern hemisphere gyres and in counterclockwisesouthern hemisphere gyres. These currents are

et al., 1997). Similarly, high lat i tude species arecarried equatorward by the Labrador, Portugal-Canaries, Oyashio, Benguela, and CaliforniaCurrents (Fig. 7.5).

The geographic disposition and species com-position of these provinces have been charac-terized in contexts ranging from broadlatitudinal and provincial summaries (Figs. 7.3.



7.4) to more detailed species-by-species docu-mentation (e.g. Bé. 1977; Hilbrecht, 1996). Thelatitudinal character of these provinces and ofthe diversity gradient implies that temperatureplays a dominant role in their disposition,although that role is probably indirect (Cifelli ,1971, but see Stehli et al., 1969, 1972). Likelycandidates for more direct influence wouldinclude temperature-correlated phenomena likeproductivity (Ortiz et al., 1995) and the la t i tud i -nal distr ibution of hydrographic barriers to geneflow. Lipps (1979) listed six hypotheses thatrelate temperature, sal inity, circulation patterns,water masses, ecosystem cores/ecotones, andenvironmental stabili ty/predictabili ty to plank-tonic foraminiferal provinciality, but concluded

that these hypotheses are more useful as toolsin paleoecological inference than as explana-tions for foraminiferal dis t r ibut ion patterns.

7.3.2 The historical development of the globaldiversity gradient

7.3.2.1

Early classic works l ike those of Stehli et al.(1969) and Stehli et al. ( 1 9 7 2 ) analyzed largescale biogeographic patterns from relativelyrestricted data bases. Recent workers such asWei and Kennet t (1983. 1986). Stanley et al.(1988) . Norris (1991a) , and Parker et al. ( i npress), have taken advantage of global compen-

114

dia like Kennett and Srinivasan (1983) , Blow(1979) , and Olsson et al. (1999) to relate paleo-biogeography to macroevolutionary patterns ofspeciation and ext inct ion as well as to morphol-ogy, life history, abundance, taxonomic affilia-tion, and paleoceanographic change.

It is clear that the well-developed global lati-tudinal diversity gradient seen in the Globigeri-nida has not been a static feature throughoutthe Cenozoic; rather, it is the cont inuing culmi-nation of the last great i terative phase of thegroup’s evolut ionary history (Cifel l i . 1969;Norris, 199la). Latitudinal environmental gradi-ents, and their consequent foraminiferal diver-sity gradients, were clearly much less steep inthe early Paleogene (Olsson, 1982; Boersma andPremoli Silva, 1983, 1991; Olsson et al. 1999)but the speciation/extinction patterns that accom-pany this transition are not well understood.

In foraminifera l studies Stanley et al. (1988).Norris ( 1 9 9 1 a ) , Feldman et al. ( 1998) , andParker et al. ( i n press) confirmed the geographicpa t te rn ( 1 , above) in Neogene p lanktonic Fora-minifera. Stehli et al. (1972) found indirectgeneric-level evidence of high tu rnove r amonglow latitude Foraminifera, but was unable tof ind similar evidence at the species level, possiblybecause of a decoupling between species andhigher-level taxic behavior (Arnold, 1982). Stan-ley et al. (1988), Norris ( 1 9 9 l a ) , Feldman et al.(1998) , and Parker et al. ( i n press) later con-firmed a pat tern (2 above) of higher species t u r n -over among low-lat i tude Foraminifera.

The causes of these pat terns were subse-quen t ly pursued by Wei and Kenne t t , (1986) .Stanley et al. ( 1 9 8 8 ) . Nor r i s (1991b . 1992).and Parker et al. ( i n press), who. in var iouscombinat ions , examined the re la t ionshipbetween d ivers i ty and factors such as mor-phology (keeled vs. unkeeled, spinose vs. non-spinose), taxonomic aff i l iat ion (within-cladespecies t u r n o v e r ) , geographic range (cosmo-poli tan vs. endemic), populat ion size (domi-nance), patchiness (occurrence in u p w e l l i n g ) ,depth d i s t r i bu t ion , biology ( symbion t re la t ion-ships and life cycle), l a t i t u d i n a l occurrence(most poleward e x t e n t ) , and l a t i t ud ina l v a r i a -tion in provinc ia l i ty . Tracing pat terns of caus-a l i t y among these factors despite ex t ens ivecovariat ion has been a central issue in theseworks. The results tend to support Stehli’searl ier work, and are f u r t h e r consistent w i t hthe expectation (Fisher , 1930; Wright , 1942)tha t the l imi ted possibil i t ies for genetic isola-t ion in widespread, a b u n d a n t cosmopolitanpanmict ic popula t ions may retard microevolu-t ionary rates and suppress speciation at highlati tude.

7.3.2.3 Speciation and extinction rates

Stehli et al. ( 1969) discussed taxonomic surv i -vorship, endemicity, and la t i tud ina l diversitytrends in Permian brachiopods, modern Bival-via, and Cretaceous planktonic Foraminifera,and noted two s t r ik ing patterns:

( 1 ) a lack of endemic taxa at high lati tudes(cold-water assemblages tend to be comprisedalmost exclusively of cosmopolitan species;Fig. 7.6); and

( 2 ) turnover rates among low-lat i tude groupsare higher than among high-lat i tude taxa (sug-ested by patterns of taxonomic survivorship) .

7.3.2.4 Biogeographic change during speciation

Superficial ly, it would seem reasonable to expecttha t dur ing lineage diversif ication, species wouldoriginate locally and then expand their biogeo-graphic ranges in to increasingly broad biogeo-graphic provinces. However, on the average.Neogene speciation events tend to result in a

7.3.2.2 The ecological role of temperature

Stehli et al. (1972) advanced the hypothesis tha tthe la t i tud ina l diversity gradient is driven bythermal control of two factors: greater ease ofentry into low-latitude niches, and an equator-ward increase in niche space. The latter factorcould be related to intensified vertical stratifica-tion at low latitudes (Lipps, 1970), an equator-ward increase in local upwelling (Stanley et al.,1988), or to an equatorward gradient in thetrophic resource continuum (Hal lock, 1987).The effect of historical changes in temperaturewill be discussed in section 7.3.2.5.



statistically significant reduction in geographicrange (Parker et al., in press). This observationimplies that the development of biogeographicpatterns may proceed from relatively cosmopoli-tan ancestors that speciate by specializing andexploring increasingly geographically restrictedniches. Indeed, it is established that the Cenozoiciterative diversifications did originate fromrelatively cosmopolitan, ‘primitive’ globigerineancestors (Cifelli, 1969; Norris, 1991a). A ten-dency toward geographic specialization mightbe verified by examining changes in distributionpatterns over the geologic history of species, butthe existing comprehensive compendia on fora-

miniferal distribution patterns do not providesufficient stratigraphic and geographic detail.However, Jenkins (1992) examined a restricteddata set and found a pattern of retreat towardthe tropics prior to extinction; if this patternholds for pseudoextinctions, then Jenkins’pattern has general implications for the biogeog-raphy of evolution as well as extinction (see alsoVermeij, 1989). Note that Hunter (1985), Hans-ard (1994), and Lazarus et al. (1995) have foundcladogenesis to be accompanied by reducedabundances, although the generality of thisobservation and its biogeographic implicationshave not been assessed.

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For most of geologic time, global climates havebeen warmer than they are at present; themodern widespread cold-temperate and arcticregions developed as a result of Late Cenozoiccooling. If the world has been warm nearlyeverywhere for much of its history, then Darling-ton’s (1959) classical view of low latitudes ascenters of radiation may lose its meaning (Stan-ley, 1979). This suggests that an examination ofNeogene cooling might be useful in understand-ing latitudinal provinciality. Thunell and Belyea(1982) have shown that Neogene Atlantic plank-tonic foraminiferal provinces shifted dramati-cally in the Middle Miocene and Late Plioceneduring the development of the East AntarcticIce Sheet and the initiation of the northern hemi-sphere ice sheets. At these times there wereequatorward migrations of cool, high-latitudeprovinces and accompanying contraction oflow-latitude provinces. Berggren and Hollister(1974) and McIntyre et al. (1972) noted that thepolar front has swept back and forth dur ing the

last 250 ky, al ternately compressing and expand-ing the tropics at least six times. The exponentialna ture of rediversification during each recoverywould tend to enhance the diversi ty gradienteven if fractional (pe r - t axon) rates of speciationwere latitudinally invariant. This is because (allother things being equal ) a biota wi th largerinitial diversity will have a faster rate of a r i th -metic growth, since diversification starts on asteeper part of the exponential growth curve(Stanley, 1979).

Stanley (1979) also emphasized that globalcooling events might be expected to cause higherextinction rates among tropical species, a predic-tion tha t is consistent wi th many observedextinct ion patterns, and a prediction later veri-fied in the Foraminifera (Stanley et al., 1988).This model carries the corollary that the distri-but ions of surviving low-lat i tude species shouldbe compressed equatorward during coolingevents (e.g. Thunel l and Belyea, 1982), which intu rn implies tha t subsequent recovery should becharacterized by reradiation from the tropics, aprocess tha t could, in itself, ma in ta in a l a t i tud i -nal diversity gradient even if the number ofniches were not la t i tude dependent. This is con-sistent with Jenkins’ (1992) observation of equa-torward biogeographic contraction prior toextinction.

Lipps (1970) emphasized the effect of sea sur-face temperatures at high lati tudes on verticaland horizontal thermal gradients. Lipps pro-posed a model suggesting tha t dur ing times ofpolar warming the absence of steep thermal gra-dients eliminates barriers that otherwise main-tain species diversity through genetic isolationand allopalry; conversely, the potential for speci-ation would be greatest when the effectivenessof thermal barriers to gene flow is enhanced bystrong localized thermal gradients caused byhigh- la t i tude cooling. Lipps’ hypothesis impliesthat Stanley’s (1979) ‘crucible of speciation’ maybe the polar front or temperate region (wheregradients would be steepest) rather than thetropics. Detailed information on the geographicdis t r ibut ion of strat igraphic first appearancesmight provide a means to test this hypothesis.

Lohmann and Schweitzer (1990) have pre-

7.3.2.5 Late Cenozoic cooling and latitudinalspecies distributions



sented evidence suggesting that the position ofa different gradient, the thermocline, may playa key role in determining the differential repro-ductive success of subpopulations of Globorot-alia truncatulinoides. Hemleben et al. (1989)have pointed out that the pycnocline and thechlorophyll maximum can play a similar role,and may act as barriers to gene flow during thespeciation process. This raises the possibilitythat the lack of a well-developed thermoclinecharacteristic of polar regions may be a keyfactor in suppressing speciation in those areas.It would then follow that equatorward move-ment of the polar front should suppress specia-tion over a broader area. Additionally, Wei andKennett (1986) suggest that increased provinci-ality during the development of polar ice maydrive the diversification process, especially in thegloborotaliids; it is also established that lati-tudinal provincialization became more devel-oped during times of polar cooling (Thunell ,1981).

miniferologists, for it is in this group that wehave the stratigraphic and phylogenetic controlto resolve the issue.

Hedgpeth (1957b) and Lipps (1979) have dis-cussed several hypotheses to explain bipolarity,including submergence, a phenomenon in whichextra-tropical cool-water species stay withintheir preferred thermal conditions by living indeeper waters at lower latitudes. The generalform of this explanation appears to be valid inthe analogous context of some antitropical plantspecies that are found in high altitude tropicalsettings (Thorne, 1972). Although submergencehas been observed in Globorotalia menardii(Hemleben et al.. 1989), Globigerina bulloides,Globorotalia inflata, and a few other cold-tem-perate and cold water species (Boltovskoy,1971b), the phenomenon is unlikely to explainbipolarity, because other limiting habitatrequirements (such as photic and nutrient levels)are not satisfied in the tropics where ideal ther-mal conditions may only be found in deeperwater.

Bipolarity might also be the result of migra-tion from more equatorial provinces into contig-uous higher-latitude water masses, or the resultof dumbbell allopatry during warming trends(McGowan, 1971; Lazarus, 1983). An additionalhypothesis explaining bipolarity suggests it is ahistorical vestige of dissection of a previouslycontinuous distribution by post-glacial warmingin the tropics, with sufficiently frequent mixingbetween latitudinally disjunct populations tomaintain genetic continuity (Bé , 1977; Bé andTolderlund, 1971).

7.3.3 Antitropicality and bipolarity

Most cool-water planktonic foraminiferalspecies, including Neogloboquudrina pachy-derma, Globigerina bulloides, and Globorotaliainflata, occur in latitudinally delineated biogeo-graphic provinces separated by equatorial watermasses (Figs. 7.3, 7.4). This can also be true ofmorphotypes – specifically coiling direction – ofsome species (e.g. Neogloboquadrina pachyderma,Globorotalia truncatulinoides). Bipolarity hasbeen the subject of investigation since the mid19th century (Hooker, 1847), and in extantgroups is usually considered to be the result ofrelatively recent Plio-Pleistocene cooling. Thefact that the phenomenon can be detected as farback as the Early Jurassic does not require thatpresent bipolarity is of ancient origin. However,the subfamilial level of differentiation in someliving bipolar mollusca suggests the phenome-non may be the result of considerable evolution-ary history (Crame, 1993). The question ofwhether bipolarity should be interpreted in aframework of vicariant evolution or dispersalhistory is deserving of closer scrutiny by fora-

7.3.4 Continental positions

High latitude foraminiferal provinces tend tohave lateral continuity. At lower latitudes, how-ever, continuity is interrupted by land masses,particularly the Americas. The Pliocene closureof the Isthmus of Panama isolated Atlantic andPacific tropical faunas and led to their indepen-dent faunal development. Today, Globigerinellaadamsi, Globoquadrina conglomerata, Globorota-loides hexagonus, Globorotalia menardii neo-f l exuasa , and Globorotalia theyeri are confined

118

to the Indo-Pacific (see Vincent and Berger.1981; Bolli and Krasheninnikov, 1977; Bé, 1977;Thompson et al., 1979), and pink Globigeri-noides ruber has disappeared from the Indianand Pacific Oceans (Thompson et al., 1979).Additionally, coiling directions in Pulleniatinaobliquiloculata cease to correlate between theAtlantic and Pacific basins after the develop-ment of the Isthmus of Panama (Saito, 1976).

In general, low-latitude species that evolvedbefore the development of the Isthmus tend toshow a more continuous circumglobal distribu-tion than late-evolving species. For example, sev-eral descendants of Globorotalia cultrata thatevolved after the Pliocene are restricted to theAtlantic basin (Vincent and Berger, 1981; Schott,1935). Globorotalia cultrata itself disappears fromthe tropical Atlantic during glacial times (Schott,1935; Vincent and Berger, 1981; Morin et al.,1970), and populations only become reestablishedin the Atlantic basin when the 18 C isothermmoves poleward of southernmost South Africa,thus allowing the species to circumvent the conti-nental barrier at high southern latitudes. Theserepopulation events are discussed by Thompsonet al. (1979), Ericson and Wollin (1968). andSchweitzer and Lohmann (1991) .

7.4 MESO-SCALE DISTRIBUTION

For example, Stanley et al. (1988) suggest tha thigher taxonomic tu rnover in globorotaliids isprobably related to the i r generally discont inu-ous distribution, possibly because many arefound in areas of ( low to mid - l a t i t ude ) upwel l ingand are symbiont-barren. Since smaller, morelocalized populations w i l l have a greater l i k e l i -hood of genetic isolation and greater vu lne rab i l -ity to localized change, sub-provincial ecologicaldiscontinuit ies are of par t icular interest for the i rpotential influence on speciation, ext inct ion, andt u r n o v e r rates, and, a temperature-mediated lat-i t u d i n a l gradient in envi ronmenta l patchinessmight be a more immediate cause of low- l a t i t udespeciation rates than temperature itself.

Boltovskoy ( 1 9 7 6 ) also presented an analy-sis of planktonic distr ibution patterns thatcontrasts sharp ly w i t h the firs t-order global-scale l a t i t u d i n a l zonations. He focused onlocalized phenomena such as upwel l ing , pecu-liar hydrographic condit ions, and complicatedcur ren t gyres, belts, f ronts , and tongues ofconverging water masses for his exp lana t ionof p l ank ton i c foramin i fe ra l d i s t r i b u t i o n pal-terns in the waters surrounding South Amer-ica. While he does not deny the existence oflarger scale global pat terns. Bol tovskoycontends tha t they are not, in themselves, anadequate framework for unders tand ing thebiogeography of p lank ton ic Foraminifera . Thisperspective is reinforced by Wang et al. ( 1 9 8 5 ) ,Ottens ( 1 9 9 1 ) , Ottens and Nederbragt ( 1 9 9 2 ) ,and Hilbrecht (1996), among others; theirwork provides clear evidence that it is at th i sscale that faunal discontinuities are most read-i l y related to hydrographic boundaries .

There are indicat ions that Boltovskoy’s focuson hydrographic detail may have critical explan-atory value as our unders tanding of speciationin the p l a n k t o n develops. One of the most prob-lematic aspects of foraminiferal evolution is themechanism of genetic isolation in the pelagicrealm. Lipps (1970, 1979), McGowan ( 1 9 7 1 ) ,Lazarus ( 1 9 8 3 ) , and others have noted the l im-ited potential for allopatric speciation in large,panmictic populations of planktonic Foramini-

7.4.1

Although large-scale foraminiferal biogeo-graphic provinces are relatively simple andmonotonous by comparison with similar-sizedterrestrial provinces (McGowan, 1971) , they arenot devoid of small-scale structure. Research onregional and local-scale variation in distributionpatterns has revealed them to be more thanmere high-resolution details of the known large-scale patterns; instead, they arise from distinctsmaller-scale oceanographic phenomena andhave different implications for evolution, diver-sity, and biogeography. Thus, the key to under-standing large-scale dis t r ibut ion patterns maynot be found in comparably large-scaled phen-omena, but in the cumulat ive effect of smaller-scale phenomena which themselves may showsystematic latitudinal variation.

7.4.2 Genetic isolation


Meso-scale distribution 119

fera. In this regard it may be relevant that asignificant number of species that Boltovskoydescribes in his South American biogeographicstudies are not among the widely recognizedRecent species (e.g. Globigerina diplostoma, G.juvenilis, G. radians, G. rosacea, G. subcretacea,G. trilocularis, Globigerinoides cyclostomus, G.suleki, Globorotalia canariensis, G. punctulata, G.seiglei, and Hastigerina involuta, among others;Boltovskoy, 1976; see also Rögl, 1985). Boltov-skoy mentions that many of these species arefound only in restricted areas as isolated speci-mens, which raises the possibility that theseareas may be the genetically isolated ‘cruciblesof speciation’ discussed by Stanley (1979). Suchareas might be expected to produce many short-lived species, most of which never become estab-lished on a global scale. Generally speaking,past micropaleontological awareness of specieshas been biased by a focus on their utility astools for stratigraphic correlation; consequently,rare, restricted, and short-lived species havebeen frequently overlooked as isolated oddities.A closer examination of the biogeographic dis-tribution of these ‘oddities’ may provide valu-able clues in understanding mechanisms ofspeciation in the plankton, and the geographicdistribution of these ‘crucibles’ may have bio-geographic implications. Suggested avenues ofresearch might include a comparative study ofmorphologic variability in these hydrographi-cally distinct areas versus other areas in theopen ocean, or a study of the stratigraphic conti-nuity of these unusual forms in relation to thehistory of their restricted habitats.

However, even at this scale, it is not clear thathydrographic discontinuities are effective geo-graphic barriers to gene flow. Ottens’ (1991)study of various Atlantic fronts and currentsfound that the faunal boundaries betweenclearly-defined water masses coincided withintervening hydrographic frontal zones. Thesefrontal boundaries were characterized by a high-diversity, low-equitability ecotonal fauna thatshared species of both adjoining water masses.The highly gradational nature of these ecotoneswas supported by multivariate analyses suggest-ing that foraminiferal populations were more

intergradational than the water masses theyinhabited.

One question that arises in the context of meso-scale circulation patterns is the effect of direc-tional advection/diffusion on the distribution ofthe species that inhabit transition zones. Olson(1986) draws attention to the question of howGloborotalia in f la ta maintains itself in the faceof a net eastward flow in the south Atlantic –specifically, how individuals are recruitedupstream to maintain the population againstadvection. Olson describes three smaller-scalemechanisms: westward transport by upstreammovement of eddy fields, recirculation cells asso-ciated with western boundary currents, and themaintenance of a region of prolonged residenceat the upstream extremity of the eastwardadvection.

This field is just beginning to influence ourunderstanding of the planktonic Foraminifera.It appears that intraspecific genotypic variationmay be seen on roughly the same spatial scaleas mesoscale hydrographic features; however,beyond drawing attention to the potential rela-tionship with genetic isolation and speciation, itwould be premature to speculate on the signifi-cance of this observation. Darling et al. (1998a)have examined various water masses for intra-specific variation in genotype; their preliminaryresults indicate significant patterns of genotypedistribution within and between water masses.The implications of this finding for biogeo-graphic studies has not been ful ly assessed, butHuber et at. (1997), Darling et al. (1998b), andde Vargas et al. (1998) have discussed crypticgenotypic species within morphotypes pre-viously believed to be monospecific. This impliesthat the traditional morphospecies concept maynot be a fully adequate basis for understandingbiogeographic patterns.

7.4.3 Directional currents

7.4.4 The biogeography of foraminiferalgenotypes

120

Boltovskoy (1971a) provided an early quan t i f i -cation of the geographic scale of abundancevariation; useful discussions can be found inWiebe and Holland (1968), Boltovskoy (1971a)and Boltovskoy and Wright (1976). The phe-nomenon is probably too ephemeral to play adirect role in genetic isolation during the specia-tion process; however, Hemleben et al. (1989)suggest that a significant portion of measuredlateral patchiness may be due to diurnal verticalmigration during sampling. Based on planktontows, Boltovskoy reported abundance variationby a factor of 90 over distances as small as onenautical mile in the South Atlant ic Ocean.

Recent work on patchiness in the planktonhas been directed at the more general questionof its underlying causes (Powell and Okubo,1994; Abraham, 1998; Levin and Segel, 1976).Abraham (1998) has pointed out that turbulentstirring of plankton by nondiffusive advectionis a likely explanation for patchiness. The con-centration spectra of plankton tend to follow apower law over scales ranging from one to100 km. Phytoplankton distributions are similarto the distribution of the physical quantit ies(especially, nutr ient) that the phytoplankton arepresumably tracking. Zooplankton concen-trations however, are more variable over shortdistances- nearly as variable as they are at largerspatial scales. The difference, according to Abra-ham, can be accounted for by differing responsetimes, i.e. longer-lived zooplankton may notreproduce quickly enough to closely track theirnutrit ional resources. This might explain thecloser correlation seen between productivity andforaminiferal abundances in small-mesh plank-ton tows noted by Berger (1969). Over theirshorter lifetimes, juvenile specimens are l ikely tohave experienced less advective transport, andtherefore are more likely to reflect recent repro-duction in resource-rich waters. Concentrationspectra in the planktonic Foraminifera have notbeen examined quantitatively in the contextof Abraham’s model; nevertheless, there maybe sufficient lifespan-dependent variation inresponse times between the long-lived genus

Globorotalia and the shorter-lived Globigeri-noides to test for consistency with Abraham’sprediction.

On an extremely f ine scale, Silver et al. (1978)have presented evidence suggesting tha t theabundance and diversity of microplankton cor-relate wi th small-scale variation in the densityof marine snow aggregates (fecal pellets, organicdetri tus, various exoskeletons, etc.). Some mayeven treat this snow as a substrate (Hilbrechtand Thierstein, 1996; see also Banerji, 1974).

It is becoming clear that one means of achievingsympatric speciation in plankton may involvegenetic isolation through intraspecific variationin the t iming of the reproductive cycle. In speciesthat time their reproduction to coincide wi thspecific ( b u t d i f f e r e n t ) parts of the lunar cycle(e.g. Bijma et al., 1990, 1994; Bijma and Hem-leben, 1994; Erez et al., 1991), or wi th seasonaloverturn of the mixed layer (e.g. Lohmann andSchweitzer, 1990; Lohmann, 1992), we may f indthat their speciation rates, and hence their pro-vincial diversity and distr ibution, may be in f lu-enced by geographic variation in the in tensi tyof seasonal upwelling, or temporal variat ion insuch factors as the depth of the thermocline,pycnocline, or chlorophyll maximum (see Weferand Fischer. 1993; Will iams et al., 1981; Sautteret al., 1991; Curry et al., 1983, 1992).

7.5 SMALL-SCALE PATCHINESS

7.6 TEMPORAL CONSIDERATIONS

7.6.1 Temporal patchiness

7.6.2 Time scale and biogeographic patterns

7.6.2.1 The effect of recovery time

It may he f ru i t fu l to consider the time scale overwhich historical events might influence biogeo-graphic patterns. It is l ikely that ecological resta-bilization after climatic change would appear tobe v i r tua l ly instantaneous when perceived on ageological t ime scale, however, it does not followthat biogeographic stabilization is beyond theresolving power of biostratigraphers. This isbecause ecological response time of the biota is


Conclusions

not the only determinant of biogeographic pat-terns. For example, evolutionary recovery playsa significant role, especially when extinction andspeciation are latitude-dependent.

What is the time scale for evolutionary recov-ery in the plankton? The average censorship-corrected species duration is about 9.17 my forthe Cenozoic planktonic Foraminifera and theexpected and realized time to recover a stablespecies age distribution after the Cretaceous/Tertiary extinction is about 15 my (Arnold, et al.,1995b; Parker and Arnold, 1997; also cf. Stanley,1990) After the post-Cretaceous recovery of astable age distribution in Cenozoic planktonicForaminifera, the mean species age fluctuatesabout an average of 5 my. With evolutionaryrecovery times of this magnitude, we shouldexpect that the effects of late Cenozoic coolingare likely to exert a lingering influence over thatcomponent of biogeographic patterns that isinfluenced by speciation and extinction rate.

On a somewhat shorter climatic time scale,poleward retreat of Quaternary climatic beltsand water masses in relation to southernmostSouth America has mediated the repopulationof the Atlantic basin by Globorotalia cultrata(Vincent and Berger, 1981; see discussion under‘continental positions’ above). In this case thelimiting factor in these repopulation events hasbeen interaction between climatic belts and con-tinental positions rather than ecological respon-siveness of Globorotalia cultrata.

If recovery times can be constrained by factorswith evolutionary or Milankovich time scales,it follows that the historical components of bio-geographic equilibration deserve attention attime scales longer than those normally seen inplankton ecology studies. Endler (1982) pro-vides a useful perspective on the relative impor-tance of ecological and historical influences ondiversity gradients.

Foraminifera. Even though keeled globorotali-ids tend to live at relatively low latitudes, theirdistribution may not be attributable to an eco-logical-adaptive (sensu Seilacher, 1970) relation-ship between keels and low-latitude habitats.There are two lines of evidence supporting thisview. First, the ecological adaptive relevance ofthe keeled morphology is challenged by the factthat during the Cenozoic iterations similar mor-phologies developed in different environmentalsettings (Boersma and Premoli Silva, 1991).Second, other low-latitude morphotypes havesimilar speciation rates, so it is likely that therelationship between morphology and turnoverrates is indirect.

These observations suggest the possibility ofa constructional interpretation for the iterativeevolution of keels, and for their nonpolar distri-bution; the larger number of steps required toreach a keeled morphology from globose ances-try virtually guarantees that keeled forms willtend to be evolutionary latecomers relative totheir globose ancestors. Consequently, weshould expect the buildup of diversity in keeledforms, even when it occurs at random with respectto adaptation, to be (a) late relative to that ofglobose forms, and ( b ) greatest and earliestwhere speciation rates are highest, namely inlower latitudes. Thus, iterative evolution in theplanktonic Foraminifera may derive from itera-tive variance expansion rather than directedselection (see Gould, 1996, for a general discus-sion of variance-driven trends), and suggeststhat the key to understanding iterative evolutionmight be to learn why small globigerine formssurvive mass extinction (Arnold et al., 1995a).

There are several important unresolved issuesin the area of modern planktonic foraminiferalbiogeography. The large-scale lat i tudinally sym-metrical faunal provinces do not appear to showa consistent relationship to comparably-scaledhydrographic features. The origins of these prov-inces are therefore l ikely to be understood byreference to other causal factors. The first of

121

7.6.2.2 Iterative evolution and the globaldiversity gradient

The repeated appearance of keeled morphotypes(Cifelli, 1969) is the most conspicuous manifesta-tion of iterative evolution in the planktonic

7.7 CONCLUSIONS

122

these is the degree to which smaller-scale hydro-graphic features such as current, gyre, and fron-tal systems combine to play a role indetermining larger-scale lati tudinal distributionpatterns. The second is the role historical pro-cesses – particularly, latitude-dependent rates ofspeciation and extinction, and the developmentof tectonic barriers – have played in establishingfaunal provinces and the global diversity gradi-ent. A number of additional factors, includingdepth habitats, bipolarity, pore size, coilingdirection, and iterative evolution, are indirectlyrelated to physicochemical characteristics of theforaminiferal habitat.

As our understanding of the basic governingprinciples of modern foraminiferal biogeogra-phy develops, it becomes easier to interpret thefossil record in the light of those principles. Bythe same token, modern distr ibution patterns,

since they are partly the result of historical pro-cesses, cannot be fully explained without refer-ence to their past development. We are soaccustomed to hearing that the present is thekey to the past that we sometimes forget thatthe past can also be the key to understandingthe present. It follows that biogeographic studiesof modern and fossil Foraminifera must neces-sarily proceed hand-in-hand.

The authors gratefully acknowledge the gener-ous assistance and advice of Richard Norris,Barun Sen Gupta, Andrew Feldman, and ananonymous reviewer. Rosemarie Raymond andTami Karl provided invaluable help in the prep-aration of the manuscript.

7.8 ACKNOWLEDGMENTS


8Symbiont-bearing

ForaminiferaPamela Hallock

8.1 WHAT ARE SYMBIONT-BEARINGFORAMINIFERA?

Of approximately 150 extant families of Fora-minifera, less than 10% harbor algal endosymbi-onts (Lee and Anderson, 1991a). Nevertheless,these families are responsible for much of thecarbonate produced by the Foraminifera,because symbiosis is prevalent in tropical largerforaminifers and planktonic foraminifers, thetwo groups that are the most prolific carbonateproducers. Globally, Milliman and Droxler(1995) estimated carbonate production at 5.7billion tons per year, of which larger foraminifersproduce about 0.5% and planktonic foramini-fers produce about 20% (Langer, 1997).

Lee and Anderson (199 l a ) , in their review ofthe biology of symbiosis in Foraminifera, listedfour miliolid, three rotaliid, and five globigerinidfamilies as hosts of algal symbionts belongingto three divisions and five classes of the algae.A few members of several families of smallerrotaliid foraminifers (e.g. Asterigerinidae) appearto host endosymbionts, but those relationshipsawait study. In addition, members of severalfamilies are able to sequester chloroplasts, whichare harvested from algal food, for days to weeks

after ingestion (Lopez, 1979; Cedhagen, 1991;Lee and Anderson, 1991a). While this is not atrue symbiosis, chloroplast sequestering doesenable these protists to benefit directly fromphotosynthesis.

Algal symbiosis appears to have arisen inde-pendently in most of these lineages of Foramini-fera, as well as in several now extinct lineages.Evidence for independent origins is strongest forthe miliolid families and subfamilies. The orna-mented Peneroplidae (Fig. 8.1.A) host symbi-onts belonging to the red algae (DivisionRhodophyta) (Fig. 8.2.A), while the unorna-mented Peneroplidae (Fig. 8.1.B) and the Arch-aiasinae (Family Soritidae) (Fig. 8.1.C) hostsymbionts belonging to the green algae (Divi-sion Chlorophyta) (Fig. 8.2B). The Soritinae(Family Soritidae) (Fig. 8.1.D) host dinoflagel-late symbionts (Division Chromophyta, ClassPyrrophyceae) (Fig. 8.2.C), and the AlveolinidaeI Fig. 8.1.E) host diatom symbionts (DivisionChromophyta, Class Bacillariophyceae). Amongthe planktonic Foraminifera (Fig. 8.3), bothdinoflagellate (Fig. 8.2.D) and chrysophyte(Division Chromophyta, Class Chrysophyceae)(Fig. 8.2.E) symbionts are common. Recent iso-topic studies (Norris, 1996a) indicate that within

Barun K. Sen Gupta (ed.), Modern Forammifera, 123–139© 1999 Kluwer Academic Publishers. Printed in Great Britain.

124 Symbiont-bearing Foraminifera

globigerinid generic lineages, symbiosis may beindependently acquired. The three rotaliid fami-lies, Amphisteginidae (Fig. 8.1.F), Calcarinidae(Fig. 8.1.G) and Nummulitidae (Fig. 8.1.H), allprimarily host diatom symbionts (Fig. 8.2.F).Current phylogenies indicate that these familiesarose independently from smaller ancestors, butproof must await molecular-genetics studies.Nevertheless, evidence is strong that foramini-fers are physiologically adapted to establishingsymbioses (Lee, 1998), and that symbiosis canbe highly advantageous under certain environ-mental conditions (e.g. Hallock, 198la; Hot-tinger, 1982).

8.2 ADVANTAGES OF ALGALSYMBIOSIS

The potential advantages of algal symbiosis toforaminifers lie in at least three major areas: a)energy from photosynthesis; b) enhancement ofcalcification; and c) uptake of host metabolitesby symbiotic algae. None of these areas has beenexhaustively studied, nor are they mutuallyexclusive. For example, both energy from photo-synthesis and uptake of or phosphaticwaste products would presumably aidcalcification.

8.2.1 Energy from photosynthesis

Hallock (198la) mathematically explored thehypothesis that algal symbiosis provides host-symbiont units with substantial energetic advan-tages over similar organisms that lack endosym-bionts. Organisms with the potential to bothfeed and photosynthesize have access not onlyto solar energy, but also to dissolved inorganicnutrients (nitrogen and phosphorus in forms

useable by organisms, i.e. NH4+, NO2

–, NO3–,

and to organic matter. In severely nut r i -ent-deficient environments within the euphoticzone of the oceans (i.e. where there is sufficientlight for net photosynthesis), the most significantconcentrations of essential nutrients are inorganic matter. Therefore, algal symbiosisenables the foraminifer to function as a primaryproducer that obtains nutr ients by feeding. Hal-lock’s ( 1 9 8 l a ) model indicated that algal symbi-osis provides the host-symbiont system withseveral orders of magnitude energetic advantageover non-symbiotic competitors in nutr ient-deticient environments. Thus, once acquired,algal symbiosis appears to give significant ener-getic advantage for specialization of the host tosymbiosis, providing considerable insight intorepeated episodes of evolution of probable sym-biont-bearing foraminifers, as judged by thefossil record (Hallock, 1982, 1985, 1987; Lee andHallock, 1987; Hallock et al., 199la).

More recent research by Falkowski et al.(1993), Lee (1998), and others, indicates thatthe host must maintain control of fixed nitrogensupply to the symbiont, which reinforcesrecognition of the relationship between nut r ien t -deficient environments and algal symbioses.Because the photosynthetic process is limited bythe availability of solar energy and symbi-onts that are severely nitrogen limited but haveplenty of sunlight can produce copious amountsof simple sugars and glycerol, which they releaseto the host. With its metabolic energy require-ments met by this photosynthate, the host canuse most of the proteins ingested in capturedfood for its own growth and reproduction. How-ever, if the symbionts have access to abundantfixed nitrogen, they keep their photosynthate forgrowth and reproduction, causing physiologicalstress for the host.

Advantages of algal symbiosis 125


The actual roles of feeding and photosynthesiscan differ substantially from theoretical predic-tions, and vary among the major taxa studied.Amphistegina spp. appear to behave most closelyto model predictions; physiological studies indi-cate that ingested food primarily provides nutri-ents, while respiratory energy comes primari lyfrom photosynthesis (ter Kuile et al., 1987). Incontrast, imperforate taxa such as Archaias, Pen-eroplis, and Sorites appear to be far more ener-getically dependent upon feeding and, in fact,the role of their symbionts is somewhat enig-matic (Lee and Anderson, 199la). At the otherextreme are some of the Nummuli t idae and Cal-carinidae, which lack primary and secondaryapertures and have not been observed to feedon anything except their endosymbionts(Röttger et al., 1984; Röttger and Krüger, 1990).Clearly this provides a mechanism for receivingproteins and phosphatic acids as well as carbo-hydrates from endosymbiosis, but does notexplain how the host-symbiont uni t uptakesessential nutrients. In culture, the foraminifermay be exposed to sufficient nutr ients to sustainsuch a relationship, but in the natural environ-ment, free-living algae should be far superiorcompetitors for dissolved inorganic nutrientsthan are symbionts that are enclosed within ahost organism. In theory, living on the host’snutrient wastes works only if the host is feeding.One possible explanation for this apparentenigma is that the nummulit ids and calcarinidsfeed upon bacteria, as Lee et al. (1980) experi-mentally showed for Heterostegina depressa.Bacterial feeding can be easily overlooked.Members of both families produce organicattachment mechanisms (Röttger and Krüger,1990) that Röttger (1973) originally describedas rigid hyaline elastic sheaths. The composition

of these sheaths should be investigated, for theymay provide additional clues to how these fora-minifers get required nutrients. When providedwith a carbohydrate-rich substrate, certain bac-teria are much more efficient at extracting lowconcentrations of essential nutrients from thewater column than are phytoplankton (Azamand Smith, 1991) . If the sheaths are carbohy-drate-rich, they may provide a substrate for‘farming’ bacteria. The foraminifers could theneither feed on the bacteria (e.g. Bernhard andBowser, 1992), or uptake the nutr ient wastes ofthe bacteria and the microplankton that cometo feed on the bacteria. Observations of possiblebacterial farming by foraminifers are relativelycommon (e.g. Langer and Gehring, 1993). Hal-lock et al. (1991b)a lso postulated tha t sediment-dwelling, flat-planispiral or discoid foraminifersmay take up nut r ien ts that are diffusing out ofsediment pore waters, whi le ut i l iz ing sunl ightfrom above.

8.2.2 Algal symbiosis and calcification

Because larger foraminifers wi th algal symbiontsare such prolific calcifiers, conventional wisdomhas long held that photosynthesis by the symbi-onts promotes calcification by spl i t t ing of bicar-bonate (ter Kui l e , 1991) and removal of(Equat ion 8.1):

McConnaughey (1989c) and McConnaugheyand Whelan (1997) have proposed the reverseinterpretat ion. They postulate tha t lack ofl imits photosynthesis in warm, shallow, a lka l ineaquatic environments and that calcification pro-

Advantages of algal symbiosis 127


vides protons (equation 8.2) that makereadily available from the much more abund-ant bicarbonate ions (equation 8.3). That is,calcification:

promotes photosynthesis:

the organic-carbon synthesis phase ofphotosynthesis.

Another l ink between photosynthesis andcalcification may simply be the production ofATP, which can be used as an energy source foractive transport wi th in the cell. Erez ( 1 9 8 3 )found essentially normal calcification rates inperforate, symbiont-bearing foraminifers thathad been treated with a herbicide that blocksthe carbon f ixa t ion step in photosynthesis, butnot the ini t ia l production of ATP. ATP providesthe energy source for concentration of the inor-ganic carbon into internal reservoirs in thelarger perforate taxa, and into vesicles in theimperforate species (ter Kuile, 1991). ATP mayalso provide the energy for removal of ions thatcan inhib i t calcification, including

and (ter Kuile , 1991). Foraminiferswith algal endosymbionts may use sunlightrather than food resources as the source ofenergy for ATP, thereby accounting for the sig-nificant enhancement of calcification by light(e.g. Duguay and Taylor, 1978; Duguay 1983;Erez 1983; ter Kuile 1991) .

The organic matrix of the test is critical inini t ia t ing and directing calcification, particularlyin perforate foraminifers (e.g. Hemleben et al.,1977; Angell, 1979, 1980; Weiner, 1986; ter Kuile,1991). The organic matrix also provides strengthand flexibility to the test (Weiner, 1986). Lee(1998) discovered that the large, heavy tests ofimperforate taxa such as Marginopora includesubstantial quanti t ies of organic matter. Simi-larly, Toler and Hallock (1998) found thatnormal Amphistegina tests have substantialorganic matter, but tha t the tests of individualssuffering from anomalous symbiont loss may begrossly deficient in organic matter, resul t ing inweakened and anomalously calcified tests. Theorganic chamber l ining of the shell matr ix ofmany foraminifers, which provides s t ructuralintegrity to the test, is composed of glycos-aminoglycans that are 99.5% polysaccharideand 0.5% protein (Weiner and Erez, 1984). Car-bohydrate from photosynthate may be contrib-uting to the organic matrix of the shell. Thisand other hypotheses concerning the role of theorganic matrix in biomineralization are fertiletopics for fur ther research.

is a simplified expression for organicmatter produced during photosynthesis, i.e.photosynthate). According to this hypothesis,the electron capture phase of photosynthesisprovides ATP for active transport of and

ions, promoting calcification and makingbicarbonate ion a viable source of for

Distributions of benthic foraminifers with algal symbionts 129

Another postulated advantage of algal symbio-sis, particularly for very large species, is thepossible role of the symbionts in removal of hostmetabolites. Protists are dependent upon pro-cesses such as diffusion, active transport, andcytoplasmic streaming for transport of materialsinto, out of, and within the cell. The assumptionbehind the hypothesis of metabolic removal isthat the larger the foraminifer, the greater thetransport problem. Presumably, having intracel-lular symbionts could partially alleviate thisproblem. While there is very little evidence eitherto support or refute this hypothesis, a logicalargument against it is that, while the symbiontsmight remove metabolites during the day,at night they produce their own metabolites,particularly which would presumablyexacerbate the need for water motion to supplyoxygen and to remove carbon dioxide and othermetabolites. However, the calcification processcould benefit from metabolite removal, because

can interfere with crystal forma-tion (e.g. ter Kuile, 1991).

Whatever the benefit to individual organisms,the advantage of such symbioses to ecosystemsin nutrient-deficient environments is tremen-dous. Algal symbiosis is one of the major mecha-nisms that allows mixotrophic nutrition, that is,the ability to both feed and photosynthesize(Hallock, 198la), in contrast to autotrophic andheterotrophic nutrition which allows one or theother. In ecosystems dominated by purely auto-trophic and heterotrophic nutrition, food websare based on autotrophic primary producers.There is typically a 90% or greater loss of energyand biomass to respiration with each heterotro-phic link in the food web. Mixotrophic nutrition,in contrast, provides essentially ‘free links’ in thefood web. That is, when a mixotrophic organismsuch as a larger foraminifer or zooxanthellatecoral captures a unit of prey, the majority of thedigestible organic matter in the prey can be used

by the host for growth and reproduction. Photo-synthesis by the symbionts provides energy forthe host’s respiratory needs (Falkowski et al.,1993). Thus, the biomass transfer from the preyto the mixotroph can potentially be far greaterthan the typical 10%. Prolific calcification,regardless of whether it promotes photosynthe-sis or is a byproduct thereof, provides substra-tum for whole ecosystems to develop andflourish. Furthermore, although the significanceof mixotrophic nutrit ion in plankton communi-ties is just beginning to be recognized (e.g.Stoecker, 1998), its contribution to recycled pro-duction in open-ocean communities appears tobe significant. Perhaps most importantly, plank-tonic Foraminifera, many with algal symbionts,account for about 20% of global carbonate pro-duction (Langer, 1997), and thereby play a keyrole in marine geochemical cycles, whether theforaminiferal tests are dissolved in corrosivedeep-sea waters or accumulate as foraminiferalooze on the seafloor.

Like most groups of organisms, the larger fora-minifers exhibit higher diversities in the Indo-Pacific region than in the central Pacific, Gulfof Aqaba, and western Atlantic/Caribbeanregions (Table 8.1). This is particularly truewithin the three larger rotaliid families (Hallock,1988a,b). The Indo-Pacific Amphisteginidae(Fig. 8.1.F) and Nummulitidae (Fig. 8.1.H) eachinclude five or six relatively well known andeasily distinguishable species, as compared toone or two variable species in the Caribbean.The third rotaliid family, the Calcarinidae(Fig. 8.1.G), is restricted to the Indo-Pacific.Among the imperforate taxa, the Alveolinidae(Fig. 8.1.E), rhodophyte-bearing Peneroplidae(Fig. 8.1.A) and Soritinae (Fig. 8.1.D) are alsomore diverse in the Indo-Pacific than in theCaribbean. However, for taxa that have chlo-rophyte symbionts (Table 8.1), i.e. the unorna-mented Peneroplidae (Fig. 8.1.B) and the

8.3 DISTRIBUTIONS OF BENTHICFORAMINIFERS WITH ALGALSYMBIONTS

8.2.4 Significance of algal symbiosis toecosystems

8.2.3 Uptake of host metabolites


Archaiasinae (Fig. 8.1.C), the trend is the oppo-site (Table 8.1). In the Caribbean, this group isrepresented by five genera and ten or morespecies, as compared to the western Pacific,where there seems to be only two monospecificgenera. Deciphering this anomaly may, in thefuture, provide insight into the paleoceano-graphic history of the Caribbean.

Depth trends of larger foraminiferal distribu-tions are a key tool for paleoenvironmentalinterpretation (e.g. Hottinger, 1983, 1997; Hal-lock and Glenn, 1985, 1986). The most thoroughstudies to date on depth distributions of Indo-Pacific living larger foraminifers are those ofReiss and Hottinger (1984), Hallock (1984), andHohenegger (1994), carried out in the Gulf ofAqaba, Belau (Palau, Western Caroline Islands),and Okinawa, respectively. Hottinger (1983)noted that the maximum depth for symbiont-bearing organisms in the Gulf of Aqaba is 130 m,

Larger foraminifers belonging to the OrderRotaliida share several important characteristicsthat enable them to effectively exploit an extens-ive depth range of euphotic habitats in warm,clear, nutrient-deficient seas (Hallock, 1988a,b).One characteristic is the ability to establishendosymbioses with several diatom species. Thisallows one species of foraminifer to exploit asubstantial range of light intensities, which arecontingent upon the photic requirements andlimitations of several different diatom species(e.g. Lee and Anderson, 1991a). The flexibilityof the endosymbiosis is complemented by the

8.3.1 Larger rotaliid foraminifers

corresponding to 0.5% of surface light intensity.Figure 8.4 summarizes distributions of fourmodern larger foraminiferal families, illustratingtrends in test shape with depth.


structural characteristics of the perforate, hya-line, lamellar, low-magnesium calcite tests (Hal -lock, 1988a,b). Calcite secretion with thecrystallographic c-axes perpendicular to the testsurface, as observed by Towe and Cifelli (1967) ,provides the potential for the development ofvery transparent, hyaline tests which cantransmit most available light energy. The lam-ellar structure permits thickening of the test wallthrough the life of the protist, which may beadvantageous in shallow, high-light environ-ments. In the Calcarinidae and Nummulitidae,the lamellar wall structure is modified into acanal system providing a variety of advantagesthat complement symbiosis ( Röttger et al., 1984;Röttger and Krüger, 1990). In the Calcarinidae,in particular, the canal system permits the thick-ening and translucency of the shell, reducinglight penetration and allowing individuals tolive in the upper meter of brightly-li t tropicalwaters. The lamellar structure and canal systemalso allow for the complex spine systems in thecalcarinids, thus providing anchoring and sta-bility in high energy reef-flat and reef-marginenvironments (Röt tger and Krüger. 1990).

Efficient precipitation and maintenance oflow-Mg calcite tests do not require greatly ele-vated carbonate saturation states. Most of thelarger rotaliid families arose during the earlyPaleogene, when atmospheric concen-trations were two or more times higher than

present levels (e.g. Berner, 1994) and so sea-surface carbonate saturation levels were signifi-cantly lower. On the other hand, these foramini-fers do not thr ive under elevated salinities, withconcomitant elevated a lka l in i ty . The potentialfor crystal poisoning by should be investi-gated as the mechanism involved, sinceincreasingly interferes with calcite precipitationas carbonate saturation state increases (Morseand Mackenzie, 1990).

(a) Amphisteginidae. The Amphisteginidae arethe most studied of the symbiont-bearing fami-lies. The best known species are Amphisteginalobifera Larsen and A. lessonii d’Orbigny(Fig. 8.1.F) in the Indo-Pacific, and A. gibbosad’Orbigny, the sibling species of A. lessonii, inthe Caribbean. All three occur abundantly atdepths less than 30 m, and are amenable to cul-ture. Around some Pacific islands, A. lobiferaand A. lessonii may be so abundant that theyare major contributors to coastal sediments(McKee et al., 1959; Hallock 1981b). They liveon firm substrates, both reefal and phytal, andmay also occur in sandy substrates (Hoheneg-ger, 1994). Generation times appear to be3–6 months at depths < 30 m (Hal lock, 1981c;Hallock et al., 1986b), but are probably longerin deeper habitats where there is less lightenergy. Generation times in A. lob i fera are6–12 months (Hallock. 1981c). Harney et al.(1998) and Dettmering et al. ( 1 9 9 8 ) documented


trimorphic life cycles in A. gibbosa. That is,besides typical alternation of sexual and asexualgenerations, one or more schizont generationsmay occur between the agamont and gamontgenerations.

In the Indo-Pacific region, Amphistegina spp.exhibit a fairly straightforward depth zonation(Fig. 8.4) that is accompanied by shape trends(Larsen, 1976; Larsen and Drooger, 1977; Hal-lock, 1979). The shallowest-dwelling taxon, A.lobifera, is by far the most robust, with thick-ness-to-diameter ratios ( t / d = minimum to max-imum diameter) typically in excess of 0.6. Theseforaminifers predominate in shallow backreefand reef-margin environments at depths typi-cally < 10m; A. lessonii somewhat overlaps A.lobifera in both range and morphology, thought/d ratios are generally 0.35–0.5, and optimumdepths appear to be 10–30 m (Hallock 1984;Hohenegger 1994). Live A. lessonii can be foundfrom the shallow subtidal down to depths of100 m if water transparency is sufficient. Theyapparently do this by cryptic behavior at theshallow end of their depth range, thereby avoid-ing damaging light intensities, and possibly byutilizing symbiont species that are adapted tolower light intensities at greater depths (Leeet al., 1980). Amphistegina radiata (Fichtel andMoll) is common at 20–50 m, and ranges tonearly 100 m in depth (Hallock, 1984; Hoheneg-ger, 1994). A. radiata has a limited geographicdistribution and does not occur in the centralPacific (e.g. Hawaii). Hottinger et al. (1993)reported a very small A. radiata-like form in theGulf of Aqaba, living at somewhat deeper habi-tats than those found in the western Pacific. A.bicirculata Larsen is similar to A. lessonii, buthas consistently lower t/d ratios of about0.2–0.35 (Larsen, 1976; Hallock, 1979). Speci-mens are seldom found at depths < 30 m, andcan be recovered live to depths > 100 m. Amphi-stegina papillosa Said is the deepest dwellingmember of the genus, capable of surviving onthe minimal light available at depths > 100 m(Larsen, 1976). Their tests are typically very flat,appearing almost paper thin, and have t inypapillae on test surfaces, the characteristic forwhich the species was named. The geographic

distribution of A. papillosa appears to be similarto that of A. radiata.

In the western Atlantic and Caribbean,Amphistegina gibbosa is the predominant speciesof this genus. Whether it is the only species iscontroversial. Test morphologies are highly vari-able, and range between a form essentially indis-tinguishable from A. lessonii and the robustlyplano-convex ‘gibbose’ forms for which thespecies was named. A. gibbosa has a wide depthdistribution similar to, though generally sl ightlydeeper than, that of A. lessonii. Live individualscan often be found at depths < 5 m on patchreefs and to 100 m on open carbonate-shelf envi-ronments, though their preferred depths appearto be ~ 15–40 m. Test shape is not as predictablewith depth as it is in A. lessonii (Mart in andLiddell, 1988).

(b ) Nummuli t idae. Habitats and geographicranges of most species of Nummuli t idae areincompletely known, because their occurrencein deep-euphotic areas (generally >30m) isbeyond prudent SCUBA sampling depth(Fig. 8.4). These protists live on both firm andsandy substrates (Hohenegger, 1994). Somenummulit ids lack true primary and secondaryapertures; instead, they have canal systems thatserve similar fundamental roles in locomotion,growth, excretion, reproduction and protection(Röttger et al., 1984). The canal system permitsthe extrusion of pseudopodia from any point ofthe marginal cord. Trimorphic life cycles appearto be the norm in this group (e.g. Leutenegger,1977a; Röttger et al., 1990), and may partlyaccount for the dearth of sexually-produced aga-monts in most populations (Drooger, 1993).Agamonts are often distinctive, even withoutsectioning to confirm microspheric embryons,because these individuals typically grow to sizessubstantially larger than schizonts and gamonts.

Heterostegina depressa d’Orbigny (Fig. 8.1.H)is the most widespread of all larger foraminiferalspecies, present in the Gulf of Aqaba andthroughout the tropical and subtropical Indianand Pacific Oceans. It is the only larger rotaliidspecies that survived the oceanographic changesin the eastern tropical Pacific associated wi ththe closure of the Central American Seaway


(Crouch and Poag, 1987). The Caribbean siblingspecies, Heterostegina antillarum d’Orbigny,appears to have diverged following the uplift ofthe Isthmus of Panama. H. depressa is the onlynummulitid commonly found at depths less than20 m, though its optimum depths are 20–60 m(Hallock, 1984; Hohenegger, 1994). Shallower-dwelling populations may be sustained primar-ily by successive asexual generations, whiledeeper dwelling populations appear to utilizesexual reproduction more commonly in their lifecycles (Röttger et al., 1990). Their very low lighttolerances (Röttger and Berger, 1972) indicatethat cryptic behavior may be necessary for themto survive at shallow depths. Individuals areamenable to culture, as demonstrated by thepioneering laboratory observations of Röttger(1972, 1973, 1974, 1976). Schizont reproductionoccurs at about 6 months of age (Röttger andSpindler, 1976). Diameters at reproduction ofH. depressa in culture range from about 2 mmfor schizonts to 4 mm for gamonts to 7–14 mmfor agamonts (Röttger et al., 1986, 1990).

Assilina ammonoides (Gronovius) is superfi-cially similar in appearance to H. depressa, butchambers of Assilina are not subdivided intochamberlets. This species is widely distributedthroughout the Indo-Pacific, ranging from theGulf of Aqaba(Hottinger, 1977; Hottinger et al.,1993) to Hawaii in the central Pacific (Hallock,1984). Assilina is common from 20–100 m, withan optimum depth of around 60 m. Though itcan be found on firm substrate, it appears toprefer sand and muddy sand habitats (Hoheneg-ger, 1994).

Nummulites venosus (Fichtel and Moll) is theonly extant species of the name genus of thefamily. Individuals may be relatively lenticularand involute as juvenile and subadult agamonts,or even as adult schizonts and gamonts. Aga-monts typically grow to much larger sizes thangamonts and schizonts. Hohenegger (1994)reported their depth range as 20–80 m, peakingin abundance at 40 m.

The two deepest-dwelling nummulitids, Het-erostegina operculinoides Hofker and Cycloclyp-eus carpenteri Brady, have classic flat, thin,‘deep-euphotic’ morphologies (Fig. 8.4). The

latter species also differs from the other num-mulitids in that the planispiral growth formdevelops into an orbitoid morphology early inlife, so that adult individuals are large, thin diskswith slightly elevated ( thicker) central regions(Song et al., 1994). Agamont generations ofCycloclypeus are apparently quite long lived,with test diameters exceeding 120mm (Koba,1978). Gamonts and schizonts reproduce at con-siderably smaller sizes (Krüger et al., 1996).Although the geographic distribution of Cyclo-clypeus is not well known, it appears to have arelatively restricted distribution in the Indo-Malay and far western Pacific. Another deep-euphotic species, Heterocyclina tuberculata(Möbius) , has been reported from the Gulf ofAqaba and from the Indian Ocean (e.g. Hot-tinger et al., 1993).

(c) Calcarinidae. The Calcarinidae, which livepredominantly in shallow, high energy reef-flatand reef-margin environments (Fig. 8.4), includefive genera: Baculogypsina, Baculogypsinoides,Calcarina, Neorotalia, and Schlumbergerella(Hohenegger, 1994; and personal communica-tion). With the exception of Neorotalia calcar(d’Orbigny), which occurs in the western IndianOcean region, the Calcarinidae are restricted tothe Indo-Malay archipelago and western Pacific(Table 8.1), and are very important carbonatesediment producers in this region. Sediment pro-duction estimates, projected from known ratesof production by C. gaudichaudii d’Orbigny(Fig. 8.1.G) from Belau, can approach those ofreef-flat corals at 3–5 kg (Hal-lock, 1981b). In the Ryukyu Islands, the famousstar-sand beaches are composed primarily of theshells of Baculogypsina (Hohenegger, 1994).

The elaborate calcarinid canal systems andspiny morphologies provide numerous points ofcontact with the external environment. Röttgerand Krüger (1990) described an attachmentmechanism in Baculogypsina sphaerulata(Parker and Jones) that consists of a durable,elastic organic cement, which enables individ-uals to adhere by a single spine to the algalsubstratum. This attachment mechanism allowscalcarinids to thrive in high energy environ-ments.


The imperforate foraminifers of the Order Milio-lida construct porcelaneous-appearing tests ofhigh-magnesium calcite. Distributions of imper-forate taxa characterized by algal endosymbi-onts are not as well known as those of similarperforate taxa. In large part, this is because oftaxonomic difficulties with miliolids, which aremorphologically more plastic, and include manyspecies that are superficially similar. From anecological perspective, the larger miliolids canbe discussed by the kind of symbionts they host.

Hallock (1988a,b) noted that the larger milio-lids are most common in shallower habitats, andtend to have a more restricted depth range thanthe larger rotaliids (Fig. 8.4). The miliolid teststructure includes a layer of randomly-orientedcrystals, covered by a brick-like layer of crystalsoriented with the c-axis parallel to the outerwall, resulting in a naturally opaque structure.To efficiently host algal endosymbionts, the shellwall over the chambers must be thinned (Hal-lock and Peebles, 1993). Thus, test structuremay account for some of the distributionallimitations on these foraminifers.

Test mineralogy may also provide otheradvantages and disadvantages, depending uponthe environment. High-Mg calcite becomesincreasingly easy to precipitate as the carbonatesaturation state of the seawater increases (Morseand Mackenzie, 1990). This may partly explainthe predominance of Archaiasinae in the westernAtlantic and Caribbean (Hallock, 1988a,b). Oce-anic salinities are 1–3‰ higher in the tropicalAtlantic than in the tropical Pacific, contribut-ing to higher alkalinity and degree ofsaturation in the Atlantic (Broecker and Peng,

1987). The divergence of tropical ocean chemis-tries occurred during the Miocene and Pliocenewith the emergence of the Isthmus of Panama.During this time, the porcelaneous, high-Mg-calcitic Archaiasinae became the predominantlarger foraminifers in western Atlantic and Car-ibbean (Frost, 1977). In the Indo-Pacific region,localities with elevated salinities, such as thePersian Gulf (Murray , 1973) and Shark Bay,Austral ia (Davies, 1970; Logan and Cebulski1970), are dominated by ornamented Peneropli-dae. ter Kui le ( 1 9 9 1 ) observed that externalsources of bicarbonate are more important thanenzymatic processes for calcification in imperfo-rate Foraminifera, providing a clue to the suc-cess of these foraminifers in high alkalinityenvironments. Because high-Mg calcite is rela-tively weak, and the miliolid shell s tructure isnot bilamellar, organic matter in the shell mayprovide necessary strength to the test.

The Alveolinidae are the only imperforatetaxa known to harbor diatom symbionts (Leeet al., 1989). In modern seas, this family is repre-sented by two genera and a few species. Alveo-linella quoyi (d’Orbigny) (Fig. 8.1.E) appears tobe geographically limited to the Indo-Malay andwestern Pacific regions. Its habitat includes fore-reef rubble and sands at depths from 5 to 50 m(Lipps and Severin, 1985; Severin and Lipps,1989; Hohenegger, 1994). The much smallerBorelis spp. are circumtropical in distributionand can be found on reef rubble at depths to atleast 30 m. Borelis pulchra (d’Orbigny) is one ofonly four symbiont-bearing foraminifers docu-mented in the eastern tropical Pacific by Crouchand Poag(1987).

Two chlorophyte-bearing species have beenreported from the Indo-Pacific (Table 8.1). Para-sorites orbitolitoides (Hofke r ) , a medium depth(10–60 m), sediment-dwelling species, occurs inNew Caledonia (Debenay, 1986), off Okinawa(Hohenegger, 1994), on the Great Barrier Reef,and on the west Australian shelf (Hallock,unpublished observation). Cheng and Zheng(1978) described an unornamented peneroplid,which they called Puteolina malayensis, occur-ring abundantly around the Xisha Islands,Guangdong Province, China. Hallock (1984)

The very limited geographic distributions ofthe Calcarinidae indicate that their dispersalpotential must be quite limited. However,factors contributing to the very widespread dis-tributions of Amphistegina lessonii and Hetero-stegina depressa are no better understood. Astudy of biological and ecological factors associ-ated with distributional patterns of larger fora-minifers is long overdue.

8.3.2 Larger miliolid taxa


found a similar unornamented peneroplid onreef flats in Belau, Western Caroline Islands.Live specimens of both species exhibit the grass-green symbiont color characteristic of chloro-phyte-bearing foraminiferal taxa. Loeblich andTappan (1987) considered Puteolina to be ajunior synonym for Laevipeneroplis.

Western Atlantic/Caribbean miliolid specieswith chlorophyte symbionts have been studiedin detail by Lévy (1977, 1991) and by Hallockand Peebles (1993). The larger, internally-com-plex archaiasines include the Androsina-Arch-aias-Cyclorbiculina group distinguished by Levy(1977, 1991). Androsina lucasi Lévy wasdescribed from hypersaline reef flats in the Baha-mas (Levy 1977), and is found very abundantlyon dwarf-mangrove flats in the Florida Keys(Levy, 1991: Hallock and Peebles, 1993). Arch-aias angulatus (Fichtel and Moll) (Fig. 8.1.C) isabundant on shallow reef (Fig. 8.4) and openshelf sites (Hallock and Peebles. 1993). Cyclorbi-culina compressa (d’Orbigny) can be found inshallow seagrass beds on the open shelf, but ismore common on the reef margin at depths of10–30 m (Fig. 8.4). Hallock and Peebles (1993)observed that chamberlet outer-wall thicknesswas distinctive in this group, with Androsinacharacterized by a relatively thick (up towall, A. angulatus by an intermediate wall thick-ness and the deeper-dwelling Cyclo-rbiculina by the thinnest wall. Hallockand Peebles (1993) postulated that wall thick-ness was an adaptation to regulate light reachingthe endosymbionts.

Lee el al. (1974) identified the chlorophytesymbionts of A. angulatus as Chlamydomonashedleyi. Live specimens of Laevipeneroplis pro-teus (Fig. 8.1.B) appear to have the same symbi-onts (Leutenegger, 1984). Lee et al. (1979)described the symbionts of Cyclorbiculina com-pressa as Chlamydomonas provasoli. Lee andBock (1976) reported that carbon gain by feed-ing was more than ten times greater than carbonfixation by photosynthesis in A. angulatus. Thus,the principal role that symbiosis appears to playis in enchanced calcification. Duguay ( 1 9 8 3 )reported that calcification rates varied wi th lightintensity and were 2–3 times faster in the lightthan in the dark.

Parasorites is also common throughoutthe Caribbean, and occurs regularly in bothsoft sediment and reef-rubble samples taken at10–30 m depth. Lévy (1977) called this genusBroeckina, and distinguished two species in theBahamas: B. discoidea ( F l i n t ) and B. orbitoli-toides (Hofker). A comparative study of theIndo-Pacific and Caribbean Parasorites andLaevipeneroplis is needed to clarify relationshipswithin these genera. Several species of unorna-mented peneroplines (Laev ipenerop l i s spp., seeFig. 8.1.B). occur throughout the Caribbean inreef and open shelf environments.

Foraminifers that host red algae (DivisionRhodophyta) as symbionts include extant mem-bers of the Peneroplidae with test-surface orna-mentation, i.e. Peneroplis, Dendritina, Sp i ro l ina ,and Monalysidium (Loeblich and Tappan, 1987).These foraminifers provide excellent opportuni-ties for fur ther study, part icular ly with referenceto morphologic variability, habitat preferences,and physiology of their symbiotic relationships.

Hawkins and Lee (1990) and Lee (1990b)have studied the unique relationship betweenthe rhodophyte symbiont, Porphyridium pur-pureum (Fig.8.2.A), and i ts foraminiferal host.Unlike other symbionts, the rhodophyte cell isnot membrane bound wi th in the host cytoplasm,and in that respect could be considered anorganelle rather than a symbiont. In culture,Porphyridium cells are surrounded by a heavyfibrous polysaccharide sheath, but when thesymbionts are located in a host, the sheath isreduced or absent. Lee and Anderson (1991a)suggested that sheath-fiber digestion by the hostmay be a mechanism of energy transfer fromsymbiont to host.

Hypersaline environments in Shark Bay,Western Australia, and the Persian Gulf aredominated by peneroplids. In Shark Bay, Davies(1970) and Logan and Cebulski (1970) reportedlow foraminiferal diversities with assemblagesdominated by P. planatus, with a few other milio-lid species, at salinities up to 70‰. Similarly,Peneroplis planatus (Fichtel and Moll) , P. pertu-sus (Forska l ) and a variety of miliolids dominateshallow-water, hypersaline habitats in the Per-sian Gulf (Murray, 1973).


Extant members of the subfamily Soritinaehost dinoflagellate symbionts. Physiologicalstudies by Lee and co-workers (Lee and Bock,1976; Faber and Lee, 199la) indicate that theseforaminifers derive most of their carbon needsfrom their food rather than from their symbi-onts. So the benefit of the symbiotic relationshipremains an open question. More recent observa-tions by Lee et al. (1995, 1997) and Lee (1998)indicate that the soritine foraminifers, like theamphisteginids, do not require a particularspecies of symbiont, but rather one of a suite ofacceptable symbionts. The physiology of thealga, which makes it capable of being a symbiontand recognizable as such by the host, appearsto be more important than taxonomic identity.This relative flexibility of the symbiotic relation-ship is of obvious advantage to the host organ-ism, which is dependent upon symbiosis but canaccept any of several possible algal speciesrather than being dependent upon a singlespecies of algae. Since the foraminiferal zygotemust acquire symbionts following zygosis, thepossibility of incorporating any of several poten-tial symbiont species may increase the survivalrates of sexually-produced individuals (Lee,1998).

Taxonomic ambiguities hinder interpretationof literature reports of geographic ranges, depthdistributions, and habitats of the Soritinae. Mar-ginopora has been used in reference to bothMarginopora and Amphisorus species, Amphiso-rus for both Amphisorus and Sorites species, andSorites for both Sorites and Parasorites. Thelarge, robust Marginopora vertebralis Quoy andGaimard probably has a geographic and depthdistribution similar to that of Calcarina spp.Marginopora can live on either firm or soft sub-strate (Hohenegger, 1994), attaching to algalthalli with an organic cement (Ross, 1972).

Amphisorus hemprichii Ehrenberg is interme-diate in robustness, and has wide depth andgeographic ranges. This species has beenreported circumtropically, from the Gulf ofAqaba (e.g. Hottinger et al., 1993) through theIndian Ocean and across the Pacific to Hawaii(Phillips, 1977), the eastern tropical Pacific(Crouch and Poag, 1987), and the Caribbean

(Lévy, 1977). It prefers firm substrates and canpartially adhere to phytal substrates. Amphiso-rus (identified by Davies, 1970, as Marginopora)occurs in Shark Bay, Western Australia, at salin-ities up to 56‰ and temperature range of14–38°C.

Several species of Sorites l ive on phyta l sub-strates or in algal-bacterial mats that stabilizesandy substrates. These foraminifers can behaveas vagile protists or as attached forms, as theycan semipermanently attach to firm substratesby an organic cement ( R ö t t g e r and Krüger,1990). The type of surface and its shape mayinfluence the growth and morphology of theforaminifer. Kloos (1980) noted that, in theNetherlands Antil les, l iving S. orbiculus (For-skal) appeared to prefer the seagrass Thalassiaas substratum.

Compared wi th benthic Foraminifera, there arerelatively few extant species of planktonic fora-minifers (e.g. Kennett and Srinivasan, 1983). Yetthese protists approach global dis t r ibut ion (e.g.Murray, 1991 a) and, as previously noted, pro-duce roughly 20% of the calcium carbonatefixed in the world’s oceans each year (Langer,1997).

Hemleben et al. (1989) , in their comprehen-sive compendium on modern species, noted that‘The presence of algal associations with spinoseplanktonic Foraminifera is one of the most obvi-ous features of l iving individuals’ (p. 86). Algalsymbionts include dinoflagellates, which occurin the Globigerinidae and the Hasterigerinidae,and chrysophytes, which are found in represen-tatives of the Globigerinidae, Candeinidae,Pulleniatinidae, Hastigerinidae, and Glo-borotaliidae (Lee and Anderson, 1991a). As ageneral rule, symbioses with dinoflagellatesappear to be obligative (Hemleben et al., 1989);the exception may be the variety of dinoflagel-lates that can be associated with the bubblecapsule of Hastigerina pelagica (d’Orbigny)(Spindler and Hemleben, 1980). On the other

8.4 PLANKTONIC FORAMINIFERAWITH ALGAL SYMBIONTS

Larger foraminifers and global change 137

hand, symbioses with chrysophytes (Fig. 8.2.E)appear to be facultative, since both Gastrich(1988) and Hemleben et al. (1989) reported thatindividuals of some species reported to hostchrysophyte symbionts commonly lack symbi-onts during winter months.

Spero (1987) isolated and described the dino-flagellate symbiont in Orbulina universa d’Or-bigny as Gymnodinium béii. (Figs. 8.2.D, 8.3).This symbiont occurs in several other species(Lee and Anderson, 199la), and may be the onlydinoflagellate species to establish symbioseswith planktonic foraminifers (Gast and Caron,1996). In their hosts, G. béii individuals are small

and coccoid; symbiontsmay occur in a single host cell (Spero andParker, 1985). When isolated from the host andincubated in culture, these dinoflagellatesdevelop flagellated gymnodinoid morphologies(Fig. 8.2.D; Spero, 1987). When the planktonicforaminifers reproduce, releasing flagellatedswarmers, algal symbionts are either lysed,digested, or released into the environment(Hemleben et al., 1989). Early in their life, thejuvenile foraminifers must encounter and incor-porate symbionts (Hemleben et al., 1989), indi-cating that suitable dinoflagellate populationsare free-living in the water column.

As discussed earlier, the potential advantagesof algal symbiosis include energy from photo-synthesis, enhancement of calcification, anduptake of host metabolites by symbiotic algae.This certainly applies to planktonic as well asto benthic foraminiferal symbioses (Hemlebenet al., 1989; Caron and Swanberg, 1990). Thehost deploys its symbionts outside the test alongthe spines within the rhizopodial networkduring the day (Fig. 8.3), and withdraws theminto the cytoplasm within the shell at night; lightreception by the symbionts triggers deployment(Caron et al., 1981; Bé, 1982). This diel cycleappears to allow maximum exposure of the sym-bionts to light during the day. By bringing thesymbionts inside the test at night, they are madeless vulnerable to micrograzers and are givenenhanced exposure to host metabolites. Thisbehavior may also provide the opportunity toharvest symbionts according to the host’s nutr i -

tional needs (Hemleben et al., 1989). Symbiosisappears to aid calcification in these foraminifers(Bé et al., 1982).

Algal symbiosis has possibly provided animportant energetic advantage in the adaptationof planktonic symbiont-bearing foraminiferallineages to low nutrient environments, especiallyin subtropical and tropical oceanic environ-ments (Hallock et al., 1991a; Norris, 1996b).

Rapidly increasing human populations are alter-ing the Earth’s environments in unprecedentedways, or at least at unprecedented rates. Majorcategories of anthropogenic change includeincreasing concentrations of greenhouse gases,which influence climate and ocean chemistry;increasing input of anthropogenic nutr ients toaquatic systems; and ozone depletion, whichincreases the intensities of biologically damagingultraviolet radiation penetrating the surfacewaters of the oceans. How will these changesaffect foraminifers with algal symbionts? Canthe histories of symbiont-bearing foraminifersaid scientists in predicting consequences ofglobal change (Fig. 8.5)?

Greenhouse gas-induced global warming mayactually be advantageous to many foraminiferswith algal symbionts. Warm episodes in the geo-logic past expanded habitats for both symbiont-bearing planktonic and larger benthic foramini-fers, as subtropical belts expanded into higherlatitudes, and as sea level rose and flooded conti-nental shelves.

Increasing atmospheric also stronglyaffects ocean chemistry, with predictable effectson photosynthesis and calcification. It is a para-dox of carbonate geochemistry that higherconcentrations of atmospheric actuallypromote dissolution of . At the sametime, higher concentrations means thatcalcification is less important as a source offor photosynthesis in aquatic systems (McCon-naughey 1989c). Doubling to tripling of current

levels, as are predicted for the 21st century

8.5 LARGER FORAMINIFERS ANDGLOBAL CHANGE

to

(e.g. Watson et al., 1990), will lower carbonatesaturation levels in surface waters of the oceans.The last time atmospheric levels were sohigh was in the Eocene (Berner 1994), whenlarger rotaliid foraminifers, coralline algae andbryozoans were the dominant producers of shal-low-water carbonates. Will these taxa againreplace the aragonitic corals and calcareousgreen algae as the predominant shallow-watercarbonate producers?

Human activities have doubled the rates atwhich fixed nitrogen is entering terrestrial eco-systems, and a substantial proportion of thatnitrogen is washing into aquatic systems (e.g.Vitousek, 1997). The consequences for coastalsystems are a spectrum of effects, from ‘nutrif i-cation’ which promotes change in benthic com-munity structure (e.g. Birkeland, 1988; Hallocket al., 1993a; Cockey et al., 1996) to ‘eutrophica-tion’ which can create or expand ‘dead zones’in bays, estuaries and deltas, as has beenobserved in the Mississippi River delta (e.g.Turner and Rabalais, 1994; Rabalais et al., 1996;Sen Gupta et al., 1996).

Inf lux of nutrients is a serious threat to ben-thic communities dominated by algal symbiont-bearing organisms. Cockey et al. (1996) com-pared foraminiferal assemblages from sedimentsamples collected along transects off Key Largo,Florida, in 1991–92 with assemblages in samplescollected in the same area in 1961 (Rose andLidz, 1977). Assemblages had changed from60–80% dominance by symbiont-bearing taxain 1961 to dominance by smaller rotaliid andmiliolid taxa by 1992. These changes are consis-tent with reported declines in populations ofreef-building corals on Florida Keys reefs(Dustan and Halas, 1987; Porter and Meier,1992), and with nearshore nutrient loadingreported by Szmant and Forrester (1996). WhatCockey et al. (1996) found appeared to be classiccommunity shift in response to nutrification (e.g.Alve 1995a).

Many researchers and scientific agencies donot consider ozone depletion to be a problemfor tropical marine communities, because inten-sities of biologically damaging ultraviolet (UVB)radiation are high and seasonally variable at


Remarks 139

lower latitudes (Frederick et al., 1989), andbecause there is the misconception that U V Bonly penetrates a few meters into seawater.Unfortunately, at least subtropical shallow-water communities may be vulnerable. Strato-spheric ozone depletion has increased biolo-gically damaging ultraviolet radiation to thedegree that pre–1960s summer solstice inten-sities are now experienced throughout summermonths at subtropical latitudes (Shick et al.,1996). Furthermore, major volcanic events suchas the El Chichon eruption in Mexico in 1982and the Mt. Pinatubo eruption in the Philip-pines in 1991 inject molecules into thestratosphere that provide additional substratefor chlorofluorocarbons to attack ozone mole-cules. The Mt. Pinatubo eruption resulted in anapproximately 4% increase in ozone depletion(Randel et al., 1995), so that UVB intensities inthe early 1990s were as much as 15% higherthan intensities in the 1960s. The idea that UVBdoes not penetrate to any significant depths inmarine waters is only partly correct. Indeed,UVB is rapidly absorbed by waters with signifi-cant amounts of plant pigments or refractoryorganic compounds (‘tannins’) of terrestrialorigin (Bricaud et al., 1984). However, clear,nutrient-deficient oceanic waters generally donot contain significant concentrations of eitherphytoplankton or tannins, and as a result, sig-nificant doses of UVB can penetrate tens ofmeters (Smith and Baker, 1979; Gleason andWellington, 1993).

There is substantial evidence that Amphisteg-ina populations are suffering damage fromincreasing UVB. Beginning in summer 1991.following the Mt. Pinatubo eruption, Amphi-stegina populations in the Florida Keys beganto exhibit visible loss of algal endosymbionts(Hallock et al., 1993b). Subsequent samplingalong both the east and west coasts of Australia,as well as at several Pacific and western Atlanticlocalities, revealed that this previously unknownmalady was widespread in Amphistegina popula-tions in the 1990s (Talge et al., 1997). Monitor-ing of populations in the Florida Keys between

Research on the biology and ecology of modernforaminifers with algal endosymbionts has anexciting future. Anthropogenically-inducedchanges in the atmosphere and ocean chemistrywill most certainly influence these foraminifers.Both field studies and laboratory experimentshold great promise for providing insights intomechanisms ranging from the role of photosyn-thesis in calcification to coral-reef decline to theglobal carbon budget (Fig. 8.5).

1992 and 1996 revealed that symbiont lossbegan to increase each March to summermaxima in June or early July , with partial pop-ulation recovery by late summer each year. Thispattern indicates a relationship to the solar lightcycle, which peaks with the summer solstice inthe Florida Keys, and not to the seasonal tem-perature cycle which peaks in August or Septem-ber (Hallock et al., 1995: Talge et al., 1997:Williams et al., 1997). The kinds of damageexhibited by the afflicted foraminifers are alsoconsistent with UVB damage, which typicallyinfluences photosynthesis, protein synthesis,DNA, and behavior in protists (e.g. Hadar andWorrest, 1991). Talge and Hallock (1995)reported progressive cytoplasmic damage thatbegins with deterioration of symbiont chloro-plasts, then digestion of the symbionts by thehost, and f ina l ly autolysis of the host cytoplasm.Afflicted populations exhibited incidences ofshell breakage of 15–40%, compared to 5%observed in populations prior to the event (Tolerand Hallock, 1998). Reproduction was pro-foundly affected (Hal lock et al., 1995; Harneyet al., 1998), with schizont broods exhibi t ing avariety of new morphologies, including encrust-ing forms. Experimental research is neededto substantiate or refute the hypothesis thatbiologically damaging UV radiation is causingsymbiont loss and associated symptoms inAmphistegina (Hal lock et al., 1995). A parallelconcern is whether planktonic foraminifers arealso being affected.

8.6 REMARKS


9Foraminifera in marginal

marine environmentsBarun K. Sen Gupta

9.1 INTRODUCTION

Marginal marine habitats, ranging from coastalmarshes to inner parts of continental shelves,are usually areas of high organic productivityand relatively high environmental variability.Numerous species of benthic Foraminifera, botheurytopic and stenotopic, have adapted to theseenvironments. Many of these taxa are so charac-teristic of marginal marine habitats that theirabundance in sediment samples immediatelybrings to the mind of the specialist words suchas brackish, coastal, littoral, shallow-water,marsh, estuarine, and reefal. This chapter looksinto the common features of distribution of suchforaminiferal species and assemblages, and intothe limits of their restriction to particular mar-ginal marine habitats. For convenience ofdescription, the foraminiferal distribution is con-sidered mainly under three major environmentalheadings – coastal marshes and mangrovestands, estuaries and lagoons, and open innershelves, although they may not be easily separa-ble from each other. The treatment is unequal;more attention is given to brackish-water envi-ronments than to those of normal marinesalinity.


9.2 COASTAL MARSHES ANDMANGROVE SWAMPS

Two groups of vegetation are common in inter-tidal zones of wet coastal areas (Fig. 9.1). Thefirst, a group of grasses, mainly prevalent in tem-perate zones, forms salt marshes; the other, agroup of trees, at places intermingled with marshvegetation, is characteristic of mangrove swamps(mangals) of the tropics or the subtropics (Chap-man, 1977). Some of the plant genera in eithergroup, e.g. the marsh grasses Salicornia, Spartina ,Juncus, Arthrocnemum, and Plantango, and themangrove trees Rhizophora, Avicennia, and Acros-tichum, are widespread in both the northern andthe southern hemispheres. These remarkable dis-tributions of the plants are probably related toancient biogeography, but the main areas of saltmarshes and mangrove swamps are on coasts pro-tected from strong wave action, or at major rivermouths (Chapman, 1977).

9.2.1 Salt marshes

The macro-environment of a given salt marshmay seem uniform, but a variety of habitats isavailable to smaller organisms (Teal, 1996).

142 Foraminifera in marginal marine environments

Bradshaw (1968) suggested that the followingfactors are beneficial to Foraminifera living inmarsh habitats: (a) lowering of temperature inshade provided by larger and smaller marshvegetation such as grass, algal mats, and algalclumps; (b) protection from desiccation pro-vided by algal cover; and (c) avai labi l i ty of dia-toms and other algae as food. There is noreliable evidence that a particular kind of marshgrass would support a particular kind of fora-miniferal assemblage (see Hayward and Hollis,1994).

There are problems with measurement of totalproductivity in salt marshes (Long and Mason,1983), but a consensus exists that the produc-tivity is very high (e.g. Chapman, 1977; Valiela,1995). This ecosystem is marked by abundantdissolved nutrients, energy-rich reduced com-pounds, and particulate matter; in some situa-tions, it may be the source of over 40% of thedissolved nitrogen in the less eutrophic, near-shore sea water (Valiela, 1995). The bulk of theprimary production is provided by marshgrasses, but a substantial proportion is con-

nected to intert idal algae (Odum, 1971; Longand Mason, 1983).

The inorganic sediment of coastal saltmarshes is derived from both terrestrial andmarine sources, whose relative importancesdepend on factors such as the amount of rivertransport, strength of t idal flow, and windeffects. In addition, accumulating organic debrismay eventually be preserved as peat and calcare-ous shell material. The organic-matter contentof the sediment is highly variable even in thenear-surface part, e.g. 50% in a Delaware orMassachusetts Spartina marsh and 9% in aMorecamb Bay ( E n g l a n d ) Puccinellia marsh(Howes et al., 1981; Long and Mason, 1983).The substrate is anoxic a few centimeters belowthe surface, except where extensively burrowed(Bertness, 1985).

The grain size of most surf icial marsh sedi-ment is fine, because of low current velocitiesthat are further diminished by the baffle of abun-dant vegetation. The finest sediments are depos-ited at the landward l imit of the tidal excursion,or at the shallow edge of the estuary (Phleger,

143Coastal marshes and mangrove swamps

1977; Chapman, 1977). The baffle effect of marshgrass on the settling rate of suspended sedimentis reflected in the fact that the highest sedimenta-tion rates are frequently at the lowest level ofcontinuous vegetation, and not at the lowestlevel of the marsh (Adam, 1990). A pure sandsubstrate is usually too mobile for marsh grassesto take hold, but salt marshes are common onsandy silt substrates (Chapman, 1977). Drainageis poor in salt marsh substrates, except neartidal channels and where animal burrows areabundant (Phleger, 1977). The salinity of sub-strate pore waters is dependent on severalfactors, one of which is the ground elevation. Inthe often-submerged lower salt marsh, salinityis relatively constant and close to that of theflooding water. In the upper marsh, however,the pore-water salinity can be highly variable.Episodes of tidal flooding are infrequent, and inthe interim, rainfall may cause a reduction ofpore-water salinity. On the other hand, duringperiods of desiccation, this salinity may increasesignificantly through evapotranspiration, whichmay lead to the formation of a saline crust atthe surface. In marsh substrates, pore-watersalinity higher than that of sea water is notuncommon (Adam, 1990).

Foraminiferal zonation. A suite of widespreadagglutinated taxa is generally regarded as typi-cal of coastal salt marshes (Phleger, 1970;Murray, 1971; Phleger, 1977). It includesAmmotium salsum, Arenoparrella mexicana,Jadammina macrescens, Miliammina fusca, Tipot-rocha comprimata, and Trochammina inflata(Fig. 9.2). In addition, a few well-known euryha-line calcareous species, such as Ammonia beccariiand A. parkinsoniana, are commonly present.Careful examinations of the distributions ofthese and other marsh species of Foraminiferareveal that low-marsh assemblages can be distin-guished from high-marsh ones on the basis ofspecies dominance. For example, along theAtlantic coast of North America, where marshesare extensive and the Foraminifera wellrecorded, the following species are usually domi-nant in the three parts of a typical salt marshthat are recognized by their elevations abovethe low-tide mark: ( 1 ) high marsh: Jadammina

macrescens, Tipotrocha comprimata; ( 2 ) middlemarsh: Trochammina inflata; and ( 3 ) low marsh:Elphidium williamsoni, Miliammina f u s c a , Ammo-nia beccarii (or A. parkinsoniana), Haynesina ger-manica (Murray, 1991b). In a particular marsh,however, the distribution may be much morecomplex than suggested by the above scheme,because of the complex interplay of biotic andabiotic factors.

The common features and the inherent vari-ability of marsh foraminiferal assemblages areboth illustrated by data from three marsh areasalong the U.S. Atlantic coast, the first two(Maine and Massachusetts) from between 41°and 45°N latitudes, the third (Georgia) at31°25N. In these zonal schemes, absence or pau-city of some species may be as important as thepresence or abundance of some other.

(a) The relationship between surface elevationand the composition of the foraminiferal assem-blage in the extensive salt marshes of the Mainecoast was studied by Gehrels (1994) along sixtransects, two of which are shown in Fig. 9.3.The foraminiferal zonation was found to be sim-ilar to that reported from the Canadian mari-time provinces by Scott and Medioli (1978,1980a). Using Scott and Medioli’s numericaldesignations of zones, the diagnostic features ofthe zonal assemblages in Maine are as follows:( 1 ) Zone 1A: ‘almost pure’ Jadammina macres-cens forma macrescens assemblage; (2 ) Zone1B: additional high-marsh species, e.g. Tipo-trocha comprimata, Trochammina inflata, andHaplophragmoides manilaensis; (3) Zone 2A:Miliammina fusca replacing Tipotrocha compri-mata and Haplophragmoides manilaensis; (4)Zone 2B: strong dominance of Miliammina fuscaand appearance of Ammotium salsum and calcar-eous species (Gehrels, 1994).

( b ) In the Great Sippewissett Salt Marsh,Massachusetts, Trochammina inflata and Jadam-mina macrescens are abundant in all marsh habi-tats and at all elevations, with J. macrescensforma polystoma becoming more abundant inhigh-salinity areas of outer marshes (Scott andLeckie, 1990). A vertical zonation of surface-sediment Foraminifera (related to salinity andground elevation) in the inner marshes is seen


in the dis tr ibut ion of a number of less commonspecies. The high-marsh zone (mean high waterto landward l imi t of tides), about 22 cm in verti-cal extent, is characterized simply by the paucityof such species, and a great abundance ofTrochammina inflata and Jadammina macrescens.The transitional high-marsh zone, just below the

mean high water, and about 30 cm in ve r t i ca lextent, is marked by the abundance of Tipot-rocha comprimata. The low-marsh zone, wi th thelowermost stands of tal l Spartina alterniflora,extends from about 25 cm below mean sea levelto about 20 cm above i t . The typical foramini-feral assemblage of th i s zone is varied, w i t h

Coastal marshes and mangrove swamps 145

abundant Miliammina fusca, Ammotium salsum,Polysaccammina hyperhalina, Arenoparrellamexicana, and subtidal estuarine species.

(c) Patterns of foraminiferal species abun-dance in Sapelo Island (Georgia) salt marsheswere reported by Goldstein and Frey (1986).When considered against a simple three-zonescheme of elevation, the dominance of Miliam-mina fusca and Ammonia parkinsoniana (A.tepida in subsequent publications of Goldstein)here would indeed be typical of the low marsh.The numerical abundance data, however, showthat A. parkinsoniana is a dominant member ofall three foraminiferal associations recognized inSapelo Island marshes (Goldstein and Frey,1986). The marsh habitats (within a >2 m tidalrange) that support the associations are as fol-lows: ( 1 ) tidal-creek banks and streamside-leveemarshes (association I ) ; ( 2 ) ponded-water

marshes (association I I ) ; and ( 3 ) marshes onmajor tidal inlets (association I I I ) . Miliamminafusca also dominates associations I and I I . Are-noparrella mexicana and Triloculina oblonga aretwo additional dominants of association I.Jadammina macrescens and Trochammina inflataare not dominant species anywhere, but they arerecognized as ‘accessory species,’ the former inassociation I, the latter in both associations Iand II. Tipotrocha comprimata is extremely rare;Haynesina germanica is not reported. Overall,the epibenthic or shallow endobenthic Miliam-mina fusca is the dominant foraminifer in Geor-gia coastal marshes (Goldstein et al., 1995),whereas in Connecticut and Massachusettsmarshes, species whose microhabitats are lessrestricted (e.g. the epibenthic to deep endoben-thic Trochammina inflata or Jadammina macres-cens) are the dominant taxa (Saffert and


Thomas, 1998); apparently, this difference isrelated to the extensive development of lowmarshes in Georgia and high marshes in NewEngland (Saffert and Thomas, 1998).

The separation between a high marsh and alow marsh fauna becomes less clear in the micro-tidal setting of the Gulf of Mexico, with a< 0.5 m tidal range along the Louisiana andTexas coasts (Murray, 1991b). For the marshenvironment as a whole, all of the species fromthe Atlantic seaboard mentioned above occurwidely in Gulf Coast marshes (see, e.g., Phleger,1955, 1960b; Scott et al., 1991).

A comparison of marsh Foraminifera fromeastern South America (35° to > 50° S latitudes)with their counterparts from North America(35° to >50° N) shows a very close similarity,and Jadammina macrescens and Trochamminainflata are common constituents of all or mostassemblages (Scott et al., 1990). The same asso-ciation is characteristic of high marshes innorthern Europe, from microtidal to macrotidalregimes (Murray, 1991b).

Biogeography, local ecology, and the patchi-ness of species distributions introduce a strongelement of variability in the vertical zonation ofmarsh Foraminifera, but a high-marsh and alow-marsh fauna are marked by the same orsimilar groups of species in discontinuous geo-graphic locations. An example of such remark-able faunal similarities is provided by asummation of Pacific Rim marsh faunas (Scottet al., 1996; see Table 9.1); the most noticeablefeatures are the overwhelming dominance ofJadammina macrescens and Trochammina inflatain the high-marsh assemblages, and the consis-tent occurrence of Miliammina fusca in the low-marsh ones.

9.2.2 Marsh Foraminifera as sea-level ortide-level indicators

Locally, the vertical limits of marsh foramini-feral zones may seem to be fixed with relationto mean tide levels. On this basis, the sedi-mentary record of marsh assemblages has beenused to identify past tide levels. For example,the foraminiferal zone boundaries and the abun-

dance peaks of Tipotrocha comprimata in Qua-ternary coastal sediments of Maine may indicatetide levels with a precision of about 15 cm, andthus may be better clues to ancient tide levelsthan marsh plants (Gehrels, 1994). Even on amuch wider regional scale, the presence and var-ying abundances of typical marsh Foraminiferahave convinced some researchers that such datacan help determine sea level or tide level with aprecision of 5–10 cm (Scott and Medioli, 1980a.1986). In this kind of paleoecological analysis,the choice of the modern baseline for the com-parison of the fossil assemblage attains a specialsignificance. For example, a well-known modelof foraminiferal habitat elevation above sea level(Scott and Medioli, 1986) does not fully applyto the marsh assemblage of coastal Georgia,because (a) species considered as typical of thehigh marsh (Jadammina macrescens, Tipotrochacomprimata), if present, range from high to lowmarsh, and ( b ) the model does not includespecies (Reophax nana, Textularia palustris ,Siphotrochammina lobata) that are regionallycommon in habitats less than 1.5 above themean low water (Goldstein and Watkins, 1999).

Environmental factors other than the ebb andflow of tides, especially unrelated salinity varia-tions in substrate pore water may have a criticalinfluence on the distribution of marsh Foramini-fera. For example, in the Great Marshes ofBarnstable, Massachusetts, the foraminiferalzonation (‘marsh fringe,’ ‘middle marsh,’ and‘marsh edge’) is related to (a) the salinity gradi-ent, which is strongly affected by precipitationand groundwater seepage, ( b ) the frequency offlooding, and (c) sediment characteristics, but itdoes not show a connection with elevationabove mean sea level (de Rijk, 1995, de Rijk andTroelstra, 1997). Thus, a global scheme of deci-phering minor sea-level changes based on fre-quency variations of salt-marsh Foraminiferawould be unreliable. Furthermore, in the contextof the small elevation differences reported formarsh foraminiferal zones, the depths of subsur-face microhabitats may become extremely sig-nificant. Common infaunal species of Nanaimo,British Columbia, Canada, show the followingdepth preferences in the substrate: Jadammina

Coastal marshes and mangrove swamps 147

macrescens , 2–8 cm; Trochammina inflata ,0–20 cm (high marsh) or 0–25 cm (low marsh);Haplophragmoides wilberti, 3–7 cm; and Miliam-mina fusca, 0–3 cm (Ozarko et al., 1997). Similardocumentation is available from other areas. Aconsiderable part of the agglutinated assemblageis found below a sediment depth of 2.5 cm inMassachusetts and Connecticut salt marshes,

with Trochammina inflata commonly present atlevels as deep as 20–25 cm (Saffert and Thomas,1998). In the salt marshes of St. CatherinesIsland, Georgia, various agglutinated species arefound wi th in the upper 10 cm of the substrate,but in deeper levels, the common species areArenoparrella mexicana and Haplophragmoideswilberti (Goldstein et al., 1995). Clearly, a sam-


pling of the uppermost one or two centimetersof the substrate would produce a misleadingmodel for the interpretation of small shifts inpast sea level (Ozarko et al., 1997). Finally,taphonomic effects must be factored in, evenwhen calcareous species (very poorly preserved,because of the acidity of marsh sediments) arenot taken into consideration. Goldstein andWatkins (1998) estimate that, in salt marshes ofthe southeastern U.S., as much as 90% of theforaminiferal assemblage in the upper 10cm ofsediment may be removed by taphonomic pro-cesses, and that some deep endobenthic species(e.g. Arenoparrella mexicana) may be muchbetter preserved than shallow endobenthicspecies (e.g. Miliammina fusca), thus introducinga significant bias in the data. Furthermore, typi-cal high-marsh species are better preserved thanlow-marsh species (see chapter 16 for a discus-sion). Thus, although modern d i s t r ibu t ionsof salt-marsh Foraminifera may permit therecognition of microhabitats separated by a fewcentimeters, especially in temperate latitudes,foraminiferal paleoecological analysis is un l ike lyto yield past elevation levels that are nearlyas precise.

9.2.3 Mangrove swamps

Mangrove swamps cover about 70% of thecoasts of the world, and many well-known fora-miniferal species of salt marshes also occur inthese swamps (Boltovskoy, 1984). In particular,two such marsh species, Ammotium salsum andArenoparrella mexicana, also dominate man-grove assemblages in diverse areas, e.g. Trinidad,Florida, Ecuador, Brazil, and Colombia (variousreports, summarized in Boltovskoy, 1984).There may be a remarkable similarity betweenmangrove foraminiferal assemblages from verydifferent longitudes. For example, species ofAmmotium, Arenoparrella, Haplophragmoides,Miliammina, and Trochammina are common tomangove-stand assemblages in Sumatra(Biswas, 1976) and Trinidad (Todd and Brönni-mann, 1957; Saunders, 1958). An exception isseen in the mangrove Foraminifera of northernNew Zealand; Miliammina fusca and two wide-

spread calcareous species of marginal marinewaters (Ammonia beccarii and Elphidium excava-tum) are the dominant species (Hayward andHollis, 1994). The t r ans i t i on from a characteris-tic mangrove-swamp foraminiferal assemblageto a lagoonal assemblage may take place ra therabruptly. On the southern coast of Puerto Rico,such a change takes place w i t h i n a hor izonta ldistance of a few meters, the true mangrovefauna being ent irely agglut inated (except forAmmonia tepida), and the lagoonal fauna beinglargely calcareous (Culver , 1990). Hor izon ta land vertical zonations of foraminiferal speciesw i t h i n mangrove swamps are unclear, but somehave been reported from the Brazilian coast(e.g. Zanine t t i et al., 1979; Scott et al., 1990). Ithas been suggested that these foraminiferalzonations may not be directly associated w i thmangroves, but are controlled by salinity, tem-perature, substrate organic content , and expo-sure to the atmosphere (Scott et al., 1990). Aparallel argument may be made for many marshassemblages.

9.3 ESTUARIES AND LAGOONS

An estuary, according to a definition commonlyaccepted in marine ecology, is a ‘semi-enclosedcoastal body of water hav ing a free connectionwith the open sea and within which the sea-water is measurably di luted wi th fresh waterderiving from land drainage’ (Cameron andPritchard, 1963). Coastal lagoons, unlike typicalestuaries, do not have a wide-open (i.e. free)connection to the open sea (McLusky, 1981).Within any particular latitudinal zone or bio-geographic province, similar foraminifera lassemblages exist wi thin true estuaries andcoastal lagoons. The broad features of theseassemblages and their distributions are summa-rized below. The common environmental featureis the brackish salinity, between 35‰ and 0.5‰.In addition, es tuar ine waters may range fromwell-mixed to highly stratified, and the salinitymay vary more than 3‰ from surface to bottom(Officer, 1983).

Foraminiferal communi t i e s of estuaries and

Estuaries and lagoons 149

lagoons may have conspicuous common ele-ments with both the local marsh or mangrovefauna and the local, inner-shelf, normal-marinefauna; large-scale distribution patterns are gen-erally related to a salinity gradient. Such apattern is well-illustrated by a comprehensivedistribution study of New Zealand marginalmarine species (Hayward and Hollis, 1994). Sev-eral foraminiferal facies (or species associations)related to salinity and tide levels can be iden-tified here on a regional scale; some of these aretypical of intertidal vegetative habitats, but theexact nature of vegetation has little effect onthe foraminiferal associations. Eight species,reported from many areas outside New Zealand,are obligate brackish in all of the studied NewZealand estuaries, harbors, inlets, and lagoons.Some are well-adapted to a considerable salinityrange, and the foraminiferal facies intergrade(Fig. 9.4). Using their overall distributions, how-ever, the species can be arranged in groups ona scale of preference for increasing salinity:(1) Trochamminita salsa (least saline);(2) Haplophragmoides wilberti, Miliamminafusca; (3) Trochammina inflata, Jadamminamacrescens, Ammotium fragile, Pseudothuram-mina limnetis; (4) Helenina anderseni (mostsaline). Several facultative brackish-waterspecies are also present in New Zealand coastalhabitats (Fig. 9.4). In the absence of adjacentmarsh or mangrove swamps, and the presenceof very high seasonal fresh-water discharge, estu-arine foraminiferal zonations may be poorlydeveloped. For example, in the Russian Riverestuary, northern California, the only aggluti-nated species of significance is Miliammina fusca.In the main channel of this estuary, the assem-blage is generally dominated by species that aretypical of shallow marine habitats of this area,but excludes species of Ammonia and Ammoba-culites that are abundant in nearby estuaries.Furthermore, the marine species invade the estu-ary only in summer when fresh-water dischargeis low, and disappear in winter when dischargeis high and the salt-water wedge is removed orreduced in size (Erskian and Lipps, 1977).

Foraminiferal differences among nearby estu-aries may relate to tide levels. On the Atlantic

seaboard of eastern Canada (Nova Scotia andNew Brunswick), such differences are seen in theassemblages of three estuaries: Miramichi, Resti-gouche, and Chezzetcook, the first mainly shal-low subtidal, the second mainly deep subtidal,and the third mainly intertidal (Scott et al.,1980). The sharpest contrast between the inter-tidal and subtidal estuaries is in the absence ofagglutinated species Ammotium cassis in theformer, which may be due to the speculatedpreference of A. cassis for bottom water withcopious suspended particulate matter (Olsson,1976; Scott et al., 1980), or to the large salinityand temperature fluctuations in this intertidalzone. Furthermore, calcareous species such asAmmonia beccarii and Elphidium williamsoni arecharacteristic of intertidal, rather than subtidal,communities. Inter-estuary faunal differencesare much less pronounced in the upper estuaries(dominated by the agglutinated Miliamminafusca) than in the lower, where the marine influ-ence is strong. In general, however, significantabundances of agglutinated species such asSaccammina atlantica, Reophax arctica, andCribrostomoides crassimargo are typical ofdeeper-water eastern Canadian estuaries. Otheragglutinated species may show very high localdominance in the deeper parts of an estuary.For example, in the western part of the Resti-gouche estuary, Eggerella advena and Ammotiumcassis may constitute more than 90% of theassemblage in areas deeper than 10 m, whereasin shallower waters, diverse species, includingthe calcareous Elphidium excavatum, Haynesinaorbiculare, and Buccella frigida, together withthe agglutinated Miliammina fusca, may becommon (Schafer and Cole, 1978).

Extreme dominance of agglutinated specieshas been reported also from several estuaries farfrom Restigouche. A striking example is thedominance of Ammobaculites crassus in Chesa-peake Bay estuaries (Virginia) in 1–15‰ salinity(Ellison and Nichols, 1970; Ellison, 1972). Avery high abundance of A. crassus is supportedby estuarine vegetation (eelgrass) and organic-rich sediment, and this may be the only fora-miniferal species in some of these areas. In sur-rounding habitats, the Ammobaculites facies is


replaced by an Elphidium facies (seaward), aMiliammina-Ammoastuta facies (in marshes), anda thecamoebian facies (upstream). Comparablerelative abundances of Ammobaculites orAmmotium have also been reported from theU.S. Gulf coast, e.g. in Sabine Lake of Texasand Louisiana (salinity < 10‰), where Ammoba-culites or Ammotium (taxonomy uncertain) mayconstitute 40–80% of the assemblage (Kane,1967). Other areas where a species of Ammotium(A. cassis) dominates a brackish-water assem-

blage include southern Brazil (Closs, 1963),Baltic Sea (Lutze, 1965; Olsson, 1976), andSweden (Olsson, 1976). Locally, the effect ofsalinity change on the relative abundance ofAmmotium is shown by the data of Phleger(1954) and Anderson (1968 ) from the same areaof the eastern Mississippi Sound, Alabama. Theforaminiferal assemblage showed a strong domi-nance ( > 9 0 % ) of Ammotium (reported asAmmobaculites sp.) when Phleger sampled thearea. Following an increase in salinity (< 10‰)

Estuaries and lagoons 151

between 1954 and 1967, probably due to theconstruction of a bridge system that divertedfresh-water drainage away from the MississippiSound, Elphidium gunteri and Ammonia parkin-soniana became the dominant species (Lamb,1972).

As in the case of Foraminifera of marshes andmangrove swamps, the species thriving at verylow estuarine salinities are usually agglutinatedtaxa. For example, Miliammina fusca and Ammo-marginulina fluvialis can construct their aggluti-nated tests at about 5‰ salinity in the HudsonRiver estuary, New York, but Ammonia tepidacan secrete only the organic lining, and not thehyaline layers (McCrone and Schafer, 1966). Inthis context, the survival of a few isolated pop-ulations of calcareous species in fresh water(section 9.4) demonstrates an extraordinaryadaptation related to the geological history oftheir habitats.

Some agglutinated species can thrive in bothbrackish and hypersaline waters. The toleranceof such species to unusually high salinities isseen in the distribution of estuarine andlagoonal foraminiferal assemblages along thewest African coast (5°–20°N). Near the mouthof the Casamance estuary, the mixohaline cal-careous assemblage is dominated by species ofAmmonia and Elphidium, but those of Bolivinaand Lagena are also present. In the upperreaches of the estuary, as the salinity increases(because of the arid climate), the relative abun-dances of calcareous species progressivelydecrease, and those of agglutinated species pro-gressively increase, with Ammotium salsum domi-nating. In the Casamance River, specimens ofA. salsum have been found even in waters with100‰ salinity. Farther south, in the nearly land-locked Ebrie Lagoon with a much higher rain-fall, salinity remains below normal marine(hypohaline), but A. salsum is still the dominantspecies (Debenay, 1990).

Among calcareous taxa, Ammonia and somespecies of Elphidium are well-known for theirtolerance to salinity fluctuations. These are pre-sent in estuarine faunas of many latitudinalzones. In the Pennar estuary, Bay of Bengal,where monsoonal river discharges cause severe

seasonal reduction of salinity, living populationsof Ammonia beccarii and Elphidium spp. arefound in a salinity range of about 0.5 to 35‰(Reddy and Jagadishwara Rao, 1984). On theArabian Sea coast of the Indian peninsula,Nigam et al. (1995) found that the relative abun-dance of Rotalidium annectens covaries withestuarine sal ini ty, and used the stratigraphicvariation in this abundance ( i n an inner shelfcore) as a tracer of past monsoonal intensities.

Lagoonal salinities may range from brackishto hypersaline, depending on local climate andtidal flushing. Foraminiferal assemblages oflagoons show great variability, but many aresimilar to the assemblages of local estuarymouths. On the other hand, different hydro-graphic characters of adjacent brackish-waterlagoons may lead to different foraminiferalassemblages. An illustration is provided by thebiotas of Alvarado and Camaronera lagoons onthe southern coast of the Gulf of Mexico(Phleger and Lankford, 1978). AlvaradoLagoon is directly connected to the Gulf by aninlet; Camaronera, with no direct l ink with theGulf, is connected to Alvarado by a narrowchannel, but is more influenced by runoffs fromsurrounding mangrove swamps. The faunas ofboth lagoons have a strong mangrove swampcomponent (e.g. Ammotium salsum and Miliam-mina fusca). A marine component (e.g. Ammoniaparkinsoniana and Elphidium spp.) is present inAlvarado, but not in Camaronera, whereAmmotium salsum usually constitutes about 90%of both living and dead assemblages. In lagoonswith significant tidal inflow, the dominanceof Ammonia beccarii or A. parkinsoniana iscommon. For example, in the lagoon of Venice,Italy, where the degree of marine- and brackish-water mixing and the seasonal variabilty ofhydrographic properties are reflected in thepresence of several foraminiferal biotopes, thedominant species is invariably Ammonia becca-rii, constituting about 50–75% of the assem-blage (Albani and Serandrei Barbero, 1982;Albani et al., 1998).

In brackish waters, the general trend of fora-miniferal species diversity, as measured by rich-ness (species count), is one of decrease with


decreasing salinity. This pattern is wellil lustrated by data from continental shelves,estuaries, and lagoons of the Black Sea, whichis entirely brackish. Foraminifera are present inthe oxic (and upper depths of the BlackSea margin, but there is a persistent diversi tygradient among the sampled areas (Yanko andTroitskaja, 1987; Yanko, 1990b, 1998), with thehighest number (79) near Bosporus, where thesal in i ty is relat ively high (26‰), because of theinf lux of Sea of Marmara waters. The lowestnumbers (< 10) are in lagoonal or deltaic areas,where the sal ini ty is depressed to < 2‰ by fresh-water discharge. A parallel decline is seen alsoin the number of Mediterranean immigrantsthat form the main component of the Black Seaforaminiferal assemblages (Fig. 9.5).

The geographic distr ibution of some brackish-water foraminiferal species covers spectacularlywide la t i tudinal and longi tudinal ranges. Thesespecies have a high tolerance to the variabilityof marginal-marine environments, but why istheir dis t r ibut ion not blocked by major oceans?Examining this question in the context of marsh,

mangrove-swamp, and tidal-flat Foraminifera ofNew Zealand, Hay ward and Hollis (1994) con-clude tha t these species travel great distancesaerially, by accidental transport (and occasionals u r v i v a l ) on the muddy feet or feathers of migra-tory seabirds, because ‘for the major i ty of thesebirds the first and last l andfa l l s on t he i r journeysare intert idal mud and sand flats.’ Such intercon-t inen ta l sweepstakes dispersal (see Simpson,1953) by seabirds has been suggested also forsmall plants, such as the common sundew (Dros-era anglica), a t i ny , carnivorous, bog p l an t t h a tis widely d is t r ibu ted in the nor thern hemisphere.The dispersal of th is plant to the H a w a i i a nislands was apparent ly by means of seeds t rans-ported on muddy feet of birds (Car lquis t , 1980).The most l i k e l y carrier is the Pacific goldenplover, which breeds in Alaska, and wintersin large numbers in Hawai i , in the h a b i t a tfavored by the sundew (H.D. Pratt , personalcommunication).

Transport by birds is also a plausible mecha-nism for many shorter-distance migrat ions offoraminiferal species, inc luding that from a

Open inner shelves 153

marine environment to a landlocked saline lakeor well (see examples in Resig, 1974). The activ-ity of other animals may also play a role inforaminiferal transport. The introduction ofAmmonia, Elphidium, and miliolids in the land-locked, brackish Salton Sea of California hasbeen ascribed to ‘birds, naval seaplanes, trans-plantation of marine fishes, and speed-boating’(Arnal, 1954). Trochammina hadai, a commonspecies of Japanese estuaries, was introduced inthe 1980s into San Francisco Bay, California,where it is now abundant; the species was proba-bly released into this habitat with ballast sea-water (McGann and Sloan, 1996).

9.4 FRESH-WATER FORAMINIFERA

Typically, the crossing of the threshold frombrackish to fresh-water environments is markedby the disappearance of foraminifers other thanthe organic-walled Allogromiida. There are,however, a few localities where both aggluti-nated and calcareous species are known tothrive in fresh water, and are interpreted to bethe ‘survivors of a prehistoric brackish fauna’(Brady et al., 1870). The best documentation ofsuch fresh-water foraminiferal taxa is fromnorthern Argentina and southern Brazil in waterdepths of a few meters and salinities as low as0.1‰ (Boltovskoy and Lena, 1971; Boltovskoyand Wright, 1976). A calcareous species, Noniontisburyensis, is the most persistent member ofthis assemblage, but agglutinated species,belonging to Miliammina, Psammosphaera, andTrochammina, are also known; all of thesespecies occur also in nearby brackish areas. Mili-ammina fusca is known to occur in Lake Mara-caibo, Venezuela, in waters of about 1‰ salinity(Hedberg, 1934).

9.5 OPEN INNER SHELVES

9.5.1 Clastic shelves

For the purposes of this discussion, the shallow-est part of a continental shelf, from the low tide

to a depth of about 30 m, is regarded as theinner shelf, although the foraminiferal biotopein many areas may not be significantly differentat somewhat greater depths (e.g. at 50 m). Awide range of species is present among inner-shelf foraminiferal assemblages, and there is alarge body of li terature on their distributions(see Botovskoy and Wright, 1976; Murray.1991b). A few examples of assemblages fromclastic substrates are given here; those from car-bonate substrates are discussed in section 9.5.2.The bottom-water salinity in these habitats iswithin the normal marine range, i.e. about34–35‰. Unless indicated otherwise, the datarefer to total ( l iv ing and dead) populations ofspecies.

Compared to inshore brackish areas, openinner shelves, including those of large bays, gen-erally support much higher numbers of fora-miniferal species, usually with the dominance ofthe calcareous group. The large-scale distribu-tion of foraminiferal taxa on inner shelvesreflects a biogeographic zonation in which tem-perature (especially its seasonal variation) is fre-quently the critical factor that promotes orhinders the proliferation of certain species orassemblages. Precise latitudinal comparisonsof inner-shelf foraminiferal communities aredifficult to make, because of uneven area andsample coverages, patchiness of small-scale dis-tributions, and non-uniform laboratory pro-cedure. Judging simply by numbers of speciesreported from entire (inner, middle, and outer)continental shelves, it is probable that for openinner shelves, there is a general diversity increasefrom higher to lower latitudes, in keeping withthe general diversity trend of shallow marinebiotas (e.g. Briggs, 1974). Locally, a significantchange in species diversity from one shallow-marine biogeographic province to the next isseen in an exceptionally well documented recordof foraminiferal distribution in equal-volumesamples taken from the Cape Hatteras region,North Carolina (Schnitker, 1971). Cape Hat-teras (35°14Ń, 75°32´W), where the Gulf Streamleaves the continental margin, is the location ofthe most pronounced marine faunal boundaryon the eastern North American continental


shelf, between the Atlantic Northern Inner Shelfand the Atlantic Southern Shelf foraminiferalprovinces (Culver and Buzas, 1981b; or the Vir-ginian and Carolinian molluscan provinces, seechapter 6). The mean numbers of species ( l iv ingand dead) found in two sample groups from20–25 m water depths (each with 10 samples)are 13 for the northern area and 33 for thesouthern (and somewhat warmer) area. There isalso a pronounced increase in total species rich-ness (s) from inshore waters to those near theshelf edge (at about 80m). In Schnitker’ssamples, the mean value of s in the 50–80 mdepth range is 35 in the northern area (5samples), and 47 in the southern area (9samples). In a large suite of samples taken fromthe Georgia continental shelf (between 30°41Ńand 32°00Ń latitudes), the values of s and theShannon-Wiener function of diversity (seeGibson and Buzas, 1973) are distinctly lower innearshore waters (where they rise steadily) thanin waters deeper than 15 m (Fig. 9.6; Sen Guptaand Kilbourne, 1974).

Several regional studies on Arctic Foramini-fera have been published, but the coverage ofthe inner shelf is poor. On the whole, aggluti-nated species such as Spiroplectammina bifor-mis, Textularia torquata, and Eggerella advenaare dominant or common (Arctic Canada;

Vilks, 1989). The calcareous component of thefauna may include several species of Elphidium(including E. excavatum), Buccella inusitata,Astrononion gallowayi, Islandiella islandica, andvarious miliolids (Alaska; Loeblich and Tappan,1953). Many of these have been reported tocontinue in water depths >100m (e.g. Schaferand Cole, 1986), but habi ta t determinations onthe basis of distributions of total populations isdifficult on high-energy Arctic shelves, becausesediment reworking is extensive (Vi lks , 1989).In the eastern Arctic, in shallow depths (< 30 m)of Freemansundet Strait (Barents Sea), Cassidul-ina reniforme (restricted to cold, northernwaters), Elphidium excavatum, and Cibicideslobatulus (epibenthic on coarse sediment) domi-nate the assemblage (Hansen and Knudsen,1992).

The effect of substrates and factors related towater depth on a cold-water nearshore fauna isreported for a 58-species assemblage fromMcMurdo Sound, Antarctica, where seven bio-topes (sediment with boulders, open deeperwater, sponge mat, sediment under sponge mat,seasonally anoxic basin, shallower water, andanchor ice) are recognized in waters < 27 mdeep (Bernhard, 1987). Several species that arerelatively rare are restricted to particular bio-topes, e.g. Notodendrodes antarctikos andChilostomella sp. to the open deeper-water bio-tope. The more abundant species are present inmultiple biotopes, but among them, Globocassi-dulina sp. cf. G. biora and Reophax dentalini-formis are more common in sediments withboulders; Epistominella exigua, Cribrostomoidesjeffreysii, and Trochammina ochracea in shallowareas; Uvigerina bassensis in open deeper water;and Tolypammina vagans and Polymorphina sp.in seasonally anoxic basins.

As in the case of estuaries, species of Elphidiumand Ammonia frequently dominate inner shelfassemblages in many lat i tudinal zones. In a totalassemblage of 22 species from an inner shelf ofthe English Channel (Lyme Bay, maximumdepth about 50 m), the dominant species areAmmonia beccarii, Elphidium excavatum, Quin-queloculina lata, and Brizalina pseudopunctatain muddy sands, and Textularia torquata in


shelly sands. The major difference between thedominance patterns of living and dead assem-blages is in the proportion of Stainforthia fusi-formis, extremely high in the former, but mostlyinsignificant in the latter, because of postmortemdestruction of its delicate tests (Murray, 1986).In the southern North Sea, Elphidium excaratumis the dominant foraminifer in about 25–30 mwater depth in the living assemblage (Murray,1992). The foraminiferal community in the inter-tidal zone of Puerto Deseado, Patagonia (salin-ity about 32–34‰) consists of about 130 species(Boltovskoy and Lena, 1970), but sizeable livingpopulations were recognized in only fourspecies: Buliminella elegantissima, Elphidiumarticulatum, Epistominella exigua, and Elphidiumgunteri (ranked according to relative abundance;Boltovskoy and Lena, 1969).

On the Georgia continental shelf, U.S.A.,Ammonia beccarii dominates the assemblages inthe shallowest waters, but at about 15 m waterdepth, where there is a shift in the diversitygradient (see above), Elphidium excavatumbecomes dominant. An inshore thanatotope,whose outer limit is close to the 25-m isobath,has been recognized in this area on the basis ofcluster analysis of relative-abundance data.Species common in this thanatotope, besides A.beccarii and E. excavatum, are Planulina exorna,Planorbulina mediterranensis, Asterigerina cari-nata, and Quinqueloculina lamarckiana (SenGupta and Kilbourne, 1976). Ammonia beccarii,Elphidium gunteri, Nonionella atlantica, andHanzawaia concentrica (among others) aredominant on the inner continental shelf of Nige-ria (0–35 m; Adegoke et al., 1976). The same orsibling species are dominant on clastic innershelves of the Caribbean Sea (e.g. Seiglie, 1966)and the northwestern Gulf of Mexico (personalobservation). On the inner shelf of Senegal(depths < 25 m), the typical species are Cribroel-phidium poeyanum, Elphidium gunteri, Haynesinadepressula, Nouria poltmorphinoides, Pileolinatabernacularis, Ptychomiliola separans, and Spir-oplectinella wrighti (Debenay and Redois, 1997).

Numerous workers, including Alcide d’Or-bigny (Heron-Allen, 1917), have studied conti-nental shelf foraminifers from the Mediter-

ranean Sea (see Murray, 1991b). The speciesdiversity of some inner-shelf assemblages is high,as illustrated by the data on replicate samplesof living populations collected from 16 points(spaced one meter apart on a sampling grid) atone locality in the Gulf of Trieste, northern Adri-atic Sea (Hohenegger et al., 1993). The waterdepth here is about 15m; winter and summersalinities and temperatures are about 36‰ and42‰, and 9°C and 23°C, respectively. Fortyspecies were found living, using the Rose Bengalstaining test. These included eight agglutinatedspecies (Reophax nana, Spiroplectinella sagittula,Cribrostomoides jeffreysii, and Eggerelloidesscabra dominating), 10 porcelaneous species(Miliolinella subrotunda and Triloculina affinisdominating), and 22 hyaline species (Brizalinastriatula, Nonionella turgida, Ammonia tepida,Elphidium advenum, E. granosum, Bulimina sp.,and Epistominella vitrea dominating).

As shown by this spotty survey, a largelycalcareous assemblage dominated by Elphidium,with or without co-dominance of Ammonia, istypical of cold-temperate to tropical, inner con-tinental shelves with clastic substrates andnormal marine salinity (Sen Gupta, 1977). Thisnearshore Elphidium-Ammonia association wasnoticed by Natland (1933) in a pioneering studyof foraminiferal depth zonation off California,and was later recognized as the characteristicelement of a biota present along the easternPacific shoreline (in depths of 0–30 m) fromCentral America to northern California (Smith,1964). Reports from many other continentalshelves indicate that one species of Elphidium,E. excavatum, may be nearly as widespread asAmmonia beccarii. This question is not fullyresolved, because taxonomic distinctions amongsome Elphidium species are confusing and highlycontroversial, due to the intraspecific variablityof retral processes. Current practice places atleast four previously recognized ‘species’ (nowlabeled ‘formas’) within E. excavatum (Feyling-Hanssen, 1972). Further taxonomic investiga-tion may result in a bigger lumping. One of thevariants, E. excavatum forma clavatum, is appa-rently restricted to a high northern lati tude belton both sides of the Pacific and Atlantic Oceans


(Smith, 1970). This is also the common form ofE. excavatum in marginal marine environments,including brackish water, in New Zealand ( H a y -ward and Hollis, 1994). In contrast, Elphidiumdiscoidale is known be a ‘typical warm-waterforaminifer’ (Boltovskoy, 1970); its presence at41°S lat i tude on the northern Argentine innershelf has been taken as indicative of the influenceof a Brazilian coastal water mass (Boltovskoy,1970).

Species of Elphidium are generally known orassumed to be inhabitants of the continentalshelf (although not necessarily the inner she l f ) ,and their presence in bathyal or abyssal sedi-ment is regarded as evidence of sedimentreworking (e.g. Phleger, 1951b). There are excep-tions, however. Populations of E. excavatumhave been recovered from waters as deep as2000 m off eastern Canada and northeasternU.S., and recognized as l iving by staining withSudan Black B or Rose Bengal (Schafer andCole, 1982; Corliss and Emerson, 1990).Another species, E. batialis, is apparentlyrestricted to deep waters; l i v ing populationshave been reported from depths of 1000 m offnortheastern Japan (Matoba, 1976).

Extraordinari ly high tu rb id i t y and volumi-nous sediment inf lux can prevent the establish-ment of foraminiferal communities on innercontinental shelves. On the Amazon shelf ofnorthern Brazil, no foraminifers were found insamples collected near the river mouth in waterdepths of 8–20m (Vilela, 1995).

9.5.2 Coral reefs

Modern larger foraminifers (adul t lest size> 1 mm) produce the bulk of the global fora-miniferal reef carbonate (Langer et al., 1997). Inthe Pacific and Indian Oceans ( for which datahave been compiled), their distr ibution and thatof reef-building corals have comparable la t i tud i -nal limits, 42°N–40°S for the former, and39°N–36°S for the latter (Belasky, 1996). Theworldwide distr ibution of symbiont-bearinglarger Foraminifera has been summarized anddiscussed in chapter 8. Many of these speciesand numerous smaller species are well adapted

to the shallow, well-lit , but nutr ient -poor watersof coral reefs and reef slopes in a l l tropical seas.

Characteristic reef-flat foramini fe ra l assem-blages are par t icular ly diverse in the Pacificand Indian Oceans, and include large, freeor attached, calcareous species wi th dis t inc t ivemorphologies, e.g. Calcarina spengleri,Amphistegina lessonii, Marginopora vertabralis,Homotrema rubra, Miniacina miniacea, and Car-penteria proteiformis (Marshall Islands; Cush-man et al., 1954). A comprehensive list offoraminiferal species constituting a typicalPacific reef-flat community would be muchlarger, as shown by Baccaert’s census (1986) ona small part of the northern Great Barrier Reef,Australia. From three reef flats off Lizard Island,104 species were identif ied; eight of these wereagglutinated, 43 porcelaneous, and 53 hyaline.The dominan t species were as follows: (a ) porce-laneous: Peneroplis planatus, Sorites orbiculus,and Marginopora vertebralis, and (b) hyaline:Amphistegina lobifera, Calcarina spengleri, Bacu-logypsina sphaerulata, and Elphidium crispum.The foraminiferal communi ty was found to l ivemain ly on or in the spongy algal cover of thereef, which provides nour i shment and protectionfrom desiccation at low tide. Some robusthyal ine foraminifers (Amphis tegina, Calcarina,Baculogypsina, and Marginopora) were foundattached by their pseudopodia to the t h a l l i ofthe calcareous alga Hal imeda.

The most widespread foraminifer genus ofcoral reefs and other shallow, tropical carbonatebanks or hard ground is Amphistegina. Fivespecies are known from the Indo-Pacific region,and four from the Gul f of Aqaba (Reiss andHottinger, 1984); two of these, A. lessonii andA. lobifera, are abundant in waters < 30 m deep.A single, indigenous, shallow-water species, A.gibbosa, is present in reefal areas of the Carib-bean Sea and Gulf of Mexico. Nummul i t i dgenera, except for Heterostegina, are mostly pre-sent in deeper waters (see chapter 8). Alveolinellaand Borelis, two porcelaneous genera of uncom-mon morphology (p l an i sp i r a l l y coiled along anelongate axis, w i t h numerous chamberlets;reminiscent of late Paleozoic fusu l in ids ) , aref requen t ly found in Indo-Pacific reef sediment


(Hohenegger, 1994); Borelis is also present inother tropical areas (see chapter 8).

In coral reef substrates off Fernando de Nor-onha, northern Brazil, Lévy et al. (1995)observed a depth separation of porcelaneousgenera within a water depth of 30 m – a soritid-Quinqueloculina-Triloculina group dominatingin depths less than 10m, and a Pyrgo-Borelisgroup in greater depths, the ubiquitous hyalinereef genus Amphistegina being associated withthe second group. Faunal differences betweenreef patches and muddy sediment are strikinglyvisible in two adjacent bays, both shallower than25 m, on the leeward side of St. Lucia, WestIndies (Sen Gupta and Schafer, 1973). Thespecies count is comparable, 138 in Choc Bay(with coral reefs) and 112 in Castries Bay, butthe dominance pattern is very different. Amphi-stegina gibbosa, Rotorbinella rosea, Sorites mar-ginalis, and Textularia conica dominate theChoc Bay assemblage, whereas Ammonia tepidaand Elphidium poeyanum dominate the CastriesBay assemblage. Quinqueloculina lamarckiana isthe only species that occurs abundantly in bothbays. As shown by observations in the Gulf ofAqaba, algal covers on hard substrates may bethe preferred habitat of many larger or smallerforaminifer species associated with coral reefs.Seasonal transport of ‘algal clouds’ lead to dis-persal of these species (Reiss and Hottinger,1984).

9.5.3 Seagrass habitats

About fifty species of marine angiosperms, com-monly known as seagrasses, inhabit today’sinner continental shelves (den Hartog, 1977).They stabilize the seafloor sediment, and pro-vide shelter, including anchor, to a most diversebiota. Thus, the presence of seagrass in subtidaland intertidal habitats may lead to significantmodifications of these habitats, causing pro-nounced changes in benthic communities,including an increase of epifauna and shallowinfauna (e.g. Posey, 1988). The trophic resourcesof seagrass meadows are large and varied, andconsiderable nutrient recycling takes place inthese environments (den Hartog, 1977; Zieman

and Zieman, 1989). Seagrass ecosystems are rec-ognized to be among the richest and most pro-ductive coastal ecosystems, a considerable partof the primary production being carried out bya variety of epiphytic algae, which directly pro-vide food and shelter to a spectrum of meiofaunaand microfauna. The adaptation of benthicForaminifera to particular species of seagrassis poorly understood, and their possibleco-evolution remains an enigma. However, asso-ciations of foraminifers and seagrass meadowsare widely reported in the literature. The best-known associations are those of the Soritidae, aporcelaneous foraminiferal family (whosemember species have dinoflagellate or chloro-phyte endosymbionts; see chapter 8), with sea-grass meadows, especially those of the tropicaland subtropical Thalassia (Bock, 1969; Murray,1991b; Martin, 1986; Hallock et al., 1986a; Lévy,1991; Hallock and Peebles, 1993). In fact, severalsoritid species (e.g. Archaias angulatus, Cyclorbi-culina compressa, Sorites marginalis, S. orbiculus,Parasorites orbitoloides) are regarded as tracersof ancient seagrass habitats, and hence as usefulpaleoenvironmental markers (Brasier, 1975;Eva, 1980; Anderson et al., 1997).

Various porcelaneous and hyaline Foramini-fera are known to be attached to the Mediterra-nean seagrass Posidonia. Examples of the firstgroup are species ofVertebralina,Sorites, Nube-cularia, and Cornuspiramia; those of the secondare Planorbulina, Miniacina, Cyclocibicides, andWebbinella ( K i k u c h i and Pérès. 1977; Murray,1991b; Langer, 1993). In addition, motile grazersand temporarily attached taxa such as speciesof Peneroplis and Rosalina are common. Langer(1993) estimates that over 95% of foraminiferalspecies living in seagrass or macroalgal sub-strates are permanently or temporarily motile.Furthermore, some of the attached seagrassForaminifera may be attached to roots or stems,and not to blades of seagrasses (Langer, 1993).For example, in the Gulf of Aqaba, large popula-tions of the hyaline species Acervulina inhaerensand Miniacina sp. are attached to the stems, andnot to the blades, of Cymodocea; the tests ofsoritids (Amphisorus hemprichii and Sorites orbi-cutlus) attached to Cymodocea and Zostera are


modified for a good fit on the stems (Reiss andHottinger, 1984). In the same area, the porcela-neous species Peneroplis planatus prefers thehorizontal rhizomes and stems of Halophila, andthe sediment underneath, over the erect blades(Faber, 1991).

The dependence of soritids on seagrass oralgal turf can be inferred from the compositionof the foraminiferal community of West FlowerGarden Bank, the northernmost modern coralreef in the Gulf of Mexico. Because of the waterdepth of the reef ( >20 m), extensive vegetativecovers are missing, and so are the soritids,although living Amphistegina and Peneroplis arepresent (Poag and Tresslar, 1981). It must beemphasized, however, that the soritid-seagrassassociation is complex, because soritid speciesmay be epiphytic on seagrass in one place, butnot in another. Archaias angulatus is the domi-nant shallow-water larger foraminifer in theFlorida-Bahamas carbonate province (Hallocket al., 1986a), and is often associated with Soritesmarginalis in seagrass habitats. However, studiesin the Florida Keys show that the first soritid,being also present in reef rubble, is more eury-topic than the second, although its preferencefor Thalassia substrates is well-documented (e.g.Martin, 1986; Hallock et al., 1986a; Hallock andPeebles, 1993). In this province, the euryhalinesoritid Androsina lucasi is reported from bothmangrove and seagrass habitats (Lévy, 1991).

Seagrass habitats are known to support fora-miniferal communities even when the wateris brackish or hypersaline. The abundance ofAmmobaculites in Chesapeake Bay, Virginia,provides an example of the first case (see sec-tion 9.3), whereas the foraminiferal biota ofShark Bay, a semi-isolated embayment of theAustralian Indian Ocean, illustrates the secondcase (Logan and Cebulski, 1970; Davies, 1970).In salinities ranging between 40‰ and 56‰,seagrass stands support a large foraminiferalcommunity, including the agglutinated Textu-laria, the porcelaneous Peneroplis, Marginopora,Quinqueloculina, and Triloculina, and the hya-line Elphidium, Amphistegina and Cibicides. Insalinities as high as 70‰, a few porcelaneoustaxa survive on substrates with algal cover; the

dominant species are Miliolinella circularis, Pen-eroplis planatus, and Spirolina hamelini. The tol-erance of Peneroplis planatus to hypersalineconditions is also demonstrated by a study inthe Abu Dhabi Lagoon, Persian Gulf. Here thespecies is epiphytic on seagrass in about 42‰salinity, and on seaweed in salinities as high as70‰ (Murray, 1970).

Foraminiferal species richness in tropical ornear-tropical seagrass meadows is high; 66species were found l iving in a small area ofThalassia in the Florida Keys, but the numberwas adversely affected by turbulence (Bock,1969). The relationship between populationdensities of foraminiferal epiphytes and those ofhost seagrasses is unknown, but in one field testin Papua New Guinea, where a soritid (Margino-pora vertebralis) is attached to blades of variousseagrasses, no correlation was found betweenthe two parameters (Severin, 1987a). As dis-cussed earlier, large populations of the samespecies flourish in sediments of Pacific reefs (seealso Ross, 1972). The dispersal of foraminiferalepiphytes on uprooted or torn seagrass bladeshas been reported (Bock, 1969; Davaud andSeptfontaine, 1995). In addition, gas bubblestrapped in decaying seagrass may help transportforaminiferal tests, as in the case of Sorites andPeneroplis in Tunisian intert idal areas (Davaudand Septfontaine, 1995).

9.6 SUMMARY

Hundreds of known benthic foraminifer specieslive in coastal marine environments. Most ofthem are rare. The dominant species are widelydistributed, many across major biogeographicbarriers. The transoceanic distr ibut ion of someabundant marsh and estuarine species is hardto explain, except by accidental transport andhigh tolerance to environmental variables. Thetransition from a brackish to a normal-marinenearshore fauna is generally marked byincreases in species diversity and the proportionof calcareous species in the community. A fewcalcareous genera are represented by the sameor sibling species on the soft, clastic substrates

Acknowledgments 159

of many inner continental shelves, spanninglarge latitudinal and longitudinal ranges. Hardsubstrates and marine vegetation in the tropicssupport a large variety of taxa, including nearlyall living species of larger Foraminifera. With afew exceptions, the biogeographic imprint onnearshore, open-marine faunas is best seen inthe composition of the entire assemblage, ratherthan in the presence or absence of a few domi-nant species.

9.7 ACKNOWLEDGMENTS

I thank Charles Schafer, Susan Goldstein, andPamela Hallock for reviewing the manuscript,and Mary Lee Eggart for drawing the figures.


10Benthic foraminiferal

microhabitats below thesediment-water interface

Frans J. Jorissen

10.1 INTRODUCTION

Benthic Foraminifera do not live exclusively atthe sediment-water interface, and can be foundalive at considerable depths in marine sediments,in many cases down to 10 cm ( Fig. 10.1) . Withinthis depth interval, large changes take place in thenatural environment, especially in the case of fine-grained sediments, the surface layer and the deepsediment layers forming two very different worlds.At the sediment-water interface, the sea water maybe rich (even saturated) in oxygen, high-qualityorganic matter is often available, and in the photiczone, there is l ight. Deep in the sediment, condi-tions are drastically different: often there is nooxygen, except in halos around metazoan bur-rows, but there may be toxic substances (e.g.instead. Furthermore, the remaining organicmatter may be mostly refractory, with a low nutri-tional value (see chapter 11) . Apparently, thedeeper sediment layers, with their poverty ofresources and lack of oxygen, form an inhospita-ble or even hostile environment for many organ-isms, and as a consequence, animal life is generallyscarce (Fenchel and Finlay, 1995). Nevertheless,

Barun K. Sen Gupta (ed.), Modern Foraminifera, 161–179©1999 Kluwer Academic Publishers Printed in Great Britain.

In most oceanic environments , only the top cen-timeters or millimeters of the sediment contain

10.2 ECOLOGICAL CONSTRAINTS ATAND BELOW THE SEDIMENT-WATERINTERFACE

a relatively important stock of i n f a u n a l organ-isms, including benthic Foraminifera, may bepresent.

There must be significant differences in themode of life between the Foraminifera l iv ing atthe resource-rich, oxygenated, sediment-waterinterface, and their counterparts l iv ing deeper inthe sediment. Understanding such differences inthe functioning of these two groups of Foramini-fera is essential for our comprehension of theecology of this important group of meiofauna,and its role in marine ecosystems. The facts thatbenthic Foraminifera fossilize well, and mayconsti tute the only tracers of ancient benthicenvironments, provide an additional reason toinvestigate the ecology of both epifaunal andinfaunal components of the assemblage.

162 Benthic foraminiferal microhabitats below the sediment-water interface

oxygen (e.g. Jørgensen and Revsbech, 1989). Theoxygen content, which usually shows an expo-nential downward decrease, is the result of theequil ibr ium between downward diffusion andthe depletion caused by the aerobic degradationof organic matter in the sediment. Macrofaunalburrows, however, may locally create oxic envi-ronments deeper in the sediment (Aller and

Aller, 1986; Meyers et al., 1987, 1988). A muchdeeper than usual oxygen penetration may befound in coarse-grained, high-energy, shallow-water environments, or in very oligotrophicdeep-sea areas (e.g. Rutgers van der Loeff, 1990).

Below the oxic zone, other oxidants are usedas electron acceptors by bacteria responsible forthe anaerobic degradation of organic matter. In

Background: Benthic foraminiferal microhabitat research 163

the microxic zone (see chapter 12), where oxygendrops to minimal values, nitrate, and

are reduced. Below this zone, in com-pletely anoxic sediments, sulfate reduction andmethanogenesis take place (Froelich et al.,1979). The precise depth at which each of theoxidants of this succession is used depends againon the downward diffusion of oxygen, and onthe amount of reactive organic matter intro-duced into the sediment. In case of an increasingflux of organic matter, a larger part tends tobe mineralized under anaerobic conditions(Fenchel and Finlay, 1995). In such situations,the lower part of the oxic zone may overlapwith the upper part of the zone of sulfate reduc-tion (Fenchel, 1969).

The majority of all marine macro- and meio-fauna are aerobes, and occur only in the oxicsurface layer of the sediment. Some species, how-ever, seem to be present exclusively in the micro-xic zone, where nitrate reduction takes place,and only a few taxa occur in the zone of sulfatereduction. All three groups are present amongprotozoans (Fenchel and Finlay, 1995), butmost infaunal organisms living in apparentanoxia may actually be microaerophiles thatdepend on oxygen cencentrations below theactual detection limits, or may survive periodsof anoxia.

The flux of organic particles from surfacewaters to the seafloor is the main food sourcefor most deep-oceanic ecosystems. Only a smallfraction of the organic matter arriving at theseafloor is directly consumable by the macro-and meiofauna. Most of these labile particlesare immediately consumed at the sediment-water interface and in the first millimeters of thesediment (Reimers et al., 1986; Carney, 1989).As a consequence, the organic matter rapidlybecomes more refractory with increasing sedi-ment depth. Deeper in the sediment, the remain-ing (refractory) organic matter has first to beconverted into bacterial biomass (Hargrave,1970; Carney, 1989), or at least be partiallydegraded by anaerobic microbial activity, beforeit can be consumed by meio- or macrofauna.The anaerobic bacterial biomass is highest inthe sediment layer immediately below the oxic

zone (Fenchel and Finlay, 1995). Because of thescarcity of predators and competitors there, thiszone will be very favorable for organisms toler-ant to the low oxygen levels.

In response to this vertical trend in food avail-ability, two main types of deposit feeders can bedistinguished in oceanic ecosystems: one livingat the sediment surface, and feeding on labilepaniculate organic matter, the other living inthe sediment, and feeding on bacterially medi-ated labile organic matter (Levinton, 1989). Ingeneral, the often intermit tent flux of labileorganic matter to the ocean floor favors con-sumers with an opportunistic life strategy,whereas the deeper sediment layers, with a foodsource that is much more stable in time, will beinhabited especially by K-strategists (Levinton,1972, 1989; Rice and Rhoads, 1989).

10.3 BACKGROUND: BENTHICFORAMINIFERAL MICROHABITATRESEARCH

A ‘microhabitat’ is a microenvironment charac-terized by a combination of physical, chemicaland biological conditions (oxygen, food, toxic-substances, biological interactions, etc.). Thesecharacteristics separate adjacent (and oftenclosely spaced) microhabitats, and make a par-ticular microhabitat attractive or at least tolera-ble for some taxa, but uninhabitable for others.In any given seafloor habitat, specific microhabi-tats are present at the sediment-water interface,in the lower part of the water column, and inthe top layer of the sediment. In this chapter Iwill focus on the microhabitats below the sedi-ment-water interface.

The notion of benthic foraminiferal life deepin the sediment is relatively recent. Unti l the1960s, the general opinion was that benthicForaminifera live at the sediment-water interface(e.g. Myers and Cole, 1957), and as a conse-quence, it was common practice to sample onlythe top one or two centimeters of the sedimentfor foraminiferal studies. Early papers thatdescribe Foraminifera deeper in the sediment(e.g. Myers, 1943b; Richter, 1961, 1964; Buzas,


1965, 1974, 1977; Boltovskoy, 1966a; Brooks,1967; Lee et al., 1969; Schafer, 1971b; Ellison,1972; Frankel, 1972, 1975a,b; Matera and Lee,1972) all concern shallow water environments,where living Foraminifera are found in consider-able sediment depths, but without noticeablecompositional changes with depth. Since the pub-lications of Thiel (1975), Coull et al. (1977), andBasov and Khusid (1983), we know that in deep-sea environments too, Foraminifera can live deepin the sediment. Corliss (1985) was the first toshow a vertical succession of deep-sea taxa in thesediment, with some species (‘epifaunal’) living inthe upper centimeters, and other species (‘infau-nal’) having clear subsurface maxima in their pop-ulations. A number of later papers (e.g. Gooday,1986; Mackensen and Douglas, 1989; Corliss andEmerson, 1990; Corliss, 1991; Rathburn and Cor-liss, 1994; Jorissen et al., 1995; Rathburn et al.,1996; McCorkle et al., 1997; De Stigter et al., 1998;Jorissen et al., 1998) have confirmed the presenceof such a vertical distribution in deep-sea environ-ments. On the basis of the presence of living Fora-minifera in sediments without measurable oxygen,Bernhard(1989, 1992, 1993, 1996), Bernhard andReimers (1991), Moodley and Hess (1992), andBernhard and Alve (1996) have suggested thatsome benthic Foraminifera may be facultativeanaerobes.

Several authors (e.g. Corliss and Chen, 1988;Murray, 1991b; Barmawidjaja et al., 1992; Rath-burn et al., 1996) have tried to highlight differ-ences in vertical distribution by defining variousmicrohabitat adaptations, such as ‘epifaunal,’‘epibenthic,’ ‘elevated epibenthic,’ ‘shallow,’‘intermediate,’ ‘deep,’ and ‘predominantly’ or‘preferentially infaunal’ taxa. On the other hand,several arguments have been raised to indicatethat such separations constitute an oversimpli-fication (e.g. Linke and Lutze, 1993).

First, the two equally important parametersthat define foraminiferal distribution, i.e. sedi-ment penetration depth and vertical abundancepattern of species, do not necessarily covary.The maximum depth at which a species occursis defined by the tolerance of the species (modi-fied by accidental transport) to a variable limit-ing factor (see Jorissen et al., 1995). The

abundance pattern, on the contrary, is relatedmainly to microhabitat preferences of thespecies. In the literature, however, species areoften attr ibuted to microhabitat categories onthe basis of both parameters.

Second, there is significant variabili ty in theexact sediment depth at which a particularspecies can be found; it may live deep in thesediment at one site, but much closer to thesediment-water interface at a different site(Fig. 10.2). Several papers (e.g. Mackensen andDouglas, 1989; Corliss, 1991; Kitazato, 1994)show this phenomenon for the genus Globobuli-mina (Fig. 10.3). Furthermore, even at a singlesite, the vertical distribution may vary throughtime (Barmawidjaja et al., 1992; Linke andLutze, 1993; Kitazato and Ohga, 1995). The

succession of foraminiferal taxa may be com-pressed or expanded, and taxa co-occurringsomewhere in the upper part of the sedimentmay occupy different microhabitats at anotherplace or time (Fig. 10.4). In view of th is largespatial and temporal variability, Linke andLutze (1993) conclude that the species’ micro-habitat should be considered as the reflectionof a dynamic adaptation to optimize foodacquisition.

Finally, it is evident that the concept of astrictly vertical stratification of taxa does notaltogether correspond to the reality. On the onehand, burrowing macrofauna, which create deepoxic environments and introduce nut r i t iousmaterial into the sediment may cause a largespatial (vertical as well as horizontal) hetero-geneity (e.g. Aller and Aller, 1986; Meyers et al.,1987, 1988). On the other hand, in the oxic zone,anoxic micro-environments may be present inthe center of organic aggregates or fecal pellets(Fenchel and Finlay, 1995).

A simplified concept with several microhabi-tat categories, however, may be very useful inpaleoceanography, provided that the penetra-tion depth, or the abundance patterns of thevarious taxa and/or microhabitat categories canbe linked to some of the environmental parame-ters. Adequate knowledge of the microhabitatcharacteristics of extant taxa is also importantfor stable isotope studies, in which the of

Evaluation of existing microhabitat data 165

the benthic foraminiferal shell is used as a proxyof bottom water ventilation and export produc-tivity. Since a significant gradient exists inthe top centimeters of the sediment, it is of primeimportance to know whether the benthic fora-miniferal species selected for analysis secretetheir tests in isotopic equilibrium, and if so,where in the sediment column this secretiontakes place.

The aim of this chapter is to describe benthicforaminiferal microhabitats within the sediment,and to summarize the ideas which have beenproposed to explain differences in vertical distri-bution in the sediment among taxa, among sites,and in time. In addition, it looks into the appli-cation of foraminiferal microhabitat information

in paleoceanographic studies. It does not includea list of microhabitat preferences of species.Existing lists of such preferences (e.g. Corlissand Chen, 1988; Murray, 1991b; Van der Zwaanand Jorissen, 1991; Barmawidjaja et al., 1992;Rathburn et al., 1996) may be useful as readyreferences, but their reliability suffers from thefact that they are often based on a mix of realobservations and assumptions about relation-ships between microhabitat and species mor-phology. Furthermore, these lists generally donot take into account the dynamic nature of theforaminiferal microhabitat; a par t icular genusor species is not necessarily ‘fixed’ in a par t icularmicrohabitat. These problems are more fully dis-cussed in a later section.


10.4 EVALUATION OF EXISTINGMICROHABITAT DATA

Most published data on foraminiferal microhab-itats are based on tests stained by Rose Bengal(Lutze and Altenbach, 1991). It is generallyagreed that this procedure is the only one thatallows a rapid gathering of numerical data froma large number of samples, but several authors(e.g. Douglas et al., 1978, 1980; Bernhard 1988,1989; Corliss and Emerson, 1990; Jorissen et al.,1995; McCorkle et al., 1997) have warned thatforaminiferal tests may stain for a considerabletime after the death of the individuals, especiallyunder low temperatures, or in anaerobic eco-systems deep in the sediment. Generally,however, the time needed for protoplasm degra-

dation appears to be very short in oxic environ-ments. In many cases, the surf ic ial sedimentlayers contain specimens that are either brightlystained or completely unstained. In the deeper,anoxic sediment layers, on the contrary, I haveoften observed a wide spectrum of staining, fromcomplete to minimal, and from bright to verydull . Thus, recognizing a foraminiferal test asRose-Bengal stained is based on subjective cri-teria. If less perfectly stained tests correspond toindividuals that have been dead for some time,then loosely applied staining criteria will leadto an overestimation of the in fauna l standingstock.

If we consider the vertical d is t r ibut ion of theent i re benthic foraminiferal assemblage, severaltypes of distribution can be distinguished. A

Evaluation of existing microhabitat data 167

number of studies report only minor variationsin the number of living Foraminifera from onedepth interval to another for a considerabledepth in the sediment (e.g. Buzas, 1974, 1977;Collison, 1980; Hohenegger et al., 1993; Muro-sky and Snyder, 1994; Lueck and Snyder, 1997).This situation is typical for the majority of shal-low-water (0–50 m) and/or coarse-grained envi-ronments. Sites at greater depths, usually withfine-grained sediments, tend to show a clearmaximum in the topmost interval, with an expo-nential downward decrease. At some sites how-ever, secondary downcore maxima have beendescribed (e.g. Corliss, 1985; Hunt and Corliss,1993; Rathburn and Corliss, 1994; McCorkleet al., 1997).

Many terms have been proposed to describethe vertical distribution of species. Those intro-duced by Corliss ( 1 9 9 1 ) are the following: (a)epifauna (taxa found living only in the upper-most centimeter of the substrate), ( b ) shallowinfauna (taxa confined to the 0–2 cm interval) ,(c) intermediate infauna (1–4 cm), and (d) deepinfauna (a subsurface population maximum

below 4 cm, usually in the anoxic zone). Theseterms, widely used in the literature, offer theadvantage of a rapid characterization of the ver-tical distribution patterns. Unfortunately, theseparation of these four categories is based ona combination of distributional data and testmorphology. The terms epifaunal and shallowinfaunal may suggest a fundamentally differentlife strategy ( l iv ing on top of the sediment versuswithin the sediment), but the distinctionbetween the two groups is completely arbitrary,since it is based on an assumed connectionbetween microhabitat and test morphology, andnot on observed patterns of vertical distribution(Corliss, 1991). Another drawback of such arigid classification is the fact that infaunal taxamay show significant variations in their preciseliving depth (e.g. Corliss, 1985; Corliss andEmerson, 1990). Several authors (e.g. Barmaw-idjaja et al., 1992; Linke and Lutze, 1993; Alveand Bernhard, 1995; Kitazato and Ohga, 1995)have suggested that even at a single site, theremay be short-time variations in this living depth(Fig. 10.5). Although the succession of shallow


infaunal, intermediate infaunal, and deep infau-nal taxa remains intact, the precise depth atwhich each of these groups is found may fluctu-ate considerably. For example, the genus Globo-bulimina is generally considered as a deepinfaunal taxon, because its preferred microhabi-tat is deep in the sediment where there is a welldeveloped vertical stratification of foraminiferaltaxa. With a very thin top layer of oxygenatedsediment, however, Globobulimina may very wellbe found much closer to the surface (Figs. 10.2,10.3). Although microhabitat labels may pro-vide a very useful characterization of speciesbehavior, the attribution of these labels shouldbe based exclusively on distributional data, andnot on pre-conceived ideas about the functionalmorphology of their test. Furthermore, it shouldnot be based on the (highly variable) exact depthin the sediment at which a species lives, butrather on the relative position of the speciescompared to that of other species, and on theshape of its vertical distribution profile.

10.5 VERTICAL DISTRIBUTIONPATTERNS

The existing data on vertical distributions ofindividual taxa reveal four main patterns

(Fig. 10.6). I wil l i l lustrate these patterns by typi-cal examples, but the reader should keep in mindthat they are highly variable in space and time,and that even for a single species, different pat-terns exist. It is important, however, to definethese different dis t r ibut ion patterns, becausethey are a reflection of the response of the organ-isms to a set of controlling parameters.

The first type of profile (Fig. 10.6, type A)shows a very clear population maximum in thetopmost interval, which in most studies is 1 or0.5 cm thick. Few individuals are found deeperin the sediment. Taxa usually showing this verti-cal distribution pattern are common in deepoceanic environments. They have been termedepifaunal (e.g. Hoeglundina elegans described byCorliss and Emerson, 1990, and Corliss, 1991;see Fig. 10.7a) or shallow infaunal (e.g. Uvigerinaperegrina, described by the same authors; seeFig. 10.7b). In reality, abundant species arenever completely limited to the topmost interval ,and are always found in small numbers at thelevels below. Buzas (1974) and Buzas et al.(1993) argue that in soft bottomed environ-ments, even taxa l iving exclusively at the top-most level are most probably infauna. Theysuggest that the term epifaunal be used only forspecies l iving on hard substrates, such as rocks,molluscs, or corals, or perhaps on bacterial films

Factors controlling vertical distribution patterns 169

at the sediment-water interface. For such lifepositions, Lutze and Thiel (1989) proposed theterm ‘elevated epifauna.’ For all taxa that usuallyshow type-A dis t r ibut ion patterns, it may beconcluded that they have a marked preferencefor the conditions found in the top part of thesediment, or do not tolerate the conditions indeeper sediment layers.

The second type of profile (Fig. 10.6, type B)shows similar densities in several successiveintervals, wi thout a clear maximum at the top-most level, or deeper in the sediment. Hopkinsinapacifica (Fig. 10.7c) in the February sample ofBarmawidjaja et al. (1992) is a typical example.Species that repeatedly show such a pattern havebeen considered as shallow infaunal (if the maxi-mum values occur in the top 2 cm), or, in caseswhere the high densities continue to muchdeeper levels, as ‘transitional’ ( R a t h b u r n et al.,1996). This type of d is t r ibut ion is relat ivelycommon in coarse grained, shallow-water envi-ronments, perhaps because the sediment isintensely burrowed to a considerable depth. Theprofile is very rare in deep-sea environments,where pore-water characteristics change rapidlywi th in a short depth in terval . This type-B distri-bution profile should be typical for taxa whichdo not have a clear preference for the topmost

sediment layer (or which do not successfullycompete there with other taxa), and which toler-ate the conditions found deeper in the sediment.

The third type of profile (Fig. 10.6, typesand shows relatively low values in the f irstin t e rva l ( s ) , and one or more downcoremaxima. Melonis barleeanus (Fig. 10.7d; Corlissand Emerson, 1990; Corliss, 1991) and Globobul-imina affinis (Fig. 10.7e; same authors) providetypical examples. Judging by the precise depthat which the downcore maxima are found,species with such distribution patterns havebeen termed intermediate (M. barleeanus) ordeep infaunal (G. affinis). Taxa with type-C dis-t r ibut ion have provoked a spirited discussion inthe l i te ra ture . The essential questions are howand why these taxa flourish in the poorlyoxygenated environment of the deeper levels ofthe substrate.

The fourth type of profile (Fig. 10.6, type D)shows a combination of a surface maximumwith one or several maxima deeper in the sedi-ment. Bulimina marginata (Fig. 10.7f; Jorissenet al., in press) or B. aculeata of Kitazato ( 1989)are typical examples. Taxa wi th such a d i s t r ibu-tion profi le apparently f i nd suitable environ-ments at the sediment surface as well as deeperin the sediment.



It is evident that these four types of verticaldistribution are reflections of the tolerance and/or preference levels of taxa with respect to oneor more controlling parameters. Until now, arather limited array of parameters has beenevoked to explain differences in the vertical dis-tribution of benthic Foraminifera. Early papers,dealing with foraminiferal occupation ofdeeper sediment layers without a conspicuousvertical succession, mainly suggest sedimentmixing by wave action, porosity, and bioturba-tion as the cause of microhabitat depth differ-ences among sites. Following the discovery of arather invariant vertical succession of species indeep-water sediments, four other factors havebeen proposed to explain the differences amongtaxa and among sites.

(1) Bottom-water oxygenation may play a rolein determining the lower vertical limit of taxawith type-A or type-B distribution. A numberof recent field and laboratory studies, however,show significant foraminiferal standing stocks(of taxa with type-C or type-D distribution) inapparently anoxic sediments, suggesting thatoxygen concentration is not a critical factor forall taxa (e.g. Bernhard, 1989, 1992, 1993; Corlissand Emerson, 1990; Bernhard and Reimers,1991; Alve, 1994; Rathburn and Corliss, 1994;Moodley et al., 1997; Jorissen et al., 1998; seealso chapter 12). However, even if several taxacan survive prolonged anoxia in laboratorystudies (e.g. Alve and Bernhard, 1995; Moodleyet al., 1997), oxygen concentration can not bedismissed as an important ecological factor forbenthic Foraminifera. It is very well possiblethat anoxic conditions may inhibit reproductionin many taxa, and thus ultimately cause theirdisappearance. The total absence of benthicForaminifera after prolonged anoxia (Bernhardand Reimers, 1991), and in Mediterranean deep-sea sapropels strongly suggests a controlling rolefor oxygen concentration. Furthermore, theupward movement of several taxa in responseto decreasing oxygen in bottom water, and prob-ably also pore water (Alve and Bernhard, 1995),

and the very clear succession of species alonga bottom-water dissolved oxygen gradient(0.02–0.5 ml/l) described by Bernhard et al.(1997) in Santa Barbara Basin, suggest the exis-tence of a lower tolerance l imit for many speciesin the microxic/dysoxic range (see chapter 12).However, several other parameters of the sedi-mentary environment, such as porosity, watercontent, alkalinity, or sulfide content covarywith pore-water oxygen concentration, and it ispossible that it is not oxygen concentrationitself, but one of the critical covarying factors,such as the concentration of toxic substances(sulfides), that restricts the foraminiferal livingdepth. Furthermore, oxygen concentration (or arelated parameter) may limit the maximum pen-etration depth, but it can hardly explain speciesabundance profiles.

( 2 ) Food availability is the other parameterthat may control the foraminiferal microhabitatdepth. In oligotrophic parts of the ocean, whereoxygen penetration can be very deep (Rutgersvan der Loeff, 1990), but where the small quan-tity of labile organic matter is rapidly consumedat the sediment-water interface (Reimers et al.,1986; Carney, 1989), benthic Foraminifera are( l ike all macro- and meiofauna) limited to thetopmost centimeters of the sediment. Here, foodlimitation best explains the absence of faunadeeper in the sediment (e.g. Shirayama, 1984;Corliss and Emerson, 1990; Jorissen et al., 1995).Foraminifera feed on a wide range of food par-ticles, but an increasing body of evidence indi-cates food selectivity in various species (e.g.Caralp, 1989b; Goldstein and Corliss, 1994;Kitazato, 1994; Rathburn and Corliss, 1994;Hemleben and Kitazato, 1995; Kitazato andOhga, 1995). For instance, Goldstein and Cor-liss (1994) report that planktonic diatom frus-tules are common in sediment parcels ingestedby Uvigerina peregrina, but are never found inGlobobulimina. Kitazato (1994) even suggestedthat the latter genus has a preference to feed onolder organic detritus.

For taxa with type-A distribution, their sur-face maximum could very well be caused by thepresence of labile, easily metabolizable, organicmatter at the sediment surface. Although part

10.6 FACTORS CONTROLLINGVERTICAL DISTRIBUTION PATTERNS


of the fresh organic matter arriving in the ben-thic ecosystem is mixed into the sediment bybioturbation, the bulk is consumed at the sedi-ment-water interface (Reimers et al., 1986;Carney, 1989). A specific case of taxa with atype-A distribution, for which the density seemsto be controlled by food availability, is found inspecies that feed on bulk deposits of fresh phyto-detritus (so-called ‘phytodetritus feeders;’ seeGooday and Lambshead, 1989; Gooday, 1993).

Taxa with type-B distribution do not liveexclusively at the sediment surface, and musttherefore tolerate the paucity of high-qualityfood items, or a lower food quality. This is evenmore true for taxa with subsurface maxima(types C and D), which must feed on materialwith a low nutritional value (Caralp, 1989b), oron labile particles made available by nitrate-,iron-, or sulfate-reducing bacteria that causeanaerobic degradation of organic matter (Alve,1990; Bernhard, 1992). Jorissen et al. (1998) sug-gest that intermediate infaunal taxa have theirlargest populations in the zone of nitrate reduc-tion, whereas deep infaunal species are the onlyremaining taxa in the zone of sulfate reduction(Fig. 10.8). They suggest that these successivetaxa feed either on the decay products of lowquality sedimentary organic matter, made avail-able by bacterial anaerobic degradation, or onthe bacterial stocks themselves. The exact depthin the sediment of the various oxidants and theiraccompanying microbial stocks depends on theinterplay between the organic flux, bottom-water oxygen concentration, bio-irrigation, andsediment porosity.

(3 ) Competition and predation have rarelybeen evoked to explain foraminiferal microhabi-tat depths. Obviously, the reduced predationalpressure in the infaunal microhabitat is anadvantage for benthic Foraminifera. Theoreti-cally, density peaks of infaunal Foraminiferamay be created by a much lower macrofaunalgrazing pressure. At present, we do not knowwhether Foraminifera actively choose infaunal

microhabitats to avoid predation. At the sedi-ment surface, habitat space is limited, andcompetition for space may occur. In food-richenvironments, however, competition forresources is minimal, and the environment wil lbe inhabited by opportunistic taxa w i t h largereproductive potentials. Because of their highturnover rate, these taxa will rapidly dominatethe assemblages. Many epifaunal and shallowinfaunal taxa with type-A distributions (wi thclear maxima in the resource-rich surface sedi-ments and an exponential decrease below) mostprobably have such an opportunistic life strat-egy. Such taxa can rapidly adjust to in termi t ten tfood supply, and will often dominate the fossilassemblage, even if they attain high densitiesonly during the most eutrophic periods (Jorissenand Wittling, 1999). In this context, species feed-ing on phytodetri tus deposits probably repre-sent an extreme.

Since the anaerobic bacterial conversion ofrefractory organic matter into labile compo-nents is a slow process (Fenchel and Finlay,1995), taxa l iving deep in the sediment areadapted to an environment wi th a relativelyconstant supply of low-quality food. Logically,such taxa will have a life strategy aimed at veryefficient food utilization, in combination with amaximum resistance to ecological stress. Undernormal conditions, their densities will be rela-tively low, but constant in time. However, suchnormally deep infaunal taxa are known to haveamazingly high densities in some cases wherebottom-water oxygen concentrations are verylow (e.g. Phleger and Soutar, 1973; Sen Guptaand Machain-Castillo, 1993). Under such cir-cumstances, the opportunistic epifaunal or shal-low infaunal taxa will probably no longertolerate the low oxygen concentration, and w i l ldisappear. The result of this partial extinctionor disappearance is that the normally deepinfaunal taxa may find the sediment-surfacemicrohabitat open, and may be able to colonize



this extremely food-rich environment, wherethey can reach very high standing stocks.

(4) Bioturbation may influence benthic fora-miniferal microhabitats in several ways: by cre-ating oxic microenvironments at depth in thesediment (Aller and Aller, 1986; Meyers et al.,1987, 1988), or by trapping food-rich particles,and partially introducing them into the sedi-ment. Thomsen and Altenbach (1993) show asignificant increase in bacterial biomass andforaminiferal densities in haloed sedimentsaround artificial burrows. Bioturbation can alsoactively transport Foraminifera to deeper sedi-ment layers, and cause accidental infaunaloccurrence of taxa that are usual ly found at thesediment surface.

The four factors explained in this section willeach have thei r ind iv idua l influence on the fora-miniferal microhabitat, but they wil l alsointeract strongly. Jorissen et al. (1995) , followingthe suggestions of Shirayama (1984) and Corlissand Emerson (1990), developed a conceptualmodel that shows the interplay between oxygenconcentration and food availabi l i ty (Fig. 10.9).They argue that in oligotrophic settings, a criti-cal food level determines the penetration depthof most species, whereas in eutrophic settings, acritical oxygen level would determine th is depth.The tolerance limits to these two factors willstrongly vary among species, explaining thedifferences in the lower depth limits describedin the literature.

Several workers have suggested a close relation-ship between test morphology and microhabitat(e.g. Corliss, 1985; Jones and Charnock, 1985;Corliss and Chen; 1988; Corliss, 1991; Corlissand Fois, 1990). The existence of such a relation-ship would be very significant, since it wouldenable us to infer the microhabitats of extincttaxa, and thus extract essential informationabout ancient ecosystems. According to Corlissand Chen (1988) and Corliss ( 1 9 9 1 ) , epifaunaltaxa are (a) plano-convex, biconvex or rounded

trochospiral, w i th large pores absent or onlyfound on one side, or ( b ) mil io l ine . In contrast,in fauna l taxa can be rounded planispiral . flat-tened ovoid, tapered and cylindrical triserial,spherical, or flattened tapered biserial, and tendto have pores all over the test. The main short-coming of th i s classification is that the pr imaryseparation between epifaunal and infaunal taxais l inked to an a rb i t ra ry boundary d rawn on thebasis of pore patterns (Corliss, 1991), and is onlyto a minor degree based on actual observations.The plano-convex, rounded, or biconvextrochospiral taxa, listed as epi faunal (Corlissand Chen, 1988; Corliss, 1991; Murray, 1991b;Rathburn et al., 1996), are indeed morphologi-cally dis t inc t from the planispiral, biserial, ortriserial taxa listed as shallow infauna. but inthe majority of field observations, the i r ver t ica ld i s t r i bu t i on patterns do not segregate alongsuch morphological lines.

Furthermore, it appears tha t even in caseswhere test form, coil ing type, and pore patternare very similar, important differences in micro-habi ta t may exist. Loubere et al. ( 1 9 9 5 ) showthat shallow and deep infaunal populations ofUvigerina peregrina have a s l igh t ly d i f fe ren tmorphology, but belong to the same species.Differences in microhabi ta t selection betweenmorphologically close species of the same genushave been reported for Bolivina (Barmawidjajaet al., 1992), Bulimina (Jorissen et al., 1998),Cibicidoides ( Rathburn et al., 1996), and Melonis(Jorissen et al., 1998). Barmawidjaja et al. ( 1992)showed that w i th in a group of closely relatedBolivina, the ornamented striatula-types arealways l imi ted to the sediment surface, whereasunornamented, but otherwise morphologicallysimilar, B. dilatata and B. spathulata have a clearin fauna l tendency. This corroborates an earlierobservation by Corliss ( 1991 ) that only shallowin fauna l taxa ( i n his data set) possess a surfaceornamenta t ion . In the genus Bulimina, B. inflatais l imited to the sediment surface, and in v i e wof its overall coarse perforation, should be con-sidered as shallow infauna l , according to thecriteria defined by Corliss ( 1 9 9 1 ) . In contrast,B. marginata, which has a s imi la r test, but aspinose, instead of a costate, ornamentation,

10.7 RELATIONS BETWEEN TESTMORPHOLOGY AND MICROHABITATS

Relations between test morphology and microhabitats 175

often has a type D-distribution (Fig. 10.6), andsometimes shows prominent maxima deep in thesediment (Jorissen et al., 1998).

An examination of the published data on fora-miniferal microhabitats shows that the observedmicrohabitat patterns for most species are veryconsistent. Although the exact depth at which aspecific taxon is found is variable, its positionwith respect to those of other taxa is very stablein most cases (Fig. 10.4). The genus Nonionellaprovides a striking exception to this rule. N.turgida is found with deep infaunal maxima inthe western Atlantic Ocean (Corliss and Emer-son, 1990) and in the Santa Monica Basin(species identified as N. stella, Mackensen andDouglas, 1989), but is the taxon with the mostevident epifaunal tendency at shallow sites inthe Adriatic Sea (Barmawidjaja et al., 1992).

In view of the large spatial and temporal vari-ability of foraminiferal microhabitats, and thelarge depth intervals over which living individ-

uals of some taxa are found, a statement aboutthe microhabitat of a species or genus may justbe a generalization. For instance, from observa-tions on hard substrates (Lutze and Thiel, 1989),Cibicides wuellerstorfi is generally considered asan epifaunal (elevated) taxon. However, non-negligible populations of the species have beendescribed also within soft sediments (e.g. Corliss,1991; McCorkle et al., 1997; Jorissen et al.,1998), which suggests that not all C. wuellerstorfisecrete their tests at the sediment-waterinterface.

In summary, the relationship between testmorphology and microhabitat is complex, andall generalizations have significant exceptions.On the basis of a statistical analysis, Buzas et al.(1993) concluded that for the taxa they consid-ered, microhabitat assignments on the basisof morphology were about 75% accurate.Although it can not be denied that there is acorrespondence between test morphology and


microhabitat, the afore-mentioned examplesshow that some taxonomically close species(with only subtle morphological differences) mayhave significant differences in their microhabi-tats. It is possible that a thorough study of minormorphological characteristics (ornamentation,pore density, pore diameter, length/width ratio,presence of a basal spine, etc.) may lead to aconsiderable improvement in our comprehen-sion of the various l inks between test morphol-ogy and microhabitat.

The stable isotopic composition of foraminiferalshells is extensively used in paleoceanography(see chapter 14). In particular, the of ben-thic Foraminifera has been used as a proxy ofexport productivity and deep water circulation.The of the oceanic bottom water dependson two main factors: the downward organic flux,which introduces -depleted organic matterproduced in the surface waters, and the venti la-tion by bottom currents, which tends to supplywaters with a high Within the sediment,the organic matter is remineralized, releasing

-depleted to the pore waters. The resultis a strong gradient in the first few centime-ters of the sediment. After the discovery of sig-nificant interspecific differences in the ofbenthic Foraminifera, it was suggested that mostspecies form their test in isotopic equi l ibr iumwith the composition of the surrounding water,and that the interspecific differences could bethe result of microhabitat differences (e.g. Wood-ruff et al., 1980; Belanger et al., 1981; Grossman,1984a,b). Several studies have confirmed thishypothesis, showing that generally, epifaunaltaxa have a high value, whereas infaunaltaxa have a lower (e.g. Grossman, 1987;McCorkle et al., 1990; Ra thburn et al., 1996).The isotopic composition of infaunal taxaappears to be strongly influenced by that of thepore water.

An excellent overview of the relations betweenforaminiferal microhabitats and stable isotopic

compositions is given by McCorkle et al. (1997).Al though the interspecific differences are clear,and apparently consistent, the almost tota labsence of a difference among specimens of deepinfauna l taxa sampled at various sedimentdepths is s t r ik ing (McCorkle et al., 1990, 1997).According to McCorkle et al. (1997) , th is mayimply tha t calcification takes place in a relativenarrow subzone of the foraminiferal microhabi-tat range. Loubere et al. (1995) , on the contrary,present data suggesting tha t the calcification ofin fauna l Uvigerina takes place in a microenvi-ronment associated wi th macrofaunal ac t iv i ty ,with a geochemistry very different from tha t ofthe average pore water. The comparisonbetween the profiles in pore waters andthose of deep infaunal taxa (e.g., Globobuliminain McCorkle et al., 1990, 1997) shows that theoffset between the two profiles in a pair increasestowards greater depth in the sediment. This sug-gests that calcification takes place preferentiallyclose to the redox front, an idea which ismatched by the suggestion of Bernhard (1992)that Globobulimina lowers its metabolism undercompletely anoxic conditions. An a l ternat iveexplanation could be that an individual foramin-ifer forms its test over a prolonged time in te rva lin a relat ively wide depth zone in the sediment,and tha t the u l t ima te isotopic composition ofits test is a reflection of the mean level w i t h i nthis depth interval .

The species Cibicides wuellerstorfi (also placedunder Fontbotia, Planulina or Cibicidoides; seeSen Gupta, 1989), which has been observed onelevated substrates, is supposed to secrete itstest in equ i l ib r ium wi th the ambient bottomwater, w i thou t being influenced by the substratepore-water chemistry. This species has been usedwidely as an indicator of bottom-water charac-teristics (e.g. Duplessy et al., 1984; Sarntheinet al., 1988). However, as slated previously,observations of live C. wuellerstorfi within thesediment suggest that not al l individuals of th i sspecies secrete their test in isotopic equi l ibr iumwith the bottom water. Furthermore, Sarntheinet al. ( 1988) speculate that regional organic-fluxmaxima could modify the isotopic compositionof the water immediately above the sediment-

10.8 MICROHABITATS AND CARBONISOTOPIC COMPOSITIONS

Paleoceanographic implications of benthic foraminiferal microhabitats 177

water interface. In areas with significant phyto-detritus deposits, a strong gradient, result-ing from the liberation of -depletedmay develop even above the sediment-waterinterface. Mackensen et al. (1993c) indicate thatsuch a phenomenon can influence the isotopiccomposition of epifaunal Foraminifera; thelarger food availability could trigger repro-duction and/or chamber formation, and calcifi-cation could thus take place during times ofstrong gradients close to the sediment-water interface. This ‘Mackensen effect’ is sup-ported by the suggestion of Jorissen andWittl ing (1999) that test production of C. wuel-lerstorfi is limited to a very short period of theyear in the distal zones of the Cape Blancupwelling area, when the organic flux is locallymaximal. As a consequence, the isotopic com-position of the tests of epifaunal taxa such as C.wuellerstorfi may represent conditions presentduring relatively short periods of time, and willnot always reflect the average, long-term, iso-topic composition of the bottom water mass.

A comparison of isotopic compositions of epi-faunal and infaunal taxa could give importantclues about the gradient wi th in the sedi-ment, and thus, about the amount of organicmatter remineralized in the benthic ecosystem(e.g. McCorkle and Emerson, 1988). Zahn et al.(1986) show an increasing difference inbetween Cibicides wuellerstorfi and Uvigerinaperegrina with an increase in organic flux.McCorkle et al. (1997) , however, argue that ifForaminifera position themselves according toa geochemical cue (such as an oxygen gradient,or an organic-rich patch) or a food-related cue(such as bacterial decomposition), then speciesfrom a wide range of sediment depths mayinhabit geochemically similar microenviron-ments. As an extreme example, in case ofstrongly dysoxic or microxic bottom waters,deep infaunal taxa may occupy the sedimentsurface, and may reflect the isotopic composi-tion of the bottom water, but not of the porewater (Fig. 10.2). Proxies such as the(epifaunal-infaunal difference) should, therefore,be used only after a clear understanding ofthe benthic environment in which the analyzedforaminiferal species actually lived.

The knowledge of microhabitats is essential fora proper utilization of benthic foraminiferalspecies as paleoceanographic tools. Severalauthors have noted that the relative proportionof infauna l taxa becomes more significant as theorganic flux increases (e.g. Corliss and Chen,1988; Corliss and Fois, 1990; Rosoff and Corliss,1992; Jorissen et al., 1995). This suggests thepossibility of developing a microhabitat basedproxy for the organic flux. Furthermore, severaltaxa with a morphology indicative of an infaunalmicrohabi ta t show a systematic populationincrease under strongly dysoxic or microxic con-ditions (e.g. Bernhard, 1986; Kaiho, 1991; SenGupta and Machain-Castillo, 1993: Bernhardet al . , 1997). The proxy for bottom-water oxy-genation developed by Kaiho (1991, 1994) isbased on this principle. Kaiho (1994) shows agood correlation between the percentage of anumber of ‘oxic’ indicators (in an assemblage of‘oxic’ and ‘dysoxic’ species) and bottom-wateroxygen concentration in the range of 1.5–3.0 ml1 . The ‘oxic’ taxa, which are considered epi-faunal, appear to have a tolerance threshold atabout 1.0m1 1 . For the range of 0–1 .5ml / l

, Kaiho (1994) proposes a bottom-water oxy-genation proxy that utilizes the relative domi-nance of a category of ‘dysoxic’ Foraminifera;this group contains taxa tha t have beendescribed as shallow, intermediate, or deepinfaunal. Rathburn and Corliss (1994), however,show that ‘low oxygen taxa,’ such as Boliv-ina, Bulimina, Globobulimina, Uvigerina andChilostomella, are rare at a number of sites inthe Sulu Sea, where bottom-water oxygen con-centration is 1.76 ml/1 or less. They concludethat the dominance of these taxa is typical ofenvironments wi th a high organic flux, ratherthan of environments wi th low oxygenconcentrations.

The parameters of bottom-water oxygenationand organic flux (food availability) are closelyinterrelated, and it is often extremely diff icul t todistinguish their separate influences. Further-

10.9 PALEOCEANOGRAPHICIMPLICATIONS OF BENTHICFORAMINIFERAL MICROHABITATS


more, bottom-water oxygenation does not nec-essarily covary with the penetration depth ofoxygen in the sediment, and thus, with the extentof the oxygenated infaunal microhabitat . Thesediment depth at which the oxygen concen-tration becomes zero may be very different atsites with very similar bottom-water oxygenconcentrations (e.g. Ra thbu rn and Corliss, 1994;Relexans et al., 1996; Jorissen et al., 1998).Within the sediment, the slope of the pore-wateroxygen profile is determined by the balancebetween oxygen diffusion from the sediment sur-face and oxygen consumption by degradingorganic matter. In areas with high organic flux,oxygen values in the substrate will rapidly dropto zero, and the depth of the oxygenated sedi-ment layer will be minimal. Of course, bottom-water oxygen content is not necessarily low insuch cases, because bottom currents may causerapid oxygen renewal. As a consequence, evena strong dominance of infaunal taxa in the sedi-ment is not always indicative of a dysoxic ormicroxic sediment-water interface.

Our best hope to find foraminiferal markersof benthic ecosystem oxygen content (speciesthat are not primarily dependent on the organicflux) lies in the deep infaunal taxa, because theycombine a high tolerance for low oxygen con-centrations with that for low-quality food. Logi-cally, the percentage of deep infauna l taxa in abenthic foraminiferal community should covarywith the importance of anaerobic degradationof organic matter. As explained below, threedifferent processes are relevant.

( 1 ) Oligotrophic-mesotrophic ecosystems: anincrease of the organic flux or export produc-tivity. When the organic flux is very low, thebulk of organic matter is consumed at the oxicsediment-water interface. Thus, very smallamounts of organic matter are mixed into thesediment by bioturbation and will be degradedin the anoxic zone. Much of the scarce organicmatter brought into the sediment will be com-pletely refractory, and wi l l u l t ima te ly be fossil-ized. As a consequence, deep in the sediment,there is a near absence of anaerobic bacterialdegradation, and thus also of deep infaunal taxa.A higher export product ivi ty w i l l increase both

the amount of organic matter introduced intothe sediment, and the importance of anaerobicdegradation processes.

( 2 ) More eutrophic ecosystems: a decrease inthe quality of the introduced organic matter.The decrease in labile components may be theresult of downslope transport or advection ofold, terrestr ial , refractory, organic mat ter fromshelf environments, a more efficient recycling oforganic matter in the surface waters, or thechanging composition of the phytoplankton/zooplankton communi ty . If the labile compo-nent of the organic matter, which is directlyusable by the epifauna and shallow infauna.decreases, the densities of these two groups willd iminish . Also, if the organic matter i n p u tremains the same, more organic matter will bedegraded under anaerobic conditions deep inthe sediment. As a consequence of the reductionof the epifauna and shallow infauna, and theincrease in organic matter degradation w i t h i nthe sediment, the proportion of deep infaunaltaxa will go up.

( 3 ) Lowered oxygen concentration in bottomwater. If bottom-water oxygenation falls belowthe critical value for a par t icu lar species, thespecies will disappear, probably as a result offa i lu re to reproduce. As a consequence, othertaxa that are more tolerant will show an increasein their proportions in the community . If a sig-nificant number of epifaunal and/or shallowinfaunal taxa disappear, much more trophic-resources will become available to deep infaunaltaxa; these may eventual ly move to the sedimentsurface, and replace taxa less tolerant to dysoxicor microxic conditions (Fig. 10.2). Under suchcircumstances, deep infaunal taxa can com-pletely dominate benthic foraminiferal faunas;this phenomenon is known to precede sapropelformation in the Mediterranean Sea (e.g. Roh-ling et al., 1997; Jorissen, 1999).

It appears tha t in most cases the percentageof deep infaunal taxa can be used as a proxy forthe depth of the zero-oxygen sediment layer.Only under extreme conditions, however, whenbottom-water oxygenation falls below a cr i t icalthreshold for most surface-dwelling taxa, canthe percentage of deep i n f a u n a l taxa be used

Acknowledgments 179

as a proxy of bottom-water oxygen values.Although Kaiho (1994) remarks that many‘oxic’ indicators are systematically absent whenoxygen values are below 1 ml/l, this putativemulti-species low tolerance limit needs con-firmation, and the exact values have to be deter-mined for important species.

A second foraminiferal group which is ofpromise in paleoceanography consists of theso-called ‘phytodetritus feeders’ (Gooday, 1988;Gooday and Lambshead, 1989; Lambshead andGooday, 1990; Gooday et al., 1992a; Gooday,1993). Smart et al. (1994) and Thomas andGooday (1996) suggest that the relative abun-dance of Epistominella exigua, Alabaminella wed-dellensis, and other phytodetritus exploitingspecies may be used as a proxy of pulsed organicmatter inputs. An opportunistic lifestyle, sharedby all phytodetritus species, enables them toprofit from short periods of abundant foodavailability. However, these periods of feast arenot necessarily connected with seasonal influxof phytodetritus; they may be related to otherprocesses that cause an intermittent organic flux.Gooday and Turley (1990) give the example ofupwelling areas, in which most of the organic-matter is delivered to the sea bottom as phytode-tritus. Although upwelling in many areas islabeled as ‘permanent,’ in reality the upwellingprocess is periodically interrupted (from a fewdays to several weeks) when the flow of deeper,nutrient-rich waters ceases (e.g. Jones and Halp-ern, 1981). A different context in which opportu-nistic ‘phytodetritus’ species may be successfulis that of a very eutrophic ecosystem with verylow seasonal bottom-water oxygen content. Insuch an environment, opportunistic, surfacedwelling species will profit from short periods

of bottom-water re-oxygenation that wouldmake abundant trophic resources accessible tothe benthic fauna.

The so-called ‘elevated epifaunal’ taxa (Lutzeand Thiel, 1989; Altenbach and Sarnthein, 1989;Linke and Lutze, 1993), such as Cibicides wuel-lerstorfi and Planulina ariminensis, have tenta-tively been proposed as indicators of bottomcurrent activity. Putatively, these taxa feed onparticles transported by bottom currents, andwould therefore be independent of any verticalflux of organic matter. However, observationsof live C. wuellerstorfi at some depth in thesediment suggest that these taxa are not neces-sarily confined to elevated positions, and thattheir use as a proxy for bottom-water currentactivity may not be realistic.

Of necessity, the foregoing discussion is quali-tative. Although our understanding of foramini-feral microhabitats has advanced significantly inthe last decade, quantification of the foraminifer-microhabitat relationships is sti l l rudimentary.This quantification remains one of the mainchallenges of foraminiferal ecology.

10.10 ACKNOWLEDGMENTS

My thinking on microhabitats has been greatlyinfluenced by a number of publications. In par-ticular, the work of Bruce Corliss, AndrewGooday, and Hiroshi Kitazato, and papers ofY. Shirayama (1984) and Robert Carney (1989)have been eye openers. I also benefited greatlyfrom many discussions with Bert Van derZwaan, Martin Buzas, Henko De Stigter,Thomas Gibson, Sophie Guichard, HélèneHowa, Thomas Pedersen, Jean-Pierre Pey-pouquet, Barun Sen Gupta, and Peter Verhallen.


11Benthic Foraminifera andthe flux of organic carbon

to the seabedPaul Loubere and Mohammad Fariduddin

11.1 INTRODUCTION

Organic carbon supply is a fundamental aspectof all biological communities, and the organiccarbon flux is generally limited for marine ben-thic organisms. Benthic organisms shrouded indarkness, at water depths greater than a fewtens of meters, are entirely dependent onimported organic carbon for their energyrequirements. As we will show in this review,areal variations in the flux of organic carbon tothe seafloor have a pervasive effect on the ben-thic community, including the Foraminifera.

Because the processes and ecology are sodifferent, we will examine separately the marineenvironments within and below the euphoticzone. Our review will be presented in four sec-tions. The first will examine the production oforganic matter in the marine realm and its deliv-ery to the ocean floor. The second will summa-rize observations concerning Foraminifera andfood supply. The third will review our basicunderstanding of the benthic response toorganic carbon flux, and present ideas on andmodels of the response of benthic Foraminifera

to that flux. These models will be examinedusing data concerning foraminiferal microecol-ogy, spatial distributions, morphology andabundances. The last section will survey thestate of our knowledge and raise importantquestions which limit our understanding of ben-thic Foraminifera and their geologic record.

11.2 ORGANIC CARBON SUPPLY

11.2.1

Organic carbon compounds are ini t ia l ly sup-plied to the marine biologic community fromthree dominant sources. These are: nearshoreproduction of benthic plants, production of theopen ocean phytoplankton and fluvial supply ofparticulate organic matter (Newman et al., 1973;Hedges and Parker, 1976; Westerhausen et al.,1993; Rice and Rhoads, 1989). Each of thesesources also supplies dissolved organic matterwhich will feed bacteria and thus enter the par-ticulate food chain. The organic matter from thethree sources can be roughly divided into three


182 Benthic Foraminifera and the flux of organic carbon to the seabed

categories based on its energy content andappeal to the biota. These are: labile, resistantand refractory (Middleburg et al., 1993). Thelabile material is of the greatest importance tobiological productivity in the ocean, and is usedup most rapidly. The resistant material is usedby a specialized population of organisms andcan survive in the marine environment forlonger periods of time. Refractory organiccarbon is nearly biologically inert. It is impor-tant to draw these distinctions of type becausebenthic organisms, including Foraminifera, willrespond mostly to the flux of labile material.These carbon compounds are not generally pre-served in marine sediments, which by and largeaccumulate only the refractory material that isno longer, and perhaps never was, of interest tothe biota. In the past it has been the practice toexamine the relationship of benthic Foramini-fera to organic carbon by comparing taxonabundances to sediment organic carbon content.However, the sediment organic material is aresidue from a variety of processes not alwaysdirectly linked to biological productivity. Recentwork on sediment organic carbon has shownthat a good deal of the preserved material isadhered to clays, and that sediment organiccarbon content is mostly a function of claycontent and surface area (Kei l et al., 1994;Mayer, 1994; Hedges and Keil, 1995). Also,research on the northwestern and northeasternAtlantic continental margins indicates thatmuch carbon transported from the shelf ontothe slope (mid-slope carbon high) and deeperwater is degraded, refractory material (Roweet al., 1986; Duineveld et al., 1997).

A global view of biological productivity andthe supply of labile organic matter to the seabedis difficult to create. This view must incorporatethree factors: euphotic zone production, the frac-tion of that production that sinks into the deep-sea, and the local flux of material transportedalong the seafloor (e.g. Reimers et al., 1992;Smith, 1987). Surface-ocean production is sea-sonally variable and can be episodic or subjectto longer term trends. Transport processes alongthe seafloor are, by their nature, localized andquite variable in time. Nevertheless, a general

picture of organic matter generation is avai lablefrom syntheses of measured euphotic zone pro-ductivity (e.g. Berger et al., 1987; Berger, 1989),satellite images of phytopigment concentrationsin oceanic surface waters (Feldman, 1994),model estimates of productivi ty based on thepigment concentrations (Longhurst et al., 1995;Antoine et al., 1996; Behrenfeld and Falkowski,1997), and the extrapolation and mapping ofbenthic respiration (Jahnke, 1996).

11.2.2 Flux to the seabed

The supply of organic matter generated in theupper layers of the open ocean can be generallydivided into two fractions: the recycled and thenew production. New production is traditionallythe part of total production which is sustainedby new ni t ra te introduced into the euphot ic zone(Eppley and Peterson, 1979; Jumars, 1993). Theratio of new production to total production isreferred to as the In any steady stateconsideration of phy top lank ton production, thenew production is that part of the to ta l whichwil l escape to the deeper ocean and be oxidizedthere by the benthos. Therefore, variat ions inthe are of considerable significance to thebenthic organic carbon supply. The range ofvalues for the ratio is from about 0.4 to 0.05.with some of the lowest values observed in thecentral equatorial Pacific ( McCarthy et al., 1996:Head et al., 1996). Lampitt and Antia (1997)show that for the open ocean there is, neverthe-less, a systematic relationship between surface-ocean biological productivity and organiccarbon flux to the seafloor.

Besides depending on the the flux ofphytoplankton production reaching the seafloordepends on water depth. This relat ionship ismost acute in the upper 1000 m of the watercolumn ( M a r t i n et al., 1987; Berger et al., 1987).The relationship between the nature of the fluxand the water depth has been examined empiri-cally using sediment trap data, and severaldifferent equations have been fi t ted to the curve.In all cases, the flux of mater ial reaching theseabed at depths greater than 1000 m is only afew percent of the euphotic zone production,

Benthic foraminiferal responses 183

indicating that efficient recycling of productionoccurs in the upper few hundred meters of thewater column. The result of this is a slim dietfor the deep-sea fauna in most areas of theworld ocean.

In certain regions, most notably the northwestIndian Ocean and the northeast Atlantic, sur-face-ocean biological productivity is highly sea-sonal and organic matter reaches the seabed inpulses, sometimes of fresh phytodetritus (e.g.Smith et al., 1996). Biological response to thesepulses is reviewed below. In other areas of theworld ocean, such as the eastern equatorialPacific, seasonality is muted and longer termcycles (El Niño) influence the flux of organicmatter to the seafloor. Where the flux is rela-tively low, it appears that labile organic matteris oxidized at the sediment-water interface.Labile matter has a life span of less than a year(Cole et al., 1987).

11.3 BENTHIC FORAMINIFERALRESPONSES

11.3.1

Since the earliest regional surveys (e.g. Phleger,1951a; Pujos-Lamy, 1972; Ingle et al., 1980), ithas been evident that benthic foraminiferal taxashow water depth zonation. Modern statisticalanalysis (e.g. Culver, 1988) uses this zonation todetermine water depths to within 50–250 metersfor selected continental margins. The reason forthe zonation of the Foraminifera has not beenclearly established since many environmentalvariables covary with water depth. One schoolof thought, developed first in the 1970s, holdsthat characteristics of oceanic water masses con-trol foraminiferal distributions (see chapter 1).To a degree this must be true, since waters inthe upper mixed layer of the ocean, except athigher latitudes, are much warmer than thosebelow the thermocline. Also, these upper watersare subject to strong variations in their proper-ties in response to seasonal changes and theweather. The sunlit portion of the oceans abovethe seasonal thermocline is in many ways a very

different environment from that found at depth.Because of this difference, we will treat the shal-low ocean separately from the deep sea (waterdepth greater than about 200 meters).

11.3.2 The shallow ocean

Although it is recognized that organic carbonavailability is important to benthic Foraminiferain the shallow ocean, it has been difficult toassess its exact effect. This is because organiccarbon flux is not usually directly measured inforaminiferal studies (organic carbon content ofsediments is only an indirect proxy for labileorganic carbon flux), and because availability offood is often covariant with many other ecologicfactors that are important to the Foraminifera.Further, it is probably also true that in manynearshore settings food availability is not a pri-mary limiting factor for the benthos. Other vari-ables such as substrate, current and waveregime, temperature, salinity, pore-water oxygencontent, and biotic interactions could often bemore significant.

In the nearshore region, the effect of labileorganic carbon availability has been best docu-mented in areas affected by sewage effluent andeutrophication in estuaries or fjords. For thelatter settings, the overconsumption of oxygenand the development of anoxia probably consti-tute the most important factors impacting theForaminifera. This subject is examined in chap-ter 12, and a review of pollution effects on estua-rine Foraminifera will be found in chapter 13and Alve (1995a). Case studies of sewage outfallareas over several decades show definite fora-miniferal response to these. Early studies suchas those of Watkins (1961) and Bandy et al.(1964b) recorded changes in nearshore, colder-water foraminiferal communities and assem-blages that related to closeness of a sewage out-fall. Most marked were areas devoid of livingForaminifera and the concentration of a limitednumber of taxa near outfalls. For example,Bandy et al. (1964b) found that Buliminella ele-gantissima and Bulimina marginata denudatawere overwhelmingly dominant in the livingpopulation of the outfall region for the Los


Angeles County sewage system in SouthernCalifornia. Further, in the nearshore, Discorbiscolumbiensis showed a positive distr ibutionalresponse to sewage outfall while Nonionellacould not tolerate the polluted environment.These observations were corroborated andextended in the follow-up study of Stott et al.(1996) who examined this setting after controlshad brought significant environmental improve-ment. In this case, foraminiferal responses aredriven by a very large input of organic matterwhich will alter not only the availabili ty of foodbut also the character of the sediments and,perhaps most importantly, the dis t r ibut ion ofoxygen in the environment. Strongly anaerobicsediments were not uncommon in the areaexamined by Bandy and colleagues. Also, studiesof sewage outfalls include chemical and metalpollution as potential factors, so the extent towhich they can be used to interpret natural set-tings is open to question. Finally, taphonomicprocesses may be enhanced in sediments withhigh organic content so that assemblages pre-served in the sediments may be quite differentfrom those found in the living community.Bandy et al. (1964b) found the abundance ofagglutinated Foraminifera much increased intheir assemblages for this reason. Nevertheless,similarities between foraminiferal communitiesof polluted environments and those found in thestratigraphic record of sediments with highorganic content were noticed early on (e.g. Seig-lie, 1968). Furthermore. Schafer et al. (1995)found a general inverse relationship of speciesdiversity to organic carbon loading in the vicin-ity of aquaculture operations in eastern Canada,and an increase in non-calcareous Foraminiferaas organic content of the sediments increased.At very high organic content (>20%,) no Fora-minifera were observed. The mechanismsresponsible for these changes probably are notlinked directly to increased food supply, and arelikely the product of changing sediment proper-ties, sedimentation rate, and oxygen concen-trations. One case where increased food supplymay be important is that found along the south-ern coast of Israel where sewage outfall enhancesthe productivity of the adjacent continental shelf

(Yanko et al., 1994c). This agrees with the resultsof Watkins ( 1 9 6 1 ) , Setty (1976) , and Clark( 1 9 7 1 ) . In the Yanko et al. study the foramini-feral abundances were elevated above back-ground and assemblages contained many large,robust specimens. The composition of assem-blages was not much different from that on theadjacent unpolluted shelf. There was no docu-mentation of the organic carbon flux to theseabed in this study, and presumably, it was lessdramatic than described in the reports men-tioned above. So. it may be that in the shallow-water environment, there is a gradient in fora-miniferal response to increasing organic carbonflux. At the low end this response may simplybe an increase in the standing stock. At higherfluxes, taxa may be progressively excluded orencouraged by environmental changes d r iven byorganic carbon accumulation and oxidationwi th in the sediments (sediment properties,oxygen avai labi l i ty) . At the extreme, Foramini-fera are excluded from the environment and a‘dead zone’ is produced. Quant i f ica t ion of thesesteps is not possible with the data at hand.

In shallow marine settings free of anthropo-genic influence, the role of labile organic carbonavailabil i ty is ambiguous. Nevertheless, anumber of studies show that biomass of Fora-minifera responds to seasonal and regional vari-abil i ty in marine plant production. For example,Murray (1985) has shown a relationshipbetween fertility and foraminiferal abundance inthe North Sea. Alve and Murray (1994) havetraced the impact of the spring phytoplanktonbloom on foraminiferal abundance in a mesoti-dal inlet in England, Schroder-Adams et al.(1990) document a likely control of foraminiferalabundances in the high Arctic by sea-ice limitedbiological productivity, and Bernhard (1987)shows a s imilar productivity control on abun-dances in the Antarctic. Lueck and Snyder(1997) compared two regions on the cont inentalshelf of North Carolina (U.S.A.) , and founddifferences in foraminiferal abundances l inkedto benthic community productivity, in this casepossibly driven by nut r ien t enriched ground-water fluxing through the sediments. Earlier, Leeet al. (1966) suggested that many littoral Fora-minifera are bloom feeders.


The exact impact of the availability of labileorganic carbon on shallow-water foraminiferalcommunities and assemblages is difficult toassess, because of the correlations that organiccarbon flux has to other important environmen-tal variables. For example, Hay ward et al. (1996)collected data for both Foraminifera and envi-ronmental variables for an ecological analysisof a tidal inlet in New Zealand. They foundassemblage changes that could possibly berelated to food supply. However, the effects ofthe environmental factors are obscured by corre-lations among organic carbon, mud content ofthe sediments, salt marsh index, total oxidizednitrogen, and dissolved reactive phosphate.Defining taxon ecologic responses to thedifferent environmental variables under theseconditions is not possible.

Finally, it is important that labile organiccarbon in the shallow-water setting comes inmany different forms, from pretreated sewageand bacteria (e.g. Goldstein and Corliss, 1994)to algal mats, algal coatings on sediment grains,and stands of macroalgae. Additionally, shal-low-water Foraminifera may bear endosymbi-onts (see chapter 8), and perhaps even farmbacteria (Langer and Gehring, 1993). Thismeans that foraminiferal taxa will vary not onlyin response to the quantity of organic matterbut also its form. The taxa present and theirabundance for a given setting will depend onfeeding type adaptations (e.g. Lipps, 1983).

11.3.3 The deep sea

The supply of labile organic carbon is muchreduced in the deeper ocean (depth > about200 m) and is much more likely to be a primarylimiting factor in benthic ecology. Altenbachand Sarnthein (1989) and Gooday et al. (1992a)provide a summary of the abundance and pos-sible importance of benthic Foraminifera to deepocean communities. In many instances, benthicForaminifera may be a dominant component ofthe fauna. For example, off Cape Hatteras onthe U.S. east coast, Bathysiphon filiformis occursin great abundance and its tubes are a promi-nent feature of the ocean floor (Gooday et al.,

1992b). It is interesting to note that much of theinformation on foraminiferal biomass and com-muni ty importance in the deep sea centers onnon-calcareous taxa, while the abundance, pro-ductivity, and community relations of the calcar-eous taxa remain obscure. In contrast, thecalcareous taxa are usually better preserved inmarine sediments, and receive most of the atten-tion in geological and paleoceanographicstudies. Gooday et al. (1997) provide an interes-ting examination of non-calcareous deep-seaForaminifera and their relationship to organiccarbon flux. A review of both agglutinated andcalcareous deep-sea Foraminifera with anemphasis on organic carbon flux may be foundin Gooday (1994). The review below wil l con-centrate on the calcareous taxa.

Causes for the depth zonation of benthic fora-miniferal communities below the thermoclinehave been the subject of debate for decades. Inmany ways the foraminiferal zonation parallelsthat seen for other benthic organisms (reviewedin Loubere, 1996), and is thus a part of thegeneral biotic response to the deep-sea environ-ment. The depth zonation of species and speciesgroups, however, is not consistent from one con-tinental margin to another (Pujos-Lamy, 1972;Miller and Lohmann, 1982; Lutze and Coul-bourn, 1983/84). Early attempts to analyze thisvariation focused on relating foraminiferal taxato deep-ocean water masses whose physical andchemical properties were supposed to controlspecies distributions (e.g. Schnitker, 1980). Morerecent water mass based studies show statisticalrelationships on a regional level (e.g. Denne andSen Gupta, 1991), but these have not been con-sistent for inter-regional comparisons (Mil lerand Lohmann, 1982; Lutze and Coulbourn,1983/84; Corliss et al., 1986; Mackensen et al.,1993). This is particularly true for the taxonUvigerina peregrina, which at different times wasassociated with warmer bottom waters and deepwaters with low oxygen content. A major short-coming of the water mass control hypothesishas been the lack of a model based on ecologicalprinciples or theory that would explain whyrelatively small physical and chemical differ-ences in ambient water would control speciesdistributions.


Regional surveys of benthic foraminiferal dis-tr ibutions show that there are horizontal as wellas vertical gradients in taxon abundances. Thisis clearly seen in Poag’s ( 1 9 8 1 ) atlas of Foramini-fera in the Gulf of Mexico, which illustratesstrong distributional changes in the vicini ty ofthe Mississippi River Delta. Similarly, Lutze andCoulbourn (1983/84) recognized lateral changesin benthic foraminiferal communities on thecontinental margin of northwestern Africa.Some of their findings are shown in Fig. 1 1 . 1which presents regional patterns of abundancefor the living taxa. These community or assem-blage distribution patterns were associated withchanging sedimentary regime, and with organic-carbon content of the sediment. A similar inter-pretation of faunal distributions was made forthe northeastern U.S. continental margin byMiller and Lohmann (1982) . In the case of theGulf of Mexico, Loubere et al. (1993a) demon-strated that the flux of organic matter to theseabed was higher on the Mississippi River deltaslope than elsewhere in the northwestern Gulf,so that lateral changes in foraminiferal commu-nities could be associated with this flux. Oster-man and Kellogg (1979) recognized the impactof surface-ocean productivity on benthic fora-miniferal assemblages in a study of surface sedi-ments from the Ross Sea, Antarctica. Sen Guptaet al. (1981) observed unusual foraminiferalassemblages on the Florida continental slopeassociated wi th upwelling. Van der Zwaan(1982) argued on the basis of geologic inter-pretation of Miocene sections in the Mediterra-nean region that food supply must be adominant controlling factor of benthic foramini-feral taxon distributions. Boersma (1985) andWoodruff (1985), in their geological investiga-tions, also concluded that food supply wasimportant. Mackensen et al. (1985) examinedforaminiferal assemblages on the continentalmargin of southwestern Norway, and found thatsome taxon distributions correlated to organiccarbon content of the sediments. A larger scaleanalysis of Rose-Bengal stained (presumedl iv ing) benthic Foraminifera from the top centi-meter of the sediments and dead assemblagesfor the South Atlantic by Mackensen et al.

(1993a) also found dis tr ibut ions that varied lat-erally. Part of thei r data is shown in Fig. 11.2,which presents assemblage distr ibutions theauthors associate wi th increased carbon flux tothe seafloor in the vicinity of the Polar Front.Two higher productivity assemblages/communi-ties are vertically separated under what Mack-ensen et al. (1993a) interpret as a water masseffect (perhaps chiefly a temperature/effect).However, the region examined is stronglyaffected by carbonate dissolution and a shoalingCCD (calcite compensation depth, the i r Fig. 4).So, changing preservation cannot be discountedas a factor contr ibut ing to vertical assemblagegradients in the South Atlantic. In this case,preservation wil l correlate with changing watermasses (Antarct ic Bottom Water vs. Nor thAtlant ic Deep Water). Schmiedl et al. ( 1997)conducted a study on the Southwest Africanmargin similar to that of Mackensen et al.(1993a). They found that stained and dead fora-miniferal taxon dis t r ibut ions were most stronglyassociated with interpreted food supply andpore-water oxygen content (nei ther directlymeasured). They examined taxon principal com-ponent correlations with water depth, porosity,carbonate content, total organic carbon, tem-perature, sa l in i ty , bottom-water oxygen content,phosphate content, and calculated TOC flux.Complete analysis of faunal responses is compli-cated by the correlations among the environ-mental variables (not given) which makedist inguishing their separate effects d i f f i cu l t .

The benthic foraminiferal assemblage rela-tionship to surface-ocean biological productivityand its related organic carbon flux to the seabedwere f i r s t unambiguously tested by Loubere( 1 9 9 1 ) in a study where productivi ty was statis-tically uncorrelated with any other significantenvironmental variable. This work showed aquant i ta t ive relationship between product iv i tyand the benthic foraminiferal assemblages, andrecognized assemblages with part icular rangesof surface-ocean biological productivity. TheLoubere ( 1991) analysis was later expanded tocover the eastern Pacific (Loubere, 1994), theAt lant ic Ocean ( Fariduddin and Loubere, 1997),the Indian Ocean (Loubere, 1998), and finally



the global ocean (Loubere and Fariduddin,1999).

These works used geographically selectedsamples taken within a limited range of waterdepths so that the biological productivity signalwould be uncorrelated to other factors thatcould influence benthic foraminiferal assem-blage composition; this approach avoids misin-terpretation of environmental effects throughspurious correlations among controlling eco-logic factors (e.g. Loubere and Qian, 1997).Figure 11.3 shows the regional patterns of ben-thic foraminiferal assemblages (factor patterns)found in the above studies for the eastern Pacificand the Atlantic. The higher-productivityupwelling areas of the two oceans are clearlymapped out on the ocean floor by theForaminifera.

There is a global uniformity in the taxa foundassociated with different ranges of productivity.Higher- and lower-productivity taxon groupingsof Loubere and co-workers (see Figs. 11.4, 1 1 . 5 )are consistent with the results of other regionalsurveys in the higher latitude South Atlantic(Mackensen et al., 1993a) and the South AfricanAtlantic continental margin (Schmiedl et al.,

1997). The global data base of taxon abun-dances for the deep open ocean has also beenused to quan t i fy the foraminiferal assemblage tosurface-ocean productivity relationship viamultiple regression. Assemblages have been usedto estimate productivi ty with an (east-ern Pacific, Loubere, 1994) and 0.89 (globalocean, Loubere and Fariduddin, 1999).

In addition to the influence on assemblages,surface-ocean productivity also seems to affectplanktonic to benthic (P/B) foraminiferal ratios(Berger and Diester-Haas, 1988) and benthicforaminiferal accumulation rates (Herguera andBerger, 1991). Both of these relationships wouldresult from a correlation between benthic fora-miniferal production and flux of organic carbonto the deep-sea floor. Li t t le information is avai l -able about benthic foraminiferal productivity(shells generated per u n i t t ime), but standingstocks are related to food supply, as seen in thesurveys of Lutze and Coulbourn (1983/84) andSchmiedl et al. (1997) . Also, examinat ion ofP/B ratios and foraminiferal shell accumulationrates must take into account taphonomic pro-cessing wi th in the sediments. This is not con-stant across all oceanic environments, and is still


poorly defined. The P/B ratio has been tradi-tionally used to estimate water depth on conti-nental margins, but also includes a productivitysignal. Analysis by van der Zwaan et al. (1990)

suggests that this signal is largely incorporatedin taxa deemed to be infaunal. The relationshipbetween accumulation rate and productivity hasbeen quantitatively calibrated at a relatively lim-


ited number of locations in the Pacific Ocean.The use of the accumulation rate as a produc-t ivi ty signal depends on the assumption thateach foraminiferal test, regardless of species, isequivalent to a set quant i ty of organic carbonreaching the seafloor. It must also be assumedthat taphonomic processes are linked to organic-carbon flux to the seafloor so that a consistentproductivity signal can be maintained throughthe transition from living community to fossilassemblage. Naidu and Malmgren (1995) testedboth the P/B and benthic foraminiferal accumu-lation rate tracers for paleoproductivity at a sitein the oxygen minimum zone of the Omanmargin in the Arabian Sea. They found thatneither appeared to properly reflect changes insurface-ocean productivity (hence organic-carbon flux to the seabed) through the past18,000 years. The favored explanation for thiswas that the low oxygen content of bottomwater placed constraints on the benthic fora-miniferal community, and that their abundancesmainly reflected changes in oxygen supply. Thelink between organic carbon flux and the P/Bratio and benthic foraminiferal accumulation

rates needs fur ther exploration over a broaderrange of environments. In particular, justifica-tion is needed for accepting the assumption tha tall foraminiferal shells, regardless of species,represent the same quant i ty of labile organic-carbon reaching the seafloor.

Finally, associations have been found betweenorganic carbon flux to the seabed and ind iv idua ltaxon abundances and taxon morphology. Cor-liss (1985, 1991) , Corliss and Chen (1988) , andCorliss and Fois (1990) have observed variationsin benthic foraminiferal morphotypes whichthey ascribe to changing organic carbon flux tothe seabed and associated microenvironments.Corliss put morphologies into three habi ta t -groups: epifaunal, shallow in fauna l ( j u s t belowthe sediment-water interface), and deeper infau-nal. Corliss and Chen divided their morphotypesinto nine groups: rounded trochospiral,plano-convex trochospiral, mil iol ine, bicon-vex trochospiral, rounded planispiral, flattenedovoid, tapered and cylindrical, spherical, andflattened tapered. They found regular changesin the abundances of the morphotype groups intransects down continental margins. Deeper-



infaunal habitat types (e.g. rounded planispiral,tapered cylindrical) decrease in abundance withincreasing water depth.

At the species level, Collins (1989) examinedmophometric variation in Bulimina aculeata andB. marginata, and found shape variations thatcould be linked to the abundance of organiccarbon and mud along the margin of the Gulfof Maine. Boltovskoy et al. ( 1 9 9 1 ) summarizedstudies showing the effects of food avai labi l i tyon the size of foraminiferal taxa. These appearto be environmentally dependent. Corliss (1979)inferred that in the deep sea, smaller size inGlobocassidulina subglobosa was associated withlimited food supply. Caralp (1989a) associatedlarger size and higher percentage of abnormaltests in Melonis barleeanus at a location on theslope of west Africa with increased supply oflittle altered organic matter.

11.3.4 Seasonality of the organic carbon flux tothe seabed

The discussion so far has treated organic carbonflux to the deeper seabed as a homogeneousecological factor. However, it is well docu-mented that the flux is often highly variable intime. In many oceanic areas, there are seasonalpeaks in surface-ocean biological productivity,and these may produce relatively short burstsof organic carbon rain on the seafloor. Forexample, Hecker (1990) and Smith et al. (1996)showed that blooms of phytoplankton can beaccompanied by accumulation of fresh organic-detritus on the seafloor. Pfannkuche (1993) sawa marked increase in the relative abundance ofbenthic Foraminifera at a North Atlantic sam-pling station (47° N, 20° W) in response to abenthic flux event. Altenbach (1992) reviewedbenthic foraminiferal response to short termevents in the deep sea. Linke et al. (1995) pre-sented experimental evidence of a rapid responseof benthic Foraminifera to an inf lux of organicmatter. Corliss and Silva (1993) and Silva et al.(1996) showed a rapid seasonal growth responsein benthic Foraminifera along the Californiaborderlands, probably in response to increasedorganic matter flux to the seafloor. Caralp

(1984) observed that certain species of deeper-water benthic Foraminifera appear to be moreabundant when supplied wi th fresh organiccarbon. Finally, Gooday (1988, 1993. 1996) andGooday and Lambshead (1989) found tha tforaminiferal species such as Alabaminellaweddellensis. Epistominella exigua, E. pusilla.Fursenkoina sp. and Globocassidulina subglobosapreferent ial ly use freshly fal len phytoplanktondetritus as a microhabitat. The organic carbonflux seasonality signal in benthic foraminiferalassemblages from deep-sea surface sedimentswas examined by Loubere and Fariduddin(1999). They analyzed a global assemblage database in relation to average surface-ocean biolog-ical productivity and a seasonality index inter-preted from Coastal Zone Color Scanner imagesof oceanic phytoplankton pigment concen-trations. Loubere and Fariduddin divided theassemblage data base into groups based on pro-duct iv i ty and seasonality, and used Discrimi-nant Function Analysis to test for separationamong these groups. Figure 11.6 shows theirresults. They found a simple patterning of theforaminiferal data with Discriminant Function1 summarizing the average annual productivityresponse and Function 2 incorporating theseasonality response. The location of groupcentroids in Fig. 11.6 shows that the seasonalitysignal in benthic assemblages is largest at higheraverage annual productivi ty (Groups 1 and 2),and decreases as productivi ty drops (Groups 7,8, and 9). At low productivities, it is difficult toidentify a seasonality driven response in thetaxa. This is intuitively satisfying, as one wouldexpect an impor tan t ecologic difference betweencommunities experiencing a substant ia l andcontinuous flux of organic matter and communi-ties receiving that f lux as a large pulse of l imitedduration, with low food supply in interveningmonths. For Discriminant Function 2, the sea-sonality axis, most of the discrimination is basedon E. exigua, C. hooperi, and C. laevigata whichare more abundant at higher seasonality. andon the hispid Uvigerina and B. alazanensis whichare more abundant at low seasonality. Addit ion-ally, comparing mean assemblages shows thatM. barleeanus, A. weddellensis, C. wuellerstorfi,

Why benthic Foraminifera reflect food supply 193

and M. pompilioides are more abundant whereseasonality is high, whereas S. bulloides and B.mexicana are more abundant under lower sea-sonality. Finally, Loubere and Fariduddin(1999) found that distinction could also be madebetween settings with a single annual pulse ofsurface-ocean productivity and those with sev-eral or intermittent pulses.

11.4 WHY BENTHIC FORAMINIFERAREFLECT FOOD SUPPLY

11.4.1

Any examination of benthic foraminiferalresponse to organic carbon flux should includea view of the response of benthic organisms asa whole. This is relevant to developing theories


concerning foraminiferal ecology and to formu-lating questions for further research (sec-tion 11.5). Our review of the benthos here willbe limited to deeper-water environments whereavailability of food is most clearly a limitingfactor.

A broad review of benthic communityresponse to food supply is presented in Pearsonand Rosenberg (1987). The environment beingconsidered is muddy, and often seen as relativelyunchanging. The dominant organisms are poly-chaetes, bivalves, peracarid crustaceans (especi-ally tanaids), nematodes, and foraminifers(Pearson and Rosenberg, 1987; Jumars et al.,1990) and the deposit feeders are the dominantfeeding guild. An early observation concerningdeep-sea organisms was their high diversity (e.g.Sanders, 1968) which seemingly conflicts withthe homogeneity of their environment. Thisdiversity is an important, but not yet completelyunderstood, clue about deep-sea ecology.

The broad scale distribution of deep-seaorganisms shows several global patterns. Thedensity of deep-sea dwellers decreases with dis-tance from the coastline (Thiel, 1983), with somevariation on continental slopes where organicmatter depocenters occur (Duineveld et al.,1997; Lampitt et al., 1986). A global map ofbenthic organism abundance (Belyayev et al.,1973) shows clearly that numbers are highestalong continental margins and beneath upwell-ing areas, and lowest beneath the subtropicalgyres.

On a regional scale, a number of studies nowshow that the flux of organic matter to theseafloor influences the distribution and abun-dance of benthic organisms. A comprehensiveexample of this is provided on the continentalslope off Cape Hatteras (Diaz et al., 1994). Astrong lateral gradient in sediment accumulationrates is accompanied by a large increase inorganic carbon deposition in the Cape Hatterasarea (DeMaster et al., 1994). This gradient isaccompanied by marked changes in benthiccommunity composition and community struc-ture (Hecker, 1994; Blake and Grassle, 1994,Hilbig, 1994). Additionally, the abundance of

benthic organisms greatly increases in responseto an increasing organic carbon flux (Blake andHilbig, 1994). As the flux goes up, the communi-ties show a decrease in diversity, increased abun-dance of normally scarce taxa, and the presenceof taxa normally limited to shallow (continentalshelf) water environments. Analogous varia-tions in benthic abundance and communitystructure are observed off western Sweden(Rosenberg, 1995), and off Southwest Ireland(Duinveld et al., 1997). In all these settings thereare complex mixes of organic matter derivedfrom the continent, which may be degraded, andpulses of labile material from the sea surface.Exactly how the taxa use these different sourcesof organic matter is unclear. Also important tothese environments is benthic disturbance andthe action of currents, which may transport con-siderable sediment and make suspension feedinga viable feeding strategy. Carney (1989) specu-lates that feeding strategies in the benthos maychange depending on the flux of labile materialto the seafloor. When rapidly sinking high nutr i -ent pulses of organic matter arrive, detritus feed-ing metazoans may consume this materialdirectly and rapidly. It is important here that inregions of high seasonality, a substantial portionof the phytoplankton bloom may reach the ben-thos (Pearson and Rosenberg, 1987; Lampitt,1985). Between the pulses, bacterial biomassderived from more refractory detritus would bea more important part of the diet.

The average size of organisms diminishes withdepth and distance from the continents. Mostdeep-sea animals are small. Intensive naturalselection for particle selection ability is seen asone reason for this (Jumars et al., 1990). Carney(1989) points out that in response to decreasedcarbon input with depth, we should expect tofind in the fauna both a decreased overall abun-dance and species replacement determined bythe efficiency of foraging. Carney also reviewsdata indicating that the nutri t ional value oforganic matter decreases with depth, fur therintensifying the pressure on the benthos tosearch efficiently, hoard resources, and maxi-mize external resources in the processing of food.

Why benthic Foraminifera reflect food supply 195

Duineveld et al. (1997) review organic carbonaccumulation and quality on several continentalmargins and find in the northeastern Atlanticthat much of the material on the slopeis degraded and refractory. Wheatcroft andJumars (1987) show that labile detritus will berapidly consumed once in the sediments whichare subject to selective mixing, so the labilematerial will not be distributed in the sedimentmixed layer much beyond its point of entry(detritus settling on the seafloor) or generation(bacterially produced labile material).

In concert with these observations, it has beenfound that abundance and taxon compositionin the larger benthos and the meiofauna changeprogressively down continental margins (Coull,1972; Coull et al., 1977; Haedrich et al., 1975;Rowe and Menzies, 1969; Rowe et al., 1974,1982), and that the habitation zone within thesediments thins with distance from the shoreline (Shirayama, 1984).

The food resources available to the benthosare subject to the dynamics of the bottomboundary layer ( B B L ) and the sediment mixedlayer (SML), and it is the properties of these towhich the benthic organisms will respond. Itappears that benthic organisms may follow threefeeding strategies (Carney, 1989; Jumars andGallagher, 1982). They may be opportunisticand rapidly consume newly arrived labile mate-rial at the seafloor. They may collect and hoardmaterial for use at their leisure. Collection maybe accomplished by hydrodynamic trapping ofless dense organic material in structures andpits, and by collection into burrows (Jumarset al., 1990; Bett and Rice, 1993). Finally, ben-thos can also harvest the bacteria which use lessdesirable, or inaccessible, organic matter. Allerand Aller (1986) showed that burrows and ben-thic structures could serve as collection pointsof organic matter, and also as centers ofbacterial activity on the deep-sea floor. Thus,structures would offer enhanced feeding oppor-tunities to the benthos. The bacteria would pro-vide not only organic carbon, but also serve toextract nitrogen from surrounding waters andprovide it in a usable organic form to the otherbenthos (Jumars, 1993, p. 41) .

Deep-sea diversity remains difficult to under-stand, but it may be partly explained by acombination of taxon feeding strategy and envi-ronmental heterogeneity. Although one mightexpect most deep-sea benthos to be opportunistsfeeding on whatever might be present, it appears,counterintuitively, that resource partitioningmay be common in abyssal environments.Jumars et al. (1990) consider an optimal forag-ing theory and conclude tha t there are advan-tages in being selective. Evidence for selectivitycan be found in holothuroids (Hammond, 1983)and worms (reviews in Fauchald and Jumars,1979; Lopez and Levinton, 1987).

The idea of environmental heterogeneity alsoseems initially counterintuitive as the deep seaappears homogeneous on the larger scale. How-ever, Grassle and Morse-Porteous (1987) andTyler (1995) argue that heterogeneity exists onthe deep-sea floor as a result of small scale physi-cal processes, episodic larger events (one mightconsider benthic storms here, e.g. Hollister andMcCave, 1984), and biogenic heterogeneity.Concepts here are reviewed in Smith (1994) .Heterogeneity would lead to a succession pro-cess with a mosaic of stages developed over theocean floor. Jumars and Gallagher (1982) sug-gest a theory for this, using Markovian succes-sion models. Different taxa would flourish insequence after a disturbance (which might be aphytodetritus pulse) as their ecological special-izations match the temporary conditions createdby the succession process and the probabilitiesgoverning community membership. A key ele-ment in this idea would be that disturbances arerare enough to allow succession to developoften, but common enough to prevent climaxand competitive exclusion. The influence of dis-turbance on benthic communities is examinedin Thiery (1982), Probert (1984) , and Thistle(1981). Thistle and Eckman (1990) present someevidence that benthic organisms associate pref-erentially wi th each other, indicating thatheterogeneity, in response to biotic factors, doesexist on the deep-sea floor.

To summarize, the response of the benthos toorganic carbon flux will be mediated by anumber of ecologic behaviors. These include:


particle size selection, efficiency in foraging, feed-ing strategies, flexibility in resource use, resourcepartitioning and community succession, benthicorganism associations, and changing distribu-tion within and upon the sediments.

11.4.2 Theoretical considerations

It is clear that patterns in benthic foraminiferalassemblages and abundances are related to theflux of organic carbon to the seafloor. So far,theoretical ideas about this have been mostlylimited to considering adaptations to microenvi-ronments in the sediments and, to a lesserdegree, resource selection. The other factorslisted in the previous section have not receivedmuch attention. Hence, a complete theoreticalexplanation of foraminiferal response to organiccarbon flux has yet to be developed, althoughSjoerdsma and van der Zwaan (1992) have pre-sented a general empirical model. Corliss (1985)observed that deep-sea benthic Foraminiferacould be classed into broad morphologic groupsand that these groups could be associated withparticular microenvironments within the sedi-ments. Support for this is presented for materialoff the northeastern U.S.A. in Corliss and Emer-son (1990). An examination of shifting morpho-type abundances on the margins of Norway(Corliss and Chen, 1988) and the northern Gulfof Mexico (Corliss and Fois, 1990) show pat-terns that can be tied to flux of organic carbonto the seafloor, with epifaunal morphotypesbecoming most abundant at greater depth wherethe flux is lowest. Loubere et al. (1993b) exam-ined assemblage changes with water depth inthe northern Gulf of Mexico in light of pore-water chemical measurements which could beused to constrain biogeochemical zonation inthe surficial sediments (upper 15 cm) and theflux of organic matter to the seafloor. Ideassimilar to those above are also presented inchapter 10 and Jorissen et al. (1995). The result sof these various studies, when combined withobservations on meiofaunal sediment concen-tration profiles, suggest that foraminiferalspecies are adapted to different microhabitatsthat are vertically stratified in the sediments.

This s t ra t i f icat ion increases and deepens in thesediment column as flux of organic carbon tothe seabed increases. Thus, certain taxa areadapted to epifaunal or surface-sediment habi-tats, others inhabit suboxic settings, while s t i l lothers exist near the pore-water anoxic bound-ary within the sediments. Demands of the micro-environment influence test architecture, and thisproduces the morphotype gradients observedabove. Since the existence of the microenviron-ments is tied to flux of labile organic carbon tothe seabed, we see changes in benthic assem-blage composition as the importance of differentmorphotype groups changes with changingmicrohabitat development. Note, for example,that most of the high-productivity group taxashown in Fig. 11.5 are ‘infaunal’ morphotypesby Corliss’ classification, and would inhabi tsuboxic microhabitats. These ideas are devel-oped in a quant i ta t ive framework in Loubere(1997). In this book, chapters 10 and 12 containmore information on microhabitats.

The review so far has emphasized a static,two-dimensional view of foraminiferal taxa thatare vertically stratified in the sediments. How-ever, areal and time dimensions must also beadded to the picture. L inke and Lutze (1993)examined the concept of habitats in dynamicterms, suggesting that simple vertical s t rat i f ica-tion within the sediment column in response togeneral pore-water chemical gradients is anoversimplified view of benthic foraminiferalecology. These authors find tha t taxa are distrib-uted in a variety of microenvironments wi th inand on the sediments, which can include suchunusual settings as the appendages of benthicinvertebrates. Staining and seasonal samplingby Gooday (1986, 1996) and Barmawidjaja et al.(1992) show that many benthic foraminiferalspecies do not have fixed vertical zonationwithin deep-sea sediments, and that such zona-tion as they have can change from month tomonth. In the subtidal environment, Hoheneg-ger et al. ( 1 9 9 3 ) and Thomsen and Altenbach(1993) observed patchy dis t r ibut ions of Fora-minifera, and noted their association wi th thesediment structures of larger organisms. Anumber of taxa appeared to live in the oxic halo

Conclusions and questions 197

of burrows. Similar observations for the deepsea (Gulf of Mexico) were made by Loubereet al. (1995), who noted that foraminiferal distri-butions were patchy and apparently concen-trated near burrow structures.

In the context of foraminiferal response toproductivity and organic carbon flux to theseabed, the critical factors controlling distribu-tion should be the availability of labile organicmatter in different microenvironments withinthe sediments, the distribution of those microen-vironments in time and space, the availability ofoxidants for respiration (oxygen being the mostchemically efficient one), and competition fromother organisms for the resources. Foraminiferaltaxa will have adapted to these factors, and taxapresent within the sediments will change as thefactors change, in response to varying flux oforganic matter to the seafloor.

Finally, moving away from the living popula-tion and considering assemblages preserved inthe sediments, taphonomy (chemical and bioticprocesses that destroy foraminiferal tests duringtheir incorporation into the sedimentary depos-its) is also an important factor. This topic isexamined in chapter 16. Also, Loubere et al.(1993b) and Loubere (1997) review taphonomicprocesses for the deep ocean as these relate toorganic carbon flux. Taphonomy apparentlyenhances the organic carbon flux signal pre-served in fossil assemblages.

11.5 CONCLUSIONS AND QUESTIONS

The mechanisms that control the benthic fora-miniferal response to organic flux are not wellunderstood, and the roles of the Foraminiferain the benthic community have not been clearlydetermined. While attention to a few largeagglutinated foraminiferal taxa under specialcircumstances has shown their importance tothe benthos (e.g. Bathysiphon, Gooday et al.,1992b), little is known about the communityposition of the many small calcareous Foramini-fera that make up the bulk of the geologic recordof the benthos in deep-sea sediments. It has beenclaimed that benthic Foraminifera can be a

dominant component of life on the seabed(Altenbach and Sarnthein, 1989; Gooday et al.,1992a), but it remains unclear how they relateto the biological theories of community ecologydeveloped for the metazoa.

Key issues from the biological perspective arethose raised for other benthos: (a) how are pop-ulations maintained in the deep-sea settingswhere food supply is severely limited? and (b)how is diversity maintained in the deep-sea envi-ronment? For other organisms, as reviewedabove, the answers to these questions rest withresource partitioning and environmental hetero-geneity, most of which is seasonal (arrival anduse of food falls), physical (benthic storms), orbiologically generated (seabed environmentalalteration by the activities of organisms, e.g. pitsand burrows). For many deeper ocean settings,one can imagine each foraminiferal species as abit player in a show that is running continuouslybut at ever changing locations, so the taxa dotheir brief routines at the appropriate time ateach spot, flourish for a moment, and thenvanish only to pop up at the next venue torepeat their act. A Markovian process was pic-tured by Jumars and Gallagher (1982) in whichenvironmental change at the seabed is pro-gressive in between disruptions (perhaps a pulseof phytodetritus from the euphotic zone), andtaxa replace one another as their fitness allowsthem to exploit the conditions of the momentin their local setting. The authors imagined astochastic succession (deterministic only ifallowed to run to termination), perhaps withsmaller organisms at the beginning and largerones towards the end. We have some hint of thisfrom Gooday’s records of taxa which respondquickly to phytodetritus falls (early stage oppor-tunists in the succession series), and in the evi-dence for a rapid physiological response of deep-sea Foraminifera to newly available organicmatter (Linke et al., 1995). Mostly, however, wehave no idea what exactly the different benthicforaminiferal taxa do for a l iving on and in theseafloor. We do not know what microenviron-ments they most exploit, and we are ignorant ofwhat stages they occupy in the succession seriesthat develop within their deep-sea environments.


It is worth noting here that these series will nodoubt vary, depending on both the averagequantity and the variability (seasonality) of theflux of labile organic matter from the sea surface.Thus, environmental heterogeneity and disrup-tion in the eastern equatorial Pacific, forinstance, will be different from those observedin the highly seasonal northwestern IndianOcean.

As for food acquisition, it is apparent thatbenthic metazoa are size selective in the materialthey ingest and that they have strategies forconcentrating organic matter (density sorting).Additionally, they have search strategies to max-imize their chances of finding new material.Finally, it also appears that larger benthicorganisms can enhance local bacterial pro-duction for their own benefit. The resources thedifferent foraminiferal taxa use, however, arepresently unknown.

As noted by Carney (1989), there are funda-mental ecologic differences among organismsthat use freshly arrived detritus, those that feedon the bacteria and other small organisms thatrapidly colonize the detritus, and those that feedon bacteria which slowly and steadily degradethe more refractory organic matter within thesediment-mixed zone. These organisms rangefrom those that must use an often highlyintermittent food supply as quickly as possible,to those that use a much less productive foodsource which is nevertheless fairly homogenousand continuously available. In between wouldbe those taxa that take advantage of enhancedbacterial production, perhaps within a burrowstructure or lining. The question is, what do thevarious taxa of the benthic Foraminifera do?There is evidence that living individuals of Uvig-erina peregrina are unevenly distributed in thesediments and associated with the structures ofother benthic organisms (Loubere et al., 1995).For Cibicides wuellerstorfi, there is evidence forraised habitat selection (Lutze and Thiel, 1987)and attachment to larger metazoa (Linke andLutze, 1993), which might be an adaptation forfeeding strategy (suspension feeding) or for loca-tion in the environment created by the largerhost. For most benthic foraminiferal taxa, how-

ever, we have no information about living distri-bution in relation to other benthos or foodresources. These resources also include oxidizingagents (e.g. oxygen) in settings where the anoxicboundary occurs within the habitation zone ofthe sediments. For example, Corliss (1985) andCorliss and Emerson (1990) show that Globobul-imina affinis lives along the anoxic boundarywithin the sediments, indicating survival in lowoxygen conditions other taxa may not tolerate.However Loubere et al. (1995) present evidencethat U. peregrina, while l iving within the sedi-ments, may select burrows as a habitat, perhapsbecause these are better ventilated.

This review shows that a number of broadtrends have been described, relating benthicForaminifera to surface-ocean biological pro-ductivity and the flux of organic carbon to theseafloor. Taxon abundances within benthic fora-miniferal assemblages change in predictableways with shifting organic carbon flux. Benthicforaminiferal accumulation rates too maychange predictably. Patterns of taxon abun-dance can also be associated with seasonalityand variability in the organic carbon flux. Theassemblage response to increasing surface-oceanbiological productivity and organic carbon fluxincludes the appearance in the deep sea of taxanormally limited to middle and upper portionsof the continental margin. The habitation zoneof Foraminifera within the sediments thickensas organic carbon flux increases (wi th in thelimits normally observed in the deeper ocean).Some taxa have shown selection for depthrelated microhabitats under higher organiccarbon flux conditions. Finally, some taxaappear to be rapid-response opportunists in col-onizing newly arrived phytodetri tus at theseafloor.

The conclusion of this review must thereforebe that we have now reached a stage in ourunderstanding in which we have identified pat-terns in benthic foraminiferal data that can beconsistently linked with organic carbon flux tothe seabed. The link has been quantified statis-tically so that reconstruction of past surface-ocean biological productivity using fossil ben-

Acknowledgments 199

thic foraminiferal data is possible. However, ourability to explain benthic foraminiferal taxonoccurrence, production, or pattern needsimprovement. Confident assessments of paleo-productivity will require a better understandingof which portion of the organic carbon signaldifferent benthic foraminiferal taxa respond to.


We are grateful to Drs. Andrew Gooday, FransJorissen, and Robert Douglas for their reviewsof the manuscript . Omissions and errors remainour own. Thanks, finally, to Figen Mekik forhelp with the S.E.M.


12Foraminifera of oxygen-

depleted environmentsJoan M. Bernhard and Barun K. Sen Gupta

12.1 INTRODUCTION

The study of foraminiferal tests from oxygen-depleted environments is of interest in a varietyof disciplines, most notably economic geology,environmental geology, ecology, and cellbiology. Fossilized Foraminifera from ancientoxygen-poor environments may help identifypetroleum source rocks. From an ecological andenvironmental-impact perspective, foraminiferaltests can be used to deduce historical, baselineconditions prior to environmental changes,including eutrophication connected to anthro-pogenic activities. Lastly, the physiology ofForaminifera capable of surviving anoxia is ofinterest to cell biologists because these protistsare traditionally considered to be obligateaerobes.

Before discussing aspects of foraminiferal distri-bution and adaptation in oxygen-depleted envi-ronments, it is necessary to define the variousterms used to describe oxygen depletion(Table 12.1). The majority of these terms origi-nated from the seemingly disparate disciplines ofgeology and physiology. In general, the adjectives‘anoxic’ and ‘anaerobic’ both indicate an absenceof oxygen. Whereas either term can be used to

Barun K. Sen Gupta (ed.), Modern Foraminifera, 201–216© 1999 Kluwer Publishers. Printed Great Britain.

describe an environment, an organism, or a chem-ical reaction, ‘anoxic’ is typically used for environ-mental descriptions while ‘anaerobic’ is generallyused as a biological descriptor. In some instances,the use of either term is somewhat problematicbecause analytical detection limits prohibit con-fident measurement of trace concentrations ofoxygen. Some authors have used the term ‘anoxic’to refer to conditions where butassociating a term that means ‘no oxygen’ withvalues above zero, however small, is confusing.Thus, we use ‘microxic’ for environments in whichoxygen is measurable but less than 0.1 ml

202 Foraminifera of oxygen-depleted environments

and restrict ‘anoxic’ to environments withoutdetectable The term is a variant of ‘microoxic,’coined by Jørgensen and Revsbech (1983), for‘environments of very low oxygen concen-trations.’ We employ ‘postoxic’ (Berner, 1981) asa subclass of ‘anoxic’ for situations where there isa lack of both oxygen and reducing conditions(‘suboxic’ of Fenchel and Finlay, 1995, but not ofTyson and Pearson, 1991). For environments with0.1–1.0 ml we employ‘dysoxic,’ which is equivalent to the ‘dysaerobic’regime of Rhoads and Morse (1971). This defini-tion of dysoxic (Fenchel and Finlay, 1995; Bern-hard, 1996) does not agree with that of Tyson andPearson (1991), who use the 0.2–2.0 mlrange. Environments with more than 1 mlare placed under the single term ‘oxic.’ Generally,‘hypoxic’ is used as a physiological term that refersto any depletion in oxygen that inhibits thenormal respiration rate of a particular organism.The term ‘microaerophile’ is used for an aerobethat requires very little oxygen, but is adverselyaffected by higher oxygen concentration

Oxygen-depleted environments are extensivein the marine realm. Over 1 % of the water

samples from the world ocean recorded in theU.S. National Oceanographic Data Centerdatabase (for the 1905 1982 period) wereseverely dysoxic or microxic (i.e. <0.2 ml/l;Fig. 12.1; see also Kamykowski and Zentara,1990). Because oxygen concentrations in sedi-ments are generally lower than of the over-lying seawater, we expect oxygen depletion inmost of the benthic environments correspondingto the shaded regions of Fig. 12.1.

The most widespread dysoxic and microxicmarine environment is the subsurface sediment.Since most aerobic, benthic organisms live nearthe sediment-water interface, oxygen consump-tion is high in this habitat. At a particularsedimentary depth, depending primarily on res-piration rates and abundances of organisms,oxygen demand will exceed supply and sedi-ments will become anoxic. The top of the anoxiczone is typically within the top few decimetersof sediment, even where overlying waters arewell-aerated.

The second most laterally extensive oxygen-depleted marine environment is termed theOxygen Minimum Zone (OMZ). The formation

Introduction 203

of an OMZ depends mainly upon large-scaleoceanic circulation, geography, and primaryproductivity (Figs. 12.2A, B). The intermediate-depth water masses of eastern oceanic marginstypically consist of ‘aged’ water that has notbeen recently aerated at the sea surface. Thus,the in these water masses is depressedcompared to surface concentrations. The inter-mediate-water will become even moredepleted if the water is situated under a regionof high primary productivity, due to the oxida-tion of the large amounts of organic debrissettling through the water column. Because thewater column of an OMZ is depleted in oxygen,the in surface sediments where the OMZimpinges upon the seafloor will also be depau-perate in oxygen.

Some silled basins and fjords also constitutelaterally extensive, dysoxic marine environmentsthat may have anoxic surface sediments. In thesetypes of basins, stagnation leading to oxygendepletion can be caused via two major path-ways: ( 1 ) from the presence of a sill that inhibitsrecharge of aerated waters, and ( 2 ) from fresh-water input that will produce a strong halocline,inhibit mixing, and lead to stratification in thebottom waters (Figs. 12.2A, C). If enoughcarbon loading occurs in either of these situa-

tions, bottom waters will become dysoxic,microxic, or anoxic.

Spatially restricted oxygen-depleted environ-ments occur at marine hydrocarbon seeps. Suchseeps have fluxes of emanating from thesediments and commonly support populationsof Beggiatoa, a large, motile, filamentous,chemolithotrophic, sulfide-oxidizing bacterium.Growth of Beggiatoa requires the presence of

in the overlying water and in the under-lying sediment (Jørgensen, 1977; Spies andDavis, 1979; Larkin and Strohl, 1983; but seealso Fossing et al., 1995; McHatton et al., 1996).Thus, an oxic-anoxic interface exists wi th in thesemats, even if they are very thin (Fig. 12.3). Thelongevity of Beggiatoa mats at hydrocarbonseeps is unknown, but they are necessarilyephemeral, ‘being controlled by the shiftingpoint sources of sea-floor hydrocarbon emission’(Sen Gupta et al., 1997). Beggiatoa mats arealso known from many environments other thanhydrocarbon seeps (e.g. silled basins, sewageoutfalls).

Another example of spatially and temporallyrestricted marine dysoxic environments is anarea of large food falls. Such areas are organi-cally enriched due to settling of dead organismssuch as whales or other vertebrates. The lateral


Diaz and Rosenberg (1995) note that ‘there isno other environmental variable of such ecologi-cal importance to coastal marine ecosystemsthat has changed so drastically in such a shortperiod as dissolved oxygen.’ Aquaculture facili-ties have also produced localized anoxic areasoccurring under fish cages (Schafer et al., 1995).Other areas that were previously only moder-ately depleted in have become severelydysoxic or anoxic (e.g. sediments in Norwegianfjords adjacent to paper mills; Nagy and Alve,1987; Alve, 1991b).

The following narra t ive is based main lyon published studies regarding Foraminiferafrom these diverse types of dysoxic to anoxicenvironments.

12.2 DISTRIBUTIONAL OBSERVATIONS

In a number of studies, benthic Foraminiferarecovered from oxygen-depleted sediments weretreated with the ‘non-vital stain’ Rose Bengal(Table 12.2). The interpretat ions of these datavaried. Reliance on the concept tha t Foramini-fera could not be anaerobes led to the conclusionthat the occurrence of stained tests in materialprocessed from anoxic deposits simply reflectedtransport from a favorable into an unfavorableenvironment (e.g. Douglas, 1981) . A contraryinterpretation was that the Foraminifera foundin these sediments actually inhabited suchoxygen-depleted environments. However, giventhat Rose Bengal is known to stain dead fora-miniferal cytoplasm for weeks to months ( Bern-hard 1988; Hannah and Rogerson, 1997) and,theoretically, for years (Corliss and Emerson,1990), it was possible that the Rose Bengalstained Foraminifera recovered from oxygen-depleted sediments were dead specimens whosecytoplasm had not yet degraded. Therefore, inorder to determine if Foraminifera actuallyinhabited dysoxic, microxic, and anoxic environ-ments, a more reliable method to dist inguishlive from dead specimens was required in con-junct ion wi th a precise method to determinepore-water oxygen concentrations. The bio-chemical assay to determine the nucleotide

extent of these enriched environments obviouslydepends on the original size of the carcass. Thetemporal persistence of such patches is on theorder of years to decades (Smith and Baco, 1997;Deming et al., 1997).

Seasonal or periodic anoxia, microxia, ordysoxia is also known from coastal areas,including open continental shelves. This isrelated to eutrophication and oxygen consump-tion linked with natural environmental factors(e.g. freshwater input, seasonal stratification) orto anthropogenic effects (e.g. nutr ient i n p u tthrough fertilizers, sewage outfalls). New YorkBight, Chesapeake Bay, Gulf of Mexico, AdriaticSea, and Orinoco-Paria Shelf are examples ofsuch areas (Boesch and Rabalais, 1991; Malone,1991; van der Zwaan and Jorissen, 1991).Regarding the effects of anthropogenic activities,

Distributional observations 205


Experimental observations 207

adenosine triphosphate (ATP) concentrationdeveloped by DeLaca (1986b) was judged as onesuch method (Bernhard, 1989, 1992). In thesestudies, polarographic microelectrodes origi-nally developed by Revsbech et al. (1980) wereemployed to determine dissolved-oxygen pro-files in sediment pore waters from which theForaminifera were recovered. The caveat inthese studies was that the live Foraminiferacould have been inhabi t ing oxygenated micro-habitats around such biogenic structures asmacrofaunal burrows and tubes, as suggestedby Langer et al. (1989) for infaunal tide-flatforaminiferal assemblages and by Moodley(1990) for deep-infaunal Foraminifera from theNorth Sea.

The core-embedding method of Frankel(1970) and Watling (1988; see also Grimm, 1992;Pike and Kemp, 1996) was recently refined topreserve Foraminifera in their life positionwithin sediments (Bernhard and Bowser, 1996).This technique approaches the issue of foramini-feral associations with aerated microhabitats bypreserving foraminiferal life position in sedi-ments where burrowing and tubicolous faunaare absent. The method combines epifluores-cence microscopy and enzymatic activity todistinguish hydrolytically active (i.e. l ive) Fora-minifera with epoxy-resin embedded coring topreserve sedimentary and organism in situ posi-tions. The use of this technique shows that Fora-minifera inhabit the microxic and anoxicsediments of the silled Santa Barbara Basin

(Fig. 12.4; Bernhard, 1996; Bernhard et al.,1997). These sediments are sulfidic, as evidencedby abundant sulfide-oxidizing bacteria Beggia-toa. However, even though such distr ibutionaldata strongly suggest that Foraminifera caninhabit anoxic environments, only experimentaldata can provide compelling evidence for thisconclusion.

12.3 EXPERIMENTAL OBSERVATIONS

12.3.1 Foraminiferal responses to oxygendepletion

Some experimental studies have been conductedto assess the response of Foraminifera to anoxia.It is important to reiterate here that when work-ing with such low , it is diff icul t to ascertainif a supposedly anoxic system is devoid of eventrace amounts of oxygen. Furthermore, it is alsoimportant to remember that all species of Fora-minifera cannot be expected to respond similarlyto oxygen depletion; some species may havedifferent physiological abilities than others.

In a behavioral response experiment, infaunalForaminifera from a periodically dysoxic fjordstarted migrating upward in the sediment whenoxygen in bottom waters decreased below 2 ml

(Alve and Bernhard, 1995); however, thet iming of species responses varied. For example,Bulimina marginata migrated toward aeratedhabitats more quickly than S ta in for th ia fusi-


formis. Also, B. marginata reproduced during themost oxygen-depleted conditions. When bottomwaters were re-aerated, some species (e.g. S. fusi-formis) migrated back into the sediments, pre-sumably tracking a particular geochemicalhorizon.

Responses of some other species to oxygendepletion have been studied on shorter timescales. In a 7-day experiment, Moodley et al.(1998b) observed that while some buriedindividuals of Quinqueloculina seminulummigrated toward aerated sediments, 40–50%remained in presumably anoxic sediments. Inthe same study, but after a 56-day experiment,the majority (57%) of Nonionella turgidaremained in sediments that had undetectable

yet the majority of ‘soft-shelled’ Foramini-fera (i.e. allogromiids and saccamminids)migrated into aerated sediments. Considerablenumbers (17%) of the soft-shelled Foraminifera,

however, remained in sediments that had unde-tectable

12.3.2 Survival of Foraminifera exposed tooxygen depletion

The survival of Foraminifera exposed to anoxiahas also been studied. Using the concentration ofsedimentary particles (food source) around theapertural region as indication ofact ivi ty, Mood-ley and Hess (1992) determined that individualsof three infaunal species (Ammonia beccarii, Elphi-dium excavatum, Quinqueloculina seminulum) sur-vived anoxic incubation for at least one day. Inthe same study, E. excavatum, Eggerella scabra,and Q. seminulum survived as well as secreted testchambers during a six-day incubation in dysoxicor microxic seawater Twolarger agglutinated Foraminifera, Pelosina arbo-rescens and Astrorhiza limicola, are known to sur-

Ultrastructural observations 209

vive putative anoxia for ten days (Cedhagen,1993). The survival period of Ammonia beccarii insuch an environment may be as long as 1–2months (Koshio, 1992, in Kitazato, 1994). Incub-ations in nitrogen-purged seawater for 30 daysshowed that some Antarctic Foraminifera (e.g.Cassidulinoides porrectus, Globocassidulina sp. cf.G. biora, Reophax subdentaliniformis, Uvigerinabassensis) are able to survive microxia and possi-bly anoxia for considerable periods of time (Bern-hard, 1993). The results of that study include theobservation that ATP concentrations in speci-mens recovered after an extended exposure todysoxia were statistically indistinguishable fromthose of control specimens incubated in aeratedseawater.

Since it is possible that Foraminifera becomedormant during exposure to adverse conditionssuch as oxygen depletion, it is of interest to deter-mine ATP concentration ([ATP]) in specimensduring their exposure to microxia or anoxia.Bernhard and Alve (1996) incubated Foramini-fera for 24 days in a nitrogen-flushed experimentalchamber and then extracted their ATP withoutaeration. Results showed that the [ATP] for spec-imens of Psammosphaera bowmanni were statistic-ally similar between controls (i.e. aeration) andtreatments (i.e. microxia). However, the [ATP] ofnitrogen-flushed specimens of other species (i.e.,Bulimina marginata, Stainforthia fusiformis, Ader-cotryma glomerata) were significantly lower thanthose of specimens extracted under aerated condi-tions. Considering all available data from thisexperiment (i.e. survival rates, [ATP] and ultra-structural observations), Bernhard and Alve(1996) concluded that foraminiferal speciesrespond differently to oxygen depletion. Somespecies are apparently unaffected, while othersmay become dormant. If encystment is consideredto be a type of dormancy, then independent evi-dence for such dormancy has been provided byLinke and Lutze (1993), who reported cysts ofElphidium incertum from an environment of puta-tive anoxia. Also, Hannah and Rogerson (1997)concluded that Foraminifera buried in an anoxiclayer become dormant and would require trans-port via bioturbation for their return to aeratedconditions. In yet another long-term anoxic-incu-

bation experiment, certain foraminiferal speciessurvived putative anoxia for 78 days (Moodleyet al., 1997). It should be noted that at some timebetween 33 and 53 days, the experimental incub-ations became sulfidic. Thus, the observationsconcerning survival response to anoxia are some-what compounded by this change in redox chem-istry for approximately the last half to two-thirdsof the experiment.

Sulfidic conditions commonly co-occur withanoxia. As noted in the introduction, the term‘postoxic’ in this chapter implies anoxia withoutreducing conditions. The experiments describedabove addressed postoxic conditions. The fewexperiments that have been conducted to assessthe survival of Foraminifera in anoxic, sulfidicconditions (Bernhard, 1993; Moodley et al.,1998a) show that some Foraminifera toleratesuch environments. After 30 days, ATP concen-trations in specimens fromtreatments did not differ significantly from thoseof aerated controls (Bernhard, 1993). Underhigher concentrations cytoplasmicmovement was observed in Foraminifera afteran incubation period of 21 days, but all speci-mens were dead by the next time point (42 days;Moodley et al., 1998a).

Although experimental results indicate thatForaminifera survive anoxia with or withoutsulfidic conditions for considerable periods oftime, no physiological mechanism responsiblefor such survival is presently known. It is estab-lished, however, that two allogromiid specieshave an alternative oxidative pathway that maybe responsible for their survival in anoxia. Travisand Bowser (1986b) found that the electron-transport inhibitor cyanide did not halt intracel-lular motility, suggesting that at least someForaminifera can survive without oxidativephosphorylation. Ultrastructural studies suggestadditional possible adaptations and mechanismsto allow foraminiferal survival of anoxia.

12.4 ULTRASTRUCTURALOBSERVATIONS

A variety of unusual ultrastructural characteris-tics has been observed in foraminiferal species


that are dominant in oxygen-depleted environ-ments. It is possible that these characteristicsreflect adaptations to extreme oxygen depletion,and possibly to sulfidic habitats, but no consis-tent ultrastructural modification has beenobserved in species from such environments.Furthermore, the published literature does notinclude quantitative, comparative studies on theultrastructure of individuals from anoxic sedi-ments and conspecific individuals from aeratedsediments. Such comparisons in the future mayelucidate the importance of the various ultra-structural modifications.

Three cases of possible bacterial symbioseshave been observed in Foraminifera fromoxygen-depleted sediments. Two species fromthe Santa Barbara Basin have putative endo-symbionts. Buliminella tenuata has numerousrod-shaped bacteria within its cytoplasm(Fig. 12.5A; Bernhard, 1996). These bacteria donot appear to be a food source, since they areintact in all chambers of this multilocular fora-minifer. Nonionella stella has bacteria within itstest, but these prokaryotes are not intracellular(Bernhard and Reimers, 1991). Lastly, infaunalGlobocassidulina cf. G. biora from shallow Ant-arctic waters is known to have intracellular rod-shaped bacteria that appear to be associatedwith pore plugs (Bernhard, 1993). One possiblerole of these putative symbionts is to oxidize

thereby detoxifying this pore-water con-stituent. Given the variance in the morphologicattributes of these three types of bacteria, how-ever, it is likely that they have different meta-bolic capabilities.

Another ultrastructural feature of some Fora-minifera from oxygen-depleted environments(Stainforthia fusiformis, Nonionella stella, Nonio-nellina labradorica) is that they sequester chloro-

Generalizations on low-oxygen foraminiferal assemblages (LOFAs) 211

plasts (Fig. 12.5B; Leutenegger, 1984; Cedhagen,1991; Bernhard and Alve, 1996). Such chloro-plast husbandry is thought to benefit other pro-tists inhabit ing anoxic environments, possiblyby providing oxygen to the host (Johnson et al.,1995). A particular complication in interpretingthe role of chloroplasts in the cases listed aboveis that the oxygen-depleted habitats are not inthe euphotic zone.

A third u l t ras t ruc tura l feature common tomany species from oxygen-depleted environ-ments involves proliferation and aggregation oftwo typical cellular organelles: endoplasmicreticulum and peroxisomes (P-ER; Fig. 12.5C).Such P-ER complexes have been observed inNemogullmia longevariabilis, Gloiogullmia eurys-toma, Nonionella stella, S tainforthia fus i formis ,Buliminella tenuata, and Fursenkoina cornuta(Nyholm and Nyholm, 1975; Bernhard andAlve, 1996; Bernhard, 1996). The role of thesecomplexes may merely be to break downhydrogen peroxide, which is a byproduct in theanaerobic metabolic pathway of glycolysis. Thisbiochemical avenue has been proposed byNyholm and Nyholm (1975) , although it is notestablished that Foraminifera rely heavily onglycolysis.

Ultrastructural investigations indicate thatorganelles which appear to be mitochondria arepresent in all Foraminifera observed to date,strongly suggesting that these species are aer-obes or microaerophiles. In addition, it has beenreported that mitochondria of Foraminiferafrom oxygen-depleted environments are concen-trated beneath test pore plugs (Leutenegger andHansen, 1979). High concentrations of mito-chondria, however, have also been observed inapertural cytoplasm (Bernhard and Alve, 1996),which is assumed to form the pseudopodiaduring network deployment. Optical micro-scopic examinations (Doyle, 1935; J.M. Bern-hard and S.S. Bowser, unpublished data) haveshown mitochondrial movements w i t h i n pseu-dopods, which can extend to at least ten timesthe test diameter of a foraminifer (Travis andBowser, 1991). Thus, it is possible that Fora-minifera inhabiting an environment with a steepredox gradient use mitochondrial act ivi ty in

extended pseudopods to maintain oxidativephosphorylation, even though their tests andcell bodies are located in anoxic sediments.

It is l ikely that benthic Foraminifera inhabi t -ing anoxic, sul f id ic environments use manyadaptations in concert to allow survival in suchseemingly hostile conditions. The two majorchemical barriers are detoxifying and sur-viving without or with very l i t t le oxygen. Asstated earlier, because all Foraminifera exam-ined to date possess organelles that appear tobe mitochondria, apparently they are aerobes.We must note, however, that organelles resem-bling mitochondria in some anaerobic protistsare in fact hydrogenosomes (F in lay and Fenchel,1989). Hydrogenosomes are organelles that per-form a variety of functions, most notably ( i n thecontext of this chapter) to ferment pyruvate,which is a byproduct of the anaerobic pathwayglycolysis. Further enzymatic studies of fora-miniferal ‘mitochondria’ wi l l establish their t rueidentity and functions. Furthermore, it has beenshown that mitochondria of certain microaero-philic protists grown under anoxia increase involume and number, suggesting that theseorganelles play a role in anaerobic energymetabolism (Bernard and Fenchel, 1996). Addi-tional biochemical studies are required beforewe can gain a full understanding of foraminiferalphysiology during exposure to microxia oranoxia. For further discussion on possiblephysiological adaptations used by Foraminiferainhabiting oxygen-depleted environments, seeBernhard (1996).

12.5 GENERALIZATIONS ON LOW-OXYGEN FORAMINIFERALASSEMBLAGES (LOFAS)

12.5.1 Systematic trends

While the Foraminifera of a number of oxygen-poor environments remain to be investigated, itis useful to make some generalizations about‘typical’ assemblages of such habitats. In general,calcareous perforate species dominate LOFAs,but agglutinated species can also occur in con-


siderable abundance. Very few miliolaceans havebeen found in natural dysoxic, microxic, oranoxic samples. A species of Pseudotriloculinawas observed in samples from Jel lyf ish Lake,Palau, where conditions were mildly dysoxic (i.e.

M. Langer and J.H. Lipps.unpublished data). Spiroloculina attenuata andEdentostomata cultrata were observed in con-siderable numbers in black, and therefore pre-sumably microxic or anoxic, sediments ofharbor inlets of the Madang Lagoon, PapuaNew Guinea (M. Langer and J.H. Lipps, unpub-lished data). Also, a variety of small miliolaceanswere common in black sediment samples frommangrove sites of Moorea ( M . Langer, pers.comm.). Specimens of Quinqueloculina stalkeri,which stained with Rose Bengal, were observedin dysoxic fjord sediments (E . Alve, unpublisheddata). As noted above, Q. seminulum can surviveanoxia, but appears to prefer aerated conditions(Moodley et al., 1998b). There are few docu-mented cases of tectinous Foraminifera inoxygen-depleted sediments. Nyholm andNyholm (1975) noted the occurrence of Nemo-gullmia longevariabilis and Gloiogullmia eurys-toma in ‘low oxygen concentrations’ of theGullmar fjord, but specific were notreported. Bernhard (1996) showed an unde-scribed allogromiid l iving among Beggiatoa fil-aments (see Bernhard, 1996, Fig. 1 ) . A newspecies of the closely related testate protistGromia is known to be very abundant at thesediment-water interface in the Arabian SeaOMZ (A.J. Gooday, pers. comm.). Pending adedicated study, it is highly l ike ly tha t tectinousForaminifera and gromids have been over-looked and that they occur in greater abun-dances in low-oxygen environments t h a npresently thought.

A survey of genus and species dis t r ibut ions,using the data presented in Table 12.2, and someaddit ional informat ion (referenced below), indi-cates some common features in LOFAs. A briefsummary is given here, in terms of major taxo-nomic groups (see chapter 2 for classification).Among the Order Rotaliida, the Nonionidaeand Chilostomellidae (Figs. 12.6A, B, C) are-typical ly common, being represented by sevenspecies of five genera (Nonion grateloupi, Nonio-nella stella, N. turgida, Nonionellina labradorica,Chilostomella ovoidea, C. oolina, Astrononionsp.). The occurrence of Nonionellina labradoricain a putatively dysoxic basin was noted by Ced-hagen ( 1 9 9 1 ) . Other genera from the OrderRotaliida are: Gavelinopsis (Figs. 12.6K, N),Rosalina, Cancris, Valvulineria, Epistominella,Oscangularia, Polymorphina, Planulina, Ammonia,and Elphidium . The last two genera are repre-sented in dysoxic or microxic habi ta ts by thewidely d is t r ibuted species Ammonia parkinso-niana (Figs. 12.6H, L), A. beccarii (Kitazato,1994), and Elphidium excavatum.

Members of the Order Buliminida are alsoconspicuous constituents of LOFAs (Figs.12.6D, E, F, G, J ) . The genera include Bolivina,Fursenkonia, Uvigerina, Bulimina, Globobuli-mina, Buliminella, Cassidulina, Cassidulinoides,Globocassidul ina, Stainforthia, Hopkinsina, Tri-farina, Brizalina, Suggrunda, and Loxostomum.

Unilocular agglutinated genera known to becommon in dysoxic environments includeAmmodiscus, Bathysiphon, Psammosphaera, Rhi-zammina, Saccammina, Saccorhiza, Technitella,and Tolypammina. In addition, Pelosina arbo-rescens and Astrorhiza limicola have beenobserved in putatively dysoxic environments(Cedhagen, 1993). Mul t i locular agglutinatedgenera of LOFAs include Reophax, Spiroplectam-



mina (Fig. 12.6I), Trochammina (Fig. 12.6M),Eggerella, Adercotryma, Bolivinopsis, Cribrosto-moides, Portatrochammina, Textularia, Recur-voides and Verneuilinulla. Also, Ammotium cassiswas observed to inhabit the redox boundary(Linke and Lutze, 1993).

It is crucial to realize that congeneric speciesalso occur in well-aerated environments; not allspecies of Bolivina, for example, are indicativeof oxygen depletion. Interestingly, none of theforaminiferal species observed to date in LOFAsis known to live exclusively in anoxic environ-ments. It is possible that certain species aremicroaerophiles but fine-scale spatial distribu-tional analyses and biochemical studies have notyet been done to confirm this possibility.

12.5.2 Test attributes

It has been suggested that small-sized Foramini-fera might survive episodes of oxygen depletionbetter than larger species, because of less oxygenrequirement (Phleger and Soutar, 1973). Indeed,a number of assemblages in microxic environ-ments are dominated by small foraminiferalspecies. For example, Nonionella stella domi-nates the Santa Barbara Basin (Bernhard et al.,1997), Stainforthia fusiformis is common inmany dysoxic areas (Alve, 1990, 1994, 1995b;Jorissen et al., 1992), Epistominella spp. arecommon constituents of LOFAs (Ingle et al.,1980; Jorissen et al., 1992) and Ammonia parkin-soniana dominates dysoxic inner-shelf areas ofthe Gulf of Mexico (Sen Gupta et al., 1996).However, a number of taxa comprising LOFAsare not particularly small (e.g. Globobulimina,Chilostomella, certain species of Bolivina).Because a standard-mesh screen hasnot been used to obtain the sample residue inall studies of LOFAs, it is still uncertain if smallspecies have a competitive advantage over largerspecies in oxygen-depleted settings. Relativelylarge-sized ( > 1 mm) foraminiferal species arenot commonly documented from dysoxic,microxic, or anoxic environments (exceptionsbeing Astrorhiza limicola and Pelosina arbo-rescens; Cedhagen, 1993). In a recent study,Moodley et al. (1997) observed that conclusions

regarding the survival of Foraminifera in anoxiawould be significantly different if one consideredthe fraction rather than thefraction that they used. Thus, they suggest that

should be used as the lower size limitwhen assessing foraminiferal response to oxygendepletion.

A number of authors (e.g. Harman, 1964;Phleger and Soutar, 1973; Bernhard, 1986) haveobserved that many calcareous species ofLOFAs have thin shells. Miliolaceans of oxygen-depleted environments in the Madang Lagoonalso have thin shells (M. Langer and J.H. Lipps,unpublished data). As noted by Sen Gupta andMachain-Castillo (1993), however, not allspecies from LOFAs are thin-shelled. Given thatthin-shelled Foraminifera are more likely to bedestroyed during standard laboratory prepara-tion of dry samples, it is possible that the impor-tance of some species has been underestimated.Thus, we suggest that samples to be analyzedfor LOFAs should be sieved and picked wet,without prior drying, to prevent excessivedamage to thin-shelled forms.

Another trend suggested for LOFA species isthat pore size and density are higher in testsfrom oxygen-depleted environments, comparedto those from well-oxygenated environments(Perez-Cruz and Machain-Castillo, 1990;Moodley and Hess, 1992). The proposed expla-nation for this observation is the widelyaccepted idea that foraminiferal pores are con-duits for oxygen supply to the intracellularmilieu (e.g. Berthold, 1976b; Leutenegger andHansen, 1979), and that larger, more numerouspores could presumably provide more oxygen.As noted above, however, mitochondrial activityin pseudopods may be more important thanthat associated with pore plugs. In addition, anumber of LOFA species (e.g. Chilostomellaovoidea, Nonionella stella) have very small pores(J.M. Bernhard, pers. obs.), while the occasion-ally abundant agglutinated species lack poresaltogether. Much more detailed study of porefunction and pseudopodial activity in Foramini-fera are needed to test the significance of poresin the context of microxia.

Lastly, it has been proposed that certain mor-


phologies occur more frequently in Foraminiferafrom oxygen-depleted environments (Bernhard,1986), but additional observations do not con-firm this trend. The planoconvex morphogroupis rare in most LOFAs observed to date, butsome other shapes that were considered indica-tive of aerated environments are well repre-sented in LOFAs (e.g. spherical: Chilostomella,Globobulimina, Psammosphaera).

12.5.3 Abundances

In a number of cases, the reported abundancesof Foraminifera in oxygen-depleted sedimentsare high. Hundreds of stained Foraminiferaper are documented in Rose Bengal treatedsamples from different sites (e.g. Phleger andSoutar, 1973; Douglas and Heitman, 1979; Ohgaand Kitazato, 1997; Jannink et al., 1998). Bern-hard and Reimers (1991) observed up to 2,176Rose Bengal stained Foraminifera per inthe microxic Santa Barbara Basin. One reasonfor such high densities in these habitats is adecrease in predation pressure, because of thesevere effect of oxygen depletion on metazoans(e.g. Josefson and Widbom, 1988). There are,however, other cases where oxygen-depletedenvironments have extremely low foraminiferaldensities. In fact, Bernhard and Reimers (1991)found only three Rose Bengal stained specimensper during another sampling in Santa Bar-bara Basin only eight months after observingthe extraordinarily high density mentionedabove. The reason for this decimation of theassemblage was inferred to be the possible con-tinuation of anoxia for weeks or months.Although it is likely that extended anoxia, incombination with prohibits the sustenanceof large foraminiferal populations, some pre-viously reported low densities are tied to sampleprocessing methods. We reiterate that a propercensus of Foraminifera surviving under dysoxia,microxia, or anoxia has to be preceded bysample washing on appropriately line-meshsieves (without sample desiccation) and has toinclude the enumeration of allogromiids.

Taphonomic changes in foraminiferal assem-blages are the focus of chapter 16, but it would

be worthwhile to make some general commentshere on the preservation of Foraminifera in sedi-ments with l i t t le or no oxygen. Because calcitedissolution is negligible in some OMZ sediments(Berelson et al., 1996). the calcareous compo-nents of the fossil foraminiferal assemblages andthe original living assemblages are unlikely tobe significantly different in these sediments. Onthe other hand, calcite dissolution rates are con-siderable in the mildly dysoxic or oxic sedi-mentary environments just above and below theOMZ (Berelson et al., 1996). Seasonally dysoxicto anoxic sediments are likely to have substan-tial rates of calcite dissolution when re-aerationoccurs (e.g. Green et al., 1993b). Thus, the calcar-eous component of these foraminiferal assem-blages might be altered greatly from originalassemblages.

12.5.4 Application to historical andpaleontological records

Understanding the ecology of Foraminifera inoxygen-depleted environments allows inter-pretations of past environmental conditionsfrom subsurface data. Questions regarding cli-mate change and anthropogenic influence onthe environment can be answered using suchapproaches. For example, using the successionof foraminiferal species observed with respect tobottom-water oxygen concentrations in theSanta Barbara Basin, subsurface data can beanalyzed to infer distinctions betweenwithin a range of dysoxia to microxia (Bernhardet al., 1997). Using this proxy model, data fromOcean Drilling Program station 893, which islocated in the Santa Barbara Basin, can be rein-terpreted, taking into account that Nonionellastella represents the most anoxia-tolerantspecies.

Analyses of foraminiferal data from subsur-face samples have already led to interpretationsof oxygen-related environmental changes. Forexample, faunal changes in a Norwegian fjordforaminiferal assemblage over the last ~ 1,000years indicate pollution effects superimposedover climatic changes (Alve, 1991b). More speci-fically, assemblages show a marked decrease in


species diversity and increase in abundance overtime, with Spiroplectammina biformis domina-ting just prior to the onset of anoxia about 1970.Another study shows that the foraminiferalrecord of the Po Delta reflects the environmen-tal history of that area for the last 160 years(Barmawidjaja et al., 1995). Strong eutrophica-tion started in 1930, as indicated by the appear-ance of ‘stress-tolerant’ species (Bolivinaseminuda, Hopkinsina pacifica, and Quinquelo-culina stalkeri), and seasonal anoxia began in1960, as indicated by the stratigraphic trends ofthe first two species.

The stratigraphic record of several inner-shelfforaminiferal species of the northwestern Gulfof Mexico demonstrates an overall increase ofoxygen stress in the past 100 years. The cluesinclude a decrease in the abundance of Quinque-loculina spp. (Raba l a i s et al., 1996), an increaseof Buliminella morgani (Blackwelder et al., 1996),and a positive trend in the relative dominanceof the more tolerant Ammonia parkinsonianaover the less tolerant Elphidium excavatum (SenGupta et al., 1996). In this area of strong sea-sonal oxygen depletion at present, the foramini-feral trends match the overall increasing trendof fertilizer use in the United States in the 20th

century, and the consequent higher nut r ientinput into the Gulf of Mexico by rivers, especi-ally the Mississippi.

12.6 CONCLUSIONS

In summary, certain benthic Foraminifera fromvarious water depths inhabi t oxygen-poor and

even anoxic environments. It is established thatat least some foraminiferal species surv iveanoxia and even sulfidic conditions for periodsup to a few weeks, but the tolerance of mostspecies to oxygen depletion is unknown.Furthermore, the physiological mechanismsenabl ing foraminiferal species to survive expo-sure to anoxia and/or sulfidic conditions are notyet identified. The available data suggest, how-ever, that al l Foraminifera are aerobic for atleast part of their life, and, in al l l ikel ihood,some species are facul ta t ive anaerobes. Obligateanaerobes have not been identified among fora-minifera l species. The information necessary tounderstand the diverse aspects of foraminifera ladaptation to oxygen-depleted environmentsmust come from experimental studies. Only withsuch biological information, it will be possibleto construct more accurate databases for use inother disciplines such as paleoecology andpaleoceanography.


We thank Elisabeth Alve, Mar t in Langer, andNancy Rabalais for thei r constructive reviews.Supported in part by NSF Grants OCE-9417097 and OCE-9711812 to JMB.

13Effects of marine pollution

on benthic ForaminiferaValentina Yanko, Anthony J. Arnold, and

William C. Parker

13.1 INTRODUCTION

13.1.1

Population growth and the resultant accelerationof domestic, municipal, industrial, agricultural,and recreational activity are the primary causesof anthropogenic pollution of the marine realm(Norse, 1993). Such pollution produces numerousobvious biological effects, including diseases inplant and animal species (e.g. Lamb et al., 1991),local or complete extinction of some species (Ver-meij, 1993), changes in community structure(Bresler and Fishelson, 1994; Suchanek, 1993),loss or modification of habitat (Nee and May,1992), and human health complications. Themarine environment, as the ultimate destinationof virtually all terrestrial runoff, is especiallyaffected by pollution, and the shallow nearshoremarine environment is particularly subject to fre-quent and extensive industrial and municipalpollution.

With increasing worldwide awareness of envi-ronmental problems, ways to detect and monitormarine pollution over time are the subject ofactive research. Numerous studies have demon-

strated the value of various animal species indetecting dangerous ecosystem contamination(James, and Evison, 1979; Organization for Eco-nomic Cooperation and Development, 1987).Species which occupy key positions in ecosystemsare especially useful biomonitors. Thus, the con-tinual global biogeochemical cycles of inorganicand organic compounds are regulated mainly bybiological activity of benthic communities, especi-ally bacteria and protozoa (Meyer-Reil, 1986;Santschi, 1988).

Marine protozoa, especially Foraminifera,play a significant role in global biogeochemicalcycles of inorganic and organic compounds,making them one of the most important animalgroups on earth (Anderson, 1988; Haynes, 1981;Lee and Anderson, 1991b). They are ubiquitousin marine environments. Their tremendous taxo-nomic diversity gives them the potential fordiverse biological responses to various pollu-tants, which in turn adds to their potential asindex species for monitoring pollution fromdiverse sources. Their tests are readily preserved,and can record evidence of environmentalstresses through time, thus providing historicalbaseline data even in the absence of background


218 Effects of marine pollution on benthic Foraminifera

studies. They are small and abundant comparedto other hard-shelled taxa (such as molluskswhich are often used for pollution monitoring),which makes them particularly easy to recoverin statistically significant numbers. They haveshort reproductive cycles (six months to oneyear; Boltovskoy, 1964), and rapid growth(Walton, 1964), making their community struc-ture particularly responsive to environmentalchange. They often show species-specificresponses to ecological conditions (Fursenko,1978). They have biological defense mechanisms(Yanko et al., 1994a) which protect them againstunfavorable environmental factors, thus provid-ing detectable biological evidence of the effectsof pollution. These characteristics make thempowerful tools for continuous in situ biologicalmonitoring of marine environments.

Barely forty years have passed since Zalesny(1959) discovered the effects of pollution on fora-miniferal distribution in Santa Monica Bay, Cali-fornia. Resig (1958) and Watkins (1961)subsequently suggested the use of benthic Fora-minifera as proxy indicators of marine pollution.Since that time, the foraminiferal literature hasseen an exponentially rising tide of papers on thebehavior of Foraminifera in polluted areas. Briefreviews have been presented by Boltovskoy andWright (1976), Alve (1991a,b), Culver and Buzas(1995), Yanko et al. (1994c) and Alve (1995a).

13.1.2 General locations of studies

The geographic locations of studies on marinepollution and Foraminifera are dictated by twomain factors: the distribution of human activitiesthat generate pollution, and the distribution offoraminiferologists with support and interest inthe study of pollution. As can be seen fromFig. 13.1, the geographic localities of studies inthis field are concentrated primarily in industri-alized countries. Studies of the effects of coastalpollution on the Foraminifera are concentratedmainly in the northern Pacific Ocean, with addi-tional studies in the south Pacific and IndianOceans, and the eastern Mediterranean Sea,northwestern Black Sea and Caspian Sea. Onlyone study has been undertaken on the Atlantic

coast of the Americas. Pollution in these areastends to be dominated by municipal sewage, butheavy metals, hydrocarbons, fertilizers, coal andfuel ash, and various other chemical pollutantsare also represented.

The study of pollution in bays and harbors(again, mainly by municipal sewage but also byaquaculture, paper mills, heavy metals, fertilizersand chemical pollution) have been undertakenin the North Pacific Ocean, North and SouthAtlantic Oceans, the Caribbean Sea, the Indiancoast, and the Gulf of Mexico. The influence ofpollution on Foraminifera in estuaries andlagoons has been studied mainly in the NorthAtlantic Ocean (Canadian). North Sea, SouthAtlantic Ocean, and along the Indian coast.Most of these studies focused on pollution fromaquaculture, paper mills, fertilizers, heavymetals, domestic sewage, and various chemicals.

13.1.3 Research strategies

The use of Foraminifera as indicators of marinepollution may involve quanti tat ive analysis of:( 1 ) foraminiferal diversity, ( 2 ) population den-sity/abundance, ( 3 ) assemblage structure, (4 )test morphology, including size and prolocularmorphology, ( 5 ) test ultrastructure, (6 ) test pyri-tization, ( 7 ) test chemistry, and ( 8 ) cytoplasmic/biological response.

These eight approaches can be complicatedby two general factors:

( 1 ) The first complication relates to covaria-tion within and among natural and anthropo-genic environmental factors. Most toxins enterthe marine system from terrestrial sources, pri-marily through coastal or estuarine ecosystemswhere steep natural environmental gradientswould exert control over foraminiferal distribu-tion patterns even in the absence of anthropo-genic effluents. Separating the effects of thesetwo coincident influences can be problematic(e.g. Collins et al., 1995). Moreover, environmen-tal factors (e.g. dissolved organic carbon, especi-ally humic acids, pH, temperature, salinity, ionicstrength, rates of biotic pollutant metabolism,and degradation) can modify the toxicity of pol-lutants (Forstner and Wittmann, 1979; James,

Introduction 219

1989; Paasivarta, 1991; Belfroid et al., 1994;Bresler and Yanko, 1995a,b).

Contaminated estuarine and coastal eco-systems, especially benthic ecosystems, may alsocontain a broad variety of pollutants. For exam-ple, the active components of oil pollutioninclude, as a minimum, numerous polycyclicaromatic hydrocarbons (PAHs), linear hydro-carbons, phenolic compounds, and heavymetals. Active components of fuel ash includevarious PAHs and heavy metals (Jenner andBowmer, 1990, 1992; Hamilton et al., 1993).These pollutants may interact to influence toxic-ity in complex and nonlinear ways (e.g. Green

et al., 1993a). Additionally, some natural con-stituents in sea water and sediments (e.g. acid-volatile sulfide, dissolved organic carbon, orother organic matter) may also interact withpollutants to modify their toxicity (Versteeg andShorter, 1992; Bresler and Yanko, 1995b). Sedi-ment-dwelling benthic organisms can also affectthe behavior of pollutants as well as the chemicalproperties of bottom sediments and water (e.g.Huttel, 1990). The biological effects of such com-plex mixtures can be more (or less) toxic thanwould be expected from simple additive effectsof a single pollutant or several pollutants(Malins and Ostrander, 1993; Newmand and


Jagoe, 1996; Howard, 1997). Moreover, effluentsources – particularly from chemical processingplants – rarely produce only a single toxin,which tends to result in covariation among toxinconcentrations; this in turn makes it difficult todetermine which toxins are producing theobserved effects on foraminiferal populations(e.g. Yanko et al., 1994c). The solution to thesecovariation problems takes three forms: ( i ) statis-tical analysis of faunal distribution patterns andtoxin/pollutant concentrations, ( i i ) laboratoryexperimentation, and ( i i i ) historical analysis.

The statistical analysis is easier where strongpoint sources of effluent interrupt natural envi-ronmental gradients, but can be complicated bynonlinear causal relationships. For example,intermediate levels of some urban and agricul-tural organic wastes can cause a ‘hypertrophic’zone (Alve, 1995a) of increased foraminiferalproductivity, while very high concentrations canresult in an ‘azoic’ (Schafer, 1970a) or ‘abiotic’zone (Alve, 1995a). As a general rule, the statisti-cal analysis of complex interactions betweennumerous species and a large number of envi-ronmental factors will require a multivariateapproach such as factor analysis (see chapter 5).A particular application of factor analysis, thetransfer function discussed in chapters 5 and 7,is a technique that would be particularly wellsuited to such situations; surprisingly, it hasseen little use in the field of foraminferalecotoxicology.

Laboratory experimentation may identifyinteractions between species and toxins by grow-ing them under controlled conditions; thisallows the researcher to experimentally resolvethe problems presented by covariation, if atten-tion is paid to the possibility of interactionamong toxins as well as with varying naturalconditions.

Historical analysis may be undertaken whenthere is sufficient stratigraphic accumulation ofa pre-industrial foraminiferal record; in that sit-uation it becomes possible to compare modernconditions with preceding unpolluted condit-ions even without a background study. Thisapproach is complicated by taphonomic effectsthat themselves may covary with (or indeed be

caused by) pollution induced changes in bottom-water chemistry.

( 2 ) A second broad problematic area relatesto the measurement of pollutants. Effluent con-centrations can be measured by extraction fromsediments, or by sampling at the sediment-waterinterface or in the overlying water column, butthe biological relevance of such measurementsis not well understood. Effluent concentrationscan also show considerable temporal va r ia t ion ,depending on the schedules of human activitythat produce and release effluents; thus, sam-pling dates and frequency may have a majoreffect on results. Addit ionally, it is not uncom-mon for effluent concentrations to be taken frompublished literature rather than measured at thetime of sampling for Foraminifera. Further,when toxin concentrations are measured in sedi-ments, the differing properties of sediments mustbe taken into account. For example, clean sandswill interact with toxins in different ways thanmuds and clays. Toxin concentrations can thuscovary with sediment type (e.g. Yanko et al.,1998), which, in turn may also influence fora-miniferal distributions.

13.2 FORAMINIFERAL RESPONSES TODIFFERING SOURCES OF POLLUTION

13.2.1

Given the recent emergence of foraminiferal eco-toxicology as a discipline, it is possible to providea relatively complete account of work on the sub-ject to date. The discussion below is divided intotwelve broad categories: municipal sewage, fertil-izers, aquacultures, pulp/paper mills, hydro-carbons, heavy metals, fuel ash, chemicalpollutants including pesticides, thermal, radioac-tive, dredging, and stream discharge. Referencesin these areas are grouped accordingly, and arevirtually complete through 1997.

13.2.2 Municipal sewage, fertilizers,and aquacultures

Marine ecosystems are sensitive to suspendedor dissolved organic matter from municipal

Foraminiferal responses to differing sources of pollution 221

sewage, agricultural fertilizers, and aquacultures.These pollutants can affect marine ecosystemschemically (by depletion of oxygen through oxi-dation and bacterial decay), biologically (by theintroduction of disease-bearing organisms suchas viruses, bacteria, and parasitic worms), andphysically (warming due to fermentation andreduced photic levels due to turbidity). Dis-solved organic material as well as other com-pounds of phosphorus, silicon, and nitrogen, areusually abundant in such areas, creating artifi-cially high nutrient levels. This organic materialis readily metabolized by marine organisms, andcan cause an increased foraminiferal abundance(e.g. Watkins, 1961; Bandy et al., 1964a; Seiglie,1971; Setty, 1976; Yanko et al., 1994c) and diver-sity (e.g. Resig, 1958, 1960; Yanko et al., 1994c;De Casamajor and Debenay, 1995). Bandy et al.(1964a) discussed a typical example of anoma-lously high living and dead foraminiferal abun-dances near a sewage outfall (see chapter 1 1 ) .Additionally, planktonic Foraminifera were fiftytimes as abundant in sediment near the outfallas elsewhere at similar depths. Bandy et al.(1964a) also noted that agglutinated specieswere most abundant among dead tests in theoutfall area, which is probably a taphonomiceffect related to dissolution in sulfide-richblack sediments. Other workers have noted thatin some areas polluted by domestic sewage,Foraminifera can have unusually large, wellornamented tests and relatively few deformedtests (e.g. Watkins, 1961; Yanko et al., 1994c).These observations suggest that artificially highlevels of nutrients may enhance the general via-bility of foraminiferal populations.

However, this is not always the case. Clark(1971) found a strong inverse relationshipbetween the density of Foraminifera in the sedi-ment and the production level of nearby aqua-culture operations. No live Foraminifera werefound by Schafer (1970a) in an ‘azoic zone’ (‘abi-otic zone’ of Alve, 1995a). Similar observationshave been made by others (Bandy et al., 1964b;Schafer and Sen Gupta, 1969; LeFurgey and StJean, 1975). The azoic zone is usually locatedin the immediate vicinity of the outfall wherebacterial breakdown of extreme concentrations

of organic material causes oxygen depletion,eutrophication, and high mortality of Foramini-fera (e.g. Bandy et al., 1965b; Schafer et al., 1991).

The existence and spatial distribution of theazoic zone is influenced by the sewage type (acti-vated or treated vs. non-activated or untreated),its geographic location (estuary, bay, or openshelf), hydrodynamic regime (current strength,direction), salinity, temperature, and effluentoutfall rates (Bates and Spencer, 1979; Alve,1995a). For example, in the eastern Mediterra-nean approximately three miles off Palmahim,Israel, a pipe fitted with a diffuser at its enddisposes of of domestic sewage ina water depth of 38 m. The activated sludge(after secondary treatment) is composed of 95%water and 5% solids. In addition to the stablebiomass, it may contain pathogenic bacteria,inorganic nutrients, and synthetic organic com-pounds. The lowest foraminiferal abundanceswere found at the mouth of the distal end of thepipeline, but there was no azoic zone. The high-est diversity and abundance were found at sta-tions located to the north and northwest of thesewage outfall, in an open coastal area downcur-rent of the outfall with salinities of 39‰ (Yankoet al., 1994c). By contrast, an azoic zone wasnoted near the Beledune Fertilizer factory inRestigouche estuary, Atlantic Canada, wheresalinity varied between 21 and 28‰, and cur-rents spread pollutants throughout the entireestuary (Schafer, 1970a). In this situation, thecombined effects of water temperature and salin-ity caused a density-stratified water column thatled to reduced overturn and local enhancementof oxygen deficiency (Schafer et al., 1995). Thismay be an example of the kind of nonlinearinteraction that complicates our understandingof the relationship between pollutants and natu-ral environmental factors.

Additional work on organic pollution bymunicipal sewage includes Alve, 1991a,b; Alveand Nagy, 1986; Bandy et al., 1965a,b; Bonettiet al., 1996; Cato et al., 1980; Collins et al., 1995;Debenay et al., 1997; Eichler et al., 1995; Govin-dan et al., 1983; Hirshfield, 1979; LeFurgey andSt. Jean, 1973, 1976; Latimer et al., 1997; Lidz,1965, 1966; Matoba, 1970; McCrone and


Schafer, 1966; Nyholm and Olsson, 1973;Nyholm et al., 1977; Resig, 1960; Schafer, 1970b,1971a, 1973, 1982; Seiglie, 1964, 1968, 1975;Setty, 1982; Setty et al., 1983; Setty and Nigam,1982, 1984; Scott et al., 1993, 1997; Yanko, 1993,1994, 1995, 1996a,b; Zalesny, 1959. Additionalwork on pollution by fertilizers includes Schafer,1970a, 1992; Seiglie, 1975; Setty, 1976; Yankoand Flexer, 1991. Work on pollution by aquacul-ture includes Grant et al., 1995; Schafer, 1970b,1973; Schafer et al., 1993; Scott et al., 1993, 1995,1997; and Preobrazhenskaya et al., 1991.

13.2.3 Pulp and paper mills

Effluent from pulp and paper mills consistsmainly of resistant organic material such as cel-lulose and lignin, major constituents of woodfibers. The most toxic compounds associatedwith this effluent are those used to break downwood fibers, rather than the wood fibers them-selves. Compounds of mercury are particularlytoxic; additionally, sulfides will, under well-oxygenated conditions (usually found downcur-rent from the point of discharge), oxidize tosulfates. The presence of sulfides (recognizableby the smell of rotten eggs) normally indicatesoxygen-poor conditions, and Foraminifera tendto have low abundances in these areas. Wheresulfate levels are high, the environment is usuallyoxygenated and nutrient-rich, and Foraminiferagrow quickly with rapid generational turnover,high productivity, and high abundances. Underthese conditions, adult specimens tend to besmaller, probably because of the rapid growthand high reproductive rates characteristic ofopportunistic ecological response. However,where sulfate concentrations reach their maxi-mum, foraminiferal abundance is often lower,probably due to coincident high sedimentationrates (Tapley, 1969). In areas surrounded bypulp mills, extreme concentrations of sulfidescan create an azoic, reducing environment wherecoal tar accumulates and Foraminifera areexcluded. This variable response to pulp andpaper mill effluent is another example of nonlin-ear faunal response to pollutant concentration.

Additional work on organic pollution by pulp

and paper mil ls includes Alve, 1994; Alve andNagy, 1986, 1988; Bartlett, 1966; Buckley et al.,1974; Latimer et al., 1997; Nagy and Alve, 1987;Schafer, 1970a,b, 1971a, 1973, 1982; Schafer andCole, 1974, 1995; and Schafer et al., 1975. 1991.

13.2.4 Hydrocarbons

In addition to 5–15% alkanes, typical petroleumproducts contain aromatic hydrocarbons,including monoaromatic hydrocarbons such asbenzene and toluene (the most frequently usedlight petroleum products). Some of these areproven to be carcinogenic (Kennish, 1992).Lethal doses of aromatic hydrocarbons formarine organisms are in the range of 0.00001 to0.01% for adults, and at the low end of thatrange for juveniles; doses as low as caninhibi t physiological activity, and cancause pathological reactions (Bokris , 1982;Rubinin, 1983). Depending on the fraction andmolecular weight, the hydrocarbons may forma film on the surface of the water, or heavier oilsuspensions and tar may sink to blanket theseafloor.

The small amount of work that has been doneon the effect of hydrocarbons on Foraminiferahas produced conflicting results. Lockin andMaddocks (1982) reported that petroleum oper-ation at Louisiana offshore petroleum platformshad only a minor negative effect on benthicForaminifera. Similar results were noted aroundEkofisk and Forties petroleum platforms in theNorth Sea (Murray, 1985). Dermitzakis andAlafousou (1987) suggested that meteoric rain-fall intensified the effect of terrestrial oil seepson the offshore marine environment nearZakynthos Island (Greece), possibly due tochanges in pH. Vénec-Peyré( 1981, 1984) studiedthe consequences of the Amoco Cadiz incident(March 16–17, 1978) on benthic Foraminiferain Cale du Dourduff, south of Roscoff, north-western France, and concluded that it did notaffect relative abundances or diversity; however,the accident did cause morphological abnormal-ities in foraminiferal tests. In contrast, a pro-nounced negative effect of oil on benthicForaminifera was noted by Mayer (1980) in the


northern Caspian Sea and by Yanko and Flexer(1991) in Odessa Bay where foraminiferal abun-dance and diversity decreased dramatically inoil-polluted areas. Similar negative effects werenoted by Witcomb (1977, 1978) in experimentalwork on calcareous (Ammonia beccarii) andagglutinated species (Allogromia laticollaris). Hefound that crude oil inhibited growth and repro-duction in both species, and that petroleumproducts produced narcosis and death of Fora-minifera, and speculated that petroleum pro-ducts might also cause a decrease in nutrientsupply (primarily diatoms). A full understandingof the biological causes of this result awaitsfurther research. V. Yanko (unpublished data)noted that respiratory functions of Foraminiferawere inhibited in Black Sea sediments with highconcentrations of petroleum products. Thebreakdown of petroleum was accompanied bythe release of ammonia, and methane, andby pH as low as 6. (Note that Bradshaw, 1961,found Ammonia tepida, a common indicatorspecies, to be very sensitive to pH.)

Work on hydrocarbons also includes papersby Akimoto et al., 1997; Bonetti et al., 1996;Buckley et al., 1974; Casey et al., 1980; Latimeret al., 1997; Schafer, 1992; Schafer et al., 1975;Vénec-Peyré, 1981, 1984; and Yanko andFlexer, 1992.

13.2.5 Heavy metals

The biological relevance of temporal variationof heavy metal toxin concentrations, and ofheavy metal concentrations in sediments versusin the water column is not fully understood and,although these factors are undoubtedly impor-tant, sampling programs have generally not beendesigned to assess their relative impact on theForaminifera. Thus, it is prudent to discuss thisresearch by separating three categories based onsampling methods. The first category includespapers concerning the distribution of living/fossil Foraminifera in sediment samples wherethe concentration of heavy metals was not mea-sured directly but taken from literature reports.The second group includes information aboutForaminifera based on correlation between their

distribution and heavy metal concentrationsmeasured in the same sediment samples. Thethird set of papers concerns ecotoxicologicallaboratory experiments on Foraminifera andheavy metals.

Studies based on literature reports of heavymetals. This body of research accounts for muchof the early pioneering work in the area of fora-miniferal ecotoxicology. Boltovskoy (1956)described a stunted fauna (small in size, lackingornamentation, with a tendency to asymmetryand monstrosity) in some lead-polluted areas ofthe northern Argentinean shelf. McCrone andSchafer (1966) noted that trace elements mayaffect morphology of benthic Foraminifera inthe Hudson estuary. Schafer (1973) found thatforaminiferal diversity decreased in an area adja-cent to a Pb–Zn smelter outfall. Setty andNigam (1984) found depauperate ( in both abun-dance and diversity) populations of benthicForaminifera, with high percentages of abnor-mal individuals, in the area adjacent to a t i ta-nium processing plant (near Trivandrum, westcoast of India) where a mixture of sulfuric acid,soluble iron, and other metallic salts were dis-charged. A similar pattern was discovered byNaidu et al. (1985) in the Visakhapatnamharbor area (east coast of India) where marinewaters were polluted by domestic sewage and avariety of heavy metals (e.g. Cu, Fe, Pb, Zn, Ni,Cr, As). These papers served to draw attentionto the fact that foraminiferal morphology – inaddition to abundance and diversity – is affectedby heavy metal pollution.

Studies based on heavy metal and foraminiferalanalyses of the same samples. This body ofresearch is generally more recent and plannedwith specific ecotoxicological analysis as the pri-mary goal. Ellison et al. (1986) investigated fora-miniferal response to trace metal (Zn, Cr, andV) contamination in the Patapsco River andBaltimore Harbor, Maryland. They discovereda very depauperate foraminiferal assemblage(fewer than 10 individuals per of sediment),composed of six species, and dominated byAmmobaculites crassus. Alve (1991a) analyzedfossil benthic Foraminifera in two short(170–190 cm length) sediment cores taken in


Sorfjo (Norway) at depths of 15–53 m, andfound a historical record of foraminiferal pop-ulations that were characterized by reducedabundances, dominance of agglutinated species,frequent occurrence of abnormal tests (w i thseven different modes of deformation), and highconcentrations of pyritized specimens in areaspolluted by heavy metals. A comprehensivestudy of Foraminifera as indicators of heavymetal pollution was undertaken by Sha r i f i(1991) and Sharifi et al. (1991) in SouthamptonWater, southern England. Of the 67 speciesfound in 250 grab samples, some were able totolerate pollution, and their relative abundanceincreased at the discharge point, whereas otherspecies developed test deformities. Banerji(1992) compared distr ibutions of heavy metals(Cd, Co, Cr, Cu, Fe, Mn. Ni, Pb, Zn) in sedi-ments and in foraminiferal tests. His resultsshow that species diversity corresponds posi-tively with Fe, Mn, and Zn concentrations inthe sediments and negatively wi th Co. Ni, andPb concentrations. He found that althoughAmmonia and Elphidium species occur together,the former prefers environments enriched wi thFe, Mn and Zn, and that an increase in concen-trations of Cd, Co, and Pb was accompanied bya decrease in the abundances of Ammonia andLagena spp. Such elements as Cu, Zn, and Crwere more readily absorbed into foraminiferaltests than Ni and Pb. At present, comparativeobservation suggests that it may be possible todevelop a scale of gradational species responseto heavy metal contamination by using theLagenida, various agglutinated species, speciesof Spiroloculina, Triloculina, Quinqueloculina,Ammonia, Cibicides, Poroeponides, and Elphi-dium, and possibly other indicator species. Thisbody of work supports the conclusion tha t Fora-minifera from areas with high concentrations ofheavy metals develop stunted tests wi th numer-ous deformities. Coccioni et al. ( 1 9 9 7 ) studiedliving and non-living benthic foraminiferal dis-tributions at fifteen sites throughout the GoroLagoon, I ta ly . The concentrations of eleven ele-ments ( V , Cr, Co, Ni, Cu, Zn, Ga, As, Pb, Th,and Cd) and total organic carbon (TOC) in thesediments were measured, and a total of 77

species from 43 genera were identified. Somesites displayed marked enr ichment in Cr, Ni ,Zn, Pb, and As, with Al-normalized valueshigher than the average values of nearby unpol-luted a l l u v i a l plain pelites. These sites alsoexhibited an increase in TOC, a general reduc-t ion in foraminiferal test size, and a decrease ofbenthic foraminiferal species richness, with aconcurrent increased abundance of tolerant andoppor tunis t ic species such as Cribroelphidiumtranslucens. A similar trend was found by Stub-bles ( 1 9 9 3 ) and Stubbles et al. (1996a,b) whostudied living and dead benthic Foraminifera inRestronguet Creek, Erme and Fowey estuaries,Cornwall. U K . Using semiquan t i t a t ive micro-probe analysis, they found higher concentrationsof several heavy metals, including Cd, in thecytoplasm of deformed Foraminifera than in thecytoplasm of non-deformed individuals . Theauthors suggest tha t if heavy metals are respon-sible for deformation of foramini fera l tests, thesemetals should be dissolved in the water ratherthan stored in the sediments. This has opened apotentially important avenue of research thatmay increase our unders tanding of the biologi-cal relevance of heavy metals tha t are seques-tered in sediments versus those dissolved in thewater column. However, due to the semiquan t i -tat ive na ture of the ins t rumenta t ion , f u r t h e ranalysis is required.

Research reported in Yanko (1994, 1995,1996a,b). Yanko et al. (1992, 1994a,b,c, 1995,1998), and Yanko, ed. (1995, 1996) was directedat the study of benthic Foraminifera as indica-tors of heavy metal pol lut ion along the easternMediterranean coast. Eighty-seven stat ions weresampled at one mile in te rva ls on a rectangulargrid covering the polluted Haifa Bay coastalarea, w i t h the relat ively clean coast of nearbyAtlit Bay as a control. The responses of benthicForaminifera to ten heavy metals (Cd. C r , Cu.Pb, Zn, As, Co, Ni, Ti, V) showed that reduceddiversity and abundance, s tun t ing of the tests,pyr i t iza t ion , and the presence of anomalousmorphologies are closely related to trace meta lcon tamina t ion ( Y a n k o et al., 1998). Accordingto the experimental results of Bresler and Yanko(1995b), there is significant biological influence


of heavy metals on foraminiferal cytoplasm.Mercury ions that penetrate the cytoplasm read-ily interact with the sulfhydril groups of proteinsby blocking them and inhibiting their function.Intracytoplasmic Cd especially interferes withsites that normally interact with calcium; partic-ularly, Cd can penetrate mitochondria andinterfere with respiratory functions. However,the Cd-sensitivity of different species, individ-uals, and even tissues, varies widely.

In general, it can be concluded that there is anegative correlation between concentrations ofheavy metals in sediments and foraminiferalabundance and diversity, and a positive correla-tion between the abundance of deformed testsand heavy metals.

Work on heavy metal pollution also includespublications by Alve and Olsgard, 1997; Banerji,1989; Bonetti et al., 1996; Kravchuk et al., 1997;Latimer et al., 1997; Schafer and Cole, 1995; VanGeen et al., 1993; Yanko and Flexer, 1991;Yanko and Kronfeld, 1992; and Yanko andKravchuk, 1996.

13.2.6 Fuel ash

The influence of coal and fuel ash pollution onbenthic Foraminifera has been studied along thecoast of Hadera, Israel, near a coal-fired powerstation (Yanko, 1993, 1994, 1995; Yanko et al.,1994c). Fuel ash particles, derived from the com-bustion of hydrocarbon fuels, dramaticallydecreases species richness and reproductive ratein Foraminifera, but does not seem to affect thetest size. Agglutinated species are less affectedby this kind of pollution than calcareous species.It has been speculated that coal and fuel ashparticles decrease the food supply (bacteria anddiatoms), and also affect foraminiferal metabo-lism directly (Yanko, 1994). Furthermore, sometrace metals and PAHs, contained in fuel andcoal ash in very low concentrations, interferewith defense systems and affect nutrient metabo-lism in Foraminifera (Yanko, 1994).

Additional papers on pollution by coal andfuel ash include work by Yanko, 1993, 1995,1996b; and Yanko et al., 1994b,c.

13.2.7 Miscellaneous chemical pollutantsincluding pesticides

There are a number of chemical pollutants,including pesticides, that affect foraminiferalabundance and diversity in much the same waysas heavy metals. Some also may be responsiblefor erosion and corrosion of foraminiferal tests(e.g. in Thana Creek, Bombay Area, India; Setty,1982). Following exposure to pesticides, fora-miniferal biotas can exhibit biochemical and his-tological alteration in some specimens. Suchexposure can also degrade immune systems andcause mutagenic changes (Komarovskiy et al.,1993).

Additional research in this area includes workby Alzugaray et al., 1979; Banerji, 1977; Bartlett,1972; Bergsten et al., 1992; Bhalla and Nigam,1986; Boltovskoy and Boltovskoy, 1968; Bonettiet al., 1997a,b; Bresler et al., 1996a,b; Buckleyet al., 1974; Geslin et al., 1997a,b, 1998; Jayarajuand Reddeppa Reddi, 1996b; Kameswara andSatyanarayana, 1979; Naidu et al., 1985; Olssonet al., 1973; Seiglie, 1973, 1975; Setty and Nigam,1980, 1984; Schafer, 1968, 1970a; Schafer et al.,1975; Varshney et al., 1988; Wright, 1968; andYanko and Kravchuk, 1992.

13.2.8 Thermal and radioactive waste

Research on thermal and radioactive waste isnot extensive. An increase in foraminiferal abun-dance and a decrease of diversity in the LongIsland Sound have been related to a power-plant-induced increase of water temperature(Hechtel et al., 1970). Attempts to relatecontamination from the Chernobyl reactor acci-dent to foraminiferal indices in Iskenderun Bay(Turkey) yielded inconclusive results (Yanko,ed., 1996).

Other works on industrial thermal pollutioninclude Hechtel et al., 1970, and Seiglie, 1975.Work on pollution by radioactive waste includesReish, 1983.

13.2.9 Dredging and stream discharge

Although the ecological effects of dredging andstream discharge have not been extensively


investigated, it is likely that they will affect tur-bidity (and therefore photic levels), and mobilizenutrients and pollutants that would otherwiseremain sequestered in sediments. It has beensuggested that these activities change the habitatand community structure of foraminiferalassemblages (Belanger, 1976), although themechanisms are not well understood.

Additional work on pollution and Foramini-fera that do not fall in the preceding categoriesinclude Alzugaray et al., 1979; Banerji, 1977;Bartlett, 1972; Bergsten et al., 1992; Boltovskoyand Boltovskoy, 1968; Boltovskoy et al., 1991;Boltovskoy and Wright, 1976; Bonetti et al.,1997a,b; Bresler et al., 1996a,b; Culver andBuzas, 1995; Geslin and Devenay, 1998; Geslinet al., 1997a,b; Olsson et al., 1973; Schafer, 1968,197la, 1973, 1975; Wright, 1968; Yanko, 1997;and Yanko and Kravchuk, 1992.

13.3 SPECIAL PROBLEMS INFORAMINIFERAL ECOTOXICOLOGY

13.3.1 Opportunistic (resistant) species

Species that are abundant in polluted areas arelikely to be tolerant (resistant) to the pollutantsfound there. However, even in these speciestoxins may produce detectable effects in theircytoplasm and test (Bresler and Yanko, 1995b;Yanko et al., 1998). Species that are sensitive topollution often express that sensitivity throughtheir absence.

Species identified as resistant in coastal zones,bays, harbors, estuaries and lagoons includeapproximately 11 agglutinated and 47 calcare-ous species (Table 13.1). The highest number ofagglutinated species (6 ) was found in estuarieswhile the highest number of calcareous species(33) was noted in coastal zones (Table 13.1).This may be an example of covariation betweena natural gradient (salinity) and foraminiferaldistribution patterns in an area affected bypollution.

Most eurytopic species are geographicallywidespread, living within a broad range of lati-tudes, and many can tolerate a wide range of

salinity and depth. For example, Ammonia tepidais distributed in the Black Sea from the Danubedelta (depth 3–5 m, salinity l–3‰) to the Bosph-orus area (102 m, 26‰) (Yanko and Troitskaja,1987; Yanko, 1990a,b). In the eastern Mediterra-nean, this species is widely distributed on theshelf at salinities in the range of 39‰ (Yankoet al., 1994a). There are also several taxa (e.g.buliminids, bolivinids, uvigerinids) which cantolerate the oxygen-deficient conditions thatoften accompany pollution. The dominance ofagglutinated Foraminifera in areas close todomestic outfalls (e.g. Bandy et al., 1964a) maybe more closely related to fresh-water input thanto discharge of pollutants or dissolution of cal-careous forms (Alve, 1995a).

Alve (1995a) concluded that , in general, thosespecies that are most abundant and geographi-cally widespread are most tolerant of environ-mental pollution. If Alve’s conclusion isgenerally valid, then these eurytopic species offerthe possibility of comparative studies in widelyseparated geographic areas – an aspect of fora-miniferal ecotoxicology that has not yet beenexplored.

13.3.2 Morphological deformity offoraminiferal tests

13.3.2.1 Distribution and correlation

Morphological deformities in fossil foraminiferaltests have been noted by researchers since thelast century (e.g. Carpenter, 1856; Rhumbler,1911). In recent years, reports of deformities inmodern Foraminifera have become increasinglycommon, and further documentation ofdeformed fossils has been made (e.g. Bogdanow-ich, 1952, 1960; Pflum and Frerichs, 1976). Mostof the available data on deformities were sum-marized by Boltovskoy and Wright (1976) ,Haynes (1981), and Boltovskoy et al. (1991),who noted that deformities may be attr ibutedto mechanical damage or environmental stress.but concluded that there is no consensus as tothe underlying causes of most deformities.Deformed tests of Foraminifera have beenreported from areas contaminated by heavy

Special problems in foraminiferal ecotoxicology 227

Effects of marine pollution on benthic Foraminifera228

metals, domestic sewage, and various chemicals,including liquid hydrocarbons. See Boltovskoyet al. ( 1 9 9 1 ) , Alve (1995a), Yanko et al. (1998)for detailed reviews of deformities and thei rprobable reasons. Examples of deformed testsfrom polluted environments can be seen inFig. 13.2.

Measures of deformity rely on the kind,degree, frequency, and species-specificity ofdeformity, but the frequency is the easiest mea-sure to quantify. The percentage of deformedForaminifera can increase dramatically in pol-luted areas (e.g. Lidz, 1965) where Foraminiferadisplay a wide variety of deformities, includingextreme compression, double apertures, twistedcoiling, aberrant chamber shape, and protuber-ances. Various other workers have cataloguedsimilar lists of deformities, but the genesis ofspecific deformities is often an unresolvedmatter. Some deformities undoubtedly resultfrom weak calcification or subsequent damageto areas that are weakly calcified. Other deform-ities (e.g. twisted keels, distortion of equatorialplane) may result from repair and overgrowthby subsequent whorls that cover such damage,resulting in distortion of the normal shell geome-try (Rö t tge r and Hallock, 1982; Wetmore, 1998).Thus, deformities that have quite differentappearances may have the same underlyingphysiological cause. Other deformities (e.g.mult iple apertures or t w i n n i n g ) are clearlydifferent in nature and may be a t t r ibutable todiffering responses to different toxins. Yankoet al. (1995), using sulfaflavine fluorescence andchlortetracycline fluorescence, were able to dis-tinguish morphological deformities caused bymechanical damage from those caused by patho-logical morphogenesis.

Compared with other pollutants, it appearsthat trace metals have the most conspicuousdeleterious effect upon Foraminifera. Like manyother k inds of pollutants, heavy metals oftencause reduced population density and diversity,and s tun t ing of tests, but increased frequency ofdeformed tests is a common aspect of v i r tua l lyall studies of heavy metal toxici ty. Yanko et al.(1998) report that at least 30% (65 species from20 calcareous families and one agglutinatedfamily) of all foraminiferal specimens l iving onthe northern Israeli cont inental shelf exhibi tedone of 11 dis t inct types of morphological defor-mity in their tests. High proportions of deformedtests in l iv ing Foraminifera (up to 10% of theentire assemblage) were also found at all sitesshowing high metal concentrations in the GoroLagoon, Italy. This contrasts with observationsof 1 % or fewer deformed specimens in natura lpopulations. The types of deformity include:abnormal coiling, aberrant chamber shape andsize, poor development of the last whorl, twistedchamber arrangement, supernumerary cham-bers, protuberances, mu l t ip l e apertures, irregu-lar keel, twinning, lateral asymmetry, and lackof ornamentat ion (Coccioni et al., 1997). A sim-ilar pattern was found in Sorfjord, WesternNorway (Alve, 1991a). and in SouthamptonWater, southern England (Sharifi et al., 1991).Deformed Foraminifera are represented amongthe porcelaneous, hyaline, and agglutinated sub-orders, among various modes of life (epifaunal ,infaunal , attached, epiphytic, symbiotic, mud-dwelling, sand-dwelling), and among differentmorphotypes (milioline, trochospiral, plani-spiral, f lattened, etc.) (Setty and Nigam, 1980;Banerj i , 1989; Vénec-Peyré, 1981). Thus, mor-phological deformities do not show di f ferent ia l



representation based on taxonomic affinity,feeding strategy, or test morphology.

There are indications, however, that sometypes of environmental stress may cause species-specific deformity. For example, Adelosina cliar-ensis exhibits increased frequency of deforma-tion in response to low salinity, whileAmphistegina lobifera appears to show anincreased incidence of deformity in response toincreased Cd concentrations, Cibicides advenumseems responsive to Cr, and Pseudotriloculinasubgranulata to Ti.

High frequencies of test deformity of livingbenthic Foraminifera are generally regarded tobe sensitive in situ indicators of marine pollutionby heavy metals. However, the biochemical andcrystallographic mechanisms of the develop-ment of such deformities remain to be studiedby culture experiments under controlled condi-tions and known heavy metal concentrations.

13.3.2.2 Wall texture of deformed tests

The study of the wall texture of abnormal tests,as a possible explanation of deformation relatedto biomineralization processes, is a new researchdomain. Geslin et al. (1998) have studied ultra-structural deformation in the genus Ammoniausing scanning electron micrographs. Abnor-malities consistently observed in the walls ofthese deformed tests involve either disorganiza-tion of the wall texture due to changes in crystal-lite arrangement and orientation (Debenayet al., 1996), or the presence of interlamellarcavities.

Normal tests of Ammonia tepida are made ofcrystallites arranged in elongate calcitic ele-ments normal to the wall. These elements areroughly continuous from one lamella to theother. In places, large cleaved crystals may form,with cleavages regularly oblique to the test sur-face. In deformed tests, calcitic elements may beoriented irregularly. This ‘crystalline disorgani-zation’ may result from introduction of alienelements in the crystalline framework duringcalcification; Sharifi et al. (1991) showed thatthe deformed tests contain a high proportion ofmetals such as Cu and Zn, and Yanko and

Kronfeld (1993) found that the deformed testsexhibit an increased Mg/Ca ratio. Interlamellarempty cavities were also observed in somedeformed specimens, even when crystallineorganization was normal. Such cavities werereported by Vénec-Peyré ( 1 9 8 1 ) . On a differentscale, these cavities may be compared with theinterlamellar cavities formed in the abnormalshells of some bivalves, part icularly of the oysterCrassostrea gigas by the hypersecretion of a jelly(Héral et al., 1981, in Alzieu, 1991). The organicprocess leading to these secretions may resultfrom a metabolic perturbation.

Early exploratory research has led to severalhypotheses regarding anthropogenic causes ofmorphological deformity in Foraminifera. Fourgeneral explanations are suggested. Test defor-mity may be caused by (1) direct physiologicalor metabolic interference of heavy metal pollu-tants; ( 2 ) pollution-induced changes in physicaland chemical environmental parameters indi-rectly resulting in pathological morphogenesis;( 3 ) poor nut r i t ional state in Foraminifera, per-haps due to the effect of habitat damage onother organisms in the food web; and (4 ) anthro-pogenic intensification of the normal (low-level)background causes of test deformity seen in nat-ural populations. It is clear that in the nearfuture, controlled laboratory experimentationwill play a central role in assessing these hypoth-eses before a full understanding of the relation-ship between foraminiferal test deformity andpollution is developed.

13.3.2.3 Morphometry and cytology

Morphometric and cytological studies of normaland abnormal Amphistegina lobifera tests fromthe north Israeli coast have been undertaken todistinguish and describe tests with varyingmorphologies and to understand the patho-genesis of abnormalities (Yanko, ed., 1995;Yanko et al., 1995). Although only a single indexof deformity was used, the deformed and unde-formed populations of specimens were statistic-ally distinct. A normal test of A. lobifera maybe described as a bi-convex lens. Several cate-gories of shell deformation were identified that


caused distortion of that natural shape. Thesedeformities include dorso-ventral asymmetry,loss of a segment of the peripheral margin, lat-eral asymmetry, irregular keel, abnormal aper-ture, and various other miscellaneousdeformations.

Of these types of deformation, only one (lossof a segment of the periphery) was associatedwith an increase of sulfaflavine fluorescence(which measures protein content in the shell),and only in the immediate area of the defect.These data indicate that segment loss may havea different pathogenesis than other abnormali-ties; namely, segment loss is likely to be a resultof shell damage and regeneration. During regen-eration, especially in the early stages of thisprocess, the protein/Ca ratio increases in thenew part of the shell, probably due to intensifi-cation of protein synthesis. This suggests thatthe other remaining test deformities may be theresult of pathological morphogenesis ratherthan of damage and subsequent repair. Whilethe cytoskeleton may play an important role innormal and pathological morphogenesis inmetazoan and protozoan cells (Albrecht-Buchler, 1977; Anderheide et al., 1977; Brandleand Gabbiani, 1983), the synthesis of shell-building proteins and their calcification is notapparently involved in pathological morpho-genesis of the shell.

It has been proposed that trace metal pollu-tants weaken the Foraminifera and enable bacte-ria to attack their cytoplasm (Alve, 199la). Thisis readily apparent from stunting of the test andmorphological deformities (Alve, 199la; Yankoet al., 1994c), and is probably related to the factthat heavy metals (e.g. Cd) dramatically increasemembrane permeability and mortality of Fora-minifera (Bresler and Yanko, 1995b).

The extent to which Foraminifera are pro-tected from pollutants is also a factor deservingsome attention, since it will increase our under-standing of the factors controlling distributionpatterns. Research in this area suggests severalpotential biological defense systems; theyinclude ( 1 ) a mucopolysaccharide coat thatforms an additional diffusion barrier and bindssome cationic xenobiotics; (2) a membrane car-

rier-mediated transport system for eliminationof anionic xenobiotics from the cytoplasm; ( 3 )active intralysosomal accumulation and isola-tion of some cationic xenobiotics; and (4) halo-peroxidases that transform xenobiotics to theirhaloderivatives (Bresler and Yanko, 1995a).

13.3.3 Pyritization

Pyritization has been found in living Foramini-fera as well as in fossils, though the percentageof pyritizated tests is significantly higher inempty tests than in tests with protoplasm. Twotaxa, Ammonia tepida and Porosononion mart-kobi ponticus , are regularly pyritizated in theBlack Sea (Yanko and Kravchuk, 1992). Thedegree of pyritization of living individual testsranged from 2% to 50%, and sometimes higher.The reasons for pyritization in marine sedimentsand foraminiferal tests are not completely clear.Some have suggested that it is connected tochemical processes that result in metabolizationof organic matter under anaerobic conditionsby sulfate-reducing bacteria, diffusion of sulfideinto sediments, or concentration and reactivityof the iron minerals. The process is clearly con-nected to the redox conditions and the concen-tration of High percentages of pyritizedforaminiferal tests have also been found inoxygen-deficient polluted areas. The frequencyof pyritized foraminiferal tests may thereforeshow promise as a parameter to indicate certaintypes of polluted environments.

13.3.4 Asexual reproduction

Foraminifera can reproduce by both sexual andasexual modes (see chapter 3). Fursenko (1978)has suggested that under stressful conditionsForaminifera preferentially revert to the asexualpart of their life cycle. The causes of stress caninclude, for example, hyposalinity (Yanko, 1989,1990a) and decreased nutrient levels (Fursenko,1978). Trace metal pollution may also stress theForaminifera by causing cellular injury and sub-sequently lead to a decrease in the efficiency ofmetabolism and protein synthesis (Ganote andVander Heide, 1987). Life-supporting metabolic


systems then function at a reduced level (Bas-erga, 1985) and the energetic cost of meiosismay be too great compared to mitosis (Effrussiand Farber, 1975). This hypothesis is supportedby the observation that megalospheric forms ofAmmonia tepida are strongly dominant wheretoxic trace metal pollution is prevalent (Yankoet al., 1994c). If a high percentage of megalo-spheric forms is characteristic of stressed envi-ronments, then this characteristic, inconjunction with other indices, may prove auseful tool in monitoring marine pollution.

13.3.5 Chemistry of deformed tests

Several studies have been undertaken to deter-mine whether elevated concentrations of heavymetals in sediments affect test chemistry andmorphology (Sharifi, 1991; Sharifi et al., 1991;Yanko and Kronfeld, 1993). The primary resultof these studies is that deformed Foraminiferashow elevated Mg/Ca ratios when compared tonon-deformed Foraminifera, especially inseverely polluted areas. Deformed tests of allstudied species are characterized by increasedMg concentration in their tests, so it is un l ike lythat this is a species-specific effect. Severalhypotheses might be suggested to explain thisobservation: One is that heavy metals directlyaffect the crystal structure of the calcite shell, orforaminiferal cytoskeleton, or both. Another isthat heavy-metal toxicity affects foraminiferalmetabolism in ways that influence Mg/Ca ratiosindirectly during calcification. A third is thatother pollution-associated environmental effectsmediate Mg/Ca ratios. The process of shell calci-fication includes the development of a glyco-protein organic matrix, anlagen, followed bymineralization by and bicarbonate in theglycoprotein centers ( Fursenko, 1978; Hemlebenet al., 1977). Other cations (e.g. Ba and Cd) canalso be included in the crystal structure of thetest (Fritz et al., 1992; Lea and Boyle, 1989). Itis l ikely that the biochemical transport systemsand sites for the binding cannot easilydistinguish between these ions. Trace metalsmay also affect the ratio of the major element(Ca and Mg) uptake (Yanko and Kronfeld.

1992, 1993). Any of these factors may affect thecrystal s t ruc ture and cause strong morphologi-cal deformities in foraminiferal tests. The cyto-skeleton, which defines the shape of theorganism, may also be affected by heavy metalsas has already been shown for the ciliates (Ande-rheide et al., 1977).

13.3.6 Cytology

Organisms have numerous adapt ive biologicaldefense mechanisms tha t protect them againstforeign chemicals in their environment (xenobio-tics). If these anti-xenobiotic defense mecha-nisms fail to protect the organisms, the resultswill be expressed as a pathological disruption ofbiological structures on various molecular toecosystemic levels of hierarchical organization.Even if the biological effect of a single toxiccompound is simple and well-understood in iso-lation, the behavior of the same pollutant incomplex natura l ecosystems inev i tab ly becomescomplicated and nonl inear . Unders tanding th i scomplexity wi l l require the application of cross-disciplinary new methodologies. An example isthe use of fluorescent microscopy and fluorom-etry to study the cytoplasmic response of Fora-minifera to pollut ion (Bresler and Yanko 1994b.1995a,b; Bresler et al., 1995, 1996a, 1997). If the‘health’ of foraminiferal species can be objec-t ively characterized by biological parameters(e.g. biophysical, morphophysiological, histo-pathological, cytogenetic, physiological, andbiochemical bioindicators) and measured usingvi ta l / supravi ta l microfluorometry, then changesin these parameters can be used as earlyresponse indicators of exposure to environmen-tal pollutants . Fluorescent probes allow the sci-entist to visualize and examine quantitativelythe s t ruc tura l and chemical organization of cellsand their organelles, including specific functions,such as genetic act ivi ty or carrier-mediatedtransport and metabolism, with great precisionand sensi t iv i ty . Such techniques would enableus to: ( 1 ) assess the interact ion of po l lu t an t andantixenobiotic biological defense mechanisms;( 2 ) determine the effect of pollutants on struc-tures and metabolic reactions; and ( 3 ) predict


the future behavior of a given species underpolluted conditions. Accordingly, the followingobjectives can be set: ( 1 ) to examine the healthof pollution-tolerant species (e.g. Ammoniatepida) under natural conditions; (2) to examinethe response of the these species to a spectrumof natural conditions (varying temperature,salinity, concentrations of natural xenobiotics,and dissolved organic matter); and (3) then toexamine how varying levels of a contaminantcan modify these natural responses to yieldpathological and pre-pathological changes thatcould serve as indicators of the degree of pollu-tion. As with other organisms, Foraminiferahave a number of defense mechanisms that canprotect them against xenobiotics (Bresler andYanko, 1995a; Yanko et al., 1994a). For example,carrier-mediated System of Active Transport ofOrganic Anionic xenobiotics (SATOA) elimi-nates many endo- and xenobiotics from thecytoplasm. Therefore, the quanti tat ive study ofSATOA in Foraminifera can be used for earlyecological monitoring and prediction of theimpact of anthropogenic pollution on eco-systems, as well as for retrospective analysis ofpaleoecosystems.

All these parameters can be examined by theuse of biophysical, cytophysiological, biochemical,and morphological vital microfluorometrical tech-niques, including fluorescent analysis at the micro-scopic level (Bresler and Nikifirov, 1981). Newdevices for vital biophysical studies, especially con-tact fluorescent microscopes and microspectro-fluorometers, can be used to examine, in situ,various biological parameters at the molecularand cellular levels and their distribution at higherlevels of biological organization. The main param-eters (and methods) of interest are the following:

(1) Monitoring of respiration and metabolicstate of mitochondria by measurement of inher-ent blue fluorescence of reduced nicotinamideadenine dinucleotide ( N A D ) and green fluores-cence of oxidized flavine adenine dinucleotide(FAD) in living cells and tissues.

(2) Detection of conformation changes oftryptophan-containing proteins by inherentultraviolet ( U V ) fluorescence. For example,inherent UV fluorescence of some tryptophan-

containing proteins has been used to study theirbinding with copper ions (Engel and Breawer,1987; Bresler and Yanko, 1995b).

(3) Determination of enzyme activity in situby using corresponding fluorogenic substratesand microfluorometry. The activity of someintracellular enzymes also may be sensitive indi-cators of cell viabi l i ty (Bresler and Yanko, 1994).

(4) The study of activity and kinetics of trans-port systems used for the elimination of xenobio-tics, such as the system of active transport oforganic anions (SATOA) and multixenobioticresistance ( M X R ) transporter, by using markerfluorescent substrates of SATOA or MXR,specific inhibitors, and microfluorometry(Bresler et al., 1975, 1979. 1983, 1985, 1990;Bresler and Fishelson, 1994; Bresler and Yanko,1995a,b; Fishelson et al., 1996).

( 5 ) The examination of cell cycle phases,functional state of nuclear chromatin, DNA con-centration and aneuploidy ( D N A variabi l i ty inindividual nuclei), and DNA damage by usingversatile probe acridine orange (AO) and two-wavelength microfluorometry (Darzynkiewicz1990; Fishelson et al., 1996).

( 6 ) Cell chemistry, i.e. content of DNA, RNA,proteins, mucopolysaccharides and carbohy-drates, lipids, thiol groups, and intra- and extra-cellular ions (especially calcium), can be studiedwith special fluorescent probes andmicrofluorometry.

( 7 ) Permeability of plasma membranes, epi-thelial layers, or histohematic barriers can beexamined by using various fluorescent markers,especially fluorescein, and microfluorometry(Bresler and Fishelson, 1994; Bresler andYanko 1995).

(8) Cell viability can be studied by using vitalstaining with AO or neutral red, fluorescentmicroscopy of their intralysomal, and micro-fluorometry (Bresler and Fishelson 1994; Breslerand Yanko, 1995b). This approach is often usedin ecotoxicology to dist inguish l iving and deadcells and tissues.

(9 ) Cell and tissue morphology and patho-morphology can be examined by using contactfluorescent microscopy and epi-microscopy todetect early signs of pathology, to identify the


type of pathology, and to identify specific targetorganelles, cells, and organs. In the field of ecol-ogy and ecotoxicology of aquatic animals,especially invertebrates, environmental pathol-ogy is clearly underdeveloped as compared withmammalian ecology and ecotoxicology (Hintonet al., 1992; Cotran et al., 1989; Wester and Vos,1994). The field of foraminiferal pathology lagseven farther behind. Contact epi-microscopy inincident light and contact fluorescent micro-scopy are promising tools for aqueous ecotoxi-cology (Bresler and Fishelson, 1994; Bresler andYanko, 1994a,b, 1995a,b; Fishelson et al., 1996).

(10) Cytological indications of genotoxicityand clastogenicity, especially micronucleus testsemploying contact fluorescent microscopy, con-tact epi-microscopy, or conventional micro-scopy are the most universally useful andsensitive methods for detecting environmentalgenotoxicity produced by chemical or physicalfactors (Fishelson et al., 1996).

13.4 CONCLUSIONS

An environmental event could be characteristi-cally transient, resulting in varying rates of fora-miniferal recovery that may range from rapidspecies-specific ecological opportunism to moredelayed recovery and even to permanent localextinction. Even when an environmental insultis continuous rather than transient, some speciesmay respond by showing a positive preferencefor the new conditions, others by showing vary-ing levels of tolerance or intolerance. Thesekinds of behavior are reflected in shifting pat-terns of foraminiferal dominance and abundancethat are not well understood – partly becausethe time scale of environmental insult is rarelywell documented, partly because foraminiferalresponses are often complex and nonlinear, andpartly because biotic patterns often covary withnatural and anthropogenic environmentalgradients that can be difficult to distinguish.Although these questions are posed here in thespecific context of foraminiferal response to pol-lutants, it is unavoidable that they will touch onmore fundamental issues relating to the nature

of opportunism, and the meaning of ecologicalspecialization or generalization in other taxa.This is one area in which basic scientific researchon Foraminifera is inseparable from the other-wise pragmatic issues of detection, monitoring,and remediation of pollution.

At the organismal level of analysis, we findthat ecophenotypic responses among Foramini-fera can range from test deformity to subtlechanges in size and age distribution. Some ofthese responses are almost certainly pathologi-cal and species-specific, and some may be toxinspecific as well. Some biological causes of mor-phological test deformity may be fundamentallygenetic, or due to disruption of normal meta-bolic processes such as calcification, leading toweak, damage-prone test walls. Controlled labo-ratory experimentation and detailed cytologicalstudies will certainly play a major role in resolv-ing some of these questions.

Coal miners once used canaries to warn themof toxic atmospheric conditions; they did so with-out any understanding of the cellular biology ofcanaries. One might suppose that, as a purelypractical expedient, we could take similar advan-tage of the Foraminifera as environmental indica-tors without understanding the underlyingreasons for their ecological responses, but this isnot the case. Foraminifera not only behavedifferently in different circumstances, but indica-tor species are rarely so obliging as to conve-niently and consistently manifest themselveswherever they are needed to assist in our effortsat monitoring and detection of pollution. Thus,not only are species unique, but virtually everylocality is unique as well, and generalizationbecomes difficult under the best of circumstances.For this reason, we are unlikely to identify speciesthat have the simple, straightforward utility of thecanary; instead, we will have to rely on a deeperunderstanding of biological and ecological pro-cesses if the Foraminifera are to achieve their fullpotential as environmental indicators.


We thank the staff of the Laboratoire de Géolo-gie and Laboratoire d’Etude des Bio-Indicat-

Acknowledgments 235

teurs Marins, University of Angers, France, forthe use of their facilities during the preparationof the manuscript. We also thank SophieSanchez and Emmanuelle Geslin for preparingfigures, and Emmanuelle Geslin for providingpictures of deformed Foraminifera. We sincerelythank Dr. J.-P. Debenay, University of Angers,France, and Dr. David Scott, Dalhousie Univer-sity, Canada, for their constructive suggestionsand comments during preparation of the manu-

script. We thank especially Dr. V. Bresler, TelAviv University, Israel, for his many helpful con-tributions and insights. Dr. Pamela Hallock ofthe University of South Florida and an anony-mous reviewer contributed very useful reviews.The University of Angers was very generous inproviding V. Yanko with a one-month visitingprofessorship during the completion of themanuscript.


PART III:GEOCHEMISTRY

OF SHELLS


14Stable oxygen and carbon

isotopes in foraminiferalcarbonate shells

Eelco J. Rohling and Steve Cooke

14.1 INTRODUCTION

Analyses of stable oxygen and carbon isotopesfrom foraminiferal shells have played a pivotalrole in paleoceanography since the pioneeringefforts of Emiliani (1955) who, building on workof Urey (1947), McCrea (1950) and Epstein et al.(1953), interpreted the isotopic record fromdeep-sea cores as a proxy for a series of Pleisto-cene climate/temperature cycles. Cores fromvarious locations in the Atlantic, Pacific andIndian Oceans provided isotopic records show-ing similar trends. Shackleton and Opdyke(1973) correlated the isotope stratigraphy withmagnetic stratigraphy, dating 22 recognizableisotopic stages. Analyzing not only records forplanktonic Foraminifera, but also for deep-seabenthic Foraminifera – which avoid the ‘noise’imposed by short-term temperature and salinityfluctuations – Shackleton and Opdyke (1973)demonstrated that the signal predomi-nantly reflects fluctuations in global ice volume,while temperature plays a secondary role. Thisdiscovery started widespread use ofrecords in global stratigraphic correlations (e.g.

Imbrie et al., 1984b, 1992). Turning attention todowncore variations, Shackleton (1977a)showed their potential significance in studyingwater mass movement and paleoproductivity,and postulated a connection between climati-cally induced changes in the terrestrial biospherewith observed carbonate dissolution cycles andthe flux of dissolved in the oceans.

Detailed age control for records aroundthe world has been established by ‘stacking’ agreat number of records in various ways to forma global curve for comparison with models ofastronomically forced ice volume fluctuations(Imbrie et al., 1984b; Pisias et al., 1984; Prellet al., 1986; Martinson et al., 1987; Imbrie et al.,1992). Consequently, oxygen isotope stratigra-phy has become not only a global correlationtool, but also an established dating tool(Fig. 14.1). In addition, the primary ice-volumecontrol on (benthic) oxygen isotope records hasled to their use in the approximation of past sealevel variations after calibration with studies ofother sea level indicators (e.g. Chappell andShackleton, 1986; Shackleton, 1987; Bard et al.,1996; Linsley et al., 1996; Rohling et al., 1998).


240 Stable oxygen and carbon isotopes in foraminiferal carbonate shells

Introduction 241

There are three stable isotopes of oxygen:and with relative natura l abundances

of 99.76%, 0.04%, and 0.20%, respectively.Research on oxygen isotopic ratios normallyconcerns ratios. There are two stableisotopes of carbon: (98.89%) and( 1 . 1 1 % ) . Basically, molecules consisting of lightisotopes react more easily than those consistingof heavy isotopes. Part i t ioning of isotopesbetween substances is called fractionation. Ifand are the heavy/ l ight ratios for any twoisotopes (e.g. ) in exchanging chemicalcompounds A and B, then the fractionationfactor is defined as Fractionationmainly results from isotopic exchange reactionsand kinetic effects. The former are also knownas ‘equilibrium isotope fractionation’ processesand are essentially temperature dependent.Kinetic effects cause deviations from equilibriumdue to different rates of reaction for the variousisotopic species. Important kinetic effects areassociated with diffusion. Detailed accounts onthe physico-chemical behavior of isotopes, andon equilibrium and kinetic fractionation may beobtained from Craig et al. (1963), Craig andGordon (1965), Ehhal t and Knott (1965) , Merli-vat (1978) , Merlivat and Jouzel (1979 ) , Garlick(1974) , Stewart (1975) , Gonf ian t in i (1986),Knox et al. (1992), Hoefs (1997) , and refer-ences therein.

While absolute abundances of minor isotopes(such as ) cannot be determinedaccurately, it is still possible to get quant i ta t iveestimates by comparing results for a knownexternal standard ( s t d ) with those for theunknown sample (sam). These differences inisotope ratios are defined as:

A positive value indi-cates enrichment in the heavy isotope, relativeto the standard, and conversely, depletion isshown by a negative value.

Stable isotopes of oxygen and carbon in car-bonates are analyzed by mass spectrometricdetermination of the mass ratios of carbondioxide obtained from the sample byreaction of carbonate with phosphoric acid:

(seeMcCrea, 1950), with reference to a standard

of k n o w n isotopic composition. The standardfor both oxygen and carbon in carbonates isreferred to as PDB (Pee Dee Belemnite), having

and by definition ( Epsteinet al., 1953). The PDB standard (no longer avail-able) is a guard from Belemnitella americana, aCretaceous belemnite from the Pee Dee Forma-tion in North Carolina, U.S.A.

Various internat ional standards have beenrun against PDB for comparative purposes. Twoare commonly used and distr ibuted by theNational Inst i tute of Standards and Technology( N I S T ) in Gaithersberg, Maryland, U.S.A., andthe International Atomic Energy Agency( I A E A ) in Vienna, Austria. They are:(a ) NBS–18 (carbonati te) , for the analysis ofcarbonates wi th and in per mil (‰)difference from Vienna Pee Dee Belemnite(VPDB) or Vienna Standard Mean OceanWater ( V S M O W ) and ( b ) NBS-19 (limestone),for and analysis of carbonates, usedto define the VPDB scale (Coplen, 1988; 1994).The isotopic compositions of these referencematerials, as given by NIST ( 1 9 9 2 ) are listed inTable 14.1. To convert VPDB to VSMOW, use

(NIST,1992; also Coplen et al., 1983).

Some fur ther corrections are needed. The Iso-tope Ratio Mass Spectrometer ( I R M S ) mea-sures two ratios: mass and mass

The final results required areand relative to VPDB, and a correctionfor the contr ibut ion is applied. A fur thercomplication results from fractionation between

in carbonate and in the produced byreaction with phosphoric acid, which mainlydepends on the temperature at which that reac-tion takes place. The analyzed is correctedfor this effect. The correction is determined byexperiment to suit the technique used to gener-


ate There is no similar fractionation effecton carbon (Swart et al., 1991).

Major contributions of and topaleoceanography in the applied sense are cap-tured in Emiliani (1955), Shackleton andOpdyke (1973), Shackleton and Kennett (1975),Savin et al. (1975), Shackleton (1977a,b), Keig-win (1979), Savin et al. (1981) , Duplessy et al.(1984), Imbrie et al. (1984b), Vergnaud-Grazzini(1985), Chappell and Shackleton (1986), Ken-nett (1986), Berger and Labeyrie (1987), Shack-leton (1987), Woodruff and Savin (1989), Savinand Woodruff (1990), Imbrie et al. (1992),Zachos et al. (1994), and Sarnthein et al. (1995),and are reviewed in, for example, Haq (1984),Kennett (1982), Crowley and North (1991),Frakes et al. (1992), and Broecker (1995). We,instead, review the fundamental controls on

(section 14.2) and (section 14.3) inforaminiferal carbonate. Several have onlyrecently been discovered, and we aim to offeran overview, with pointers to the relevant spe-cialist literature. Since isotope ratios in carbon-ates to a great extent reflect those in the ambientwater, the following sections first evaluate theprocesses governing and in seawater,and then those causing fractionation during car-bonate formation. To facilitate evaluation of thepaleoceanographic value of and sec-tion 14.4 summarizes the various controls andhighlights analytical strategies to minimizecomplications.

14.2 OXYGEN ISOTOPES

14.2.1 Oxygen isotope ratios in seawater

Seawater is intimately linked with thehydrological cycle, consisting of evaporation,atmospheric vapor transport, and return offreshwater to the ocean via precipitation andrunoff, or iceberg melting. Furthermore, long-term freshwater storage in aquifers and (especi-ally) ice sheets significantly affects seawater(Fig. 14.2). Seasonal sea ice formation and melt-ing impose strong local variability. Finally, thespatial distribution in the oceans depends

on advection and mixing of water masses fromdifferent source regions.

14.2.1.1 Evaporation

Isotopic exchange at the sea-air interface isgiven by

Because of higher vapor pres-sures, the lighter molecular species are preferen-t ial ly enriched in the vapor phase. Thefractionation factor for equilibrium exchangeis The mostcommonly used relationship betweenand temperature is

with T inKelvin, illustrating a decrease in fractionationwith increasing temperature (Majoube, 1971).The difference between seawater and vaporthen equals which at 20°C amountsto 9.8‰. The equil ibr ium enrichment factorequals and is reported as a ‰ value.

In addition, there is kinetic fractionationduring molecular diffusion within the boundarylayer between the water-air interface and theful ly turbulent region where no fur ther fraction-ation occurs (e.g. Craig and Gordon, 1965;Ehhalt and Knott , 1965; Stewart, 1975; Merlivatand Jouzel, 1979; Gonfiantini, 1986). The mag-nitude of kinetic enrichment depends on relativeair humidity in the turbulent region, changingby about 0.7‰ for every 5% change in relativehumidity (Gonfiantini , 1986), and to a lesserextent on roughness of the water-atmosphereinterface, with a threshold around near-surfacemean wind speeds of (Merlivat andJouzel, 1979). In exceptional settings, this rough-ness threshold may have been persistentlyexceeded in the geological past (e.g. Rohling,1994). Finally, the of newly evaporatedwater also depends on that of the surface water,and of the vapor already present in the turbulentregion of the atmosphere (full set of equationsin Gonfiantini, 1986).

Preferential uptake of lighter isotopes duringevaporation increases values in the remain-ing surface waters. Because factors such as rela-tive humidi ty are difficult to assess for thegeological past, geological studies best consider

Oxygen isotopes 243

equilibrium fractionation and a constant valuefor kinetic fractionation, using likely ranges ofchange in kinetic fractionation to determineconfidence intervals.

14.2.1.2 Precipitation and atmospheric vaportransport

Fractionation during condensation is basicallythe same as during evaporation, but acts inopposite sense. Normally, kinetic effects are neg-ligible, so that droplets are near equilibriumwith atmospheric vapor (Ehhalt and Knott,1965; Stewart, 1975). The isotopic compositionsof original vapor, precipitation, and remainingatmospheric vapor are related through basicRayleigh distillation (Dansgaard, 1964; Garlick,1974). Consequently, the first precipitation hasa similar to the original seawater, whilelonger pathways from the source region, withprogressively more rain out, cause increasingdepletion in vapor and associated new precipita-tion (Fig. 14.3). Successive condensations duringtransport towards colder regions cause a quasi-linear relationship of betweenof precipitation and temperature (valid between

–40 and +15°C). Consequently, high latitudeprecipitation is significantly more depleted thanthat in the tropics (reaching –60‰ or less inAntarctica; Lorius, 1983; Rozanski et al., 1993).Above +15°C, the so-called ‘amount effect’dominates, with 1.5‰ depletion in the ofprecipitation for every 100 mm increase in rain-fall. For further reading, see Dansgaard (1964),Craig and Gordon (1965), Jouzel et al. (1975),Stewart (1975), Rozanski et al. (1982, 1993),Merlivat and Jouzel (1979), Joussaume andJouzel (1993), Hoefs (1997), and Hoffmann andHeimann (1997).

Changes in of precipitation affect oce-anic surface waters through addition of the freshwater, either directly, or via run-off. Whereasarid areas show the evaporative surface water

enrichment, regions in reasonable proximityto a river mouth are affected by the volumetri-cally weighted average isotopic composition ofprecipitation over the catchment basin. A high-latitude river imports freshwater with generallylower values than a low- latitude river, e.g.Arctic McKenzie (pre-Aswandam) Nile and Parana (Argen-


tina) (overview in Rohling andBigg, 1998).

Long-term storage of precipitation causes twomain delayed responses. Icebergs calving fromcontinental icesheets import continental fresh-water with fossil isotopic signatures. Ice coresin the Greenland and Antarctic ice sheetsinclude ice older than 100,000 years (Lor iuset al., 1985; Taylor et al., 1993; Grootes et al.,1993; Jouzel et al., 1993) to even 400,000 years(Petit et al., 1997), so that the isotopic signaturesof bergs from those icesheets should not be con-sidered as a result of the modern freshwatercycle. Similarly, but less importantly, aquifersmay accumulate waters as old as 35,000 years(e.g. Rozanski, 1985), and at later stages contrib-ute to discharge.

14.2.1.3 Glacial ice-volume

Apart from delayed return of fossil signals tothe ocean, long-term storage in glacial icesheetsand, to a lesser extent, in major aquifers, alsoaffect the global budget. Because storagetime-scales in the order of years exceedthose of ocean ventilation (in the order of

years), the storage effects influencevalues equally in surface and deep waters.

The most important fluctuations are relatedto the volume of glacial ice sheets. These arebuilt up by high latitude precipitation at verylow temperatures towards the end of the Ray-leigh distillation (Fig. 14.2), and so recordextremely low values (Fig. 14.3). Preferen-tial sequestration of in ice sheets leaves the

Oxygen isotopes 245

oceans enriched in At the same time, buildup of ice volume lowers global sea level.Research on changes in fossil carbonate,with accurate constraint of sea level variationsfrom fossil coral reef studies, illustrates that therelationship between sea level lowering andmean oceanic increase approximates

(Aharon, 1983; Labeyrieet al., 1987; Shackleton, 1987; Fairbanks, 1989).Although this relationship provides a soundworking model for well matured ice sheets, theprocesses behind it may invoke a more nonlin-ear relationship for growing or recently maturedicesheets (see Mix and Ruddiman, 1984).

14.2.1.4 Sea ice freezing and melting

Newly formed sea ice is 2.57 ± 0.10‰ enrichedrelative to seawater (Macdonald et al.,1995). This difference imposes a distinct seasonalfluctuation associated with ice formation andmelting (cf. Strain and Tan, 1993). These seasonalinfluences do not necessarily cancel out in thelong term, since increases in surface-water salinitydue to sea ice formation may lead to convectionand transport of existing surface waters into theocean interior; the replacement waters likely werenot affected as much by freezing processes (Roh-ling and Bigg, 1998). Large errors may arise ininterpretations of oxygen isotopic change near(present or past) sea-ice margins when freezing/melting effects are overlooked.

14.2.1.5 Advection

Advection and mixing of water masses fromdifferent source areas are very important for thebasic composition at any site. Each sourcearea concerns a basin or region, which may bevery remote from the study site, where surfacewaters are imprinted with a certain com-position by the freshwater cycle, freezing/meltingof sea ice, etc. This pre-set composition behavesas a virtually conservative property for the newlyformed watermass, provided this watermass doesnot come into contact with further sinks orsources. In practice, therefore, is a usefulconservative tracer for watermass transport andmixing in the subsurface ocean (e.g. Weiss et al.,

1979; Fairbanks, 1982; Paren and Potter, 1984;Kipphut, 1990; Frew et al., 1995).

The of a mixing endmember is a volumet-rically weighted average of the compositionsof its components. Hence, any change in the rela-tive proportions or isotopic compositions of themixing components affects the basic endmember

Changes in at any site must, therefore,be viewed within the broader context of watermass formation and mixing on basin-wide scales,instead of being ascribed purely to local changesin surface forcing (e.g. freshwater budget). Empha-sizing the importance of advection, Rohling andBigg (1998) and Schmidt (1998) called for cautionwhen interpreting past variations; after thenecessary correction for ice volume effect, surfaceforcing processes of both local (direct) and remote(through advection mixing) origin need to beconsidered. This contrasts with the classical pale-oceanographic interpretation that deals with localprocesses only.

14.2.2 Oxygen isotope ratios in foraminiferalcarbonate

Equil ibr ium fractionations between water andthe various carbonate species

determine an important temper-ature influence on the of foraminiferal car-bonate. In addition, several processes causedeviations from equil ibr ium, both in planktonicForaminifera (e.g. Shackleton et al., 1973; Fair-banks and Wiebe, 1980; Duplessy et al., 1981;Bouvier-Soumagnac and Duplessy, 1985) and inbenthic Foraminifera (e.g. Duplessy et al., 1970;Woodruff et al., 1980; Vincent et al., 1981; Weferand Berger, 1991).

14.2.2.1 Equilibrium fractionation.

The overall reaction for precipitation of carbon-ate is:Between 0 and 500°C, the equi l ibr ium fraction-ation factor between calcite and waterchanges according to

wi th T in Kelvin (O’Neilet al., 1969). Recently, Kim and O’Neil (1997)showed a more detailed relationship where


the change with temperature is morepronounced at low temperatures (up to

) than at higher temperatures(around ). The temperature depen-dence of fractionation fueled initiatives todevelop ‘isotopic paleothermometers’ or ‘paleo-temperature equations’ (e.g. Urey, 1947;McCrea, 1950; Epstein et al., 1953; O’Neil et al.,1969; Shackleton, 1974; Erez and Luz, 1983). Acomprehensive summary, including new cal-ibrations using data from cultured Foraminifera,was presented by Bemis et al. (1998).

Since temperature decreases with increasingdepth in the surface ocean, vertical migrationsinfluence equilibrium fractionation. Manyplanktonic foraminiferal species show aincrease with growth that suggests calcificationin progressively deeper, colder, waters (amongothers, Emiliani, 1954; Berger, 1971; Emiliani,1971; Berger et al., 1978; Fairbanks et al., 1982;Bouvier-Soumagnac and Duplessy, 1985; Kroonand Darling, 1995). There are, however, alsosuggestions that a species l ike Globigerina bul-loides calcifies at depth as a juvenile and latermigrates to shallower waters (Spero and Lea,1996; Bemis et al., 1998).

14.2.2.2 Deviations from equilibrium inforaminiferal calcite

14.2.2.2.1 Research is beginning to l inkdisequilibrium in foraminiferal shells to variationsin seawater chemistry and depth-specific habitats,but the reports are largely descriptive. Five maincauses of disequilibrium have been identified: theontogenic effect; the symbiont photosynthesiseffect; the respiration effect; the gametogeniccalcite effect; and the effect of changes in

The various effects may operate in oppo-site ways, masking one another. All are importantfor planktonic Foraminifera, but a great varietyof deviations from equilibrium also exists in deep-sea benthic Foraminifera (e.g. Duplessy et al.,1970; Woodruff et al., 1980; Vincent et al., 1981;Wefer and Berger, 1991). Since these benthicspecies live in an environment with very stablelow temperatures and a complete absence ofphotosynthetic activity, the disequilibria suggest

an important role of microhabitat differentiationcombined with pore water chemistry and foodsupply. The various effects are not strictly sepa-rate, and there may be considerable overlapbetween their regulating processes.

14.2.2.2.2 Ontogenic effect In laboratoryexperiments with constant and temper-ature, Globigerina bulloides shows a progressive

increase of up to 0.8‰ with shell develop-ment: j uven i l e chambers are strongly depleted(around 1 . 1 5 ‰ ) , while the f inal chamber is lessdepleted (around 0.30‰), relative to equ i l ib r ium(Spero and Lea, 1996). The mass-balancedaverage of the individual chambers gives a system-atic whole-shell depletion of around 0.7‰. Sincea similar trend of increasing values throughontogeny was observed in an explanationwas offered in terms of incorporation of metabolic(respired) duringcalcification.Higher meta-bolic rates in juveniles would cause the strongestdepletions, while adults gradually trend towardsequil ibrium.

The trend is to some extent corroboratedby reports of a size-dependent trend in G.bulloides (e.g. Kroon and Darling, 1995), althoughthe trend in those real-ocean results is a factor oftwo smaller than that observed under laboratoryconditions. Spero and Lea (1996) found a s imilardifference when comparing laboratory resultswith data from fossil G. bulloides from ChathamRise, speculating that the reduced signal wascaused by vertical migrations from deeper coolerwaters during early stages to very shallow, warmerwater during later stages (see also Bemis et al.,1998).

14.2.2.2.3 Symbiont photosynthesis In thephotosynthetic symbiont-bearing planktonicforaminiferal species Globigerinoides sacculifer,Spero and Lea (1993) observed no variat ions inshell wi th ontogeny wi th in the size range

support ing earlier conclusions thatgrowth alone does not cause disequi l ibr ium inthis species ( Erez and Luz, 1982, 1983; Wefer andBerger, 1991). However, a distinct chamberdecrease is seen with increasing irradiance levels(Spero and Lea, 1993), A similar but weaker

Oxygen isotopes 247

decrease with increasing irradiance occurs inphotosynthetic symbiont-bearing Orbulina uni-versa (Spero, 1992; Spero and Lea, 1993; Speroet al., 1997). In addition, increased growth rateswere observed with increasing light intensities,corroborating observations of light-enhancedcalcification rates under elevated irradiance inphotosynthetic symbiont-bearing corals (Chalkerand Taylor, 1975) and larger Foraminifera (TerKuile and Erez, 1984). McConnaughey (1989a)and Wefer and Berger (1991) reported decreasingskeletal values with increasing growth rates.The processes involved center around increasingkinetic discrimination against the heavy isotopesduring diffusion through the skeletal mem-brane, with rapid reactioncycles (McConnaughey, 1989b; Spero and Lea,1993).

14.2.2.2.4 Respiration Studies on photosyn-thetic symbiont-bearing corals indicate that theprocess of photosynthesis per se invokes no appre-ciable fractionation effects for (Swart, 1983).Respiration, on the contrary, does causedepletion (Lane and Doyle, 1956). Relative toambient dissolved oxygen, the oxygen used in res-piration is depleted by 21‰ in near-shore, shallowwaters (Kroopnick, 1975), and 11‰ in the deepocean (Grossman, 1987). The of ambientdissolved oxygen in surface waters commonlyranges around +24 to +26‰ (SMOW)(Kroop-nick et al., 1972; Kroopnick, 1975). In NorthAtlantic station Geosecs II , preferential respira-tory utilization causes a marked peakin dissolved oxygen (+31‰ SMOW) around1000 m depth (Kroopnick et al., 1972). Utilizationof depleted respiratory products during calcifica-tion (Belanger et al., 1981; Grossman, 1987)mightcause skeletal depletion.

14.2.2.2.5 Gametogenic calcite Several plank-tonic foraminiferal species deposit a veneer ofcalcite on the surface of their shell at the end ofthe life-cycle (Bé, 1980; Duplessy et al., 1981;Deuser, 1987; Spero and Lea, 1993; Bemis et al.,1998). Globigerinoides sacculifer secretes the addi-tional calcite over a period of up to 16 hoursbefore gamete release (Bé, 1980), and its gameto-

genic calcite layer comprises 18 to 28% of theshell mass (Bé , 1980; Duplessy et al., 1981)(around 26% in Orbulina universa; Bouvier-Soumagnac and Duplessy, 1985). Specimenscovered by gametogenic calcite are calledthick-walled. Gametogenic calcite is enrichedrelative to earlier (thin-walled) stages of the shell.These layers are, therefore, very important forwhole-shell isotopic analyses.

Duplessy et al. ( 1 9 8 1 ) speculated that the earlystages of G. sacculifer are deposited at distinctdisequilibrium in warm shallow waters, whereasthe gametogenic layer is deposited in colderwaters at depths of up to several hundreds ofmeters, possibly in near equilibrium. Bouvier-Soumagnac and Duplessy (1985) presented sim-ilar cases for O. universa, Neogloboquadrinadutertrei, and Globorotalia menardii. Kroonand Darling (1995) apply such arguments toreconstruct changes between last glacial maxi-mum and Holocene vertical temperature gradi-ents in the Arabian Sea and Panama Basin. Speroand Lea (1993), on the contrary, considered thatvertical distribution studies of living planktonicForaminifera do not support calcification at greatdepths, so that another, unidentified, mechanismshould cause the enrichments in gametogeniccalcite. However, in a subsequent study by theseand other workers (Bemis et al., 1998), the calcifi-cation-at-depth hypothesis was invoked again,without further discussion. Clearly, the nature ofthe enrichment in gametogenic calcite is yet to beresolved.

14.2.2.2.6 Carbonate ion concentrations Speroet al. (1997) subjected specimens of Orbulinauniversa to variations in at constantalkalinity, under both high and low irradianceconditions. They observed a constant offsetbetween the high and low irradiance experiments,while the ratio of change in shell with changein remained similar for both groups. Asecond experiment with manipulation of

by changes in alkalinity with constantcorroborated the results of the first experi-

ment. A third experiment concerned Globigerinabulloides, which bears no symbionts, and again achange was observed in shell with


variations. Spero et al. (1997), therefore, con-cluded that foraminiferal decreases withincreasing that the magnitude of thisresponse is species-specific, and that symbiontphotosynthesis plays no role. These findings forbiological carbonates endorse McCrea’s (1950)observations on inorganic precipitates, suggestinga common, abiological, kinetic fractionationeffect, which may be related to calcification ratesand the pH dependent balance betweenhydration and hydroxylation (McCrea, 1950;McConnaughey, 1989b; Usdowski and Hoefs,1993; Spero et al., 1997; and references therein).

Bemis et al. (1998) re-evaluated data on thebenthic Foraminifera Uvigerina and Cibicidoidesand found that the epifaunal Cibicidoides precipi-tates its shell close to oxygen isotopic equil ibriumwith ambient seawater, while Uvigerina showsmild enrichment. Those authors speculatedthat this enrichment might result from a moreinfaunal habitat with low pore-water pH anddecreased

14.2.2.3 Aragonite versus calcite

Some benthic Foraminifera (e.g. Hoeglundinaelegans) construct their test of aragonite ratherthan calcite. H. elegans is enriched relative tothe equilibrium value for calcite by 0.78 ± 0.19‰(Grossmann, 1984a). This agrees well withexperimental observations that, at room temper-ature, inorganically precipitated aragonite isabout 0.6‰ enriched relative to inorganicallyprecipitated calcite, while theory suggests anenrichment of 0.79‰ (Tarutani et al., 1969). Thetemperature dependence of the aragonite-waterfractionation is similar to that of the calcite-water fractionation (Grossman and Ku, 1986).

14.3 CARBON ISOTOPES

14.3.1 Carbon isotopes and the global carboncycle

There are two main carbon reservoirs: organicmatter and sedimentary carbonates. For com-prehensive schematics of fluxes within the globalcarbon cycle, see Compton and Mallinson

(1996) , Mackenzie (1998) , and referencestherein.

The organic carbon cycle revolves aroundf ixa t ion into organic biomass through

photosynthesis, in both the marine and theterrestrial biospheres: + energy(sunl igh t ) Respiration under thepresence of oxygen follows the reverse reaction.The organic carbon cycle acts on a wide rangeof time scales, from alteration between daytimephotosynthesis and night-time respirationwi th in plants to cycles in the order of years.where organic carbon is stored in sediments,only to become exposed and oxidized muchlater.

Weathering of most ordinary types of exposedor uplifted rocks also draws down fromthe atmosphere. Schematically representing therocks as calcsilicates the weather-ing reaction follows:

The dissociates in water, u t i l i z -ing more (see below). Long-term cycles oforogeny and weathering (of order years),therefore, cause fluctuations of atmosphericconcentrations, which also equilibrate wi th totaldissolved inorganic carbon in the oceans.

The inorganic carbon pool in the oceans isgoverned by the carbonate reactions. Most ofthe in water is contained in ( thebicarbonate ion), due to

while a fur ther (weak) reaction may dis-sociate according to

At normal seawater pH of 7.8–8.3,dominates and there are only small

amounts of Total dissolved inorganiccarbon (DIC) consists of anddissolved Calcium carbonate, biogenic andabiogenic, interacts with the inorganic carbonpool via the precipitation/dissolution equat ion

The average of the carbonate reservoiris around 0‰, while the organic carbon reser-voir averages around –25‰ (Fig. 14.4; alsoHoefs, 1997). Extremely depleted values areknown from methane in the form of gas-hydrates within the continental slope, wi th typi-cal values between –35‰ and – 8 0 ‰ . Seepageof gas-hydrates (clathrates) may cause consider-

Carbon isotopes 249

able depletions in infaunal benthic Fora-minifera (Wefer) et al., 1994).

There is a clear dis t inct ion between thedepletions in terrestrial ( – 2 6 ‰ ) and marineorganic matter ( – 2 2 ‰ ) (Fig. 14.4). Swart(1983) argued that dissolved is the maincarbon species involved in photosynthesis inthe oceans, wi th and uti l izedonly at lower efficiencies. Since dissolvedis strongly depleted relative toand not much different from gaseous(Fig. 14.5), Swart proposed that the heavier

signature of marine algae stems fromdifferent assimilat ion mechanisms in ter-restrial and aquatic plants, and absence oftranslocation processes in the non-vascularalgae. The abi l i ty to u t i l i ze howeve r ,was later found to differ between phy top lank-ton taxa, compromising Swart’s arguments(e.g. Morel et al., 1994; Riebesell and Wolf-Gladrow, 1995).

Photosynthesis is strongly discriminative infavor of and marine phytoplankton formsorganic matter with values of –20 to–23‰ relative to ambient water . Photosynthe-sis is restricted to the euphotic layer and due tothe preferential uptake of du r ing photosyn-thesis, the dissolved carbon in suface waters isrelatively enriched in . Through equilibra-tions, this enrichment affects surface water

and the carbonates formed thereof(Fig. 14.6).

As organic matter is remineralized, its lowvalues are released into the water column,

again equi l ibra t ing with and so affectingcarbonates. Where remineral iza t ion occurswi th in the mixed layer, th i s effect to some extentoffsets the enrichment due to photosynthesis.

14.3.2 Carbon isotopes in seawater.

14.3.2.1 Photosynthesis, respiration, exportproductivity, and surface-deep gradients


However, export production from the mixedlayer constitutes a loss of depleted marineorganic matter to deeper waters. Upon reminer-alization at depth, an effective transfer of

has occurred from surface to deep water. Hence,increases in export product ivi ty wi l l enhancegradients between increased in surfacewaters and decreased values in deep waters,

Carbon isotopes 251

which will be recorded in calcareous fossils(Figure 14.6).

Remineralization at depth releases not onlydepleted but also nutrients, into deep

water. Consequently, enhanced depletion inthe present-day oceans correlates well withenhanced nutrient concentrations, where theexpected relationship between ( in ‰) andphosphate concentrations ( in ) is–0.93‰ per (see Broeker, 1982;Broecker and Peng, 1982, pp. 308 and 309).There are similar relationships betweenand nitrate concentrations (Ortiz et al., 1996).If sufficient validation is possible from indepen-dent evidence, this nutrient correlation hasgreat potential in paleoceanographic applica-tions, as demonstrated by the applications ofpaired and Cd/Ca analyses pioneered byBoyle and Keigwin (1982; 1985/86; 1987) andBoyle (1986).

Lateral gradients in deep water may beused to trace the history of deep water from itssource area. The deep water reflects;( 1 ) time of exposure to organic matter decay(true age); ( 2 ) the amount of organic matterdecayed within the deep water (i.e. export pro-duction along its pathway); and (3) the rapidityof organic matter decay, which is temperaturedependent (respiration rates roughly double foreach 10°C temperature increase; Swart, 1983).This technique of deep water tracing is oftencalled ‘ageing’ of deep water, where age obvi-ously is just a relative concept. The age of deepwater provides a powerful tool for reconstruc-tion of ocean circulation. For example, the rela-tively high values in the present-day deepNorth Atlantic ( + 1 . 0 ‰ , with average surfacewaters at +1 .6‰; Kroopnick et al., 1972) cor-rectly identify it as a basin with active deepwater formation and consequently young deep


waters. Low North Pacific deep watervalues ( – 0 . 2 ‰ , with average surface waters at+1.5 to +2.0‰; Broecker and Peng, 1982;p. 308) successfully identify these waters as old,derived from remote source-regions. Lynch-Steiglitz and Fairbanks (1994) used Cd/Caratios to deconvolve signals into a partrelated to the age of deep water (associated withnutrient enrichment) and a part related to theair-sea exchange defined in the deep water for-mation area (see Broecker and Maier-Reimer,1992). Thus, likely glacial deep water sourceareas were identified that are very different fromthose of today.

Geographic shifts of deep water sourcesgreatly affect the world ocean’s surface-deep

gradients, which are low in actively over-turning basins and high in non-overturningbasins with old deep waters. Such ocean-widepatterns should, therefore, be established beforepast local/regional variability in surface-deep

gradients can be used to quantify exportproduction.

14.3.2.2 Interactions with of atmospheric

Interactions between of atmosphericand the marine reservoir (Fig. 14.6) depend on:( 1 ) spatial variability in the equilibrationbetween atmospheric and dissolved inor-ganic carbon, and (2) geographically widespreadtemporal variability in the of atmospheric

For atmospheric signals to be recorded inthe marine reservoir, a signal of sufficient magni-tude and duration is needed. Because the atmo-spheric reservoir is orders of magnitudesmaller than the marine reservoir, a recordablesignal transmitted by the atmosphere shouldinvolve the terrestrial biosphere and/orlithosphere.

Differences in photosynthetic pathways causeplants to become much more depleted

than plants (Kelly et al., 1993). Cerling et al.(1993) argued that the late Miocene saw anincrease in dominance of plants, whichinclude many grasses, relative to plants, ofwhich most trees are a subset (Leavitt, 1993).

This would have reduced the mean relativeatmospheric enrichment caused by ter-restrial plants. This signal, anchored in the ter-restrial biosphere, was sufficiently strong andlong-lived to help explain the late Miocene shiftto lower values in marine carbonates(Derry and France-Lanord. 1996). Because ofits long-term characteristic, the signal affectedsurface and deep waters equally, in contrast withexport production or deep water age fluctua-tions that influence gradients between surfaceand deep waters.

14.3.2.3 Carbon burial and global isotope shifts

14.3.2.3.1 Organic carbon On the long term,the water column is in steady state, so that theparticulate transport of depleted organicmatter is matched by upwelling of nutrient-rich,

depleted waters. However, some periods ingeological history were characterized by higherthan average organic matter preservation andremoval from the system by inclusion in sedi-ments. Such a situation not only constitutes asink of carbon, so that eventually the atmo-spheric concentration should drop, butsimultaneously causes a residual enrichmentthroughout the oceans and atmosphere. Thisline of reasoning was developed to explain the‘carbon shift’ associated with the widely docu-mented Middle Miocene cooling (Vincent andBerger, 1985), where the appointed organiccarbon sink was the deposition of the MontereyFormation of California.

14.3.2.3.2 Inorganic carbon Weathering of thetotal sedimentary carbonate reservoir reflects itsmean which during the Neogene was verystable around 1.8 ± 0.2‰ (Derry and France-Lanord, 1996). The stabili ty of this valueallowed these authors to develop relativelystraightforward isotopic balance equations toestimate the fractions of organic carbon in thetotal eroded carbon and in the total carbonburial flux. These relationships center around

the mean isotopic difference between thesedimentary carbonate and organic carbonbeing eroded, and the mean isotopic differ-

Carbon isotopes 253

ence between carbonates and organic carbondeposited at time t. If we use a rough approxi-mation that the relationships indicatethat the ratio between mean carbonate and

of carbonate formed at time t dependsmainly on the difference between the fractionsof organic carbon eroded and buried at time t.This would imply that variations in the organiccarbon pool drive global fluctuations,while the inorganic carbon pool instead moni-tors or records the changes.

14.3.3 Carbon isotope ratios in foraminiferalcarbonate

14.3.3.1 Equilibrium fractionation

14.3.3.1.1 Equilibrium between carbonate anddissolved inorganic carbon Grossman (1984b)analyzed for both calcitic and aragonitic(Hoeglundina elegans) benthic Foraminifera,evaluated the results against inorganic precipi-tates, and presented new equilibrium equationsfor aragonite and calcite. The isotopic enrich-ment factor for calcite (c) versus bicarbonate (b)was with T inKelvin. Grossman’s (1984b) equation for calcitereturns values about 1.5‰ lower than that ofEmrich et al. (1970), which concerned a mixtureof aragonite and calcite (see also Fig. 14.5).Romanek et al. (1992) reported a different, tem-perature independent, relationship between the

values of equilibrium carbonate and bicar-bonate: Aragoniteshows a weak inverse relationship with temper-ature (Grossman, 1984b; Grossman and Ku,1986; Wefer and Berger, 1991).

Often, carbonate equilibrium is reportedrelative to the of total dissolved inorganiccarbon (i.e. the of ratherthan relative to the of bicarbonate. This isbecause the value for can be either ana-lytically determined (Kroopnick, 1974), or esti-mated from apparent oxygen utilization rates(Kroopnick, 1985), whereas the of bicar-bonate can only be obtained indirectly fromcalculations using

where f indicates

the mole fraction per dissolved inorganic species.The mole fraction for is very small atnormal seawater pH of 7.8–8.3, so tha tis only slightly (0.2 to 0.4‰) lower than

due to dominance of overInformation on pH and the concen-

trations of the various inorganic carbon speciesis essential for accurate evaluation of the equilib-rium state of carbonate precipitation, which isnot a t r iv ia l problem when sampling natura lenvironments.

14.3.3.1.2 Apparent disequilibria: differentialdepth habitats or microhabitat effect Changesin depth of calcification during growth anddifferences among preferred depths of differentplanktonic foraminiferal species may causeapparent deviations from surface waterequi l ibr ium, because the gradient in issteep between the surface and the thermocline(Kroopnick et al., 1972; Garlick, 1974; Kroop-nick 1985; Tan, 1989). Hence, these calcificationdepth preferences must be taken into accountbefore decisions are made on the degree of dis-equilibrium and its potential causes (e.g. Bou-vier-Soumagnac and Duplessy, 1985; Wefer andBerger, 1991; Ravelo and Fairbanks, 1995; Ortizet al., 1996). Since temperature drops in theoceans with increasing depth, there is also astrong relationship with calcification depth(see section 14.2.2.1). Covariations betweenincreasing and decreasing wi thgrowth in several planktonic Foraminifera sug-gest that calcification at later growth stagesoccurs well below the mixed layer (Bouvier-Soumagnac and Duplessy, 1985). Ravelo andFairbanks (1995) assessed the potential of thesecovariations for reconstructions of past surfacewater hydrography, concluding that non-spi-nose species offer the greatest potential becausethey are less affected by biological fraction-ation effects.

Concerning benthic Foraminifera, the ques-tion of equilibrium should be viewed within thecontext of ambient pore water at thespecies’ preferred l iving depth or microhabitat(Woodruff et al., 1980; Belanger et al., 1981:Grossman, 1984a.b; 1987; McCorkle et al., 1985;


1990; Zahn et al., 1986; Wefer and Berger.1991; Loubere et al., 1995). McCorkle et al.(1990) consistently found lower values indeep dwel l ing taxa t han in shal low dwel l ingtaxa. Pore-water gradients may reach1‰ depletion per cm depth w i t h i n sedimentdue to decomposition of sedimentary organicmatter (Grossman, 1984a,b; McCorkle et al.,1985; Grossman, 1987). There are add i t iona lintraspecific controls on the deplet ions by theamount (Zahn et al., 1986; Loubere, 1987) andmechanisms (Loubere , 1987) of food supplyw i t h i n the sediment. The epibenthic speciesCibicides wue l lers tor f i (also described underCibicidoides, Planulina, and Fon tbo t ia ) formsits test nearest to e q u i l i b r i u m and so providesthe best measure for bottom watervar ia t ions through t ime (e.g. Woodruff et al.,1980; Graham et al., 1981; Zahn et al., 1986;Grossman, 1987; Wefer and Berger, 1991;Mackensen et al., 1993), but see Chapter 10for possible complications.

14.3.3.2 Deviations from equilibrium inforaminiferal carbonate

14.3.3.2.1 Foraminiferal disequilibriummay be caused by: (1) u t i l i z a t i o n of metabolic

during shell formation, ( 2 ) photosyn-thetic activity of symbionts, ( 3 ) growth rate,and ( 4 ) var ia t ion in carbonate ion concen-trations in ambient waters. The effects are notstr ic t ly separate; there may be strong overlapsbetween regulating processes. For detailedoverviews, see Grossman (1987), Ravelo andFairbanks (1995) , Spero et al. ( 1 9 9 1 ; 1997),and references therein.

14.3.3.2.2 Respiratory ‘vital’ effectsVital effects are reflected in the incorporationof isotopically l ight metabolic i n to thecarbonate skeleton (among others K e i t h andWeber, 1965; Weber and Woodhead, 1970;Vinot-Ber toui l le and Duplessy, 1973). Thevi ta l effect magni tude is propor t ional to theamount of metabolic w i t h i n the organ-ism’s in te rna l pool (Erez, 1978), which ,in turn, reflects the organism’s ability for gas-

exchange w i th amb ien t wa te r . Organisms fromoxygen m i n i m u m zones a round the worldshow the least influence of v i t a l effects, sug-gesting t h a t they are special ly adaptedfor efficient gas-exchange (Leutenegger andHansen, 1979; Grossman. 1984a. 1987).

Respired products are depleted relativeto unused oxygen (section 14.2.2.2.4) wh i l e thefood source ( sed imentary organic m a t t e r )would cause likely depletions in metabolic

(see Lane and Doyle, 1956; Degens et al.,1968; Kroopnick , 1975; De Niro and E p s t e i n ,1978) . Hence, the incorpora t ion of metabol iccarbon-oxygen compounds should causereduct ions of both ske le ta l andHowever, t h i s expected re l a t ionsh ip holds onlyto a limited extent (Grossman, 1987), andlaboratory c u l t u r e s show tha t large v a r i a t i o n sin of food used by Orbulina universa andGlobigerina bulloides cause only negl ig ib les h i f t s in shell (Spero and Lea, 1993, 1996:see also Ortiz et al., 1996). Ortiz et al. ( 1 9 9 6 )concluded that the major cause for shellfluctuations is not food bu t metabol icrates control led by temperature . This is sup-ported by reduced values in gastropodshells and corals due to enhanced metabolicactivity associated with spawning (Wefer andBerger, 1991; Gagan et al., 1994). Photosyn-thet ic symbiont -bear ing larger Foraminiferaalso sh i f t to very low values in thereproduc t ive period (Wefer and Berger, 1991) .

14.3.3.2.3 Symbiont photosynthesis A w i d erange of photosynthetic (symbiont bearing)organisms t h a t precipi ta te calc ium carbonatedisplay increasing ske le ta l e n r i c h m e n tw i t h increas ing l igh t i n t e n s i t y ( M c C o n -naughey, 1989a). Spero and Lea ( 1 9 9 3 ) notedsuch a r e l a t i onsh ip in Globigerinoides sacculi-fer, ascribing it to elevated utilization ofby photosynthetic symbionts, which increasesthe calcifying microenvironment inand so produces enriched chambers. Asimilar relationship is known for Orbulina uni-versa , a l t h o u g h the r e l a t i o n s h i p disappearswhen photosynthetic activity is prevented(Spero and Williams, 1988). At very low light

Summary 255

levels, values of G. sacculifer shift slightlybelow equilibrium, suggesting that photosyn-thetic effects become suppressed and that somerespired gets incorporated into the shell

(to a proportion of 0–3% of shell carbon;Spero and Lea, 1993). Similar values wereobserved for O. universa (Spero, 1992). Inf lu-ences of light intensity or photosynthetic activ-ity cannot be easily accounted for in data fromForaminifera grown in natural dark-lightalternations, unless the proportions are knownof the shell fractions deposited dur ing darkand light periods (40 and 60%, respectively,for O. universa; Spero et al., 1991).

14.3.3.2.4 Changes with growth Romaneket al. (1992) found no significant fraction-ations due to differences in calcification ratesalone. However, most Foraminifera experiencemajor physiological changes during growth. InGlobigerinella aequilateralis and Orbulina uni-versa, symbiont density increases with test size(Faber et al., 1985; Spero and Parker, 1985),which in turn increases total gross photosyn-thesis so that each new chamber showsincreasing enrichment. An analysis ofwhole-shell gives an integrated value ofthe masses and different compositions ofall individual chambers (Spero et al., 1991),and will therefore be different for the samespecies in different size-classes. However, pro-gressive increases in in Orbulina universain the natural environment suggest migrationto progressively deeper habitats wi th lowerlight intensity during growth, causing pro-gressive depletion which may (par t ia l ly)offset the enrichment due to increased symbi-ont density (Ravelo and Fairbanks, 1995).

In non-symbiont-bearing species, a changewith size is expected in the depletion causedby contamination of shell with metabolicor respiratory Depletions should bestrongest in small specimens from early lifestages with high metabolic rates, decreasingtowards equilibrium in adult stages (cf. Bergeret al., 1978; Wefer and Berger, 1991). Bouvier-Soumagnac and Duplessy (1985) reportedsuch trends for Globorotalia menardii and Neo-

globoquadrina dutertrei. Ravelo and Fairbanks(1995) confirmed the trend in N. dutertrei, butobserved little to no size-dependent fraction-ation in G. menardii, Globorotalia tumida, Glo-borotalia inflata, Globorotalia crassaformis,Globorotalia truncatulinoides , or Pulleniatinaobliquiloculata.

Deep-sea benthic Foraminifera show no sig-nificant change in skeletal with size (V in -cent et al., 1981; Dunbar and Wefer, 1984;Grossman, 1984; 1987; Wefer and Berger,1991).

14.3.3.2.5 Carbonate ion concentration Sim-ilar to foraminiferal decreases withincreasing The signal magnitude isspecies-specific, and symbiont photosynthesisplays no role (Spero et al., 1997). These resultscombined with abiogenic data (McCrea, 1950)suggest a common, abiological, kinetic frac-tionation effect (cf. section 14.2.2.2.6).

14.3.3.3 Aragonite versus calcite

The aragonitic benthic foraminifer Hoeglun-dina elegans shows constant values withdepth in the California borderland study area,whereas increases with depth (Gross-man, 1984a). This may suggest a negativetemperature dependence of bicarbonate-arago-nite fractionation (also Grossman, 1984b;Grossman and Ku, 1986). To date, fraction-ations associated with aragonite formationremain poorly understood.

14.4 SUMMARY

Table 14.2 summarizes the main processes deter-mining seawater at any study site, andthose determining fractionations betweenof foraminiferal carbonate and of seawater,including typical magnitudes of the isotopicchanges due to each effect. Table 14.3 is similar,but for

To investigate the main controlling processesand eliminate the noise introduced by minorones, specific analytical strategies have been


adopted in paleoceanographic research. Thevital effect is commonly considered to be species-specific, and avoided by study of monospecificrecords. The effects of symbiont density, gameto-genic calcite formation, and changes in calcifi-cation depth dur ing growth are avoided byanalyzing either thin-walled, or thick-walled,specimens of the selected species from similarontogenic stages, using narrowly constrainedsize-fractions. No studies have yet established insufficient detail the temporal changes in oceanic

to allow assessment of their impact onforaminiferal isotope records.

The ice volume effect exerts by far the mostimportant control on records, allowingboth global correlations and absolute dat ing(Figure 14.1) . Also very important is the inf lu-ence of ambient temperature during calcifica-

tion. In a ‘glacial world,’ this influence is lessrelevant for deep-sea benthos, since oceanicdeep-sea temperature f luctuations are un l ike lyto exceed 1 to 2°C. However, larger deep-seatemperature fluctuations may have prevailed inprevious geological periods when the deep-seawas f i l led wi th so-called warm saline deep water,such as is found today in isolated basins l i ke theRed Sea and the Mediterranean. For planktonicforaminiferal records, temperature influ-ences are always very impor tant . Temperatureeffects may be constrained through the use ofother paleotemperature indicators, such astransfer funct ions or geochemical proxies (e.g.alkenone records).

Secondary influences on benthic foraminiferalrecords originate from the microhabitat

and effects, which likely are related, but

Summary 257

still are not fully understood or quantified. Awayfrom sea-ice margins, secondary controls onplanktonic records are exerted by localfreshwater cycle effects and variations.Temporal variations due to the effectare not yet sufficiently known. The assumptionthat, through time, a systematic relationshipshould exist between salinity and due toaction of the freshwater cycle has given rise tothe term ‘salinity effect.’ Recent work is castingdoubt on this assumption, and thus on thepotential of oxygen isotopes in the determina-tion of paleosalinity. Temporal changes in sub-surface water sources, advective pathways, andmixing of water masses appear to complicateinterpretation of records, especially forplanktonic species.

For the major controls are: global shifts

related to changes in terrestrial vegetation and/or large-scale bur ia l oxidation of sedimentaryorganic matter, and the interrelated influencesof export production, respiration at depth, andage of deep water. The global effects are estab-lished by inter-comparison of a large number ofrecords from var ious worldwide locations. Theeffect of export production, etc.. may be esti-mated from comparison of planktonic recordswith records for epiphytic benthic species knownto calcify near equi l ibr ium. This approach ismost successful when paired wi th analyses ofother nu t r ien t proxies, such as Cd/Ca ratios.The age of deep water is assessed similar ly, butin a wider geographical context.

Other influences on benthic foraminiferalare due to the microhabitat effect, and the

effect, which l ike ly are related to one


another. Seepage of clathrates may cause verystrong anomalies in the values of infaunalbenthic species. Additional control on plank-tonic foraminiferal records is exerted by

f luc tua t ions through time. This effectmay be important , but is not yet well quan t i f i ed .


We thank David Lea, Paul Aharon, and BarunSen Gupta for construct ive reviews, comments,and suggestions, and Kate Davis for drawingservices.

15Trace elements in

foraminiferal calciteDavid W. Lea

15.1 INTRODUCTION

The trace element composition of calcitic fora-minifer shells has become an important meansby which paleoceanographers deduce past oce-anic conditions. Pelagic foraminifer shells arecomposed of extremely pure calcite, typicallyabout 99% by weight Trace elementssuch as Mg, Sr, Ba and Cd comprise the remain-ing 1% and occur in calcite foraminifer shells atindividual abundances of 0.25% or less. Traceelements are incorporated directly from sea-water during shell precipitation. For this reason,shell composition reflects both seawater com-position and the physical and biological condi-tions present during precipitation.

The idea that chemical signals encoded intoskeletal carbonates could be used to assess pastenvironmental and climatic information datesback to at least the early part of the twentiethcentury (Clarke and Wheeler, 1922). This ideadid not come to fruition unt i l decades later,however, when Harold Urey and his group atthe University of Chicago were able to demon-strate the potential of oxygen isotope variationsfor paleothermometry (Epstein et al., 1953; Emi-liani, 1955). The trace element component of

climate proxy research has always lagged behindthat of isotopic research. This might be due tothe at t i tude prevalent in the Chicago school thattrace element incorporation was not l ikely to beas systematic (S. Epstein, pers. comm., 1992).

The direct investigation of trace elements in fora-minifer shells was hindered by the difficulty of traceelement determination in the small samples typicalof these shells. The first studies to show real poten-tial were those of Michael Bender and his studentsat the University of Rhode Island, which focusedon using shell Sr, Mg, and Na to establish Cenozoicocean chemical histories (Bender et al., 1975;Graham et al., 1982). Arguably though, trace ele-ments did not become an important paleoceano-graphic tool until Edward Boyle’s pioneeringstudies at the Massachusetts Institute of Technol-ogy, in which he demonstrated that foraminiferalCd could be used to assess past nutrient phosphateconcentrations (Boyle, 1981; Boyle and Keigwin,1982; Hester and Boyle. 1982). Boyle’s researchpushed foraminiferal trace element research into anew realm because Cd is a unique nutrient proxythat is integral to defining past ocean circulationchanges (Boyle and Keigwin. 1982, 1985/1986,1987). In addition, Boyle’s findings set new stan-dards of analysis for the extremely low levels of


260 Trace elements in foraminiferal calcite

metals present and the care with which such deter-minations had to be made (Boyle, 1981). Traceelements in Foraminifera are no longer just a curi-osity needed for chemical bookkeeping but havebecome a unique tool to understand the past. Thisparadigm shift drives trace element research todayas we endeavor to refine our toolbox of elementalproxies while continuously pursuing new leads forproxy development.

We are currently in the midst of a revolution inthe investigation of trace elements in Foraminifera,and our knowledge in this area is increasingrapidly. This is especially true for minor elementslike Mg, which appears to have potential as apaleotemperature proxy. This f lurry of activity islargely driven by improvements in analytical capa-bilities and an expansion in the number oflaboratories undertaking such investigations. Cul-turing of live individuals has also played an impor-tant role in this proxy development, because thepotential usefulness of trace elements can be veri-fied directly by experimentation.

In this review, I focus on the abundance andapplication of four broad groups of trace ele-ments incorporated in foraminifer shells:

(1) ‘nutrient’ proxies such as Cd and Ba, whichprovide information on seawater nu t r ien t ,carbon and carbonate levels;

(2) ‘physical’ proxies such as Mg, Sr, F, and Bisotopes, which dominantly reflect physicalparameters such as temperature andpressure;

(3) ‘chemical’ proxies such as Li, U, V, Sr, andNd isotopes, which provide diverse informa-tion on the history of ocean chemistry; and

(4) ‘diagenetic’ proxies such as Mn, whichreflect secondary post-depositionalprocesses.

Naturally, there is some overlap among thesebroad groups, but the divisions are a helpfulway to view the toolbox of elemental proxiesavailable to the paleoceanographer.

15.2 TRACE ELEMENTS IN THE OCEAN

The diverse oceanic behavior and dis t r ibut ionof the trace elements are the key to ut i l iz ing

elemental var iat ion in foraminifer shells. Chemi-cal oceanographers broadly group elementalbehavior in the ocean according to the biogeo-chemical cycling of the elements in the ocean(Broecker and Peng, 1982; Bruland, 1983).These groups include: (1) nutr ient- l ike elements,those that act as biological nutrients or mimicsuch behavior; ( 2 ) conservative elements, thosethat occur in fixed proportion to the major saltsin seawater and are nearly unaffected by biologi-cal cycling; and ( 3 ) particle-reactive elements,those that are dominated by solid particle–sea-water interactions.

Nut r i en t - l ike elements (Cd, Ba, Zn) showlarge and systematic variat ions in their seawaterchemistry which result from involvement in bio-logical cycling (Bruland, 1983). Minimum nutri-ent concentrations are found in oligotrophicsurface waters due to algal removal of nutrients ,whereas maximum concentrations are found inPacific deep waters due to decomposition ofnutr ient - r ich particulate matter. Deep watermasses have unique trace element imprints dueto variat ions in source waters and patterns ofoceanic mixing. In the modern ocean, minimumdeep-water nutr ient concentrations are found inNorth Atlantic bottom waters and maximumconcentrations in Pacific bottom waters. Cd,which follows phosphate, has almost a thou-sand-fold concentration range in the oceans. Baand Zn, which follow a lka l in i ty and silicic acidrespectively, vary by five to ten fold. The largemodern ocean variation in these elements isexpected to be reflected in the shell chemistry ofForaminifera calcifying in different hydro-graphic settings. The impact of physical and/orbiological processes on calcification can alsoinfluence the presence of these elements in theforaminifer shells (Elderfield et al., 1996).

The ratio of conservative elements (Mg, Sr, B,Li, F, V, U) to Ca is nearly fixed in seawater, andamong the three groups, conservative elementshave the longest oceanic residence limes. Only Vand U are present in seawater at t ru ly trace con-centrations Any variations inthese elements in foraminifer shells found inmodern samples must reflect the impact of physi-cal and/or biological processes on calcification.

In shells from older sediments, variations in theabundance of a conservative element relative toCa might also reflect changes in seawater chem-istry, which responds to shifting oceanic sourceand sink patterns. Both Sr and B have importantisotope systems which can be monitored usingforaminifer shells (see below).

Particle reactive elements (Mn, Nd) arerapidly cycled and have typically short oceanicresidence times They are less regularly distrib-uted in the oceans, and can be enriched in thesurface ocean by the dissolution of aeolian par-ticles. Solid phase Mn is released in suboxic(li t t le or no present) pore-waters by reduc-tion to soluble and this behavior leadsto the deposition of Mn in or on foraminifershells. Nd displays a strong isotopic variationin seawater because the isotopic composition ofits sources varies between ocean basins.

15.3 INCORPORATION OF TRACEELEMENTS IN FORAMINIFERALCALCITE

15.3.1

The ideal situation from a geochemical point ofview is that trace elements are incorporated homo-geneously into calcite and regulated by strict phys-ical (thermodynamic) laws. This ideal of purethermodynamic control is an important concept,because it predicts regular, reproducible behaviorfor the incorporation of trace elements. There isabundant evidence, however, that the incorpora-tion of trace elements in foraminiferal calcite doesnot take place in such an ideal, thermodynamicmanner. Foraminifera, as living organisms,actively precipitate their shells, affecting both thestructure and chemistry of shell calcite. Active pre-cipitation argues for significant biological orkinetic (processes affected by the rate of reactions)controls on trace element substitution.

15.3.2 Thermodynamics of trace elementincorporation

A primary goal in interpreting trace elementcompositions in precipitated minerals is to relate

those concentrations to the composition andphysical conditions at the time of precipitation.This is most commonly accomplished by the useof a constant that relates mineral compositionto fluid composition. The relationship betweenshell calcite composition and seawater is bestexpressed by an empirical partition coefficient D,which is defined for the specific case of Fora-minifera in seawater by the relationship:

The equilibrium constant for reaction ( 2 ) isdefined by:

Incorporation of trace elements in foraminiferal calcite 261

where the bracketed concentrations indicate theactual concentration ratios of trace element (TE)to Ca in calcite and seawater (Morse andBender, 1990; Mucci and Morse, 1990). If D isgreater than 1, the trace element is preferentiallyconcentrated in the shell. If D is less than 1, thetrace element is preferentially excluded from theshell. It is important to realize that the partitioncoefficient is not a thermodynamic property ofthe system, but rather represents an empiricalmeasure of the trace element to calcium ratio inthe shell relative to the same ratio in seawaterfor a specific set of physical and biologicalconditions.

The partition coefficient is distinct from thethermodynamic equilibrium or distribution con-stant (occasionally termed distribution coeffi-cient) K, which can be derived from an exchangereaction:

where a is the activity of solid and solutionphases. Activities, which represent thermo-dynamic or effective concentrations, are noteasily measurable and do not relate in any neces-sarily simple way to bulk measured concen-trations. Because the distribution constant K isan intrinsic thermodynamic property of thesystem, it can be calculated from the thermo-dynamic properties of the products and reac-


tants. Given that there is no simple way todetermine solid phase activities and that theempirical partition coefficient generally does notreflect thermodynamic equil ibrium, the bestpractice is to determine the partition coefficientD by empirical means, and use the thermo-dynamic constant K as a point of comparisononly.

The thermodynamic constant K wil l changewith properties such as temperature if the solu-bility of the pure trace metal phase changesdifferentially relative to pure calcite. A docu-mented example of this is the solid solution of

in aragonite, for which the solubili ty ofincreases to a greater extent with rising

temperature than for aragonite, leading to pro-gressively lower Sr/Ca (less solid ) athigher temperatures. This thermodynamic rela-tionship is exploited as a paleotemperature toolin corals (Beck et al., 1992). The extent to whichD will change with environmental parameters isdependent on both thermodynamic and kinet ic(biological) factors. Any parameter that changesthe rate of calcification also has the potential tochange D (Lorens, 1981), although it is not easyto predict the potential magnitude of suchchanges in biological systems. For example,calcification rate increases with rising pH, whichincreases the incorporation of Sr in calcite(Morse and Bender, 1990). One of the challengesfaced by researchers is sorting out the extent towhich thermodynamic and kinetic influencesdetermine the dependence of trace elements suchas Mg on temperature. True thermodynamicdependence, such as is observed for oxygen iso-topes, is most l ikely to lead to robust proxiesthat will not be undermined by unpredictablekinetic influences.

There are two general mechanisms for traceelement incorporation in foraminiferal calcite:direct solid solution, in which the trace elementsubstitutes directly for in the calcite struc-ture, and trapping, in which the trace elementoccurs as a discrete phase or absorbed ion (Pin-gitore, 1986). Substitution by isomorphous solidsolution undoubtedly provides the more robustmechanism for trace element incorporation,because it is most likely to be primarily regu-

lated by thermodynamics. Trace elements w i thionic radii compatible with the site andchemical s t ructures isomorphous with calciteare most l ike ly to exhibi t regular ionic subst i tu-tion into foraminifer shells (Reeder, 1983)(Table 1 5 . 1 ) . Trace element occurrence by trap-ping is far less l ike ly to lead to homogeneousmineral composition, and trapping is morelikely to be affected by kinet ic factors such asprecipitation rate. It must also be recognizedthat some trace elements might be incorporatedby a combination of factors, in which case theelement might be uniformly distr ibuted by solidsolution but also concentrated preferent ia l ly insome parts of the crystal by trapping.

15.3.3 Biology of trace element incorporationand role of live culturing

Foraminifera are l iv ing organisms, and, there-fore their biology influences the precipitation ofshell calcite. Geochemists have termed th is the‘vital effect,’ a term tha t generally encompassesthe sum of biological influences wi thou ta t tempting to unravel t h e i r causes. Comparisonof empirical part i t ion coefficients ( D ) wi th pre-dicted thermodynamic d is t r ibut ion constants( K ) indicates that the biology of calcif icationoffsets foraminifer shells from equilibrium values(Elderfield et al., 1996). Shell calcification is rela-tively rapid, variable in time, and influenced byexternal factors, all of which contribute to non-equi l ibr ium precipitation (Lea et al., 1995).

Empirical part i t ion coefficients are most com-monly determined by calibrating foramini fera lshell chemistry from core-top sediments w i t hestimates of seawater chemistry and physicalconditions (Hester and Boyle, 1982; Lea andBoyle, 1989; Boyle, 1992; Rosenthal et al.,1997b). These calibrations implicitly include allvi ta l effects, as well as any possible post-deposi-tional factors. Core-top calibrations, however,cannot be used to separate and a t t r ibu te indivi-dual biological influences or determine how v i ta leffects might vary spatially, especially throughthe secondary influence of oceanographicparameters.

Live cu l tur ing is an impor tan t means by

Incorporation of trace elements in foraminiferal calcite 263


which such biological effects can be unraveled.For example, factors that are known to influenceForaminifera, such as light (via its influence onsymbiotic dinoflagellates), temperature, salinity,and pH, can be varied systematically by experi-mentation. Since the early 1980s, live culturingof Foraminifera has become an important toolto assess trace element incorporation in shells.Culturing offers the advantage of direct experi-mentation, which removes much of the ambigu-ity associated with calibration by indirectmeans. To date most culturing studies havefocused on spinose planktonic Foraminifera, butsome activity has been directed towards cultur-ing benthic species and non-spinose planktonicspecies (Bé et al., 1977a; Hemleben et al., 1989;Chandler et al., 1996).

Pioneering studies conducted by Peggy Dela-ney and Allan Bé assessed Cd, Mg, Sr, Na, andLi incorporation in tropical spinose Foramini-fera (Delaney et al., 1985; Delaney, 1989). Subse-quently, different research groups haveinvestigated Ba, Cd, B, and Ca uptake (Lea andSpero, 1992; Lea and Spero, 1994; Lea et al.,1995; Sanyal et al., 1996; Mashiotta et al., 1997),U and V uptake (Russell et al., 1994; Hastingset al., 1996b), and Mg uptake (Nürnberg et al.,1996; Mashiotta et al., in press). Culturingstudies are beginning to reveal the detailed bio-logical influences on trace element uptake. Oneexample of such an influence is the observationthat symbiotic dinoflagellates sequester Cd, thusreducing the Cd content of shell calcite (Mashi-otta et al., 1997).

Many of the trace elements determined in fora-minifer shells are in very low abundances, andthe presence of extraneous phases which containhigh trace element levels can obscure the deter-mination of the primary material. It is thereforenecessary to purify the foraminifer shells by bothphysical and chemical steps. Rigorous purifica-tion procedures were developed by EdwardBoyle to determine the very low levels of Cd in

shells (Boyle, 1981; Boyle and Keigwin, 1985/1986). These consist of alternate steps of physi-cal agitation to remove detrital grains and chem-ical treatment, including oxidation of organicmatter, reduction of Fe and Mn oxides, and acidleaching of adsorbed ions. Boyle’s purificationtechniques, with various degrees of modificationdepending on individual circumstances for eachelement, are the accepted standard for preparingforaminifer shells for trace element determina-tion. Modifications of this purif icat ion cleaningmethod have been made for foraminiferal Ba(Lea and Boyle, 1993) and improved Cd deter-mination (Rosenthal et al., 1997a).

Given the range of trace elements determinedin foraminifer shells, it is not surprising thatthere are a number of methods used to makemeasurements. Because trace elements havebeen routinely determined in foraminifer shellsonly since about 1980, the analytical techniquesare less standardized than for stable isotopedeterminations. Among the predominant ana-lytical techniques are:

Atomic Absorption Spectrophotometry (AAS):AAS has been used to determine Ca, Mg, Na,Sr, Li, Mn, Cd, and Zn in foraminifer shells(Boyle, 1981; Delaney et al., 1985). AAS relieson the unique atomic absorption spectra of eachelement; trace element abundances are quant i -fied by comparing the absorption of a sampleto that of a known standard. Graphite furnaceAAS (GFAAS) is an extremely sensitive tech-nique which is used to determine the very lowlevels of Cd and Zn in foraminifer shells.

Inductively Coupled Plasma Mass Spectro-metry (ICP-MS): ICP-MS has been used todetermine Ca, Mg, Sr, Mn, Ba, Cd, U, and V inforaminifer shells (Lea and Boyle, 1993; Russellet al., 1994; Hastings et al., 1996b; Lea andMartin, 1996; Rosenthal et al., 1997b). ICP-MSuses a quadrupole or magnet to directlydifferentiate the masses of individual isotopesionized in a plasma. Trace element abundancesare quantified by either isotope dilution, internalstandardization, and/or reference to gravimetricstandards. ICP-MS is comparable in sensitivityto GFAAS but offers the advantage of simulta-neous determination of elements.

15.4 SAMPLE PREPARATION ANDANALYTICAL TECHNIQUES

Nutrient proxies: Cd and Ba 265

Thermal Ionization Mass Spectrometry(TIMS): TIMS has been used to determine Sr,Sr isotopes, B, B isotopes, Ba, U, and V(DePaolo and Ingram, 1985; Russell et al., 1994;Hastings et al., 1996b; Sanyal et al., 1996). TIMSuses a magnet to differentiate the masses of indi-vidual isotopes ionized from a solid filament.Trace element abundances are quantified by iso-tope dilution; isotope ratios are quantified byreference to standards with known ratios. TIMSis a relatively slow technique but offers superiorprecision by a factor of 10–1000 over ICP-MSand AAS.

A technique likely to become important inthe near future is High Resolution Multi-Collec-tor ICP-MS. This technique combines theprecision of TIMS with the rapid throughput ofICP-MS (Halliday et al., 1998). It is likely thatin the future, geochemists will be able to deter-mine both low level trace elements such as Cdand high precision isotope ratios such asby this technique.

Abundances of trace elements in Foraminiferaare commonly presented in molar units (molelement per mol Ca) or sometimes in weightunits (usually ppm, which denotes of the traceelement per g of calcite). Molar units are prefera-ble because they can be directly related to ele-mental ratios in seawater. To convert betweenunits, use the following equation:

ppm = mol element/mol Ca

× atomic weight/100 g

example:

0.1 Cd/mol × 112.411 g Cd/mol/100 g

= 0.112 ppm = 112 ppb

Fifteen trace elements have been sufficientlydocumented so that their actual presence in shellcalcite (as opposed to in extraneous phases suchas organic compounds, oxides, or clays) is rea-

sonably certain (Table 15.1; Fig. 15.1). Four ele-ments, Mg, Na, Sr, and F, are present atabundances of greater thanBecause these elements occur at levels of up to0.25% by weight, they are often termed minorelements. Five of the trace elements, B, Li, Mn,Zn, and Ba are present at abundances between

and The remaining six traceelements, Fe, Cu, Nd, Cd, V, and U are presentat abundances between andThe metals Mg, Sr, Mn, Zn, Ba, Fe, Nd, and Cdare known to form solid solutions isomorphouswith either calcite or aragonite (Table 15.1)(Speer, 1983). Therefore these metals are mostlikely to be directly interpretable in terms oftheir chemical behavior in shells.

The most developed and well understood traceelement proxies are those used to assess pastnutrient concentrations, mainly Cd and Ba.Understanding the concentration and distribu-

15.6 NUTRIENT PROXIES: Cd AND Ba

15.6.1

15.5 ABUNDANCE OF TRACEELEMENTS IN FORAMINIFERALCALCITE


tion of nutrients and carbon in ancient oceansis a prime problem in paleoceanography ( Boyle,1990). Using planktonic and benthic Foramini-fera, nutrient proxies can be used to reconstructnutrient and carbon chemistry in surface anddeep waters. Levels of surface water nutr ientsare directly linked to the cycle of carbon dioxideand oceanic productivity by Redfield ratios(Broecker and Peng, 1993). Because the distri-bution of nutr ients in the deep ocean is a directreflection of the thermohaline flow of abyssalwaters, deep-water nutr ient distr ibutions can inturn be used to deconvolute water mass mix ingor to fingerprint source waters.

15.6.2 Cadmium

The oceanic behavior of Cd closely mimics thatof phosphate in the water column, and Cd isthe most direct nutr ient analog available(Fig. 15.2a) (Boyle, 1976, 1988a). Cd also formsa solid solution with calcite, and therefore, Cdis expected to exhibit systematic behavior whenincorporated into shells. Cd occurs at very lowconcentrations in the oceans, ranging from

Nutrient proxies: Cd and Ba 267

in the most nutrient depleted sur-face waters to in the most nutr ient-enriched deep waters (Bruland, 1983). It followsthat the abundance of Cd in foraminifer shellsis also very low, ranging fromin tropical spinose planktonic species suchas Globigerinoides sacculifer and G. ruber to0.250 in benthic genera Cibicidoidesand Uvigerina from the Pacific. The low levelsof shell Cd make shell purification particularlycritical and Cd analysis challenging.

Regular uptake of Cd into foraminifer shellshas been demonstrated by comparing the Cd/Ca of core-top benthic Foraminifera to bottomwater Cd concentrations (Fig. 15.2b) (Hesterand Boyle, 1982; Boyle, 1988a, 1992). Thesestudies demonstrate that the partition coefficientD for Cd in benthic foraminifer shells is between1 and 3. Research indicates a depth (pressure?)effect on Cd incorporation, and Boyle has pro-posed that this effect can be corrected by inter-polating between D values of 1.3 (at depths< 1150 m) and 2.9 (at depths > 3000 m) (Boyle,1992). There are insignificant differences in Damong calcitic species. Potential complicationsin using benthic Cd include: ( 1 ) the diageneticaddition of sedimentary Cd trapped or addedby Mn-carbonate overgrowths (see below)(Boyle, 1983); (2 ) influence of pore water Cd onbenthic Foraminifera, particularly those withinfaunal modes of life (McCorkle and Kl ink-hammer, 1991; Martin et al., 1996); and ( 3 ) apossible dissolution effect on shells depositedbelow the lysocline (McCorkle et al., 1995).

The vast majority of effort in studying shellCd has been directed at determining bottomwater concentrations of Cd, mainly with theobjective of assessing shifts in abyssal circula-tion. Cd records were instrumental in establish-ing that the flux of North Atlantic Deep Water( N A D W ) was weaker during cold glacial cli-mate periods (Figs. 15.3a, b) (Boyle and Keigwin,1982, 1985/1986, 1987; Boyle, 1990, 1995; Boyleand Rosener, 1990; Boyle and Rosenthal, 1996;Rosenthal et al., 1997a). Boyle used Cd to estab-lish the ‘deepening’ of nutr ients during glacialepisodes, which might have contributed to theatmospheric drawdown (Boyle, 1988b,c),

and to assess changing mean ocean nutr ients(Boyle, 1986, 1992). Boyle’s findings have beenverified and extended by other workers (Lynch-Steiglitz and Fairbanks, 1994; Ohkouchi et al.,1994; Oppo and Rosenthal, 1994; Bertram et al.,1995; Lea, 1995; Martin and Lea, 1998; Lynch-Steiglitz et al., 1996; van Geen et al., 1996). Theuse of Cd has been extended to the aragoniticgenus Hoeglundina for studies of intermediatewaters (Boyle et al., 1995; Marchitto et al., 1998),and to neritic benthic species to reconstructpaleo-upwelling in the California Current (vanGeen et al., 1992: van Geen and Husby, 1996).Some attempts have been made to investigateCd in pre-Pleistocene sediments, but the poten-tial for diagenetic influence is recognized as con-siderable (Delaney and Boyle, 1987; Delaney,1990).

There has been less progress in utilizing Cdsignals in planktonic Foraminifera. Boyle’s earlywork showed that Cd could be measured inplanktonic species and that differences in Cd/Ca between species tracked known depth prefer-ences (Boyle, 1981). Because the limited surfacewater Cd range makes it difficult to do core-topcalibrations, Cd uptake in planktonic species isbest assessed by culturing studies (Fig. 15.2c)(Delaney, 1989; Mashiotta et al., 1997). Thesestudies demonstrate uptake of Cd with a parti-tion coefficient of about 2. Mashiotta et al.(1997) further demonstrated that certain symbi-ont-bearing species have much lower uptakecoefficients (0.1 to 0.4), most probably due tosequestration of Cd by symbiotic dinoflagellatealgae. Published down-core work has mostlybeen confined to the polar species Neogloboqua-drina pachyderma (Boyle, 1988b; Keigwin andBoyle, 1989), with recent work demonstratingsignificant sub-Antarctic nutrient shifts in N.pachyderma and Globigerina bulloides records(Mashiotta and Lea, 1997; Rosenthal et al.,1997a).

Barium behaves like a nut r ien t in the oceans. Incontrast to Cd, Ba is less readily regenerated

15.6.3 Barium


Physical proxies: Mg, Sr, F, and 269

from sinking particles and therefore is most sim-ilar to the refractory properties alkalinity, sumof excess base, and silicic acid (Lea and Boyle,1989, 1990b; Lea, 1993). Ba is depleted in surfacewaters through the precipitation of barite,

(Bishop, 1988). Deep waters are enrichedby the dissolution of this barite, which predomi-nantly dissolves on the seafloor (Chan et al.,1977). The oceanic distribution of Ba reflects acombination of biogeochemical cycling andabyssal circulation, with concentrations rangingfrom in the nutrient depletedPacific surface waters to inthe most nutrient-rich waters of the northPacific (Ostlund et al., 1987).

Benthic Foraminifera reflect the distributionof bottom water Ba concentrations, rangingfrom about 2 in the North Atlanticto about 5 in the North Pacific (Leaand Boyle, 1989). They take up Ba with a parti-tion coefficient of about 0.35, with small differ-ences among species. A partition coefficient lessthan 1 indicates that Ba is discriminated againstduring precipitation, probably because it has anionic radius sufficiently large to favor incorpora-tion in the more open orthorhombic structure(Table 15.1). Foraminiferal Ba concentrationsare about 20 times higher than Cd, but shellpurification requirements are still considerable,because of the potential for barite contamina-tion (Lea and Boyle, 1991, 1993). Ba incorpora-tion in shells might also be affected bydissolution in sites below the lysocline, or alter-natively by pressure affects (McCorkle et al.,1995).

The paleoceanographic application of Ba hasfocused on reconstructing circulation changesand alkalinity shifts. Downcore records from theAtlantic ocean indicate that Ba increased inbottom waters by about 50% during glacial epi-sodes (Figs. 15.3a,b) (Lea and Boyle, 1990a,b).In contrast, Ba was only 10–20% higher in gla-cial Circumpolar Deep Water (CPDW) andabout 20% lower in glacial Pacific deep waters(Lea and Boyle, 1990b; Lea, 1993, 1995). Theimplication of these changes is that reduced pro-duction of NADW during glacial episodes essen-tially eliminated the large gradient in bottom

water Ba that exists today between the At lant icand Pacific. The picture of glacial abyssal circu-lation derived from benthic Ba is somewhatdifferent than that from Cd and and cur-rent research focuses on understanding thesedifferences and how they provide clues to shiftsin physical, chemical and biological factorsbetween glacial and interglacial episodes(Martin and Lea, 1998). Ba has also been usedto estimate alkalinity changes in Antarcticwaters. Results from the glacial sections ofSouthern Ocean cores suggest that alkal ini tyshifts due to circulation changes are too smallto account for the glacial drawdown in atmo-spheric (Lea, 1993, 1995).

Culturing results and core-top determinationsdemonstrate that Ba is incorporated into spi-nose planktonic shells with a partition coeffi-cient of 0.15, less than half of D for benthic shells(Lea and Boyle. 1991; Lea and Spero, 1992,1994). This difference presumably relates tocalcification rate differences between planktonicand benthic Foraminifera. There is evidence thatnon-spinose species incorporate considerablymore Ba, although an explanation is wanting.Downcore Ba records from planktonic Fora-minifera have not revealed climatically signifi-cant shifts (Lea and Boyle, 1990a, 1991)

Physical proxies are those elements for whichshell variability is primarily mediated by physi-cal factors such as temperature, salinity, pres-sure, or pH. The best candidates are thoseelements that behave conservatively in theoceans, and therefore occur in nearly constantproportion to calcium in seawater. (Boron iso-topes are unique among the physical proxies;see below.) The controls on shell chemistrymight occur through the direct influence ofphysical factors on the trace element partitioncoefficient, or alternatively, occur indirectlythrough the effect of physical parameters on

15.7 PHYSICAL PROXIES: Mg, Sr, F,AND

15.7.1


biological factors such as calcification rate. Theinfluence of calcification rate on trace elementincorporation is probably related to shifts inmass transport and surface reaction kinetics(Morse and Bender, 1990). Paleoceanographersare inclined to establish relationships betweenshell trace elements and physical parameters byempirical means, and leave the details of thechemical and biological controls to futurestudies. But if Mg, Sr, and F incorporation ismediated by a complex indirect pathway involv-ing calcification rate, it is less l ikely that theseelements will be robust proxies of physicalchanges in the past. One area of particular con-cern is that there is a general relationshipbetween Mg and Sr in shells, suggesting thattheir incorporation might be linked (Carpenterand Lohmann, 1992).

factor on planktonic foraminiferal Mg, usingcore-top, sediment trap, sediment, and culturedsamples, failed to yield an unambiguous rela-t ionship between Mg and inferred growth tem-perature (Savin and Douglas. 1973; Bender et al.,1975; Delaney et al., 1985).

Mg/Ca in planktonic Foraminifera variesfrom about 0.5 to 5 mmol/mol, with a increasein Mg from cold to warm waters. Surface-dwell-ing spinose species contain more Mg than theirdeeper-dwelling non-spinose counterparts, pre-sumably because of temperature control (Savinand Douglas, 1973; Bender et al., 1975; Delaneyet al., 1985; Rosenthal and Boyle. 1993). Benthicforaminifer Mg/Ca ranges from 0.5 to 10 mmol/mol, wi th the highest values in shells from theshallowest (warmest) sites ( I zuka , 1988; Ra th-burn and Deckker, 1997; Rosenthal et al.,1997b). Given that seawater Mg/Ca is 5.17 mol/mol (Bru land , 1983), the part i t ion coefficient forforaminifer shells is of order 0.001, indicatingthat shell precipitation strongly discriminatesagainst Mg.

Interest in using shell Mg as a proxy of seasurface temperature (SST) has intensified in the1990s. Culturing and surface sediment studieshave demonstrated a strong dependence of bothplanktonic and benthic shell Mg/Ca on growthtemperature (Figs. 15.4a,c), while down-corestudies suggest that systematic oscillations inshell Mg with climate change do exist in thedeep-sea record (Nürnberg, 1995; Nürnberget al., 1996; Mashiotta et al., in press; Ra thburnand Deckker, 1997; Rosenthal et al., 1997b).Parallel studies, however, have suggested that

15.7.2 Magnesium

The study of Mg in carbonate fossils (includingForaminifera) has been an area of geologicalinterest for almost a century (Clarke andWheeler, 1922). At that time it was already rec-ognized that carbonate shells precipitating inwarm water tended to contain higher levels ofMg than their counterparts in cold waters. Twodown-core records from the subantarctic IndianOcean first indicated that planktonic shell Mgvariations correlate with climate change in thelate Quaternary, with higher levels of Mg associ-ated with warm climate periods (Cronblad andMalmgren, 1981). However, early systematicattempts to isolate temperature as a controlling

Physical proxies: Mg, Sr, F, and 271


there are strong post-depositional effects onshell Mg in some species, most likely due topreferential dissolution of Mg-enriched portionsof the shells (Fig. 15.4b) (Savin and Douglas,1973; Hecht et al., 1975; Lorens et al., 1977;Rosenthal and Boyle, 1993; Russell et al., 1994;Brown and Elderfield, 1996).

Sorting out the controls and potential useful-ness of Mg is a most important contemporaryproblem in foraminiferal trace element research.If shell Mg can be used for paleothermometry,it would become a critical tool in paleoceano-graphic and paleoenvironmental research.Because shell Mg and can be measured inthe same phase, it is possible to calculate the

composition of the water from which theshell precipitated, if Mg can be converted totemperature (Mashiotta et al., in press). BenthicMg/Ca might be the best information on thehistory of deep-water temperatures. Researchwill be required on many fronts, including: ( 1 )establishing why shell Mg varies wi th temper-ature (i.e. thermodynamic control versus kineticor biological factors); ( 2 ) why different specieshave different shell Mg/Ca, and how that relatesto foraminiferal habitat; and (3) what secondaryfactors might influence Mg, including post-depositional dissolution, and how these effectsvary from species to species.

record (Cronblad and Malmgren, 1981) suggeststhat shell Sr variations correlate with climatechange.

Recent studies, focused on benthic Foramini-fera (Fig. 15.4c) (McCorkle et al., 1995;Elderfield et al., 1996; Rathburn and Deckker.1997; Rosenthal et al., 1997b), have demon-strated that there is a systematic decrease inbenthic shell Sr wi th water depth throughoutthe oceans. Temperature, pressure and calcitesaturation have all been suggested as potentialcontrols. However, the l ineari ty of the Srdecrease with depth and the uniformity of thisrelationship in the oceans suggest tha t pressureis the most likely cause of the change.

Foraminifer shells record small but systematicshifts of about 5% in Sr/Ca over the last250 kyrs (Martin et al., 1997). These shifts areclearly correlated with cl imate episodes, andprovide tantal iz ing evidence that oceanic Sr con-centrations might have oscillated in response tochanges in the part i t ioning of shelf carbonates(h igh in Sr) and pelagic carbonates (depleted inSr) (Stoll and Schrag, 1998). However, confi-dently ascribing secular shifts in shell Sr to cor-responding shifts in seawater Sr/Ca requireseliminating all other potential influences, includ-ing physical properties such as temperature, andsecondary influences such as dissolution, whichalso change synchronously wi th climate.

15.7.3 Strontium

Strontium is a conservative element in seawaterwith a long residence time of about 5 My. Insimilar fashion to Mg studies, systematicattempts to isolate the factors controlling fora-miniferal Sr, using core-top, sediment trap, sedi-ment and cultured samples, have failed to yieldunambiguous relationships (Bender et al., 1975;Delaney et al., 1985). These studies, however,demonstrate that Sr/Ca is much more uniformthan Mg/Ca in planktonic Foraminifera, vary-ing from about 1.2 to 1.6 mmol/mol, and thatSr is incorporated with a partition coefficient ofabout 0.16. An 80 My record of shell Sr suggeststhat oceanic Sr concentrations have changedsignificantly (Graham et al., 1982; Delaney andBoyle, 1986), and a published late Quaternary

15.7.4 Fluorine

Fluorine is a conservative element in seawaterwith a residence time of 0.5 My. Fluoride is oneof the few anions that has been studied in car-bonates (others include borate and sulphate),partly because anion incorporation is much lessunderstood than cation incorporation. Theoreti-cal considerations suggest that the proportionof F to Ca might reflect salinity variations(Rosenthal and Boyle, 1993). Recent studiesdo not demonstrate consistent relationshipsbetween shell F/Ca and temperature and salinity(Opdyke et al., 1993; Rosenthal and Boyle, 1993;Rosenthal et al., 1997b). A decrease in F/Ca ofplanktonic shells wi th increasing water depthdemonstrates that post-depositional dissolut ion

Chemical proxies: Li, U, V, and 273

modifies the fluorine of deposited shells (Rosen-thal and Boyle, 1993).

15.7.5 Boron isotopes

The ratio of to (denoted ) does notvary within the ocean. There is, however, a largeisotopic fractionation between the two aqueousspecies – ‘boric acid, and borate,

(Spivack et al., 1993). The ratiobetween boric acid and borate is a strong func-tion of pH. If the charged borate species is theonly one that is incorporated into foraminifershells, the composition of shells serves asa proxy of pH, a relationship demonstrated byboth core-top and culturing studies (Spivacket al., 1993; Sanyal et al., 1995, 1996). Studies ofancient sediments suggest that shell recordssubstantial oceanic shifts in pH between glacialand interglacial episodes. However, the impliedpH shifts are less homogeneous than might beexpected, suggesting that oceanic pH changes incomplex ways, or alternatively, there are otherundocumented influences on shell

15.8 CHEMICAL PROXIES: Li, U, V,AND

15.8.1

Chemical proxies record secular changes inocean chemistry. Like the physical proxies,chemical proxies are generally conservative inseawater. They differ from the physical proxiesbecause variability in shell content over time isthought to be primarily mediated by changes inseawater composition. Seawater composition ofthese elements is controlled by inputs and out-puts that are sensitive to climate change or tec-tonic reorganization. The chemical proxiesinclude the isotope systems of Sr and Nd. Secu-lar variations in the Sr isotopic composition ofseawater are well established over geologicaltime and have proven to be an important strati-graphic and geochemical tool.

15.8.2 Lithium

Li is a conservative element in seawater with along residence time (> 1 My). One of its majoroceanic sources is the hydrothermal interactionof seafloor basalt and seawater (von Dammet al., 1985). Therefore, on long time scales, sea-water Li might vary with shifts in the extent ofseafloor spreading (Delaney and Boyle, 1986).Delaney attempted to document such shifts, andconcluded that the limited variation in shell Li/Ca over the last 100 My constrains potentiallong term changes in hydrothermal venting ofLi (and by implication production of seafloorbasalt) to ± 30%.

15.8.3 Uranium and Vanadium

Both U and V, nearly conservative in seawater,have major oceanic sinks in suboxic ( l i t t l e or nooxygen) sediments, where reduction of U and Vleads to their incorporation into insolublephases. Thus, it is hypothesized that shifts in theareal extent of suboxic sediments woulddecrease the seawater concentrations of U andV, and this change would be recorded in fora-minifer shells (Russell et al., 1994, 1996; Hastingset al., 1996a,b). Uranium and V occur as oxy-anions in seawater and therefore would not beexpected to substitute into shell calcite in anysimple way. Russell et al. (1996) and Hastingset al. (1996a,b) used planktonic cul turing todemonstrate the U and V are incorporated intoshell calcite in proportion to their seawater con-centration, both with partition coefficients ofabout 0.01. Down-core records of these elementsare somewhat equivocal as to the extent of sea-water shifts in U and V, partly because foramini-fer U/Ca and V/Ca are subject to post-depositional change.

15.8.4 Strontium isotopes

The ratio of seawater is constantthroughout the ocean because of the 5 My resi-dence time of Sr ( Faure, 1986). But on long timescales, seawater changes, because itreflects shifting balances between the various


source and sinks of dissolved Sr. Over the last24 My (since the late Oligocene), theratio of the oceans, as recorded in foraminifershells and bulk deep-sea carbonates, has risenquite dramatically from about 0.7082 to the pre-sent value of over 0.7091 (Fig. 15.5). The nearlymonotonic rise over the period serves as a usefulstratigraphic tool (DePaolo and Ingram, 1985;Hodell et al., 1991). The cause of this increaseis hypothesized to be changes in the isotopiccomposition and flux of Sr from rivers draininguplifted continental areas such as the Himala-yas, which include rocks enriched in radiogenicSr (high ) (Raymo et al., 1988; Edmond,1992; Raymo and Ruddiman, 1992).

Foraminifer shells contain about 1.4mmol/mol Sr/Ca (Fig. 15.1). Some researchers haveused them exclusively for Sr isotopic work, andothers argue that the same results can beachieved using bulk carbonate (Richter andDePaolo, 1988). Because all of the Sr in foramin-ifer shells is precipitated from seawater, andbecause these shells are likely to be less proneto diagenesis than the finer carbonate fraction,

it seems prudent to use foraminifer shells for Srisotopic work.

15.8.5 Neodymium isotopes

In contrast to Sr, Nd is particle reactive and hasa low seawater concentration

and a relatively short residence time(Bruland, 1983). The ratio of sea-water varies from about 0.5120 in the Atlant icOcean to 0.5125 in the Pacific Ocean (Faure,1986). This difference arises because averagecontinental rocks are depleted, whereas oceanic-basalts are enriched, in The Atlan-tic Ocean derives its Nd from the many riversdraining a dominantly continental terrain (forexample the Amazon, Congo, and Mississippi).The Pacific derives its Nd from far fewer majorrivers, which drain a dominantly basalt terrain,and from interaction with the great ridges ofyoung basalt that characterize the Pacific basin.

Nd might be incorporated into Foraminiferavia solid solution, although is isomor-phous with aragonite rather than calcite (Speer,

New frontiers in trace element paleoceanography 275

1983). There have been a number of efforts touse the isotopic composition of foraminiferal Ndas a recorder of shifts in weathering patterns(Palmer and Elderfield, 1986). Because Nd hasa strong affinity for the Mn and Fe oxide phasesthat coat shells, it is very difficult to be certainthat the measured Nd actually comes from shellcalcite (Palmer, 1985; Palmer and Elderfield,1986).

These are proxies that reveal information aboutthe post-depositional history of foraminifershells. Although diagenetic proxies do not pro-vide primary information about past environ-ments, they are a critical source of informationabout the long-term integrity of the primarychemical signal encoded in shells. Mn is themost important of the diagenetic proxies,because in most environments its presenceabove background levels indicates that Mn hasbeen added to the shells by secondary precipita-tion. The physical proxies Mg, Sr, and F alsoappear to reflect aspects of the diagenetic historyof foraminifer shells. In the context of usingthese elements as recorders of physical parame-ters, it is imperative that researchers separatethe influence of primary and secondary factorson shell composition.

followed by precipitation of (Boyle,1983). Mn-carbonate is less soluble than calcite,and therefore the coatings cannot be easily sepa-rated from primary shell material. Mn-carbon-ate coatings are distinct from the Mn-oxidecoatings which are far more common but canbe removed by chemical reduction dur ingsample preparation (Boyle, 1981). Mn-carbon-ate coatings either contain or t rap high levels ofcertain trace elements such as Cd and Ba. Anadditional complication is that in fauna l benthicForaminifera incorporate pore water Mn intotheir shells, and pore water levels can vary bytwo orders of magnitude ( M a r t i n et al., 1996).

precipitates appear to be ubiquitousin deep-sea cores, and in some oceanic regionsit is difficult to find a site in which shells arenot coated by precipitates. Researchers disagreein their definit ion of what is considered anacceptable level of shell Mn/Ca, from as low as50 to as high as > 150(Boyle, 1983; Boyle and Keigwin, 1985/1986;Delaney, 1990; Ohkouchi et al., 1994). With theexception of in faunal benthic Foraminifera, pri-mary shell material has < 1 Mn/Ca.Because Mn-carbonate shell coatings are a criti-cal l imi t ing factor for foraminiferal trace ele-ment proxies like Cd, investigations of how Mn-carbonate forms, w h y it appears to be precipi-tated heterogeneously between various foramin-ifer species, and how coatings might be removedfrom primary shell material wi l l all fur ther fora-miniferal trace element research.

A major issue in the study of any chemical proxyin marine sediments is the extent to which theprimary chemical signature might be altered bypost-depositional processes. One way in whichthis might happen is the precipitation of second-ary coatings on shells. An example of such coat-ings is Mn-carbonate, a mineral tha t forms inthe reducing conditions typical of ocean-floorsediments. Under the suboxic conditions tha ttypically underlie productive oceanic regions,solid phase Mn is mobilized and released intopore waters by reduction to which is

Geochemists undoubtedly wi l l continue tosearch for new foraminiferal trace element prox-ies. Most of the trace elements tha t would beexpected to substi tute in foraminifer shells atmeasurable concentrations have already beenstudied (Table 15.1). The prime remaining can-didate is the transit ion metal Zn. Seawater Znis a nutrient proxy somewhat intermediatebetween Cd and Ba, and it shows a strong oce-anic association with silicic acid (Bruland, 1983).

15.9 DIAGENETIC PROXIES

15.9.1

15.9.2 Manganese 15.10 NEW FRONTIERS IN TRACEELEMENT PALEOCEANOGRAPHY


This association suggests that Zn might be aunique candidate for the reconstruction of silicicacid concentrations in past surface waters. Znalso forms a solid solution in the calcite series(Reeder, 1983). The biggest potential drawbackto utilizing foraminiferal Zn is that it is highlycontamination prone (Boyle, 1981). Othertrace elements that might be worthy of investiga-tion in Foraminifera include:

( 1 ) Na and K, and possibly Rb and Cs, whichare conservative alkali metals that could possi-bly serve as physical proxies. Levels of Na inforaminifer shells are about 5 mmol/mol, but aspecific control has not been demonstrated(Bender et al., 1975; Delaney et al., 1985).

(2 ) Fe, Co, Ni, Cu, and Ag are all transitionmetals which are possible nutr ient and/or par-ticle-reactivity proxies (Bruland, 1983; Martinet al., 1983; Martin and Gordon, 1988). Shell-bound Fe will be extremely diff icult to deter-mine, because of contamination from Fe bearingoxides and clays (Boyle, 1981). Both Co and Agare present at in seawaterand will be consequently very low in foramini-fer shells.

(3) REE, the rare earth elements includingLa, Ce, Nd, Sm, Eu, and Yb, might be useful asseawater chemistry and particle-reactivity prox-ies (Elderfield and Greaves, 1982; de Baar et al.,1985).Preliminary researchsuggests that it isdifficult to separate shell bound REE fromoxide-bound REE (Palmer, 1985).

Much of the research on nutr ient proxies likeBa and Cd has focused on deep-water benthicForaminifera, because of the interest in estab-lishing changes in abyssal flow. The applicationof trace elements to the study of thermoclineand upper intermediate waters is a relativelynew, uncharted area (Rosenthal et al., 1997b;Marchitto et al., 1998). There are other impor-tant questions that might be answered usingnutrient proxies in planktonic Foraminifera. Cd,in particular, appears to be a promising tool tocharacterize changes in nutr ient supply andutilization in surface waters. Ba might be a sensi-tive tracer of riverine and melt water discharge.

Another frontier is the application of traceelements to studies of anthropogenic perturba-

tion. It has already been demonstrated thatHolocene shallow-water benthic Foraminiferarecord changing seawater Cd due to upwel l ingand pol lut ion (van Geen et al., 1992; v a n Geenand Husby, 1996). It should be possible to usethis technique to demonstrate changes in coastalwaters in response to pol lut ion.

Finally, the application of foraminiferal traceelements to longer, mil l ion year time scales hasso far been limited to only a handful of records(Graham et al., 1982; Delaney and Boyle, 1986,1987; Delaney, 1990). Elements present at t r u l ytrace concentrations, such as Cd, wi l l be neces-sarily more difficult to study on these time scales,because the potential for diagenetic addition ishigh. But minor elements such as Mg and Sr,which might be less prone to diagenetic alter-ation, offer the potential to investigate someimportant problems, including the evolut ion ofseawater temperatures and chemistry in theTertiary.

15.11 SUMMARY AND CONCLUSIONS

Trace elements in foraminifer shells are con-trolled by seawater composition and thephysical and biological conditions dur ing calci-fication. Because it is possible to calibrate shellcomposition against the controlling factors,foraminiferal trace elements provide researcherswith a toolbox of powerful proxies to investigatethe chemical, physical, and biological evolutionof the oceans. Some of the most important chal-lenges faced by trace element researchers are to(1) establish precise relationships among shellchemistry, seawater composition, and physicaland biological factors; ( 2 ) to apply elementaltracers to the past and take into account therange of potential complications that affectproxy interpretation; and (3) to establish whichsecondary factors such as diagenesis may affectpost-depositional shell chemistry. With a preciseknowledge of the factors that control shell com-position, and in conjunction wi th stable iso-topes, foraminiferal trace elements shouldprovide a very powerful tool to study ocean andclimate evolut ion.

Acknowledgments 277


I thank Ed Boyle, MIT, for introducing me tothe foraminiferal trace element field. Thanks goto Pam Martin, Lui Chan, and Jeff Hanor forcomments and suggestions on the manuscript,to Tamara Garcia for organizing references, andto Mary Lee Eggart for improving the figures.

The work and ideas of collaborators and stu-dents, especially Howie Spero, Glen Shen, YairRosenthal, Harry Elderfield, Pamela Martin,and Tracy Mashiotta have greatly contributedto my understanding of trace elements in Fora-minifera. NSF and NOAA support has beencritical in providing the resources for myresearch in this field.


PART IV:PRESERVATION

OF RECORD


16Taphonomy and temporal

resolution of foraminiferalassemblages

Ronald E. Martin

16.1 INTRODUCTION

The surface mixed layer of sediment, whichranges in thickness from a few centimeters to asmuch as a meter, acts as a low-pass filter thatdamps high frequency signals before their incor-poration into the historical record. This damp-ing mechanism is referred to as time-averaging,which is the process by which fossils of differentages are mixed into a single assemblage. Becauseof time-averaging, a fossil assemblage representsa minimal duration of (at best) a few decades,and more likely hundreds to thousands of years,unless the assemblage is rapidly preserved byunusual conditions ( Lagerstätten). Time-averag-ing occurs because the generation times oforganisms are inherently much shorter than netrates of sediment accumulation and burial (Kid-well, 1993). The mixed layer is also a taphonom-ically active zone (Davies et al., 1989) in whichstratigraphic signals are damped by biologicalmixing (bioturbation) and dissolution.

This chapter reviews what little is reallyknown about the taphonomy and temporalresolution of foraminiferal assemblages in major

depositional settings. Although post-mortemtransportation of tests has been demonstratedto vary with respect to such factors as test size,shape, and density (e.g. Kontrovitz et al., 1978,1979; Zhang et al., 1993), studies of assemblagessuggest that little post-mortem transport ofForaminifera normally occurs (e.g. Snyder et al.,1990a,b). Therefore, the effects of bioturbationand dissolution on the formation of foramini-feral assemblages are emphasized.

16.2 BIOTURBATION: TEMPORALRESOLUTION AND PORE WATERCHEMISTRY

The most popular bioturbation models arebased on the concept of diffusion (see Matisoff,1982; Cutler, 1993; Martin, 1993, for reviews).Diffusion-based models assume that mixing is arandom redistribution of sediment particles bylarge numbers of organisms over many indivi-dual transport events, and that, taken collec-tively, small transport events move particlesover large distances ( M a r t i n , 1998, derives the


282 Taphonomy and temporal resolution of foraminiferal assemblages

relevant equations using a random walk model).The Guinasso-Schink (1975) model, in particu-lar, may be reduced to a dimensionless parame-ter (G ) that represents the ratio of bioturbation(‘biodiffusion’) rate (D) , sedimentation rate (v ) ,and mixed layer thickness (m):

Reported biodiffusion coefficients vary by aboutsix orders of magnitude and decrease from shal-low water to the deep sea

Matisoff, 1982; biodiffu-sion coefficients are also often stated in terms ofthousands of years). Biodiffusion coefficientsalso typically decrease with depth, even withinthe same environment (Fig. 16.1;Aller and

Cochran, 1976; Benninger et al., 1979; Benoitet al., 1979; Cochran and Aller, 1979).

Equation ( 1 ) has been criticized on a numberof grounds. For example, according to the equa-tion, a thick mixed layer should result in abetter-preserved signal than a smeared one(Wheatcroft, 1990; Wheatcroft et al., 1990; seeMartin, 1998, for review of other criticisms).Nevertheless, G is heuristically useful in under-standing the interplay of bioturbation and sedi-mentation rates and mixed layer thickness ingenerating a stratigraphic signal. When G issmall ( rapid v or slow mixing), an impulsetracer (such as a microtektite or volcanic ashlayer) is transferred through the mixed layerbefore it can be extensively re-worked, andits concentration profile is bell-shaped or‘Gaussian’ (Fig. 16.2). When G is large ( slowv or rapid mixing) , the tracer exhibits an expo-nential decrease upward and a nearly uniformdistribution in the mixed layer (Fig. 16.2).

Under conditions of a th in mixed layerand rapid bioturbation, equation

( 1 ) reduces to a box model, in which tracers areassumed to be rapidly and homogeneously dis-tributed in the mixed layer ( Figures 16.1, 16.2),an assumption that is often unjustified (Bergeret al., 1979). The most frequently cited boxmodel is that of Berger and Heath (1968):

where P = probability of f inding a particle inthe mixed layer, L = thickness of sedimentdeposited on the layer, and m = mixed layerthickness.

Integrating ( 2 ) results in a decay formula:

Thus, if species z becomes extinct, the distr ibu-tion of the species is given by:

where concentration of z at a dis-tance of m below the level of extinction, and

thickness above (after) theextinction.

According to (4 ) , the concentration of an

Bioturbation: temporal resolution and pore water chemistry 283

extinct species above its true level of extinctiondecreases upward exponentially according to thethickness of sediment deposited after its extinc-tion. Based on equation (4) , Berger and Heath(1968) calculated the proportion of the originalconcentration of a species z at a distanceabove its disappearance. By specifying accept-able levels of reworking (contamination), thelevel of stratigraphic resolution was calculated.In their example, if and contaminant

level (due to reworking) is 10% of the originalconcentration of the species, then the originalextinction level may be as much as 9 cm deeperin the section (Fig. 16.3; see also Fig. 16.4). Fora sedimentation rate of this meansa resolution of 9000 years; for a rate of

a resolution of 2250 years isobtained. According to the model, the exact levelof extinction is indicated when the concentrationof the species is 1/e or 0.37 times its maximum


concentration below, and is independent of themixed layer thickness (Berger and Heath, 1968).Similar models were developed by these authorsfor species appearances: first appearance datums(FADs) tend to be smeared downward muchless than last appearance datums (LADs) aresmeared upward, because bioturbators arelargely confined to the mixed layer, and tend toremain near the sediment-water interface ( S W I )as sediment is deposited at the SWI from thewater column (see also Glass, 1969).

Reworking of substantially older (ca. hundreds-of-thousands to millions-of-years) or youngermicrofossils into younger (or older) sediments by‘leaking’ or ‘piping’ (remanié) is not usually a seri-ous problem, and is all but ignored by biostrati-graphers. In most cases, microfossil-based bio-stratigraphic zonations are sufficiently preciseat such time scales that reworked specimens aretypically recognized by their anomalous strati-graphic occurrence and qualitative state of preser-vation (surface degradation, breakage, i n f i l l i ngwith foreign sediment). Berger and Heath (1968)concluded that bioturbation would not normallybe responsible for such reworking, as the concen-tration of the reworked marker would probablybe on the order of of its original concen-tration when, in their example, the thickness of

sediment separating Recent from older materialwas as little as 1 m. They suggested that erosion isthe dominant process mixing older assemblagesinto younger pelagic sediments. Cutler and Flessa(1990) came to a similar conclusion for shallow-water assemblages: bioturbation is a relativelyinefficient means of producing stratigraphic disor-der, but physical reworking disorders sequencesrapidly.

In the case of ecostratigraphic studies. Bergerand Heath (1968) concluded that serious s t ra t i -graphic errors may occur if the stratigraphic rangeof a species is similar in thickness to the mixedlayer; this is likely to occur in the deep-sea dur ingtimes of climatic fluctuations, when species mayalternately appear and disappear relatively rapidly,leaving sufficient time for substantial biologicalreworking (cf. Fig.16.4d). Such signals are moreeasily deciphered under regimes of higher sedimentaccumulation rates (e.g. Mart in et al., 1993; Mar t inand Fletcher, 1995, for shallow continental slopeof the northeast Gulf of Mexico). On even shortertime scales, size-selective transport of sedimentparticles (e.g. Foraminifera versus coccolithopho-rids, microtektites) back to the SWI by bioturba-tors may produce artifactual peaks (McIntyreet al., 1967; Glass, 1969; Robbins, 1986; Wheatcroftand Jumars, 1987; Wheatcroft, 1992; cf. Ruddimanand Glover, 1972; Ruddiman et al., 1980).

Besides smearing s t ra t igraphic signals, bio-turba t ion also affects pore water chemistryand hardpar t preservation. Typically, beneath asurficial oxidized zone, bioturbat ion oxidizesorganic mat ter and sulfides to produce carbonicand sulfuric acids, respectively (Walter andBurton, 1990):

Conversely, bacterial sulfate reduction increasespore water a l k a l i n i t y ( t o t a l dissolved bicarbon-ate and carbonate ion, and smaller con t r ibu t ionsof other ions such as borate), thereby enhancingshell preservation (Walter and Burton.1990):

Preservation and temporal resolution in marine settings 285

Alkalinity may also increase deeper in the sedi-ment column as a result of other oxidation-reduction reactions involving organic carbonthat use different electron acceptors (see Can-field and Raiswell, 1991, for review).

16.3 PRESERVATION AND TEMPORALRESOLUTION IN MARINE SETTINGS

16.3.1 Carbonate shelves

Large reef-dwelling Foraminifera, such asAmphistegina gibbosa and Archaias angulatus,

often form highly-abraded, current-winnowedlags in shallow-water carbonate environments(Martin, 1986; Martin and Wright, 1988) thatmay dominate assemblages to the point ofobscuring reef zonations (Mar t in and Liddell,1988, 1989, 1991). These and other specieswould therefore be expected to persist in sedi-ment for relatively long periods of time and tobe mixed extensively both upward and down-ward in the mixed layer, which may be up to~ 1 m thick in carbonate sediments (Walter andBurton, 1990).

Kotler et al. (1991, 1992) and Martin andLiddell ( 1 9 9 1 ) conducted laboratory and fieldexperiments that simulated abrasion, dissolu-tion, and bioerosion of common reef foramini-


feral species based on energy conditions anddepositional setting (‘taphofacies’) under whichassemblages form (Liddell et al., 1987; Liddelland Martin, 1989). With the exception of fragilespecies such as Planorbulina acervalis, the Fora-minifera examined were resistant to abrasion.Abrasion-resistant forms varied substantially insusceptibility to dissolution, however: Archaiasangulatus, which is prevalent in back-reef envi-ronments, dissolved rapidly, whereas Amphisteg-ina gibbosa, which characterizes the reef crestand shallow fore reef, dissolved much moreslowly. Differences in dissolution rate probablyresulted from differences in both test architec-ture and mineralogy; tests of Amphistegina gib-bosa and Archaias angulatus are, for example,characterized by 4–5% and 14–16% Mg-calcite,respectively.

Although Kotler et al. (1991, 1992) experi-mentally reproduced some natural abrasion anddissolution-related test surface features, surfacefeatures obtained in bioerosion experiments didnot resemble natural features. This is not to saythat bioerosion does not occur in carbonatesediments, as the process has been documentedin a number of cases. Biological destruction offoraminiferal tests is caused by microbes (e.g.fungi), especially in quiet-water environments,and from selective or indiscriminate ingestion oftests by invertebrates and vertebrates, althoughthe intensity of destruction varies considerably(see Martin and Liddell, 1991, for discussion andreferences). Nevertheless, in studies to date,shells of large taxa, such as bivalves, appear tobe destroyed primarily by bioerosion (Aller,1995; Cutler, 1995), whereas foraminiferal testsare lost primarily to dissolution (Buzas, 1965;Green et al., 1992, 1993b; Martin et al., 1995,1996; Powell et al., 1984 noted similar behaviorfor juvenile molluscs).

Based on the slow rates of experimental testdegradation versus the highly degraded natureof many natural tests, Kotler et al. (1991, 1992)and Martin and Liddell ( 1 9 9 1 ) concluded thattest degradation is inhibited in carbonate sedi-ments. Indeed, subsequent radiocarbon datingdemonstrated that pristine to highly degradedtests of Amphistegina and Archaias from natural

assemblages range from modern to > 2,000 cal-endar yrs (ages corrected for reservoir and vitaleffects; Martin et al., 1995, 1996). Mixing ofolder material with younger sediment appearsto be extensive in carbonate-rich environmentsbecause high sedimentary levels bufferdissolution and promote time-averaging.Indeed, based on amino acid racemization tech-niques, Murray-Wallace and Belperio (1995)found that the large reef-dwelling foraminiferMarginopora vertebralis was reworked from latePleistocene (ca. 125,000 ka) into modern carbon-ate tidal flat sediments, and that reworked speci-mens (remanié) were indistinguishable frommodern ones.

Kotler et al.’s (1992) results are in markedcontrast to the results of Waller and Burton(1990), who found that red algal ( 1 8 mol%Mg-calcite), echinoid ( 12 mol% Mg), and coral(aragonite) substrates dissolved relativelyrapidly in field experiments. The carbonate sub-strates utilized by Walter and Burton (1990)would appear to be far more reactive, however,than Foraminifera (Kot l e r et al., 1992). Thus,differential solubility of carbonate particles incarbonate environments probably results notonly from differences in mineralogy, but alsofrom differences in ( 1 ) substrate size, shape, andsurface area (surface/volume ratio; relativelyhigh in red algae, low in Foraminifera), ( 2 )organic matter content, and ( 3 ) microstructure(‘Sorby Principle’; Folk and Robles, 1964).

16.3.2 Siliciclastic tidal flats

It is almost axiomatic in taphonomy that, ingeneral, the bigger the shell, the longer it lasts(depending on mineralogy, microstructure. etc.).One deduction from this tenet is that big shellsshould be older, and should appear older, thansmall shells from the same horizon. Macrofossilassemblages should therefore exhibi t muchgreater variation in the durat ions of time-aver-aging than microfossil assemblages from thesame deposit (Martin and Liddell, 1991; Martin,1993; Kowalewski, 1997). Comparison of time-averaging of hardparts belonging to differenttaxa bears on such crucial topics as dist inguish-


ing reworking from survivorship across extinc-tion horizons (Signor-Lipps effect; Signor andLipps, 1982; Flessa, 1990; Meldahl, 1990; Mac-Leod and Huber, 1996), and biostratigraphiczonations based on different taxa that are usedto assess the rates and mechanisms of extinction.

Martin et al. (1995, 1996) tested the abovehypotheses by comparing the state of preserva-tion (taphonomic grade) and age of Chione(bivalve) and foraminiferal tests from Holocenetidal flats of Bahia la Choya, Mexico (northernGulf of California). They found that hardpartsize and taphonomic grade are not infallibleindicators of shell age, preservability, or tempo-ral resolution of fossil assemblages, as did Flessaet al. (1993; contrary to Brett and Baird, 1986;Brandt, 1989). Disarticulated Chione collectedfrom the SWI exhibited an age range of severalhundred years to ~80–125 Ka based on Accel-erator Mass Spectrometer ( A M S ) dates andamino acid racemization (D-Alloisoleucine/L-Isoleucine) values, and old (or young) valvesranged from highly altered to virtually pristine.Their age range is much greater than thatreported by Flessa et al. (1993) from the samearea (see also Wehmiller et al., 1995; Flessa andKowalewski, 1994).

Foraminiferal tests at Choya Bay were sur-prisingly old (up to ~2,000 calendar years),despite their pristine appearance, which sug-gested a young age (Martin et al., 1995, 1996;dated tests consisted of Buccella mansfieldi andElphidium cf. E. crispum). The substantial agedifferences between bivalves and Foraminiferahinted that the means of test preservationdiffered from that of bivalves. Foraminiferareproduced in discrete ( ~a few weeks) seasonalpulses, which were followed by periods ofintense dissolution of several months durationrelated to low sediment accumulation rates

Flessa et al., 1993) and inten-sive bioturbation (oxidation of organic matterand sulfides to produce carbonic and sulfuricacids, respectively; equations 5 and 6). Aftereach seasonal reproductive pulse ofsome tests are apparently rapidly incorporatedinto a subsurface shell layer (up to ~ 1 m belowthe SWI) by Conveyor Belt Deposit Feeders

(CDFs; van Straaten, 1952; Rhoads and Stanley,1965; Meldahl, 1987) and preserved there, as therest of the pulse quickly dissolves. Ultimately,some of these older tests, as well as bivalves, areexhumed by CDFs and storms, which biasesassemblages toward ages older than those pre-dicted (cf. Shroba, 1993). Indeed, Meldahl et al.(1997) found that durations of time-averagingof bivalve assemblages decreased to a few hun-dred years in settings of apparently higher sedi-ment accumulation rates elsewhere in the Gulfof California.

At Choya Bay, however, foraminiferal abun-dance tends to increase to the north across theflat, indicating that conditions suitable for testpreservation can vary dramatically over rela-tively short distances. The depth to the subsur-face shell layer shallows northward from> 60 cm on the southern flat to ~10 cm in someplaces over a Pleistocene outcrop. Burrow densi-ties (estimated visually) also tend to decrease tothe north, especially when sediment thickness is

The shallowness of the Pleistoceneplatform on the northern margin of the bayapparently inhibits the intensity of bioturbation(i.e. bioturbators cannot burrow to their pre-ferred habitat depth), and this allows alkalinityto build-up via sulfate reduction, especially inthe summer (see seasonal geochemical data inMartin et al., 1995).

16.3.3 Marshes

Not surprisingly, marshes and other coastalenvironments have received considerable scru-tiny from sedimentologists, stratigraphers, andgeomorphologists because of their accessibility,their ecological and economic importance, andtheir sensitivity to sea-level change, especially inlight of natural Holocene sea-level rise that isconfounded with apparent anthropogenic globalwarming. Foraminifera have been used toreconstruct high-frequency (decadal to millen-ial) , low amplitude ( < 1 0 m ) changes of Holo-cene sea level to ±5–10 cm (Scott, 1976a; Scottand Medioli, 1978, 1980a, 1986; Williams, 1989,1994; Thomas and Varekamp, 1991; Varekampet al., 1992; Gehrels, 1994; Nydick et al., 1995;


Varekamp and Thomas, 1998; see also chap-ter 9). This resolution surpasses that of (1)marsh plants (e.g. Spartina alterniflora;Goldstein, 1988b; Gehrels, 1994), which exhibi tcoarser zonations and may decay beyondrecognition; ( 2 ) the Holocene portion of themarine oxygen isotope curve; and ( 3 ) coral reefterraces (e.g. Wheeler and Aharon, 1991).

Marshes would appear to exhibi t in t r ins ica l lyhigh temporal resolution. Bioturbat ion in saltmarshes ‘does not constantly churn sedimentsas is commonly the case in shallow subtidalsettings’ (Goldstein etal., 1996, p. 11) because,although dense halophyte roots pump oxygeninto surficial sediment (which would ordinari lypromote bioturbation), they also impede biotur-bation by crabs, insects, and polychaetes ( Basanand Frey, 1977; Frey and Basan, 1981; Howardand Frey, 1985; Sharma et al., 1987; Nydicket al., 1995). Bioturbation in marshes is alsocounteracted by high rates of sedimentation (e.g.Sharma et al., 1987; Fletcher et al., 1992; Nydicket al., 1995), which should decrease a t ten tua t ionof stratigraphic signals by rapidly transmittingsignals through the mixed layer (Fig. 16.2). Forexample, assuming (cf.equation ( 1 ) ; e.g. Church et al., 1981, 1987;Krishnaswami et al., 1980; Sharma et al., 1987;Luther et al., 1991), the transit time through themixed layer is only ~40– 60 years, whichsurpasses the of ~2,000–5,000 years formany deep-sea cores

used in ‘high-resolution’ paleoclimatestudies (Schiffelbein, 1985, 1986). Rates of bio-turbat ion in marshes and mixed layer thicknesstend to increase into the lower marsh, however,as subtidal settings are approached.

Hippensteel and Mar t in (1999) conducted astudy of temporal resolution in South Carolina(Folly Beach) marshes and back-barrier over-wash fans based on the Guinasso-Schink ( 1 9 7 5 )model (equation ( 1 ) ) . Using deep-sea microtek-tite (tracer) concentration profiles. Officer andLynch (1983) solved for G:

where and are the slopes (fitted by leastsquares) of the base and upwardly-smeared por-tions ofthe tracer layer, respectively (cf. Figures16.2, 16.4); i.e. the vertical concentration gradi-ent. Hippensteel and M a r t i n (1999) calculated

and from the slopes of the base andupwardly bioturbated portions of washoversfans ( ~ 2 5 c m in thickness); these fans wereenriched in Oligo-Miocene Foraminifera ( t rac-ers) that had been eroded from subtidal offshoreoutcrops by storms and redeposited in back-barrier marshes. Using equation ( 1 ) , and assum-ing and (Sharmaet al., 1987), Hippensteel (1995) calculated anaverage D of

Confidence In te rva l ) fora high marsh site ( n = 2 washovers). At two siteslocated at the high marsh-low marsh boundary,average D was and

respectively; (n = 3) for each site). Fora streamside site, D was

(n = 3). Theserates correspond to observed burrow densitiesin the marsh. Low and intermedia te marsh bio-turbation rates fall at the low end of the rangefor intertidal-shallow subtidal environmentssuch as Long Island Sound

Matisoff, 1982). whereas high marshvalues approach low deep-sea rates

Matisoff, 1982), which argues forexcellent temporal resolution (low signal attenu-ation) in marsh sediments.

Hippensteel ( 1 9 9 5 ) also restored washoverevents to their presumed original levels. Theoriginal da tum can be restored from theobserved tracer (Oligo-Miocene Foraminifera)peak by

(Officer and Lynch, 1983; see also Officer, 1982;Officer and Lynch. 1982). Using equations (8)and (9). Hippensteel (1995) calculated displace-ments and corresponding temporal offsets ofwashovers that generally agree with the trend

and


of increasing bioturbation from high to lowmarsh. For a high marsh site, he calculated adisplacement of 5–13 cm and a temporal offsetof 28–65 years for n = 2 washovers. For twosites at the high–low marsh boundary, displace-ments and temporal offsets were 7–34 cm and~40–170 years, respectively (total n = 6), butfor a stream-side site only 0.4–14 cm and2–68 years (n = 3). These values again indicateresolution that potentially surpasses that ofdeep-sea cores.

Much of the dynamics of formation of marshforaminiferal assemblages has been overlooked,however (Jonasson and Patterson. 1992;Goldstein and Harben, 1993; Hoge, 1994, 1995;Goldstein et al., 1996). Differential preservationof foraminiferal assemblages can, for example,mimic the magnitude and frequency of sea-levelchange determined from foraminiferal assem-blages (Fig. 16.5). As van de Plassche (1991,

p. 176) warns, ‘until … higher age and depthresolution is obtained, the precise relationbetween the nature and magnitude of … low-amplitude sea-level movements … and causesand effects of climate change … remainsunknown.’ Alteration of surface assemblages iscritical because marsh zonations, and corre-sponding inferences about sea level, are recog-nized downcore primarily using either relative(%) or absolute (number of tests sedi-ment) abundances of key species. In lowmarshes, fragile agglutinated (e.g. Ammotiumsalsum, Miliammina f u s c a ) and calcareous (e.g.Ammonia beccarii) Foraminifera are often lostvia oxidation of organic test cements and dis-solution, respectively, so that the fossil assem-blage may be dominated by typical high marsh,robust agglutinated species (such as Jadamminamacrescens and Trochaminna inflata) that com-prised much smaller proportions of the original


living assemblage at the SWI (Jonasson andPatterson, 1992; Goldstein and Harben, 1993;Patterson et al., 1994; Goldstein et al., 1996;Fig. 16.5; cf. Scott and Medioli, 1980b). Anumber of sea-level curves are in fact based onabundance changes of J. macrescens and otherrobust species. The lack of Foraminifera in high-est high marsh and non-marine sediments hasalso been widely employed as a sea level indica-tor, but this condition does not necessarily implya non-marine origin. Test loss in the high marshno doubt also occurs during early diagenesis,just as in the low marsh. Although not yet inves-tigated for Foraminifera, differential preserva-tion of marsh assemblages may also varyaccording to latitude because of differences inmetabolizability of organic matter (Reaves,1986).

Differential preservation of infaunal speciesmay also affect the formation of marsh assem-blages and, potentially, sea-level interpretations.Goldstein and Harben (1993; see also Goldstein,1988b; Goldstein et al., 1996) found that theabundance of the common marsh species Areno-parrella mexicana changed from ~5% at thesurface to ~50% within the top 3–5 cm of sedi-ment because of large infaunal populations. Thisspecies, which may live to depths of ~30 cmand ‘bypass’ the mixed layer, is resistant todegradation and may dominate high marshdeath assemblages despite small livingpopulations.

16.3.4 Offshore shelf and slope environments

Gradients in water energy and surface produc-tivity ( and organic carbon) and oxygenavailability occur across the shelf and into slopeenvironments (Fig. 16.6; Berger and Killingley,1982; Ekdale et al., 1984). Nevertheless, just asin shallow-water settings, sedimentation rate,which decreases with water depth, may be theoverriding factor in the formation and time-averaging of microfossil assemblages in shelf andslope settings. Lin and Morse (1991) concludedthat off the Mississippi Delta and Texas–Louisi-ana shelf, for example, rates of sulfate reduction(and alkalinity generation; cf. equation ( 7 ) ) and

pyrite concentration generally decrease expo-nentially wi th increasing water depth, al l ofwhich reflect decreasing sedimentation rates( L i n and Morse, 1991; Loubere et al., 1993a,b;Middleburg et al., 1997). Sulfate reduction ratesin this region are intermediate between those ofshallow nearshore organic carbon-rich sedi-ments and carbon-poor deep-sea sediments(Canfield, 1991; euxinic basins are an exception;e.g. Berger and Soutar, 1970; see also Canfieldand Raiswell, 1991). At high sedimentationrates, labile organic matter undergoes a shorterperiod of oxic and suboxic degradation beforeit is incorporated into subsurface layers whereit can support sulfate reduction (Canfield, 1991;Lin and Morse, 1991). The decline in sulfatereduction rates across the shelf and slope, andespecially beyond the shelf-slope break, may berelated not only to a decline in sedimentationrates in deeper settings (Nozaki et al., 1977;Carpenter et al., 1982; Smith and Schafer, 1984)but also to decreased surface water productivi ty,as a commonly-observed peak in foraminiferal(benthic and planktonic) abundance occurs nearthe continental shelf edge (e.g. Bandy, 1953). Asrates of sulfate reduction decline across the shelfand slope (Lin and Morse, 1991), rates of biotur-bation must either decline or be counteractedby increased input of or sediment forgood preservation to occur.

In the case of microfossils, the exact relation-ships between sedimentation, shell inpu t , sulfatereduction, etc., and the formation of foramini-feral assemblages on the deeper shelf have onlyrecently begun to be explored in detail. Douglaset al. (1980) concluded that life and death assem-blages of the upper slope (100–400m) of thesouthern California borderland are stronglysimilar (based on surface samples), but Loubereand Gary (1990; see also Loubere et al., 1993a,b)concluded that there was substantial specimenloss in the upper 10 cm of boxcores from off theMississippi Delta and the western Gulf ofMexico continental slope. Denne and Sen Gupta(1989) came to similar conclusions for Texas–Louisiana slope assemblages: they found thatbathyal calcareous species could be groupedinto those that are well-preserved (increasing



downcore), moderately preserved (no t rend) ,and poorly preserved (decreasing downcore).Agglutinated species were either resistant to dis-aggregation (no trend) or disaggregation-prone(decreasing downcore; see also Smith, 1987;Murray, 1989).

Benthic Foraminifera in slope and deep-seaenvironments also frequently exhibit depthstrat if ication and microhabitat preferences tha treflect changes in surface productivi ty, organiccarbon inf lux, and pore water oxygen content(Corliss, 1985; Loubere et al., 1993a,b; Rathburnand Miao, 1995). Depth s t ra t i f i ca t ion mayrepresent a s i tuat ion analogous to i n f a u n a lmacroinvertebrates mixing wi th long dead epi-faunal species (K. Flessa, 1993, personal com-munication); changes in pore water chemistrywi th depth in sediment may also affect stableisotope ratios of tests of foraminifers l iv inginfaunal ly (McCorkle et al., 1990). Corliss andEmerson (1990) concluded that habi tat depthin sediment is related to organic carbon inpu t(which decreases with water depth) and dis-solved oxygen in the pore waters (based ondissolved profiles). Shelf species tend tobe epifaunal (shallow oxic layer), whereas on thecontinental slope and rise, the oxidized surfacelayer is relatively thick and Foraminifera areprimarily deep infaunal species (see also Loubereet al., 1993a).

Unfortunately, because of a paucity of dates,durations of time-averaging of shelf and slopeforaminiferal assemblages must for the presentbe based on the accumulation of macroinverte-brate hardparts (cf. results for Choya Bay).Flessa and Kowalewski (1994; see also Flessa,1993(compiled 734 published radiocarbon dates(many conventional and uncal ibra ted) frommodern nearshore (< 10m) and shelf (> l 0 m )habitats, assuming that the maximum age of ashell serves as an estimate of time-averaging.Deep shelf shells (n = 126 localities total) exhib-ited a bimodal distribution: slightly more than25% (33 localities) fell into the 0 3,000 yearclass, whereas ~25% (31 localities) fell into the9,000–12,000 age class, with a median of9,435 years. Nearly 70% (42 localities) of near-shore shells (66 localities total) fell into the

0–500 year class. The median age of a l l shellswas ~1,255 years. For both deep and shal lowshelves, the number of shells in greater ageclasses declined rapidly toward the m a x i m u mage class of 36,000–39.000 years, which is nearthe upper l i m i t of radiocarbon dating.

Flessa ( 1993) suggested a number of explana-tions for the general increase in duration of time-averaging away from shore (see also Flessa andKowalewski, 1994). Shells may tend to be youn-ger in nearshore settings because of faster ratesof des t ruc t ion (especially via bioerosion but alsobecause of abrasion and f ragmentat ion, and pre-dation); greater sediment accumulat ion rates,which ought to leave younger shells nearer theSWI barring other processes; higher rates ofshell production, which would bias assemblagestoward younger ages; the possible counteract ionof increased sedimentation on bioturbation; andthe Holocene rise in sea level: very old shellsmay not have been able to accumulate in manynearshore settings because sea level reachedwithin ~ 10 m of its present position only~ 7,000 years ago. Thus, the relatively recentrise in sea level may have restricted the potentialdurat ion of time-averaging in nearshore sedi-ments, while shells continued to accumulate f u r -ther offshore.

16.3.5 Deep sea

The onset of dissolution in the deep-seabegins ~0.5–1 km above the lysocline (Emersonand Bender, 1981); the lysocline tends to shallowtoward the continental margins because of oxi-dation of greater amounts of organic mat ter ofboth marine and terrigenous origin (Bé, 1977;Berger, 1977). In the sediment itself, dissolutionis concentrated in the mixed layer (Archer et al.,1989), which is normally on the order of5–10 cm thick.

Much of the work on dissolut ion of calcare-ous hardparts has been on planktonic Foramini-fera because of their use in biostrat igraphic andpaleoceanographic in terpre ta t ion. Douglas(1971) developed a dissolution-susceptible scalefor planktonic Foraminifera (later modified byMalmgren, 1987). Planktonic species that have


somewhat higher Mg test concentrations aremore susceptible to dissolution (Savin andDouglas, 1973; Bender et al., 1975); also, speciesthat are most susceptible to test dissolution tendto settle the most slowly (e.g. Berger, 1967, 1968,1970a, 1971; Parker and Berger, 1971; see Bé,1977, for review). This is because most shallow-dwelling species harbor symbiotic dinoflagel-lates and typically have small thin-walledporous tests in order to remain afloat in thephotic zone (e.g. Globigerinoides ruber), whereasdeeper-dwelling species often have dissolution-resistant features such as thick test walls andrope-like keels that decrease their buoyancy (e.g.Globorotalia menardii). Preferential settling ofcertain species may also affect their dissolutionbehavior: in the case of Globorotalia truncatuli-noides, for example, the exposed cone of the testwas more severely affected by dissolution thanthe flat (spiral surface) in experiments (Bé et al.,1977b). Morphological features may also differin their mineralogy and dissolution susceptibil-ity (Brown and Elderfield, 1996), and sedimentinfilling tends to confine dissolution to the outersurfaces of tests (Hecht et al., 1975; Keir andHurd, 1983).

Although planktonic tests are typically nottransported far as they settle through the watercolumn, they begin to dissolve, especially afterthey have reached the ocean bottom, as a resultof the oxidation of organic matter and sulfides(equations (5) and (6); Adelseck and Berger,1977). Consequently, the number of ‘assem-blages’ present in the plankton may be reducedin number in sediment: Bé and Hutson (1977)found that in the tropical and subtropical IndianOcean six ‘life assemblages’ were reduced to twothanatocoenoses in sediment and that thenumber of species in the sediment assemblageswas greater than in the planktonic assemblages.The apparent sea surface temperature (SST)reflected by the thanatocoenosis may thereforebe inaccurate (e.g. Bé and Hutson, 1977). Leand Thunell (1996) developed a method whichfilters out the effect of differential dissolution onthe calculation of SSTs.

Broecker et al. ( 1991 ) developed a radiocar-bon-based age (mixing) model for deep-sea

assemblages based on the Berger-Heath (1968)approach. This model is based on the assump-tion that dissolution within the mixed layer isproportional to the residence (replacement) timeof biogenic grains within the mixed layer, andthat the age and thickness of the mixed layerreflect the extent of dissolution. Broecker et al.(1991) hypothesized that there are three basicforms of dissolution in the deep sea: ( 1 ) homo-geneous dissolution, in which each grain loses aconstant fraction of its mass per unit time (irre-spective of grain type): homogeneous dissolutionshould shift the mass distribution of assemblagestoward younger grains because the replacementtime of grains in the mixed layer by new grainsfrom the pelagic rain will be reduced; therefore,the greater the extent of homogeneous dissolu-tion, the younger the age (based on dates)of core top assemblages; (2) sequential dissolu-tion, in which grain type A dissolves completelybefore grain type B begins to dissolve, and soon: in this case, core top ages should increasewith the extent of dissolution; and ( 3 ) interfacedissolution of all sediment grains at the SWIbefore burial: like sequential dissolution, inter-face dissolution increases the replacement timeof grains in the mixed layer and thus increasesthe radiocarbon age of the core top.

To determine where in the spectrum dissolu-tion actually occurs, Broecker et al. ( 1 9 9 1 )employed two approaches. One was to comparemixed layer depths calculated from downcoreradiocarbon dates on bulk with thosecalculated from (a) actual core-top ages and (b)Holocene accumulation rates, assuming asteady-state system (based on the Berger-Heathmodel) with no dissolution. In this model, calcu-lated mixed layer thicknesses are proportionalto radiocarbon age. Therefore, to the extent thathomogeneous dissolution has occurred, the cal-culated mixed layer thickness will be smallerthan the measured thickness. The secondapproach was to compare radiocarbon dates oncore tops from a range of water depths (andtherefore range of dissolution), but all collectedwithin a relatively small area so as to minimizevariation in pelagic rain rates of biogenic par-ticles (planktonic Foraminifera, etc.). In the first


test, measured mixed layer thicknesses were lessthan thicknesses calculated from the model (i.e.homogeneous dissolution does not occur). Inthe second test, ages approximate those forsequential or interface dissolution (i.e. ages areolder than those predicted by the model).

Broecker et al. ( 1991 ) concluded, however,that neither interface or sequential dissolutioncould be occurring. They ruled out interfacedissolution because dissolution appears to occurwithin the sediment (Archer et al., 1989), andnot exclusively at the SWI. Sequential dissolu-tion was also ruled out because in the deepestcores (near or below CCD), planktonics areabsent and benthics nearly so (Broecker et al.,1991, table 3); i.e. microfossil componentsappear to be degraded at nearly equal rates.Since homogeneous dissolution also does notappear to occur, these authors sought an expla-nation for core top assemblage ages based onchanges in deep-water ion concentrationthrough time. They suggested that Pacific watersbecame more corrosive, and Atlantic waters lessso, during the last glacial–interglacial transition.Under such conditions, Holocene accumulationrates would have been reduced by chemical ero-sion in the Pacific, thereby increasing the likeli-hood of reworking older (glacial) sediments intothe mixing zone (cf. Berger and Heath model;see also Murray-Wallace and Belperio, 1995).Broecker et al. (1991) determined that radiocar-bon ages for Pacific deep-sea core tops were8,000–10,000 years greater than those for Atlan-tic core tops from comparable depths below thelysocline.

Differential preservation in deep-sea sedi-ments may be more complicated than Broeckeret al. (1991) concluded, however. Dissolution isneither purely homogeneous or sequential: ben-thic Foraminifera tend to be more resistant thanplanktonics (Berger, 1968; Corliss and Honjo,1981; Bé, 1977). The benthic/planktonic ratio,for example, has often been used as an index ofpost-mortem alteration of deep-sea assemblages(Thunell, 1976) and even planktonic tests mayshow differential resistance (Berger, 1968). Ben-thic Foraminifera also differ in their resistanceto dissolution, but the relationship between fora-

miniferal ecology, microstucture, habitat, andpreservation is unclear. Corliss and Honjo(1981), for example, found that the reef-dwellingAmphistegina was much less resistant to dissolu-tion than characteristic bathyal and abyssalspecies, such as Nuttallides umbonifera, whichprefers waters beneath the CCD (Bremer andLohmann, 1982).

Thus, l ike differential preservation of Fora-minifera on shallow shelves, dissolution-resis-tant benthic (or planktonic) Foraminifera mayerroneously increase deep-sea core-top age esti-mates (cf. Rathburn and Miao, 1995). Indeed,all forms that co-occurred in sediment ofBroecker et al.’s ( 1 9 9 1 ) study showed evidenceof partial dissolution. Moreover, DuBois andPrell (1988) found that in the tropical Atlantic,mixed layer ages of sublysocline (> 4400m)cores decreased (by ca. 500–1,000 years) relativeto core tops from above the lysocline. Theyfound that increased weight percent fragmenta-tion and percent resistant planktonics coincidedwith changes in age at this depth. Therefore, insediments below the lysocline, the radiocarbonage structure of the mixed layer in the Atlantic-is opposite to that of the Pacific (see alsoBroecker et al., 1991). Decreased corrosiveness(relative to the Pacific) of overlying waters andhigher carbonate content of sediments haveapparently allowed a type of sequential dissolu-tion to proceed in Atlantic sublysocline environ-ments that produces younger (not older) coretop ages; i.e. old skeletons are removed fasterthan young ones so that mixed layer agesdecrease (DuBois and Prell, 1988). In terms ofmixed layer age, this is just the opposite ofsequential dissolution as defined by Broeckeret al. (1991) . DuBois and Prell (1988) concludedthat in the case of dissolution, the steady-statemodel is inappropriate for calculating temporalresolution and that stratigraphies fromdifferent preservational settings cannot be strictlycompared: although sediment may have the sameradiocarbon age, the proportions of the compo-nents producing that age may not be the sameif the particles have different preservationalhistories.

To complicate matters further, Loubere

Deconvolution: the reconstruction of signal inputs 295

(1989) found that, based on the Berger-Heath(1968) model, significant variation in speciesabundances occur in the mixed layer as a resultof taxon depth stratification. Infaunal taxaincrease non-linearly in abundance with depthto the level of their true habitat, below whichtaxon abundance remains constant, whereas epi-faunal assemblages may be significantly modi-fied. He concluded that the best representationof total taxon abundance occurs at the base ofthe bioturbated zone (see also Denne and SenGupta, 1989; cf. Rathburn and Miao, 1995).

Loubere (1991; see also Loubere, 1997) alsofound that certain deep-sea (East Pacific Rise)Foraminifera respond to surface productivity(organic carbon) gradients. Significantly, somespecies appear to be highly adaptable ( in termsof microhabitat preference and depth stratifica-tion) to changes in food availability and environ-mental conditions (Linke and Lutze, 1993). Atgreat depths, deep-water epifaunal species pre-dominate because organic carbon (food)becomes limiting.

16.4 DECONVOLUTION: THERECONSTRUCTION OF SIGNAL INPUTS

In theory it is possible to reconstruct any inputto the stratigraphic record. Unfortunately, suchapproaches have so far met with only limitedsuccess. A number of attempts have been madeat direct deconvolution (unmixing or ‘unfilter-ing’) of sedimentary signals (e.g. based onthe Berger-Heath and Guinasso-Schink mixingmodels (Berger et al., 1977; Schiffelbein, 1985,1986), but the deconvolution overestimatedmixing intensity and produced artificial over-shoots and offsets, including artificial meltwaterspikes (Jones and Ruddiman, 1982). Christensen(1986) and co-workers (Christensen and Bhunia,1986; Christensen and Goetz, 1987; Christensenand Osuna, 1989; Christensen and Klein, 1991;see also Robbins, 1982) were more successful inreconstructing fluxes of pollutants and radio-tracers in lake sediments using both the Gui-nasso-Schink (1975) and Berger-Heath (1968)mixing models; they assumed that bioturbation

and sedimentation rates are constant and theytreated sediment compaction effects by assum-ing particular porosity profiles. Although theseassumptions appear valid for the thin mixedlayer of lacustrine environments (~5–10cm)where Christensen et al. worked, they do notappear to hold for most marine environments,with the exception of the deep-sea, which is alsotypified by a thin mixed layer.

In response to these difficulties, Bard et al.(1987) developed a technique based on a discret-ized version of the Laplace transform. They firstdeconvolved abundance curves of species ofplanktonic Foraminifera and then the isotopicsignals stored in their shells. Other workers havenoted that even at an abrupt lithologic or paleo-climatic boundary, abundant species above andbelow the boundary that are indicative of cli-mate change are worked upward and downwardacross the boundary (Berger and Heath, 1968;Hutson, 1980; see also Andree et al., 1984;Broecker et al., 1984; Peng and Broecker, 1984;Andree, 1987). In Bard et al.’s (1987) technique,comparison of actual data with unmixed curvesenabled recognition of bioturbation. Neverthe-less, restored signals may be erroneous whenspecies abundances approach zero; the tech-nique also assumes that bioturbation and sedi-mentation rates remain constant (box model ofBerger and Heath, 1968).

Peng et al. (1977, 1979) developed numericalmodels of continuous inputs (as opposed toimpulse signals like those discussed above). Insuch models, the Guinasso-Schink or Berger-Heath models (or modifications thereof) aresolved ‘in reverse’ by specifying various sedi-mentary parameters (e.g. m, v, D) and solvingfor the unknown (e.g. test inputs). Given thespatio-temporal variation in test inputs, how-ever ((Buzas, 1965, 1968, 1969, 1970; Green et al.,1993b; Martin et al., 1995, 1996; see Murray,1991b, for brief review), it is probably best touse averaged inputs (determined from seasonalstudies) in an attempt to smooth data and pre-vent artificial overshoots. Actual test inputs canthen presumably be determined by varying testinputs into the model (while holding otherparameters constant) unt i l preserved concen-


trations predicted by the model are similar tothose sampled in cores.

Although numerical models have the advan-tage of removing amplif icat ion of noise, l ike ana-lytical models, they have the disadvantage ofnot providing unique solutions. In theory,different equations or values of sedimentaryparameters may produce the same result (Bou-dreau, 1986a,b, 1997; Bard et al., 1987) and smallerrors in measurement may swamp the system(Simon, 1986). Considering the difficulties ofanalytical solutions, however, if estimates of sed-imentary parameters (D, m, v) can be reasonablyconstrained, numerical models may provide thegreatest promise for reconstructing stratigraphicsignals. For example, Pizzuto and Schwendt(1997) modeled six thousand years of sedimentaccumulation and autocompaction in a Dela-ware (U.S.A.) marsh using a FORTRAN pro-gram (SQUISH3) based on finite- consolidationstrain theory:

where is the submerged uni t weight ofsediment, G is a finite strain consolidationcoefficient, and z is the volume of solids per unitarea above an arbitrary datum, and

in which and are the void ratios at thebeginning and end of primary consolidation,respectively, and is the effective stress. Themodel was applied to an accumulat ing columnof sediment consisting of sediment layers of spec-ified void ratios deposited at specified timeintervals. Material properties of the sedimentwere determined in i t ia l ly from laboratory andfield studies and rates constrained by radiocar-bon dates. The model was then used to repro-duce the d is t r ibut ion of void ratios w i t h i n avibracore, the actual thicknesses of sedimentaryunits , and the history of elevation changes ofthe SWI that was consistent with both a pre-viously-determined sea-level curve for the Dela-ware coast and the downcore sequence ofpaleoenvironments. According to the model,horizons have been lowered as much as 2.3 m

by autocompaction alone, the rate of wh ich hasranged from one-half to one-third of the rate ofsea-level rise!

16.5 THE CIRCUMVENTION OF TIME-AVERAGING

Methods of minimizing time-averaging are ofcritical importance in the s tudy of paleoclimatesignals preserved in deep-sea cores. Schiffelbein(1984; see also Schiffelbein. 1985, 1986) con-cluded tha t in deep-sea cores wi th sedimentat ionrates of up to 7 cm/ka, high frequency (ca.3,000 yr) signals show severe attenuation. Oneway to accentuate signal-to-noise ratios is to‘slack’ records from dif ferent sites (e.g. Imbrieet al., 1984a).

By contrast, methods of c i rcumvent ing t ime-averaging have received much less a t t en t ion inshallow-shelf settings. McKinney and Frederick(1992; see also McKinney and Allmon. 1995;McKinney, 1996; McKinney et al., 1996) exam-ined patterns of local ext inct ion using the abun-dances of 25 species of benthic Foraminiferacollected at 1 m in terva ls from a single sectionof the Eo-Oligocene Ocala Limestone of north-ern Florida. They analyzed the populat ionabundance fluctuations through time(upsection)using a fractal-based technique called rescaled-range analysis (Sugihara and May, 1990). Thismethod appears to minimize the effects of time-averaging and potential hiatuses (Sadler andStrauss, 1990) because it is fractal-based ( inde-pendent of scale). Let equal the abundanceof a species dur ing a par t icular t ime in t e rva l t,and let represent the normalized devia t ionsof abundance for each tbetween 0 and T or the entire time interval].The rescaled range is then

where Variations in R(T) throughtime are then analyzed with a fractal model

where c is a propor t ional i ty constantand where F = the f rac ta l

Acknowledgments 297

dimension. F = 1 for a straight line and F = 2for a plane; if F = 2, then H = 0.5, which meansthat the plane is ‘filled’ by the curve and repre-sents a random walk (Sugihara and May, 1990).For H = 0.5, the time series ( the collection ofover the entire time interval T) of rescaled abun-dance variations R represents a random walk(Brownian motion) no matter what the scale of

(duration of observation); abundance fluctu-ations show no ‘persistent’ trend in a particulardirection (increase or decrease). As F decreasesfrom 2 to 1, H increases above 0.5, and Rbecomes less-and-less plane-filling (tendingtoward a line). In this case, there is a persistenttrend of increasing variation in abundance atevery scale of There will be ‘higher highs’and ‘lower lows’ because as increases, varia-tion also increases. If, on the other hand, Hdecreases to < 0.5, variation decreases (‘anti-persistent’). McKinney and Frederick (1992)found a significant negative correlation (r =–0.60; p < 0.05) between H of a species and itsstratigraphic range, and concluded that popula-tions with greater abundance fluctuations goextinct sooner than those that maintain rela-tively stable populations.

16.6 CONCLUSIONS

Shells of different taxa may be degraded bydifferent pathways in the same depositional set-ting because of differences in size, mineralogy,microstructure, sedimentation rate, and porewater chemistry. Thus, intui t ively obvious gen-eralizations about taphonomy may be false (e.g.Martin et al., 1996; Martin, 1998). Moreover,most actualistic studies of foraminiferal tapho-nomy have concentrated on shallow-water envi-ronments, no doubt because of their accessibilityand perhaps also funding, whereas much of thefossil record formed in deeper shelf and slopeenvironments. Generalizations based on shal-low-water settings may prove to be inapplicableto deep-water settings.

Some depositional settings are better-suitedfor particular types of investigations than others,depending on the desired scale of temporal reso-

lution (Kowalewski, 1997). Realistically, thebest temporal resolution that can probably beattained in most cases is in the deep sea. whererelatively continuous cores normally provideadequate temporal resolution. But even in thissetting, signals may be damped (Schiffelbein,1984) and the effects of bioturbation and erosionunderestimated (Berger et al., 1979; Martinet al., 1993; Mart in and Fletcher, 1995). On theother hand, sites of rapid burial , such as deltas,may be suitable for paleobiologic investigationson ecologic scales, al though on longer (evolu-tionary-biostratigraphic) scales, the cont inu i tyof section may become an impediment becauseof delta lobe-switching or sea-level change, andmust be evaluated (e.g. Martin et al., 1993;Mart in and Fletcher. 1995).

Although it is viewed negatively by mostworkers, time-averaging is often an advantage,since short-term noise is damped ( Behrensmeyerand Kidwell, 1985). For example, modernmacroinvertebrate death assemblages from soft-bottom habitats are comparable to repeated(and expensive!) biological surveys in assessingthe ‘long-term’ dynamics (hundreds of years) ofbiological communities (Kidwel l and Flessa,1995). Given the sensitivity of Foraminifera toenvironmental change (e.g. Alve, 1995a), micro-paleontology is well-suited to contr ibute to theparadigm shift in the earth sciences fromresource exploitation to resource conservation.But, micropaleontologists must begin to accen-tuate what can be regained from the fossil recordrather than what is lost ( Behrensmeyer and Kid-well, 1985; Mart in, 1991, 1995). They must seekmore quanti tat ive models of the distr ibution andpreservation of microfossils, the reconstructionof the shell original inputs (signals), and theimplications for community homeostasis. Thiswill be no small feat, given the difficultiesencountered so far. but we can only learn bytrying.


The author’s investigations of foraminiferaltaphonomy have been supported by the


National Science Foundation; this support isvery gratefully acknowledged. Barbara Brogedrafted figures and Cheryl Doherty typed por-tions of the manuscript. Scott Hippensteel

kindly produced Fig. 16.5. The manuscript bene-fitted substantially from reviews by LaurieAnderson, Sue Kidwell, Scott Snyder, and BarunSen Gupta.

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General Index

abnormal testschemistry, 232morphology, 226–231, Fig. 13.2pollution as cause, 226–230

abrasion, in taphonomy, 285–286, 292Acadian fauna/province, 99–100adenosine triphosphate, see ATPAdriatic Sea, 204, Table 12.2advection, water, 5, 119, 120, 245agamont, 48, 49, 51, 52, 54, 55, Fig. 3.14Alabama, 150Alaska, 100, 102, 152, 154Aleutian fauna/province, 98, 100alkali metals, 276alkalinity, 127, 131, 134, 171, 247, 260, 269,

284–285, 287, 290ALSCAL, 83alternation of generations, 4, 37, 48–49, 51, 54,

Table 3.1Amazon Shelf, 156amino acid racemization, dating technique, 286, 287anaerobic, 162, 163, 166, 172, 178, 184, 201, 211, 231analysis of variance (ANOVA) , 85angular data, 72anlage, 45, 46, 47, 232, Fig. 3.10anoxia/anoxic, 43, 142, 154, 163, 164, 166, 167, 171,

176, 178, 183, 196, 198, 201–214, 215, 216,Fig. 10.2, Tables 12.1, 12.2

AntarcticBottom Water (AABW), 5, 186

fauna/province, 94, 100seas, 45, 83, 94, 98, 100, 109, 154, 184, 186, 209,

210, 269anthropogenic effects, 137–139, 184, 201, 204, 215,

276, 287, Table 12.2; see also pollutionanti tropicali ty, 117apogamic, 51, 52, Table 3.1apparent oxygen utilization, 253aquaculture, 204

foraminiferal response, 220–222Arabian Sea, 212, 247, Table 12.2aragonite, 4, 15, 17, 19, 22, 32, 33, 58, 59, 65–67,

138, 248, 253, 255, 262, 265, 267, 274, 286aragonitic wall, see wall , aragoniticArctic

fauna/province, 94, 97, 98, 100, Fig. 6.3Ocean, 94, 97, 98, 100, 111, 154, 184

Argentina, 153Atlant ic

Northern Inner Shelf fauna/province, 98, 100,Figs. 6.3, 6.4

Northern Outer Shelf and Slope fauna/province,100, Figs. 6.3, 6.4

Ocean, 5, 94, 97, 98, 100, 102, 109, 111, 116, 117,118, 119, 120, 121, 129, 132, 134, 139, 143,153–154, 155, 182, 183, 186, 188, 192, 195, 218,239, 260, 267, 269, 274, 294, Figs. 11.2, 11.3

Southern Shelf fauna/province, 99, 100, Figs. 6.3,6.4

atmospheric 252

354 GENERAL INDEX

atmospheric vapor, 243–244, Fig. 14.3ATP, 39, 125, 207, 209Australia, 134, 135, 136, 139, 156, 158autogamous, 53, 54

bacteria, 6, 39, 40, 42, 43, 126, 132, 136, 162, 163,168, 172, 174, 177, 178, 1 8 1 , 185, 195, 198, 203,207, 210, 217, 221, 225, 231, Fig. 12.5,Table 12.2

bacterial mat/film, 6, 132, 168–169, 203, 207Bahamas, 98, 135, 158Baja California, Table 12.2Baltic Sea, 150barium, 267–269, Figs. 15.1, 15.3, Table 15.1Belau, 130, 133, 135Berger-Heath bioturbation model, see bioturbation,

Berger-Heath (box) modelBermuda, 94bilamellar wall, see wall, bilamellarbinary fission, 51, 52, Table 3.1biodiffusion, 282bioerosion, 285, 286, 292biogeographic province, 5, 6, 96, 153–154biogeography, 93–102, 103–122, Figs. 6.1–6.4, 7.3,

7.4, 7.6bioturbation, 164, 171, 172, 174, 178, 209, 281–285,

287, 288, 289, 290, 292, 295, 297analytical versus numerical models, 295–296Berger-Heath (box) model, 282–284, 293, 294, 295Guinasso-Schink model, 282, 288, 295pore-water chemistry, 284–285, 292size-selective feeding, 284

bipolarity, 117birds, transport by, 152–153Black Sea, 108, 152, 218, 223, 226, 231, Fig. 9.5boron, 273, Fig. 15.1, Table 15.1Brazil, 148, 150, 153, 156, 157British Columbia, 146budding, 51, 52, Table 3.1

and plants, 252cadmium, 259, 260, 266–267, Figs. 15.1–15.3,

Table 15.1calcification, 44, 45–48, 58, 59, 67, 124, 126–129,

134, 135, 137, 139, 176, 177, 228, 230, 231, 232,234, 247, 248, 253, 254, 256, 257, 260–261, 262,270, 276

calcitedissolution, 33, 104, 106, 129, 137, 186, 215, 221,

226, 267, 269, 285–286, 287, 289, 292–295gametogenic, 247high-Mg, 19, 22, 27, 33, 58, 131, 134, Fig. 2.8

incorporation of trace elements, 261–264spicules, 15, 19, 22, 28, 33, 57–58, Figs. 2.9, 4.1

calcium, 259, 261–262, Fig. 15.1, Table 15.1California, 149

borderland basins, Table 12.2continental slope, Table 12.2

Californian fauna/province, 98, Fig. 6.3Cambrian, 3, 33, 37Canada, 146, 149, 154, 156, 184, 221canal system, 32, 61, 63, 64, 65, 131, 132, 133, Figs.

4.6, 4.11, 4.15Cape Hatteras, faunal boundary, 153–154carbon cycle, see global carbon cyclecarbon isotopes, 6, 164 –165, 176–177, 239, 241–242,

248–255, 257, Figs. 14.4–14.6, Tables 14.1, 14.3disequilibrium, 253–254fractionation, 253–255global shifts, 252–253gradients, 249–252

carbon–14 dating, see radiocarbon datingcarbonate ion concentration, 247–248, 255carbonate production, 123, 129, 138Carboniferous, 33Caribbean Sea, 5, 94, 97, 98, 105, 129, 130, 131, 132,

133, 134–135, 136, 155, 156, 157, 218, Table 8.1carnivory, 39, 42, 44Carolinian fauna/province, 99, Fig. 6.3Caspian Sea, 218, 223catalase, Fig. 12.5Cenozoic, 102, 108, 114, 115, 116–117, 121, 259centers of origin, 100–102Challenger expedition/report, 5, 10, 94chamber formation/construction, 45–48, 57–70,

Figs. 3.10, 4.1–4.17chamber wall, see wallChesapeake Bay, 149, 158, 204China, 134chloroplast, 43, 45, 123, 139, 210–211, Figs. 8.2, 12.5classification, 7–36, Figs. 2.1–2.11, Tables 2.1–2.3

by Brady, 10by Carpenter et al., 10by Cushman, 1 1 – 1 4by d'Orbigny, 7, 10, 18by Galloway, 11by Haynes, Table 2.2by Jones, 10by Lee, Table 2.2by Lister, 10by Loeblich and Tappan, 14, 15–19, Fig. 2.7,

Table 2.2by Rauzer-Chernousova and Fursenko, 15by Reiss, 15

GENERAL INDEX

by Reuss, 10revised (Loeblich and Tappan), 16–33, Figs. 2.8,

2.9, Table 2.2clathrates, 248, 258cluster analysis (CA), 74–77, 80, 96, 97, Fig. 5.1

atmospheric, 252metabolic, 246, 254, 255

coal and fuel ash pollution, foraminiferal response,225

coastal marsh, see salt marshcoccolithophorids, 284coefficient, 76, 77, 84, 85cold-water benthic faunas, 94, Figs. 6.1, 6.2Colombia, 148communalities, 80compaction of sediments, 295, 296competition, 172–174, 197Connecticut, 147conservative elements, 260–261copper, 276, Fig. 15.1, Table 15.1coral reefs, 133, 138, 139, 156–157Cortez fauna/province, 98Cretaceous, 17, 19, 27, 32, 33, 102, 114, 121currents, effect on latitudinal provinces, 112, 119cyst, 39, 40, 42, 45, 46, 47, 209cytology, effect of pollution, 230–231, 232–234

gradients, 249–252data transformation, types of, Table 5.1deconvolution, sedimentary signals, 295–296deep-water age, 251–252deformity, pollution as cause, see abnormal tests,

pollution as a causedendrogram, 74, 76, 77, Fig. 5.1deposit feeding, 39, 42depth distribution/zonation, 4, 97, 100, 109–111,

114, 130, 131–135, 153–155, 156, 157, 183, 185,196, 247, 255

diatom, 40, 42, 43, 44, 123, 124, 130, 134, 142, 171,223, 225

dimorphism, 4, 48, 51, 54, 55, Table 3.1; see alsoalternation of generations

dinoflagellates, 123, 136–137, Figs. 8.2, 8.3diploid, 48, 51discriminant function analysis (DFA), 83–84, 192,

Figs. 5.7, 11.6, Table 5.4dispersal, 100–102, 117, 134, 152–153, 157, 158dissolved organic carbon (DOC), 39, 43Drammensfjord, Table 12.2dredging, foraminiferal response, 225–226dvsaerobic, 202

dysoxia/dysoxic, 171, 177, 178, 202–209, 211–216,Fig. 10.2, Tables 12.1, 12.2

East African fauna/province, 94East Indian fauna/province, 94ecotone, p lanktonic , 119Ecuador, 148eigenvalue, 77, 78, 79, 82, Table 5.2eigenvector, 77–82, 83Elphidium-Ammonia association, 155El Salvador, Table 12.2encystment, see cystendemism, 5, 96, 114, Fig. 7.6endoplasmic reticulum, 211, Fig. 12.5English Channel, 154–155Eocene, 33, 59, 138, 296epifluorescence microscopy, 207, Fig. 12.4estuaries and lagoons, 138, 148–153, 183, 212, 214,

218, 219, 221, 223, 224, 226, 228euclidean distance, 76, 77, 83euphotic/photic zone, 39, 42, 43, 45, 108, 109, 110,

124, 130, 132, 133, 161, 181, 182, 197, 211, 293eutrophication, 138, 201, 204, 216, 221evaporation, 242–243, Fig. 14.2extinction, 33, 103, 114, 115, 116, 118, 121, 122, 172,

217, 234, 282–283, 287, 296, 297

355

f rat io, 182factor analysis (FA), 74, 77, 80–82facul tat ive anaerobes, 164, 207–209fer t i l iza t ion , 48, 51, 53, 54, Table 3.1filopodia, 38first appearance da tum ( F A D ) , 284Florida, 94, 98, 135, 138, 139, 148, 158, 186, 296fluoride, 272–273, Fig. 15.1, Table 15.1food supp ly , benthic foraminifers, 1 7 1 – 1 7 2 ,

196–197, Fig. 10.9food vacuole , 39, Figs. 3.4, 3.7food web/chain, 129, 181, 230foraminal plate, 63–65, Fig. 4.12foraminiferal assemblages in sediment, temporal

resolution, 281–298, Figs. 16.1–16.6foraminiferal preservation and temporal resolution

carbonate sediments, 285–286, 294deep sea, 282, 284, 288, 289, 290, 292–295, 296,

297marshes, 287–290, 296, Fig. 16.5shelf and slope, 290–292, 297t ida l flats, 286–287

foraminiferal response to pollution, see pollution,foramini fera l response

fractals, 296; see also rescaled-range ana lys i s

GENERAL INDEX356

France, 222fresh-water Foraminifera, 153Frierfjord, Table 12.2

gamele, 19, 23, 44, 48, 51, 52–53, 54, 55, 247,Table 3.1

amoeboid, 19, 23, 52, 53, 54, Table 3.1biflagellated, 19, 23, 48, 52, 53, 54, Fig. 3.15,

Table 3.1triflagellated, 52, 53, Table 3.1

gametogamous, 48, 52, 53, Table 3.1gamic, 51, 52, Table 3.1gamont, 48, 49, 51, 52, 53, 54, 55, Fig. 3.14,

Table 3.1gamontogamous, 53, 54, Table 3.1gas-hydrates, 248gene flow and planklonic biogeography, 113, 116,

117, 119genotypes, biogeography of, 119Georgia, 72, 87, 145, 146, 147, 155global carbon cycle, 248–249, Figs. 14.4, 14.6global change, 116, 137–139, 287, Fig. 8.5glycolysis, 211glycosaminoglycans, 45, 128Grand Banks, 87, 100granular wall, see wall, granulargranuloreticulopodia, 18, 37; see also reticulopodiagrazing, 39, 40, 43Great Barrier Reef, 156Greece, 222green algae, 123, 134–135, 138growth, 45–48Guinasso-Schink bioturbation model, see

bioturbation, Guinasso-Schink modelGulf of Aqaba, 129–130, 132, 133, 136, 156, 157Gulf of California, 83, 287, Table 12.2Gulf of Maine, 192Gulf of Mexico, 82, 97, 98, 100, 146, 151, 155, 156,

158, 186, 196, 197, 204, 214, 216, 218, 284, 290,Figs. 6.3, 6.4, 12.6, Table 12.2

hydrocarbon seeps. Table 12.2Inner Shelf fauna/province, 98, 100, Figs. 6.3, 6.4Outer Shelf and Slope fauna/province, 100, Figs.

6.3, 6.4Gulf of Trieste, 155

haploid, 49, 51Hawaii, 152heavy metal pollution, foraminiferal response,

223–225heteroscedasticity, 85heterothalamy, 55

historical factors, 94, 1 0 3 – 1 0 4 , 1 0 6 , 1 1 0 , 1 1 3 – 1 1 7 ,120–121

Hudson River estuary, 151hydrocarbon pollution, foraminiferal response,

222–223

hydrocarbon seep/vent, 6, 203, Fig. 12.6, Table 12.2hydrogen sulfide, 152, 161, 203, 207, 209, 210, 211,

215, 223, 231, Fig. 12.3hydrogenosome, 211hydrothermal vent, 6hypersaline environments, 106, 135, 151, 158hypoxic, 202

ice volume, 239, 244–245imperforate wall, see wall, imperforateIndia, 151, 223, 225Indian Ocean, 94, 109–118, 132, 133, 136, 156, 158,

183, 186, 198, 218, 239, 270, 293Indo-Pacific area, 94, 129, 130, 131, 132, 133, 134,

135, 136, 156, Table 8.1inner cont inental shelves, 5, 98, 100, 110, 153–156,

Figs. 6.3, 6.4inner organic l in ing ( I O L ) , 45, 46, Fig. 3.11instar, 62inter locular spaces, 61–63, Figs. 4.7, 4.8Ireland, 94iron, 276, Fig. 15.1, Table 15.1isotope fract ionat ion, 241, 242; see also under

carbon isotopes and oxygen isotopesisotope strat igraphy, 239, Fig. 14.1Israel, 129–130, 132, 133, 136, 156, 157, 184, 221,

225Ita ly , 151, 155, 175, 216, 224, 228iterative evolut ion, 114, 115, 1 2 1

Japan, 153, 156, Table 12.2Jurassic, 19, 32, 66, 117

Kendall’s horseshoe, 78Kriging, 72, 88, 89

lagoons, see estuaries and lagoonslamellar wall , see wal l , lamellarlarger foraminifers, 42, 43, 123, 129–136,137–139,

156, 158, Figs. 8.1, 8.4, 8.5, Table 8.1last appearance datum ( L A D ) , 284life cycle, 38, 48–55, Fig. 3.14, Table 3.1life position, 40, 168–169, 207, Fig. 12.4linear regression, 83lithium, 273, Fig. 15.1, Table 15.1loadings, 77, 78, 79, 80, 83, 86Louisiana, 146, 150, 222, 290, Table 12.2

GENERAL INDEX 357

Lusitanian fauna/province, 94lysocline, 104, 267, 269, 292, 294

macrofaunal province, 98–99Madang Lagoon, 212, 214magnesium, 259, 260, 270–272, Figs. 15.1, 15.4,

Table 15.1Maine, 102, 143, 146, Fig. 9.3manganese, 260, 275, Fig. 15.1, Table 15.1mangrove swamps, 148, Fig. 9.1marginal marine environments, 141–159, Figs.

9.1–9.6, Table 9.1marsh, see salt marshMassachusetts, 143–145, 146mating types, 54McMurdo Sound, 154, Table 12.2Mediterranean

fauna/province, 94Sea, 38, 94, 107, 108, 152, 155, 157, 171, 178, 186,

218, 221, 224, 226, 256megalospheric test, 48, 51, 54, Table 3.1meiosis, 48–49, 51, 52, 54metabolic 246, 254, 255metabolic rate, 246, 254Mexico, 151microaerophiles, 202, 211, 214microelectrode, 207, Fig. 12.3microhabitat, 5, 6, 37, 43, 145, 146–148, 161–179,

192, 196, 197, 198, 204–207, 253, 256, 257, 292,295, Figs. 10.1–10.9

microoxic, 202microspheric test, 48, 51, 54, Table 3.1microtubules, 38, 39microxia/microxic, 163, 171, 177, 178, 201–209,

211–216, Tables 12.1, 12.2Miocene, 33, 102, 116, 134, 186, 252, 288Mississippi River delta, 138, 186, 290mitochondria, 39, 45, 70, 211, 214, 225, 233,

Fig. 12.5mixotrophic nutri t ion, 129monocrystalline wall, see wall , monocrystallinemonolamellar test, 45, 46monolamellar wall, see wall, monolamellarMonte Carlo technique, 77Monterey Formation, 252Moorea, 212morphogenesis, 45–48morphogroup/morphotype, 6, 117, 119, 121,

174–176, 190–192, 196, 215morphological deformities, distribution, 226–230multicollinearity, 85multidimensional scaling (MDS), 74, 82–83, Fig. 5.6multiple broods, 52

neodymium, 274–275, Fig. 15.1, Table 15.1isotopes, 274–275

Neogene, 102, 114, 116New York Bight, 204New Zealand, 148, 149, 152, 156, 185, Fig. 9.4nitrate, 163, 172, 182, 251, Fig. 10.8non-lamellar wall, see wall, non-lamellarNorth Atlant ic Deep Water ( N A D W ) , 5, 186, 266,

269North Sea, 155, 207, 222Norway, 186, 196, 204, 215, 224, 228, Fig. 12.6,

Table 12.2Nova Scotia, 149, Table 12.2Nova Scolian fauna/province, 100nuclear dimorphism, 51, 54, Table 3.1nutrients, 43, 106, 108, 110, 117, 120, 124–126, 129,

130, 137–138, 142, 156, 203, 204, 216, 221, 222,223, 225, 231, 252, 257, 259, 260, 265–269

Okinawa, 130, 134Oligocene, 59, 274, 288, 296OMZ, see Oxygen Minimum Zoneontogeny, 11, 109, 111, 246, 255, 256opportunism, response to pollution, 226ordinary least squares (OLS), 85Ordovidan, 33Oregon, 83Oregonian fauna/province, 98, Fig. 6.3organic carbon supply, 181–182organic matter, 2, 5, 40, 43, 57, 124, 128, 129, 134,

161, 162, 163, 171, 172, 176, 177, 178, 179, 181,182, 183, 184, 185, 186, 188, 192, 194, 195, 196,197, 198, 219, 220, 231, 233, 248, 249, 250, 252,254, 264, 284, 286, 287, 290, 292, 293

degradation, 40, 162–163, 172, 178, 188flux to the seafloor, 163, 178, 182–183, 192–193

seasonally, 192–193labile, 5, 163, 171, 172, 178, 182, 183, 184, 185,

190, 194, 195, 196, 197, 198, 290organic median layer, 59Orinoco-Paria shelf, 204Oslo Fjord, Fig. 12.6oxic, 152, 162, 163, 164, 166, 174, 177, 178, 179, 196,

202, 203, 215, 290, Fig. 10.2, Tables 12.1, 12.2oxidation, in sediment, 184, 285, 287, 289, 292, 293oxygen

bottom water, 5, 43, 45, 171, 177–179, 185, 186,190, 201–204

isotopes, 6, 239–248, 259, 262, 288, Figs.14.1–14.3, Tables 14.1, 14.2

disequilibrium, 246fractionation, 241, 242, 243, 245–248

358 GENERAL INDEX

Oxygen Minimum Zone (OMZ), 5, 190, 202–203,212, 215, 254, Figs. 12.2, 12.6, Table 12.2

Pacific Ocean, 94, 97, 98, 109, 1 1 1 , 117, 118, 129,130, 131, 132, 133, 134, 136, 139, 155, 156, 158,182, 183, 186, 188, 190, 198, 218, 239, 260, 267,269, 274, 294, 295, Fig. 11.3, Table 8.1

Pacific Rim, 146, Table 9.1paleoceanography, 6, 114, 130, 164–165, 176,

177–179, 185, 216, 239, 242, 256, 259, 260, 266,270, 275–276, 292

Paleogene, 33, 79, 114, 131Paleozoic, 33, 48, 157Panama Isthmus, 117, 118Panamanian fauna/province, 94, 98, Fig. 6.3Papua New Guinea, 158, 212parallel evolution, 15parasitism, 39, 42–43particle reactive elements, 261Patagonia, 155patchiness of distribution, 114, 118, 120, 146, 153,

196pathogenesis, 230–231Pearson’s correlation coefficient, 76, 77peduncle, 38Permian, 67, 114peroxisome, 211, Fig. 12.5Persian Gulf, 158Peru-Chile Trench, Table 12.2pesticides, foraminiferal response, 225pH, 218, 222, 223, 248, 253, 262, 264, 269, 273phosphate, 108, 109, 185, 186, 251, 259. 260, 266photic levels, 108, 109, 110, 117, 221, 226photic zone, see euphotic/photic zonephotosynthesis, 44–45, 123, 124–126, 128, 129, 135,

137, 139, 248, 249, 254–255, Fig. 14.4phytodetritus, 5, 39, 42, 172, 177, 179, 183, 195, 197,

198phytodetritus feeders, 172, 179planktonic/benthic (P/B) ratio, 188–190planktonic foraminifers, 3, 6, 10, 15, 19, 22, 23, 37,

42, 43, 44, 46, 47, 48, 52, 65, 70, 103–122, 123,129, 136–137, 139, 188, 221, 239, 245, 246, 247,253, 256, 257, 264, 266, 267, 269, 270, 272, 273,276, 290, 292, 293, 294, 295, Figs. 2.5, 2.8,7.1–7.4, 7.6

abundance, 104, 105, 106, 108–109biogeography, 103–122, Figs. 7.3, 7.4, 7.6diversity gradient, 103, 1 1 1 – 1 1 7 , 121genetic isolation, 114, 116, 118–119, 120

plasmotomy, 52, Table 3.1plastogamy, 52, 53

Pleistocene, 102, 117, 239, 286, 287Pliocene, 116, 117, 118, 134Po Delta, 216polar ordinat ion, 87, 88pollution, 6, 183–185, 215, 217–231, Figs. 13.1, 13.2,

Table 13.1effect on test texture, 230foraminiferal response, 220–232, Fig. 13.2research strategies for foraminiferal studies,

218–220study locations, 218

ponticuli, 61, 65, Fig. 4.8pore ( tes t ) , 45, 46, 48, 55, Figs, 3.11, 3.12, 3.16

formation of, 58, 59, 69–70size, 107–108. 214, Fig. 7.1

pore water (sediment), 5, 126, 143, 146, 169, 171,176, 177, 178, 183, 186, 196, 207, 210, 246, 248,261, 267, 275, 281–285, 292, 297

postoxic, 202, 209, Table 12.1predation, 172–174pressure, see water pressureprimary organic l ining, 46principal components analysis (PCA), 74, 77, 78–80,

Figs. 5.2–5.5, 11.3, Tables 5.2, 5.3productivity, 5, 108, 109, 110, 113, 120, 141, 142,

165, 176, 178, 182, 183, 184, 185, 186, 187, 188,189, 190, 192, 193, 196, 197, 198, 199, 203, 220,222, 249–252, 266, 290, 292, 295, Figs. 11.4,11.5

proloculus, 48, 52, 54, 55pseudopodia, 4, 7, 18, 37, 38–39, 40, 42, 45, 46, 47,

70, 132, 137, 156, 211 , 214, Figs. 2.2, 3.1–3.3,3.6

pseudopores, 70Puerto Rico, 148pulp and paper-mill pollution, foraminiferal

response, 222pycnocline, 107, 110, 117, 120pyrite, 290pyritization, as response to pollution, 231

Q-mode, 74, 76, 77, 78, 79, 80, 82, 83, 86, 87

R-mode, 74, 76, 77, 78, 79, 80, 82, 87racemization, amino acid dat ing technique, 286, 287radial wall, see wall, radialradioactive waste, foraminiferal response, 225radiocarbon dating, 286, 292, 293, 294, 296rare earth elements, 276recurrent group analysis, 87red algae, 123, 135Red Sea, 94, 256

GENERAL INDEX 359

reproduction, effect of pollution, 223, 225, 231–232rescaled-range analysis, 296–297respiration, 38, 39, 129, 182, 197, 202, 223, 225, 247,

249–251, 254reticulopodia, 4, 18, 38, 39, Figs. 2.2, 3.6; see also

pseudopodiaretral processes, 61, Fig. 4.8reworking, 283, 284, 286, 287, 294rhizopod, 37–38Rose Bengal stain, 69–70, 155, 156, 166, 204, 212,

215, Table 12.2Russian River estuary, 149

Sagami Bay, Table 12.2salinity, 4, 5, 6, 106, 108, 109, 110, 113, 131, 134,

135, 136, 141, 143, 146, 148, 149, 150, 151, 152,153, 155, 158, 183, 186, 218, 221, 226, 230, 231,233, 239, 257, 264, 269, 272, Fig. 9.4

salt marsh, 141–148, 287–290, Figs. 9.1–9.3,Table 9.1

grasses, 141, 142Foraminifera

as sea-level indicators, 146–148, 287–290,Fig. 16.5

taphonomy, 146, 148, 287–290, Fig. 16.5widespread agglutinated species, 143, Fig. 9.2.

Table 9.1zonation, 143–148

organic matter, 142productivity, 142sediment, 142–143

San Diego Trough, Table 12.2San Nicolas Basin, Table 12.2San Pedro Basin, Table 12.2Santa Barbara Basin, 45, 171, 207, 210, 214, 215,

Figs. 7.2, 12.6, Table 12.2Santa Catalina Basin, Table 12.2Santa Cruz Basin, Table 12.2Santa Monica Basin, Table 12.2sapropel, 108, 171 , 178sarcode, 7, 38schizont, 51, 54, Fig. 3.14scores, 77, 79, 80, 83, 86, Figs. 5.3–5.5, 5.7, 11.3scree plot, 78, 79, 80, Fig. 5.2sea ice, 109, 184, 245sea level, 137, 144, 146, 148, 239, 287, 289, 290, 292,

296, 297seagrass, 135, 136, 157–158sediment-water interface (SWI), 5, 40, 161–163, 164,

169, 171, 172, 175, 176–177, 178, 183, 190, 202,212, 220, 284, 287, 290, 292, 293, 294, 296

Senegal, 155

sewage, foraminiferal response, 183–184, 185,220–222

shell repair, 48siliceous wall, see w a l l , siliceousS L I N K , 76, 77sodium, 259, Fig. 15.1, Table 15.1Sorby Principle, 286South Carolina, 72South China Sea, Table 12.2Southern Ocean, 269species

diversity, 3, 87, 100, 103, 104, 108, 111–117, 119,120, 121, 122, 129–130, 151–152, 153–154, 184,194, 195, 197, 215–216, 217, 218, 221, 222, 223,224, 225, 228, Figs. 9.5, 9.6

durat ion, 121origination, 100–102, 104, 1 1 4 – 1 1 5pairs, 48

standing stock, 108, 109, 166, 171 , 174, 184, 188step-wise regression, 85, Fig. 5.9, Table 5.6St. Lucia, 157stratigraphic sections, con t inu i ty , 297stratigraphic signal inputs, reconstruction, 295–296strontium, 259, 272, 273–274, Figs. 15.1, 15.4, 15.5,

Table 15.1isotopes, 273–274, Fig. 15.5

suboxic, 196, 202, 261, 273, 275, 290subsutural canals, 61–63, Figs. 4.10, 4.1 1sulfate reduction, 163, 172, 284, 287, 290Sulu Sea, 177, Table 12.2Sumatra, 148surface mixed layer, sediments, 281, 282, 284, 285,

288, 290, 292, 293, 294, 295, Figs. 16.1, 16.2Surian fauna/province, 98suspension feeding, 39, 40, 43Sweden, 150, 194symbiont, 70, 123–124, 129, 246–247, 254–255, 256,

Figs. 8.2, 12.5, Table 8.1symbiosis, 43, 123, 124–129, 131, 135, 136, 137, 210

Tanner Basin, Table 12.2taphonomic grade, 287taphonomy, 33, 146–148, 184, 188, 190, 197, 215,

220, 221, 281–297, Figs. 16.1–16.6temperature, 5, 6, 94, 100, 102, 105, 106–108, 110,

113, 114, 116, 117, 118, 136, 139, 142, 148, 149,153, 155, 166, 183, 186, 218, 221, 225, 233, 239,241, 245, 246, 247, 248, 253, 256, 260, 262, 264,269, 270, 272, 276, 293, Fig. 14.5

test wa l l , see wallTexas, 146, 150, 290thermal pol lu t ion, foraminiferal response, 225

360 GENERAL INDEX

time-averaging, 281, 286, 287, 290, 292, 296–297,Fig. 16.6

circumvention, 296–297scale, 296

toothplate, 15, 16, 19, 22, 29, 65total organic carbon (TOC), 186, 224trace elements, 259–276, Figs. 15 .1–15 .5 , Table 15.1

abundance, 265analysis, 264–265as chemical proxies, 273as diagenetic proxies, 275as nutrient proxies, 265–266, Fig. 15.3as paleoceanographic proxies, 260, 265–266,

269–270, 273as physical proxies, 269–270biological factors, 262, 264cul ture studies, 262–264incorporation, 261thermodynamics, 261–262

t ransfer funct ion, 86, 105–106, Fig. 5.8, Table 5.5t r ans i t ion metals, 275–276trend surface analysis, 86, 88Triassic, 33tr imorphism, 51–52, Table 3.1Trinidad, 148trophic mechanisms, 39–45Tunisia, 158

ul t ras t ruc ture , 39, 45, 46, 58, 59, 67, 209–211, 230umbil ical cover plates, 63–65, Figs. 4.5, 4.6,

4.12–4.14U P G M A , 76, 77upwelling, 109, 1 1 2 , 114, 1 1 8 , 1 2 0 , 252, 267, 276uran ium, 273, Fig. 15.1, Table 15.1U.S. Gulf Coast, estuaries, 150

vanad ium, 273, Fig. 15 .1 , Table 15.1VARIMAX, 78, 79Venice, 151ver t i ca l d i s t r i b u t i o n of species, subst ra te , 168–174,

Figs. 10.3–10.8vicariance, 102, 1 1 7Virginian fauna/province, 100vital effect, shell geochemistry, 6, 111, 254, 262, 286

wallaragonit ic, 15, 17, 19, 22, 32, 33, 65–67, Fig. 2.8bi lamellar , 15, 19, 22, 28, 30, 32, 46, 59–60, 66,

67–69, Figs, 2.8, 4.3, 4.4, 4.17granula r , 14, 15, 29, 30, 31, 59, Fig. 2.6imperforate , 10, 14, 23, 26, 27, 25, 30, 33, 35, 58lamel lar , 22, 58–69monocrystal l ine , 58monolamel lar , 15, 19, 22, 28, 59, Figs. 2.8, 4.2non-lamel lar , 58radia l , 14, 15, 29, 30, 31, 32, 35, 59, Figs. 2.5, 2.6siliceous, 16–17, 18, 19, 32, 35, Fig. 2.8

Ward’s minimum variance, 76, 77warm-water b e n t h i c faunas, 94, 102, Figs . 6.1, 6.2water mass, 5, 97, 100, 102wate r pressure, 260, 267, 269, 272West African fauna/province, 94West I n d i a n (Car ibbean) fauna/province, 94, 98,

100, 102Western Caroline Islands, 130, 134–135western Africa, 151, 155, 186, Fig. 11.1

xanthosomes, 39, 40

Yucatan, 98

zinc, 275–276, Fig. 15 .1 , Table 15 .1

Taxonomic Index

FORAMINIFERA

Acervulina, 31A. inhaerens, 157Acervulinacea, 31Acervulinidae, 31Adelosina cliarensis, 230, Fig. 13.2A. intricata, Fig. 13.2A. pulchella, Fig. 13.2Adercotryma, 26, 214A. glomerata, 209, Table 12.2Agathistègues, Fig 2.3Alabaminella weddellensis, 179, 192Al l ia t ina , 33Allogromia, 23, 38A. laticollaris, 48, 49, 52, 53, 54, 223, Fig. 2.9,

Table 3.1Allogromiida, 18, 19, 23, 33, Figs. 2.8, 2.9, Tables

2.2, 2.3Allogromiidae, 19, 208, 209, 212, 215, Table 2.1Allogromiina, 15, Fig. 2.7Allomorphina, 31Alveolinacea, 28Alveolinella, 28, 156A. quoyi, 134, Fig. 8.1, Table 8.1Alveolinellidae, Table 2.1Alveolinidae, 28, 43, 123, 129, 134, Table 8.1Alveophragmium, 26Ammoastuta, 26, 150Ammobaculites, 26, 149, 150, 158A. crassus, 149, 224, Table 13.1

A. exiguus , Table 9.1A. salsus, Table 13.1Ammocibicides, 26Ammodiscacea, 15, 23Ammodiscidae, 23, Table 2.1Ammodiscus, 11, 23, 212, Fig. 2.9A. gullmarensis, Table 12.2Ammoflintina, 23Ammoglobigerina, 26Ammolagena, 23Ammomarginulina, 26A. fluvialis, 151, Table 13.1Ammomassilina, 27Ammonia, 32, 38, 63, 64, 68, 149, 151, 153, 154, 155,

212, 224, Fig. 4.12A. annectens, Table 13.1A. beccarii, 42, 143, 148, 149, 151, 154, 155, 208,

212, 223, 289, Figs. 2.9, 9.4, Tables 9.1, 13.1A. caspica, Table 13.1A. dentata, Table 13.1A. parkinsoniana, 143, 145, 151, 212, 214, 216,

Fig. 12.6, Table 12.2A. sobrina, Table 13.1A. tepida, 45, 51, 54, 145, 148, 151, 155, 157, 223,

226, 230, 231, 232, Figs. 3.10, 3.12, 13.2, Tables3.1, 13.1

Ammosphaeroidinidae, 26Ammotium, 26, 148, 150A. cassis, 149, 150, 214A. fragile, 149, Fig. 9.4

362 TAXONOMIC INDEX

A. salsum, 143, 145, 148, 151, 289, Figs. 9.2, 9.3,Table 9.1

Amphicoryna, 28, Fig. 2.4Amphisorus, 28, 70, 136A. hemprichii, 46, 136, 157, Fig. 8.2, Table 8.1Amphistegina, 31, 69, 70, 126, 128, 131–132, 139,

156, 157, 158, 286, 294, Fig. 2.1, Tables 2.1, 8.1A. bicirculata, 132A. gibbosa, 42, 51, 131–132, Table 3.1A. lessonii, 79, 131–132, 134, 156, 157, Fig. 8.1A. lobifera, 46, 131–132, 156, 230–231, Table 13.1A. papillosa, 132A. radiata, 132Amphisteginidae, 31, 43, 124, 129, 131–132, Fig. 8.4,

Table 8.1Androsina, 135A. lucasi, 135, 158Angulogerina, 29Annulopatellina, 30Annulopatellinacea, 30Annulopatellinidae, 30Anomalinidae, Table 2.1Anomalinoides, Fig. 2.1Archaias, 28, 126, 135, 286, Fig. 2.1A. angulatus, 135, 157, 158, 285, 286, Figs. 8.1, 8.2Archaiasinae, 123, 129, 134, Table 8.1Arenoparrella, 26, 148A. mexicana, 143, 145, 147, 148, 290, Fig. 9.2Articulina, 28Assilina, 133A. ammonoides, 133Astacolus, 28, Fig. 2.1Asterigerina, 31, 61, Fig. 4.9A. carinata, 155Asterigerinacea, 31, Fig. 2.1Asterigerinidae, 31, 123Asterorotalia, 32Astrammina rara, 42, 45, 52, Fig. 2.2Astrononion, 31, 63, 212, Fig. 4.14, Table 12.2A. gallowayi, 154Astrorhiza, 23A. limicola, 40, 42, 208, 212, 214Astrorhizacea, 23Astrorhizida, 19, 23, 33, Figs. 2.8, 2.9, Tables 2.2, 2.3Astrorhizidae, 10, 23, Table 2.1Ataxophragmiacea, 26

Baculogypsina, 32, 133, 156B. sphaerulata, 133, 156, Table 8.1Baculogypsinoides, 133, Table 8.1B. spinosus, Table 8.1Baggina, 30

Bagginidae, 30Bathysiphon, 23, 212B. filiformis, 185, Table 12.2Bdelloidina, 26Beella, 32B. digitata, Fig. 7.3Berggrenia, 32Bigenerina, 27Biloculinella, 27Bolivina, 29, 151, 174, 177, 212, 214, Fig. 9.4B. albatrossi, Fig. 12.6, Table 12.2B. argentea, Table 12.2B. di latata, 174, Table 12.2B. interjuncta, Table 12.2B. lowmani, Fig. 2.9B. ordinaria, Table 12.2B. pacifica, Table 12.2B. rankini, Table 12.2B. seminuda, 216, Table 12.2B. spathula ta , 174, Table 12.2B. spissa, Table 12.2B. subadvena, Table 12.2B. subaenariensis, Table 12.2B. vaughani, Table 13.1Bolivinacea, 29Bolivinella, 29Bolivinellidae, 29Bolivinidae, 29Bolivinita, 29Bolivinitacea, 29Bolivinitidae, 29Bolivinopsis, 214B. cubensis, Table 12.2Bolliella, 32B. adamsi, Fig. 7.3Borelis, 28, 134, 156, 157, Fig. 2.1B. pulchra, 134Brizalina, 212, Table 12.2B. pseudopunctata, 154B. striatula, 155Broeckina, 135B. discoidea, 135B. orbitolitoides, 135Buccella frigida, 149, Fig. 9.4, Table 13.1B. inusitata, 154B. mansfieldi, 287Bulimina, 7, 29, 155, 174, 177, 212B. aculeata, 169, 192, Table 12.2B. alazanensis, 5, 192, Fig. 11.5B. elongata, Table 12.2B. excilis, Table 12.2B. inflata, 174

TAXONOMIC INDEX 363

B. marginata, 169, 174, 183, 192, 207–208, 209, Figs.10.7, 10.8, 12.6, Table 12.2

B. marginata denudata, Table 13.1B. mexicana, 193, Fig. 11.5B. striata, Table 13.1B. subornata, Table 13.1B. translucens, Fig. 11.5Buliminacea, 15, 29, 35Buliminella, 29, 212B. elegantissima, 155, 183, Table 13.1B. morgani, 216, Table 12.2B. tenuata, 210, 211, Figs. 12.5, 12.6, Table 12.2Buliminellidae, 29Buliminida, 16, 17, 19, 33, 35, 59–60, 65, Figs. 2.8,

2.9, Tables 2.2, 2.3Buliminidae, 11, 29, Table 2.1

Calcarina, 32, 133, 136, 156, Fig. 2.1, Table 8.1C. gaudichaudii, 133, Fig. 8.1C. hispida, Fig. 8.2C. spengleri, 156Calcarinidae, 42, 43, 124, 126, 129, 131, 133–134,

Fig. 8.4, Tables 2.1, 8.1Calcituba, 27C. decorata, 79C. polymorpha, 46, 47, 52, 58Camerinidae, Table 2.1Cancris, 30, 212, Fig. 2.1C. inaequalis, Table 12.2Candeina, 32C. nitida, 110, Fig. 7.3Candeinidae, 32, 136Carpenteria proteiformis, 156Carterina, 28, 57, Fig. 4.1C. spiculotesta, 57, Fig. 2.9Carterinacea, 15Carterinida, 18, 22, 28, 33, 57, Figs. 2.8, 2.9, Tables

2.2, 2.3Carterinidae, 28Carterinina, Fig. 2.7Cassidulina, 29, 35, 212C. crassa, Fig. 2.6C. hooperi, 192C. laevigata, 5, 79, 192, Table 12.2C. neocarinata, Table 12.2C. reniforme, 154Cassidulinacea, 15, 29, 35Cassidulinidae, 29, 35, Table 2.1Cassidulinoides, 29, 212C. porrectus, 209, Table 12.2Ceratobulimina, 32, 66Ceratobuliminacea, 32

Ceratobuliminidae , 32Chiloguembelinidae, 32Chilostomella, 31, 154, 177, 214, 215, Fig. 3.11C. oolina, 212, Table 12.2C. ovoidea, 212, 214, Fig. 12.6, Table 12.2Chilostomellacea, 31, Fig. 2.1Chilostomellidae, 31, 212, Table 2.1Cibicides, 31, 60, 80, 158, 224, Figs. 2.1, 15.4C. advenum, 230, Table 13.1C. aknerianus, Table 13.1C. floridanus, 79C. kullenbergi, Fig. 15.2C. lobatulus, 154C. refulgens, 43, 80C. wuellerstorfi, 5, 40, 175, 176, 177, 179, 192, 254,

Fig. 15.2Cibicididae, 31Cibicidoides, 31, 174, 176, 248, 254Clavatorella, 32Clavulina, 7, 27Conicospirillinoides, 32Cornuloculina, 27Cornuspira, 11, 27Cornuspiracea, 27Cornuspiramia, 157Cornuspiridae, 17, 27Coscinophragmatacea, 26Coscinophragmatidae, 26Cribrobigenerina, 27Cribroelphidium, 32C. poeyanum, 155C. translucens, 224, Table 13.1Cribrospiroloculina, 27Cribrostomoides, 26, 214C. crassimargo, 149C. jeffreysii, 154, 155, Table 12.2C. wiesneri, Table 12.2Cribrothalammina alba, 45, 55, Figs. 3.1, 3.2, 3.4,

3.16, Table 3.1Cristellaria, Fig. 2.4Crithionina, 23Cruciloculina, 27Cushmanella, 33, 66Cyclammina, 26Cyclamminidae, 26Cyclocibicides, 31, 157Cycloclypeus, 32, 69, 133C. carpenteri, 48, 133, Table 8.1Cycloflorina villafranca, Fig. 13.2Cyclorbiculina, 28, 135, Table 8.1C. compressa, 135, 157Cyclostègues, 7, Fig. 2.3

364 TAXONOMIC INDEX

Cylindrogullmia alba, 52Cymbaloporetta, 31Cymbaloporidae, 31, Table 2.1

Delosina, 29Delosinacea, 29Delosinidae, 29Dendritina, 28, 135, Fig. 2.1, Table 8.1Dendrotuba, 23Dentalina, 28, Fig. 2.4D. albatrossi, Fig. 2.9D. pauperata, Fig. 4.2Dimorphina, Fig. 2.4Discocyclinidae, Table 2.1Discorbacea, 30, 35, Fig. 2.1Discorbidae, 30Discorbinella, 30Discorbinellacea, 30Discorbinellidae, 30Discorbis, 30, 35D. columbiensis, 184, Table 13.1D. mediterranensis, 52, 54, Table 3.1D. ornatissima, 54D. patel l i formis , 52, 53, Table 3.1D. pulvinata, 53–54D. vilardeboanus, 43, 49, Table 3.1Discospirina, 27Discospirinacea, 27Discospirinidae, 27Dyocibicides, 31

Edentostomina, 27E. cultrata, 212Eggerella, 27, 214, Table 12.2E. advena, 149, 154, Fig. 13.2, Table 13.1E. scabra, 208, Table 12.2Eggerellidae, 27Eggerelloides scabrus, 155, Table 13.1Ehrenbergina, 29Eilohedra, 30Ellipsodinidae, Table 2.1Ellipsoglandulina, 29Ellipsolagenidae, 28Elphidiella, 32, 63, Fig. 4.10E. arctica, Fig. 4.11Elphidiidae, 32, 35, 44, 59Elphidium, 4, 32, 35, 38, 61, 63, 64, 150, 151, 153,

154, 155, 156, 158, 212, 224, 287, Figs. 1 .1, 2.1,4.8, Table 9.1

E. advenum, 155, Fig. 9.4E. articulatum, 155, Table 13.1E. bartletti, Table 13.1

E. batialis, 156E. caspicum, Table 13.1E. charlottensis, Fig. 9.4E. clavatum/incertum group, Table 13.1E. craticulatum, 63, Fig. 4.15E. crispum, 40, 42, 48, 49, 51, 54, 156, 287, Table 3.1E. discoidale, 156E. excavatum, 148, 149, 154, 155, 156, 208, 212, 216,

Fig. 9.4, Tables 12.2, 13.1E. granosum, 155E. gunteri, 151, 155E. incertum, 209E. lidoense, Table 13.1E. margaritaceum, Table 13.1E. norvangi, Table 13.1E. orbiculare, Table 13.1E. poeyanum, 157, Table 13.1E. translucens, Table 13.1E. williamsoni, 143, 149Enallostègues, Fig. 2.3Entomostègues, Fig. 2.3Entosolenia marginata, 42Epistomariidae, 31Epis tomina, 66Epistominella, 30, 212, 214E. exigua, 5, 154, 155, 179, 192, Table 12.2E. pusilla, 192E. smithi, Table 12.2E. vitrea, 155, Table 12.2Epistominidae, 32Eponidacea, 35Eponides, 30, 35, Fig. 2.1E. antillarum, 79Eponididae, 30

Favusellacea, 19, 22, 32, Fig. 2.8Fischerina, 27Fischerinidae, 27, Table 2.1Fissurina, 28F. marginata, 42, 52, Table 3.1Floresina amphiphaga, 42, 52Florilus boueanum, Table 13.1F. grateloupii, Table 13.1F. scaphus, Table 13.1Fontbotia, 176, 254Foraminifera, 16, 18Foraminiferida, 15, 18Frondicularia, 28, Fig. 2.4Fursenkoina, 29, 192, 212F. apertura, Table 12.2F. bramlettei, Table 12.2F. cornuta, 211, Table 12.2

TAXONOMIC INDEX 365

F. pontoni, Table 13.1F. seminuda, Table 12.2Fursenkoinacea, 29Fursenkoinidae, 29Fusulinida, 18, 19, 22, 27, 33, 48, Figs. 2.8, 2.9,

Table 2.2Fusulinidae, Table 2.1Fusulinina, 15, Fig. 2.7

Gallitellia, 32, 33Gaudryina, 26Gavelinellidae, 31Gavelinopsis, 30, 35, 212G. translucens, Fig. 12.6, Table 12.2Glabratella, 30G. lauriei, 79G. sulcata, 51, 52, 54, Table 3.1Glabralellacea, 30Glabratellidae, 30Glandulina, 28, Fig. 2.4Glandulinidae, 28Globigerina, 7, 32, Fig. 2.5G. bulloides, 108, 110, 117, 246, 248, 254, 267, Figs.

7.3, 15.2G. calida, 110G. diplostoma, 119G. falconensis, Fig. 7.3G. juvenilis, 119G. quiniqueloba, 108, Fig. 7.3G. radians, 119G. rosacea, 119G. rubescens, Fig. 7.3G. subcretacea, 119G. trilocularis, 119Globigerinacea, 15, 19, 32Globigerinella, 32G. adamsi, 110, 117G. aequilateralis, 42, 110, 255, Fig. 7.3G. calida, Fig. 7.3Globigerinida, 10, 19, 22, 32, 33, 43, 59–60, 123,

124, 136, Figs. 2.8, 2.9, Tables 2.2, 2.3Globigerinidae, 10, 32, 126, Table 2.1Globigerinina, Fig. 2.7Globigerinita glutinata, 110, Fig. 7.3G. uvula, 108, Fig. 7.3Globigerinoides, 32G. conglobatus, Fig. 7.3G. cyclostomus, 119G. ruber, 24, 108, 118, 267, 293, Figs. 2.9, 7.3, 15.4G. succulifer, 48, 109, 246, 247, 254, 255, 267, Figs.

7.3, 15.4G. suleki, 119

G. tenellus, Fig. 7.3G. triloba, Fig. 7.3Globobulimina, 29, 164, 168, 169, 171, 176, 177, 212,

214, 215, Figs. 10.3, 10.7, 11.5G.affinis, 169, Figs. 10.7, 10.8, Table 12.2G. hoeglundi, Table 12.2G. pacifica, 42, Figs. 3.7, 12.6, Table 12.2Globocassidulina, 29, 154, 212G. biora, 154, 209, 210, Table 12.2G. subglobosa, 192, Fig. 11.5Globoquadrina conglomerata, 110, 117, Fig. 7.3Globorotalia, 32G. canariensis, 119G. crassaformis, 255, Fig. 7.3G. cultrata , 118, 121G. hirsuta, 46, Fig. 7.3G. inflata, 111, 117, 119, 255, Fig. 7.3G. menardii, 42, 46, 117, 247, 255, 293, Figs. 7.3. 15.4G. punctulata, 119G. scitula, Fig. 7.3G. seiglei, 119G. theyeri, 117G. truncatulinodies, 46, 107, 117, 255, 293, Fig. 7.3G. tumida, 255, Fig. 7.3Globorotaliacea, 19, 32Globorotaliidae, 32, 136, Table 2.1Globorotaloides hexagonus, 117, Fig. 7.3Globotextularia, 26Globotextulariidae , 26Globulina, 28, Fig. 2.4Gloiogullmia eurystoma, 211, 212Glomospira, 23Goesella, 27Gordiospira, 27Granuloreticulosa, 18Gromidae, 10Guembelitriidae, 32, 33Guppyella, 26Guttulina, 28, Fig. 2.4Gypsina, 31Gyroidina, 31Gyroidinoides, 31

Halyphysema tumanowicizii, 52Hansenisca, 31Hantkeninidae, Table 2.1Hanzawaia, 31, Fig. 2.1H. concentrica, 155Haplophragmiacea, 26Haplophragmoides, 26, 148, Table 9.1H. manilaensis, 143, Fig. 9.3, Table 9.1H. wilberti, 147, 149, Fig. 9.4, Table 9.1

366 TAXONOMIC INDEX

Haplophragmoididae, 26Hastigerina, 32H. involuta, 119H. pelagica, 42, 65, 110, 136, Figs. 4,17, 7.3Hastigerinella digit at a, 110Hastigerinidae, 32, 136Hastigerinopsis, 32Hauerina, 27Hauerinidae, 27Haynesina, 31H. depressula, 155, Fig. 9.4, Tables 9.1, 13.1H. germanica, 143, 145, Table 13.1H. orbiculare, 149Helenina, 30H. anderseni, 68, 149, Fig. 9.4Heleninidae, 30Hèlicostègues, 10, Fig. 2.3Hemigordiopsacea, 27Hemigordiopsidae, 17, 27Hemisphaeramminidae, 23Heronalleia, 30Heronallenidae, 30Heterocyclina tuberculata, 133Heterohelicacea, 19, 32Heterohelicidae, Table 2.1Heterostegina, 32, 69, 156, Table 8.1H. antillarum, 133, Table 8.1H. depressa, 44, 48, 51, 126, 132, 133, 134, Fig. 8.1,

Table 3.1H. operculinoides, 133Heterotheca lobata, 55. Table 3.1Hippocrepina, 23Hippocrepinacea, 17, 23Hippocrepinidae, 23Hoeglundina, 32, 66, 267H. elegans, 168, 248, 253, 255, Fig. 10.7Homotrema, 31H. rubra, 156Homotrematidae, 31Homotremidae, Table 2.1Hopkinsina, 29, 212H. pacifica, 169, 216, Figs. 10.5, 10.7, Table 12.2Hormosina, 26Hormosinacea, 23Hormosinidae, 23Hospitella, 23Hyalinea, 31Hyperammina, 23Hyperamminidae, Table 2.1Hyrrokkin sarcophaga, 43

Involutinida, 17, 19, 22, 32, 33, 35, Figs. 2.8, 2.9,Tables 2.2, 2.3

Involutinina, 17–18, Fig. 2.7Ioanella, 30Iridia, 23I. lucida, 51, Table 3.1Islandiella, 29, 35I. algida, Fig. 2.6I. islandica, 154

Jaculella, 23Jadammina, 26J. macrescens, 143, 144, 145, 146, 147, 149, 289, 290,

Figs. 9.2, 9.3, 9.4J. macrescens forma macrescence, 143, Table 9.1J. macrescens forma polystoma, 143, Table 9.1

Karreria, 31Karreriella, 27Karreriidae, 31Keramosphaeridae, 28, Table 2.1Komokia, 23Komokiacea, 23Komokiidae, 23

Laevipeneroplis, 135, Table 8.1L. malayensis, 134–135, Table 8.1L. proteus, 135, Fig. 8.1Lagena, 28, 35, 151, 224, Fig. 2.4Lagenammina, 23Lagenida, 19, 22, 28, 59, 224, Figs. 2.1, 2.8, 2.9,

Tables 2.2, 2.3Lagenidae, 10, 28, Fig. 2.4, Table 2.1Lagenina, Fig. 2.7Lagynidae, 19, 23Laryngosigma, 28Laterostomella, 32Laticarinina, 30Lenticulina, 28, Fig. 2.1Lepidocyclina elephantina, 37Liebusella, 26Lingulina, 28, 59, Fig. 2.4Lituola, 26Lituolacea, 15, 26Lituolida, 19, 22, 23, 33, Figs. 2.8, 2.9, Tables 2.2,

2.3Lituolidae, 10, 26, Table 2.1Lituotuba, 26Lituotubidae, 26Loftusiacea, 26Loftusiidae, Table 2.1Loxosiomatacea, 16, 29Loxostomum, 33, 212L. pseudobeyrichi, Table 12.2

TAXONOMIC INDEX 367

Marginopora, 28, 128, 136, 156, 158, Table 8.1M. vertebralis, 136, 156, 158, 286, Fig. 3.8Marginulina, 28, Fig. 2 .4M a r t i n o t t i e l l a , 2 7M. communis, 80, 83, Table 13.1Mass i l ina , 27Meandrospira , 27Melonis, 31, 174, Fig. 2.1M. barleeanus, 5, 169, 192, Figs. 10.4, 10.7, 10.8, 11 .5M. pompilioides, 61, 193, Figs. 4.5, 4.6, 11.5M. zaandami, 5, 83Metarotaliella parva, 53, Table 3.1M. simplex, 53, Table 3.1M. tuvaluensis, 43Miliammellus, 16, 33M. legis, Fig. 2.9Miliammina, 23, 148, 150, 153M. earlandi, Table 13.1M. fusca, 143, 145, 146, 147, 148, 149, 151, 153,

Figs. 9.2, 9.3,9.4, Tables 9.1, 13.1Miliolacea, 27Miliolida, 16–17, 18, 19, 22, 27, 33, 43, 46, 58, 153,

154, Figs. 2.1, 2.8, 2.9, Tables 2.2, 2.3Miliolidae, 10, 28, Table 2.1Miliol ina, 15, 16, Fig. 2.7Miliolinella, 27M. circularis, 158M. subrotunda, 155, Table 13.1M warreni, Fig. 2.9Miniacina, 31, 157M. miniacea, 156Miogypsinidae, Table 2.1Mississippina, 30Mississippinidae, 30Monalysidium, 28, 135M. sollasi, Table 8.1Monostègues, 7, 35, Fig. 2.3Monothalamea, 35Myxotheca, 23, 35, 45, Fig. 3.9M. arenilega, 55, Table 3.1

Nautilus, 7Nemogullmia longevariabilis, 52, 211, 212, Table 3.1Neoconorbina, 30Neoeponides, 30Neogloboquadrina, 32N. dutertrei, 108, 110, 247, 255, Figs. 7.3, 8.2, 15.4N. pachyderma, 109, 110, 117, 267, Figs. 7.3, 15.4N. pachyderma forma superficiaria, 108Neorotalia, 133N. calcar, 133, Table 8.1Neoschwagerinidae, Table 2.1

Neusinidae, Table 2.1Nodobaculariella, 27Nodogenerina, 30Nodophthalmidium, 27Nodosaria, 28, Fig. 2.4N. subsoluta, Fig. 4.2Nodosariacea, 15, 28, Fig. 2.1Nodosariida, Table 2.2Nodosariidae. 28Nodulina, 23Nonion, 31, Fig. 2.1N. boueanum, Table 13.1N. grateloupi, 212, Tables 12.2, 13.1N. labradoricum, 61N. tisburyensis, 153Nonionacea, 31, 35, Fig. 2.1N o n i o n e l l a , 3 1 , 1 7 5 , 1 8 4N. atlantica, 155N. stella, 175, 210, 2 1 1 , 212, 214, 215, Figs. 12.5.

12.6, Table 12.2N. turgida, 155, 175, 208, 212, Table 12.2Nonionellina, 31N. labradorica, 210, 212, Fig. 12.6Nonionidae, 31, 44, 212, Table 2.1Normanina, 23Notodendrodes, 23N. antarctikos, 43, 154Notodendrodidae, 17, 23Nouria, 26N. polymorphinoides, 155Nouri idae, 26Nubecularia, 27, 157Nubeculariacea, 27Nubeculariidae, 27Nummul in idae , 10Nummuli tacea , 32, Fig. 2.1Nummulites, Fig. 2.1N. venosus, 52, 53, 133, Table 8.1N u m m u l i t i d a , 156Nummul i t idae , 30, 43, 48, 51, 52, 53, 65, 124, 126.

132–133, Fig. 8.4, Table 8.1Nuttallides, 31N. umbonifera, 5, 294, Figs. 11.5, 15.2

Oolina, 28Operculina, 32, 69Ophiotuba, 23Ophthalmidi idae, 27, Table 2.1Orbitoidacea, 15Orbitoididae, Table 2.1Orbitolinidae, Table 2.1Orbulina, 32

368 TAXONOMIC INDEX

O. universa, 42, 108, 110, 137, 247, 254, 255, Figs.7.3, 8.2, 8.3, 15.2

Orcadia, 32Oridorsalidae, 31Oridorsalis, 31Osangularia, 31, 212O. culter, Table 12.2O. rugosa, Table 12.2Osangulariidae, 31Ovammina opaca, 52, 55, Table 3.1Ozawaia, 32

Palmerinella, 31Pararotalia, 32P. spinigera, Fig. 13.2Parasorites, 28, 134, 135, Table 8.1P. discoidea, 135P. orbitolitoides, 134, 157, Table 8.1Paratrochammina, 214P. antarctica, Table 12.2Parrellina, 32Patellina, 28, 58, 69P. corrugata, 48, 49, 51, 53, 54, 55, Table 3.1Patellinela inconspicua, Fig. 9.4Patellinidae, 28Paumotua, 30Pavonina, 29Pavoninidae, 29Pegidia, 30Pegidiidae, 30, Table 2.1Pelosina, 23P. arborescens, 40, 208, 212, 214, Figs. 3.5, 3.7Peneroplidae, 28, 43, 123, 129, 134, 135, Table 8.1Peneroplis, 28, 38, 126, 135, 157, 158, Fig. 2.1.

Table8.1P. elegans, Fig. 8. 1P. pertusus, 42, 135, Fig. 8.2P. planatus, 135, 156, 158, Fig. 13.2Pileolina tabernacularis, 155Placopsilina, 26Placopsilinidae, 26, Table 2.1Planispirillina, 32P. papillosa, Fig. 2.9Planispirillinidae, 17, 18, 32Planispirina, 27Planorbulina, 157P. acervalis, 286P. mediterranensis, 155Planorbulinacea, 30, Fig. 2.1Planorbul inidae, 31, Table 2.1Planularia, Fig. 2.1Planulina, 31, 176, 212, 254

P. ariminensis, 40, 179, Table 12.2P. exorna, 155Planu l in idae , 30Pleurostomella, 29Pleurostomellacea, 29Pleurostomellidae, 29Polymorphina, 28, 154, 212, F ig. 2.4, Table 12.2Polymorphinacea, 28Polymorphinidae, 28, Fig. 2.4, Table 2.1Polysaccammina hyperhalina, 145, Table 9.1Polystomella crispum, 40, 48Polythalamea, 35Poroeponides, 30, 224Porosononion martkobi, 231Protelphidium paralium, Table 13 .1Protista, 18Protoctista, 3, 18Psammatodendron, 23Psammophaga simplora, 52Psammosphaera, 23, 153, 212, 215P. bowmanni, 209, Table 12.2P. parva, Table 12.2Psammosphaer idae , 23Pseudogaudryina, 27Pseudogaudryinidae, 27Pseudonodosinella, 26Pseudoparrellidae, 30Pseudorotalia, 61, 68, Figs. 4.7, 4.13Pseudothurammina limnetis, 149. Fig. 9.3, Table 9.1Pseudo t r i l ocu l ina , 212P. subgranulata, 230, Table 13.1Ptychomiliola separans , 155Pullenia, 31Pulleniatina, 32P. obliquiloculata, 42, 110, 118, 255, Fig. 7.3Pu l l en ia t in idae , 32, 136Puteolina, 134P. malayensis, 134Pyrgo, 27, 157Pyrulina, F ig . 2.4

Quadrimorphina, 31Quadrimorphinidae, 31Quinqueloculina, 27, 216, 157, 158, 224, Fig. 9.4Q. jugosa. 79, 83Q. lamarckiana, 155, 157Q. lata, 154

Q. rhodiensis, Table 13.1Q. seminulum, 208, 212, Table 13.1

Q. stalkeri, 212, 216

Ramulina, 28, Fig. 2.4Rectobolivina, 29

TAXONOMIC INDEX 369

Rectuvigerina, 29Recurvoides, 26, 214, Table 12.2Remaneica, 26Remaneicacea, 26Remaneicidae, 26Reophacidae, Table 2.1Reophax, 23, 212R. arctica, 149, Table 13.1R. bilocularis, Table 12.2R. curtus, 79R. dentaliniformis, 154, Table 12.2R. excentricus, Table 12.2R. gracilis, Table 12.2R. moniliforme, Fig. 9.4R. nana, 146, 155, Table 9.1R. subdentaliniformis, 209Reticulomyxa, 37Reussella, 29Reussellidae, 29Rhabdammina, 23Rhabdamminidae, 23Rhizammina, 23, 212R. irregularis, Table 12.2Rhizamminidae, Table 2.1Rimulina, 28Robertina, 32Robertinacea, 15, 32Robertinida, 17, 19, 22, 32, 33, 65–67, Figs. 2.8, 2.9,

Tables 2.2, 2.3Robertinidae, 33Robertinina, 17, Fig. 2.7Robertinoides, 33R. charlottensis, Fig. 2.9Robulus, Fig. 2.4Rosalina, 30, 35, 157, 212R. bertheloti, 79, 83R. columbiensis, Table 12.2R. floridana, 45, 46, 47, 48, 67, 69, 80R. floridensis, 83Rosalinidae, 30Rotaliacea, 15, 31, 35, Fig. 2.1Rotalidium annectens, 151Rotaliella elatiana, 43, 55, Table 3.1R. heterocaryotica, 49, 51, 53, Table 3.1R. roscoffensis, 53, 54, Table 3.1Rotaliellidae, 44–45Rotaliida, 16, 17, 19, 22, 30, 33, 43, 59–60, Figs. 2.1,

2.8, 2.9, Tables 2.2. 2.3Rotaliidae, 10, 31, Table 2.1Rotaliina, 15, 16, Fig. 2.7Rotorbinella rosea, 157Rubratella intermedia, 53, Table 3.1

Rupertianella, 28Rupertiidae, Table 2.1Rupertina s tabi l i s , 40Rutherfordoides cornuta, Table 13.1Rzehakinacea, 23Rzehakinidae, 23

Saccaminidae, 208Saccammina, 23, 35, 212S. alba, 52, 55, Table 3.1S. atlantica, 149S. comprima, Fig. 2.9, Table 12.2S. sphaerica, 52, 55Saecamminidae, 23, Table 2.1Saccorhiza, 23, 212, Table 12.2S. ramosa, 42Sagrina, 29Saracenaria, 28, Fig. 2.4Schlumbergerella, 133S. f l o r e s i a n a , Table 8.1Seabrookia, 28Sidebottomina, 33Sigmavirgulina, 29Sigmoilina, 27Sigmoilopsis, 27Sigmomorphina, 28Silicinidae, Table 2.1Silicoloculinida, 16, 17, 19, 22, 33, 35, Figs. 2.8, 2.9,

Tables 2.2, 2.3Silicoloculinidae, 33Silicoloculinina, 16, Fig. 2.7Siphogenerina, 29Siphogenerinoididae, 29Siphonaper ta , 27S. sabulosa, 79Siphonina, 30Siphoninacea, 30Siphoninidae, 30Siphonodosaria, 30Siphotextularia, 27S. affinis, Fig. 2.9Siphotrochammina lobata, 146Soritacea, 28, Fig. 2.1Sorites, 28, 126, 136, 157, 158, Table 8.1S. marginalis, 157, 158S. orbiculus, 136, 156, 157, Fig. 8.1Soritidae, 28, 43, 123, Fig. 8.4Soritinae, 123, 129, 136, 157, 158Sphaeroidina, 30S. bulloides, 193, Fig. 11.5Sphaeroidinella, 32S. dehiscens, 110, Fig. 7.3

370 TAXONOMIC INDEX

Sphaeroidinidae, 30Spirillina, 11, 28, Fig. 2.9S. vivipara, 48, 53, 54, Table 3.1Spirillinacea, 15Spirillinida, 17, 19, 22, 28, 58, Figs. 2.8, 2.9, Tables

2.2, 2.3Spirillinidae, 28Spirillinina, Fig. 2.7Spirolina hamelini, 158Spiroloculina, 27, 224S. atlantica, 83S. attenuata, 212S. excavata, Table 13.1S. hyalina, 47, 51, 58, Fig. 3.3, Table 3.1Spiroloculinidae, 27Spiroplectammina, 26, 212–214S. b i f o r m i s , 154, 216, Tables 12.2, 13.1S. earlandi, Fig. 12.6, Table 12.2Spiroplectamminacea, 26Spiroplectamminidae, 26Spiroplectinella sagittula, 155S. wrighti, 155Squamulina, 27, 35Squamulinacea, 27Squamulinidae, 27Stainforthia, 29, 212S. fusiformis, 155, 207–208, 209, 211 , 214, Fig. 12.6,

Tables 12.2, 13.1Stainforthiidae, 29Stetsonia, 30Stichostègues, Fig. 2.3Stilostomella, 30S. antillea, 80Stilostomellacea, 29Stilostomellidae, 30Stomatorbina, 30, 60Suggrunda, 33, 212S. eckisi, Table 12.2

Tappanella, 28Tawitawia, 27Technitella, 23, 212, Table 12.2T. legumen, 52Tenuitella, 32Textularia, 27, 158, 214, Table 12.2T. agglutinans, 79T. candeiana, 47T. conica, 79, 157T. earlandi, Fig 9.4T. kattegatensis, Table 12.2T. palustris, 146T. torquata, 154

Textulariacea, 26Textulariella, 26Textulariellidae, 26Textulariida, 18, 22, 26, Figs. 2.8, 2.9, Tables 2.2, 2.3Textulariidae, 10, 11, 27, Table 2.1Textulariina, 15, Fig. 2.7Textulariinae, 10Tinophodella, 32Tipotrocha, 26T. comprimata, 143, 144, 145, 146, Figs. 9.2, 9.3Tolypammina, 212T. vagans, 154, Table 12.2Tretomphalus bulloides, Table 3.1Trifarina, 29, 212T. bradyi, Table 12.2Triloculina, 27, 38, 157, 158, 224T. affinis, 155T. barnardi, 48T. brevidentata, Table 13.1T. marioni, Fig. 13.2, Table 13.1T. oblonga, 145, Figs. 3.13, 3.15Tritaxis, 26Triticites, 27T. secalicus, Fig. 2.9Trochammina, 26, 148, 153, 214, Table 12.2T. globigeriniformis, Table 12.2T. hadai, 153T. inflata, 143, 144, 145, 146, 147, 149, 289, Figs. 9.2,

9.3, 9.4, Tables 9.1, 13.1T. nana, Fig. 2.9T. ochracea, 154T. pacifica, Fig. 12.6, Tables 12.2, 13.1Trochamminacea, 26Trochamminida, 19, 22, 26, Figs. 2.8, 2.9, Tables 2.2,

2.3Trochamminidae, 26, Table 2.1Trochamminita salsa, 149, Fig. 9.4, Table 9.1Trochamminoides, 26Trocholinopsis, 32Tubinella, 28Tubinellidae, 28Tubinoidaea, 10Turborotalia, 32Turrilina, 59Turrilinacea, 29

Uvigerina, 29, 176, 177, 192, 212, 248, Figs. 11.5,15.2

U. akitaensis, Table 12.2U. bassensis, 154, 209U. curticosta, Table 12.2U. dirupta, Table 13.1

TAXONOMIC INDEX 371

U. juncea, Table 12.2U. laevis, Table 12.2U. peregrina, 42, 168, 171, 174. 177, 185, Figs. 10.4.

10.7, 11.5, Tables 12.2, 13.1Uvigerinidae, 29

Vaginulina, 28, Fig. 2.4Vaginulinidae, 28Valvulineria, 212V. mexicana, Table 12.2Valvulinidae, 27, Table 2.1Verneuilinacea, 26Verneuilinidae, 26, Table 2.1Vernueilinulla, 214, Table 12.2Vertebralina, 27, 157V. striata, Fig. 13.2Victoriellidae, Table 2.1Virgulinella, 29Virgul inel l idae, 29Vitrewebbina, Fig. 2.4Vulvulina, 26

Webbinella, 28, 157Wiesnerella, 27

OTHER TAXA

Acrostichum, 141Adamussium colbecki, 41Artemia, 42Arthrocnemum, 141Avicennia, 141

Bacillariophyceae, 123, Table 8.1Beggiatoa, 203, 207, 212, Fig. 12.4Belemnitella americana , 241

Chione, 287Chlamydomonas hedleyi, 135, Fig. 8.2

C. provasoli, 135Chlorophyta, 43, 123, 129, 135Chrysophyceae, 123, 136–137, Fig. 8.2, Table 8.1Crassostrea gigas, 230Cymodocea, 157

Drosera anglica, 152

Enteromorpha, 41

Gromia, 36, 212G. oviformis, 36Gymnodinium béii, 42, 137, Fig. 8.2

Halimeda, 156Halophila, 158

Juncus , 141

Nitzschia panduriformis, Fig. 8.2

Plantango, 141Porphyridium, 135P. purpureum, 135, Fig. 8.2Posidonia, 157Puccinellia, 142Pyrrophyceae, 123, Table 8.1

Rhizophora, 141Rhodophyta, 43, 123, 135, Fig. 8.2, Table 8.1

Salicornia, 141Spartina, 141, 142S. alterniflora, 144, 288Symbiodinium, Fig. 8.2

Thalassia, 136, 158

Zostera, 157

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Modern Foraminifera