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Paleoecology, Biostratigraphy, Paleoceanography and Taxonomy

Series C: Mathematical and Physical Sciences - Vol. 327

AGGLUTINATED FORAMINIFERA: AN INTRODUCTION

CHRISTOPH HEMLEBEN AND MICHAEL A. KAMINSKI

Geologisches Institut,University of Tiibingen Sigwartstr. 10,D-7400 Tiibingen, FRG GEOMAR. Wischhofstr. 1-3, 0-2300 Kiel, FRG

Unicellular protozoans are among the oldest fossils which we can recognize from the Precambrian. Presumably, foraminifera1 ancestors were among the earliest of them, but had not yet benefitted from being sheltered by a biomineralized test. During the earliest Cambrian the first agglutinating foraminifera made their first appearance in the geologic record. These "primitive" forms built their test of foreign particles held together by an organic cement. This organic cement may have been secreted by the foraminifer in cytoplasmic vacuoles as is the case with Recent agglutinating foraminifera. Yet, the capability to biomineralize calcite did not evolve until after another 60 million years when the fusulinids developed their microgranular wall. Calcitic cemented agglutinates occur even later, at the base of the Carboniferous. Thus, in the fossil record the agglutinated foraminifera occur as a twofold group with a rather distinct evolution.

The long geologic history of the agglutinated foraminifera, the fact that most modern groups of these organisms are represented as fossils make them ideally suited for evolutionary studies. The challenge set out for future studies is to select meaningful morphologic characters which can serve as a base for reconstructing the phylogeny of agglutinated foraminifera and thereby derive a "natural" system of classification.

One proposal which is quickly gaining acceptance is to develop a suprageneric classification which takes into account the structure of the agglutinated wall and the nature of cement. Traditionally, all foraminifera with agglutinated walls have been placed in a single suborder, the Textulariina. During the session on Taxonomy at the Tubingen Conference, several researchers gave presentations on wall structure and the nature of cement. These presentations made abundantly clear the point that several fundamentally different types of wall structure exist which can serve as a basis for a higher-order classification of the Textulariina. Already in 1988, Br6nnimann and Whittaker proposed that non-caniculate forms which have an agglutinated wall bounded by an internal and external organic lining ought to be placed in a separate suborder, the Trochamminina. Undoubtedly, the composition of cement and the layering of the wall are conservative traits which are manifestations of underlying differences in the genotype.

After the technical session on taxonomy, an ad-hoc working group convened to discuss which criteria would be most acceptable for an eventual revision of the suprageneric classification of the agglutinated foraminifera. All those present agreed that more observations are necessary on the type and structure of cement, the nature of pores or canaliculi, and the layering of agglutinated grains. Although unable to participate in the Tubingen Conference, Vera Podobina (this volume) places strong emphasis on the relative proportions of cement vs. agglutinated material or "xenosomes" using the terminology of Schr6der et a1.(1988).

C. Hemleben et al. (edr.). Paleoecology, Biostratigraphy, Paleoceanography and Taxonomy of Agglutinated Foraminifera, 3-11. O 1990 by Kluwer Academic Publishers. Printed in the Netherlands.

In this introduction, we wish to point out some aspects in the classification of agglutinated foraminifera which are essentials in the development of a new systematics and that deserve further attention.

Wall structure: Already in 1964, Loeblich and Tappan used the structure of the foraminifera] wall as the highest criterion in the suprageneric classification of the foraminifera. Shortly after the Tiibingen meeting, Loeblich and Tappan (1989) proposed subdividing the agglutinated foraminifera into four separate suborders based upon the wall structure and composition of the cement. Loeblich and Tappan's proposal, based primarily on studies of test ultrastructure conducted at Tiibingen University (Bender and Hemleben, 1988a,b, Bender, 1989) has a sound conceptual basis, but presents quite a challenge for re- searchers who are doing any serious work on the taxonomy of agglutinated foraminifera. For one thing, only a small fraction of the 624 genera of agglutinated foraminifera discussed in the "new treatise" of Loeblich and Tappan (1987) have been seriously studied in terms of their wall structure.

But just how many different types of wall structure are there? In his study of Upper Paleozoic agglutinated foraminifera with microgranular-agglutinated wall structure, Piller (this volume) points out that the distinction between some Paleozoic forms traditionally classified in the suborder Fusulinina (e.g. paleotextulariids, tournayellids and endothyrids) would be placed in the Textulariina had they been described from post-Paleozoic strata. According to Piller, the separation of these Paleozoic "fusulinids" and Mesozoic taxa with microgranular wall structure (e.g. the Nautiloculinidae, Barkerinidae, Mesoendothyra, and others) into two different suborders is largely artificial. Clearly, we must reassess the current classification of these forms based on detailed phylogenetic studies. Perhaps future studies will place the microgranular-agglutinated forms in proper perspective.

A major question is can we actually use microstructural criteria for understanding the evolutionary history and phylogeny of agglutinated foraminifera? Taphonomic and diagenetic changes in the wall structure and composition of cement can present a major stumbling block in investigations of fossil material. The organic cement of fossil material is often preserved as silica. We have selected an example which illustrates the potential of using cement type in classification (Plate 1, Fig. 1, 2). Plate 1, fig. 1 shows organic cement coating agglutinated grains in a modern specimen; in fig. 2, coatings of cement are also visible, but in this case the specimen is from the Upper Cretaceous of DSDP Hole 543A, and the organic cement is preserved as silica. Selecting the nature of cement as a primary criterion for the suprageneric classification of 624 genera will require much more tedious observation.

Presence o f per forafions: Over the past decade there has been a tendency to separate genera of agglutinated foraminifera which utilize calcareous cements into 2 groups, based on the presence or absence of "pores", "protopores", "pseudopores" or "canaliculi". Many solid- walled and canaliculate forms are quite homeomorphic, for example, Desai and Banner's (1987) Dorothia and Praedorothia. This raises the question just how important are wall perforations for taxonomy? To answer this, we first must tackle the question "What is the function of porous wall structures and what environmental advantage do they bring?".

In their now classic revision of the textulariids, Banner and Pereira (1981) remarked that perforate wall structure was acquired by various lineages mainly after the late Paleocene. Other genera never acquired perforations, and some lineages acquired them only in the

Neogene. This observation, if verified among other groups, opens the possibility that porous wall structure may have developed in various distantly-related generic groups in response to some yet undetermined environmental forcing function. T o extend the analogy, surely if birds didn't have porous bones, they wouldn't fly.

Although this discussion concerns mainly forms with calcareous cement, we find analogous pore structures among forms with organic cement. Berggren and Kaminski (this volume) provide an example of analogous "pore" development among the cyclamminids. Perhaps it is no coincidence that the earliest representatives of the alveolar genus Cyclanlrnirla (the genus Reticulophragrnoides) first evolved from a small, solid-walled Haplophragrnoides ancestor during the Paleocene (see above), and only have alveoles in their later (largest) chambers. This implies some relationship between porous structures, their function and size and/or wall thickness of the test. This leads to additional questions: Do larger foraminifers need thicker walls, and therefore need to construct a pore system? Is there a relationship between the acquisition of pores and phylogenetic size increase? Speculations in the literature about the function of perforations varies. Berthold (1976) suggested that they are useful for the exchange of dissolved gasses and cations through the wall. Some further insight may be given by the fact that calcitic cemented species are porous, while organically-cemented species lack such a system, except those which build a rather thick wall. The latter need to develop an analogous system, an alveolar system. In terms of functional morphology, are these constructional features linked to lightening the test, to gas exchange, or in the case of forms inhabiting the photic zone, to improve environmental conditions fo r symbionts?.

Now with the successful development of oxygen microelectrodes and their use in helping understand the microenvironments of planktonic foraminifers (Jdrgensen et al., 1985), the technology is now available to address this problem. Tests need to be performed on forms with both perforate and organically-cemented, non-porous walls under varying oxygen conditions to determine whether the presence of pores gives any physiological advantage. It is interesting that under conditions of low oxygen in the Drammenfjord, a non-perforate form, Glornospira, seems to be the most successful foraminifera (Alve, this volume). This form, though, has a large surface area due to its discoidal shape. Agglutinated foraminife- ra from late Cretaceous oxygen-poor environments in Israel (Almogi-Labin et al. this volume), include a mixture of flattened or angular solid-walled forms as well as perforate forms that are more rounded. From these observations it seems that the more rounded forms are most sensitive to low oxygen conditions, whether they have pores or not.

Grain selectiorl: During the winter of 1916, the halls of the British Microscopical Society were host to a livid exchange of ideas between Edward Heron-Allen and Sir Ray Lankester, the eminent Physiologist. On the occasion of one of his addresses as president of the society, Heron-Allen displayed examples of the remarkable selective capability of certain species of agglutinated foraminifera to select, for example, a single sponge spicule of a given length, or grains of gem minerals when such grains are rare in the sediment. Heron-Allen remarked that his agglutinates possess "faculties akin to intelligence" that would certainly be ascribed to them had they been higher animals. Sir Ray opposed the use of the word "intelligence" and the pair agreed that in the case of agglutinated foraminifera, one cannot use the strict sense of the word "as currently defined in the Oxford Dictionary".

There has been much speculation about the adaptive benefits of grain selection, but exactly 75 years after Heron-Allen's presentation, the fundamental question of how certain

foraminifers select grains of a particular composition remains unanswered. Tappan and Loeblich (1988) explained some apparent selectivity of agglutinated material as the result of preference of a newly settling embryo for a particular substrate. Considering the importance of grain selection for taxonomy, there are surprisingly few experimental studies to determine whether selectivity for size or composition has a true genetic basis.

From our own experimental work, we know that some investigated species do not possess the capability to select chemotaxically, instead they are able to select a certain grain size out of a larger spectrum. Different sizes are used which are adequate to their morphological posi- tion. A specimen of Clavulina nodosaria was maintained in laboratory culture in order to test the selectivity. Spiculae were used for the general wall, smaller voids were filled with small artificial (Carborundum) grains, but the aperture was built out of small particles only (Bender, 1989). We think that the grain size selection is masked sometimes by the chemotaxic selection. In the cases we observed in laboratory cultures, specimens choose a certain grain size from the available spectrum of grains regardless of their composition. Still, much experimental work remains to be done.

Growth and Reproduction: We now know from sediment-trap studies carried out in the open ocean that the supply of food to the deep-sea is highly seasonal (Bishop et al. 1977), and that benthic organisms can react very quickly to metabolize this annual or semi-annual bounty (Gooday and Turley, 1990). One of the main unsolved problems is how this seasonal flux of organic matter affects the growth (and lifespan) and reproductive activity of benthic foraminifers. What acts as a trigger for reproduction? On recent cruises of the R/V Meteor, which coincided with the spring bloom. we observed a high amount of juvenile foraminifera. When we collected deep-sea foraminifera just after the fall bloom, they reproduced in the laboratory shortly thereafter. This leads us to another question: Do the same species behave differently under different annual cycles of particulate organic flux, for example in the high latitudes where only one (2-3 weeks duration) bloom occurs each year (Wefer et al. 1982) vs. the mid latitudes with its spring and fall bloom? How much is the size of the population affected by a yearly variable primary productivity in the photic zone. These and other questions are necessary to be solved. How much do these biological triggered changes in the environment effect reproduction schedules, and therefore the exchange of gene pools between different populations? Does food supply affect the onset of reproductive maturity, and is it therefore a forcing function for the evolutionary mechanisms of paedomorphosis and progenesis?

Phylogeny: As pointed out by Hohenegger (this volume), the current use of classification system based on phenetics (morphologic traits) for the foraminifera is contrary to all the taxonomic principles accepted by biologists since the rise of "New Systematics" (Huxley, 1940). However old habits die hard. Since nearly all the taxonomic work on agglutinated foraminifera over the last century-and-a-half was carried out by the Paleonto- logic community, the systematics now in use are based almost entirely on attributes such as chamber arrangement, position of the aperture, and other aspects of overall morphology. This remains an inherited burden which we as paleontologists must bear, even though we are all too aware of instances of convergent evolution and the repeated evolution of certain successful traits. A "natural" system of classification must be based on shared derived characters, which can only be determined by detailed studies of the stratigraphic record. This

is a point which had already been stressed by R.J. Schubert in 1908. In this paper, Schubert referred to some of his early work on Textularia, stating "the name Textularia is not a taxonomic unit. It is rather a randomly assembled homeomorphic name for similar phylogenetic phases from different lineages".

Perhaps the most important single postulate for deriving a classification of organisms, as Hohenegger (this volume) points out is the consistency of criteria used for classifying objects: or to paraphrase his oral presentation at the Conference, "during the development or any system of classification, the criteria upon which the system is based must not be changed. Berggren and Kaminski (this volume) termed this "Hohenegger's Law".

In his classic textbook on Foraminifera, Joseph Cushman proposed the first modern phylogenetic scheme which was based to a large extent on studies of the fossil record. Cushman began his phylogenetic studies with the assumption, prevalent at the Harvard School at the time, that the principles of recapitulation can ultimately be used to derive the phylogeny of a given group of organisms. Although Cushman's views were later influenced by his stratigraphic studies, his phylogenetic tree published in the fourth and final edition of his textbook (reproduced in Figure 1) still displays obvious traces of his early recapitulationist views. Cushman made it clear, however, that he regarded his proposal as a working hypothesis to be verified later by stratigraphic studies.

Figure 1. Phylogeny o f foraminifera1 families, after Cushman (1948) .

TEXTULARIEUIDAE

PSNDOBOLIVINIDAE

WNOTROCHMINIDAE SPlROClCLINlDAE

HADNNI IDAE C Y C M l N l D A E

COSC INOPHRAWIAT IDAE

ORB ITOPSELLIOE LABY R I N T H I r n T IDAE CHARENTI IDAE

HAPLOPHIURI IDAE

MYI lC lN IDAE

TELMINIDAE R Z E H A K ~ N ~ D E HAPLOPWUh'JlDIDAE

t \ f THCWSINYLIDAE

NOTODENDRODlDAE

DRYORHIZOPSIDAE POLYSACtAmlNIOAE

LAGYNIDAE \ / PHTHANOTROCHIDAE VLOG~HI HOSPITEUIDAE

/ M Y L I S O R I IDAE

1 Figure 2. Fanlily phylogeny of agglutinated foraminifera (after Tappar1 and Loeblich, 1988).

The four-part subdivision of the agglutinated foraminifera into separate sub-orders based on wall structure (Loeblich and Tappan, 1989) is already evident in the new phylogeny of agglutinated foraminiferal families proposed by Tappan and Loeblich (1988), reproduced in figure 2. In this phylogenetic scheme, the nominate families of the four new suborders (Astrorhizina, Haplophragmiina, Textulariina, and Trochamminina) serve as nodes from which other families branched off.

But is our assumption that cement and wall structure forms the highest-order criterion for classification a sound one? The basis for an envisaged suprageneric classification, and indeed the current subdivision proposed by Loeblich and Tappan (1989) rests upon the assumption that the evolution of certain traits are unique evolutionary events. If, for example, the ability to utilize a given type of cement evolved more than once among different lineages, then strictly adhering to the "New Taxonomy" would result in the multiplication of suprageneric names. Berggren and Kaminski (this volume) pointed out one such example among the Cyclamminidae. This is indeed the case among the planktonic foraminiferal groups.

Loeblich and Tappan (1987) considered wall microstructure to be of major importance and placed genera with perforations into separate families and superfamilies. There is, however, a problem with this view. Desai and Banner (1987) pointed out that the phylogenetically more advanced canaliculate wall has evolved repeatedly from non-canaliculate ancestors. They demonstrated that the canaliculate genus Dorothia may polyphyletic, having evolved at least twice.

In their recent review of the problem, Loeblich and Tappan (1989) consider perforate wall structure as a systematic feature characterising the superfamily Textulariacea, "rather than having repeatedly evolved within a single genus or lineage". However, evidence for the repeated evolution of perforate wall structure is mounting. Piller (this volume) gives convincing proof that some Paleozoic microgranular-agglutinated forms had also acquired pores.

Many of the topics we addressed in this brief review were discussed at the Tijbingen Conference, and the papers presented in this volume pose quite a few new questions concerning the classification and systematics of agglutinated foraminifera. We hope that by outlining some important outstanding problems, we can inspire research that will eventually lead to the fulfillment of Schubert's unrealized dream: to derive a "natural" classification based on phylogeny and biologic principles.

References

Banner, F.T. and Pereira, C.P.G. (1981) Some biserial and triserial agglutinated smaller foraminifera: Their wall structure and its significance. Journal of Foraminifera1 Research 11, 85-1 17.

Bender, H. and Hemleben, Ch. (1988) Constructional aspects in test formation of some agglutinated foraminifera in Gradstein, F.M. and Rogl, F. (eds), Second Workshop on Agglutinated Foraminifera : Abh. Geol. Bundesanstalt, Bd. 41, p. 13-21.

Bender, H. and Hemleben, Ch. (1988) Calcitic cement secreted by agglutinated foraminifers grown in laboratory culture : J. Foram. Res., v. 18(1), p. 42-45.

Bender, H., 1989, Gehauseaufbau, Gehausegenese und Biologie azlutinierter Foraminiferen (Sarcodina, Textulariina) : Jb. Geol. B.-A., v. 132, p. 259-347.

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Foraminifera : J. Foram. Res., v. 6(1), p. 22-29. Bishop, J.K.B. Edmond, J.M. Ketten, D.R. Bacon, M.P., and Silker, W.B. (1977) The chemistry, biology

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of biogenic components from sediment trap deployment in circumpolar waters of the Drake Passage : Nature, v. 299(5879), p. 145-147.

'I. . - 3.. .

Plate 1. 1-2. Examples of organic cement in (1) a recent specimen of Bathysiphon sp., and (2) an Upper Cretaceous specimen (Bathysiphon sp.) from DSDP Site 543 in which the cement is preserved as silica; the dashes measures IOpm and 2pm respectively.