THE ROLE OF FORAMINIFERA IN THE TROPHIC STRUCTURE OF MARINE COMMUNITIES

JERE H. LIPPS A N D JAMES W. VALENTINE

I ipps, J. H., & Valentine, J. W.: The role of Foraminifera in the trophic struc- ture of marine communities. Lethaia, Vol. 3 , pp. 279-286. Oslo, July 15th, 1970.

Foraminifera are recorded as feeding chiefly upon bacteria, small diatoms, and nannoplankton in a wide variety of marine environments. Thus their food items are usually below 50 p and commonly below 25 p in size. Predators upon Fora- minifera range from highly specialized microcarnivores that feed largely on Foraminifera to less selective ones that include Foraminifera in a mixed diet and to generalized feeders that ingest Foraminifera along with much other material.

Foraminifera thus form part of a key link in marine food chains, assimilating energy available from minute autotrophs and also retrieving energy available during the final stages of degradation of organic debris. In turn, they support a variety of larger organisms and thus contribute to the diversity and secondary productivity of ecosystems.

J . W. Ihlentine, Department of Geology and Institute of Ecology, University of Cali- fornia, Daris, California ; J . H. Lipps, Bodega Marine Laboratory, Bodega Buy , California ; April 27th, 1970.

An important aspect of any group of organisms from both ecologic and evolutionary points of view is the part played by that group in channeling the flow of energy within the community in which it lives. Although Fora- minifera have been widely studied from taxonomic and biostratigraphic points of view, little is known of their place in the economy of the bio- sphere. The ecology of living Foraminifera has been investigated by many workers, but chiefly in a fashion designed to lead to more sophisticated biostratigraphic and paleoenvironmental interpretations. This work has consisted of the description of foraminiferal associations (usually omitting other organisms) and of the distribution of these associations, and occasion- ally of the correlation of the patterns with environmental factors. Of the dynamic attributes of foraminifera1 ecology-such as reproductive strate- gies, population densities and fluctuations, and biotic interactions-only very little evidence is available, although research on these subjects has begun. Our purpose is to collate records and observations of the food and predators of Foraminifera, and to present a trophic model that may provide a basis for further paleoecologic as well as evolutionary studies.

Although the food materials of Foraminifera have not been adequately studied in nature, there is evidence to indicate that Foraminifera feed primarily upon very minute organisms (<50 p). For example, Lee & al.

280 JERE H. LIPPS AND JAMES w. VALENTINE

(1966) recorded 27 species of diatoms, 6 species of bacteria and 3 other forms, all of which averaged less than 50 p in size, associated with a high density foraminifera1 population off Long Island. The precise food items of the Foraminifera were not determined. However, bacteria and small diatoms in this size range have been identified as food sources in some natural situations (Myers, 1943 ; unpublished data, paleobiology group, Bodega Marine Laboratory), and bacteria may be a required food item of most Foraminifera (Muller & Lee, 1969). In culture, Foraminifera appear to ingest small materials (Bradshaw, 1961; Lee & al., 1966; Murray, 1963; Myers, 1943 ; Sliter, 1965).

In the following sections we summarize present knowledge of the trophic position of Foraminifera in communities inhabiting a number of distinctive marine environments.

Muddy-bottom shelf communities

Marine muds contain a variety of small material suitable as food for micro- herbivores. Marine marshes, for example, contain a great abundance of organic detritus, bacteria and epiphytes of various kinds (Odum & LaCruz, 1963; ZoBell & Feltham, 1942; Lackey, 1967), the former constituting an important link in the food chain between large primary producers and secondary producers. Many larger invertebrates cannot utilize such small food items or do not feed where this material occurs. Many detrital feeders, however, ingest minute organisms, and some are known to digest bacteria (as Hq'drobia ; Korringa in Darnell, 1967). Smaller herbivores can generally utilize small food. Protozoa, particularly ciliates (Lackey, 1967) and Fora- minifera, and metazoa such as rotifers, nematodes, some polychaetes and others, consume a large amount of bacteria and small epiphytes. Although marine marshes are dominated by only a few species of arenaceous Fora- minifera, they are often present in great density (Phleger, 1960).

Mare (1942), in a splendid study of the interrelations of marine micro- organisms, stressed the significance of marine Protozoa in the food chain of the subtidal mud communities off Britain, and their importance in the cycling of organic matter. Perkins (1958) has further demonstrated the general importance of bacteria and of diatoms in the diet of marine Protozoa. In deeper offshore areas where light is limited, bacteria are probably the main constituents of protozoan diets. In these areas, too, Foraminifera may attain high densities-up to 29 million living individuals in each square meter have been reported (Phleger, 1960). Foraminifera must be important herbivores in mud bottoms.

The microcarnivores that feed on Foraminifera in muddy environments are diverse. Some detritus feeders incidentally include Foraminifera in their food, such as do some species of the gastropods Xenophora and ilstraea (Morton, 1959), but it is unlikely that Foraminifera are staple items in the diets of these larger forms. Other carnivores more particularly search

FORAMINIFERA AND TKOPHIC STRUCTURE 281

out Foraminifera, like the small prosobranch Bittium (Graham, 1955) and the crustacean Gonoplam (Mare, 1942) and some hermit-crabs of the genus Eupagurus (Orton, 1927; Turpayeva, quoted in Sokolova, 1957). Some are even specialized to feed on Foraminifera, for the small bullomorph opistho- branchs Retusa and Cylichna have ‘gizzards’ or mills which can crush foraminiferal tests ; they have been recorded as predators upon muddy- bottom Foraminifera (Bacescu & Carcaio, 1956; Morton, 1958 ; Moore, 1961). Although these data are incomplete, it appears that Foraminifera, as well as other Protozoa, have a distinctive place in the trophic structure of muddy bottom communities.

Sandy-bottom shelf communities

In general, as grain size increases in sedimentary substrates, the amount of organic matter present declines. Thus on progressively coarser sands there is progressively less fine organic debris, and bacterial abundance probably declines as well. Standing crops of Foraminifera are expected to decline also in coarser sediments, as their food sources diminish. This theoretical expectation accords well with observation. Collecting records from various Recent sands confirm that Foraminifera are least abundant in coarse sand sediments (for example, Uchio, 1960), and micropaleontological experience is that foraminiferal abundance tends to be lower in coarse sand sediments. Foraminifera are nevertheless present and locally diverse in coarse sediments. Many Foraminifera that live in sands have special feeding habits which are probably associated with the low food supply; for example, species of Elphidium extend pseudopodial nets which cover relatively large areas (Jepps, 1942).

A remarkably early observation of predation on sandy-bottom Forami- nifera is recorded by Anton van Leeuwenhoek in 1702 (Hoole, 1807, pp. 271-272, Fig. 37), who noted that shrimp and other organisms eat Foramini- fera. Other foraminiferal feeders include scaphopods (Lacaze-Duthiers, 1856), species of Olivella (Olsson, 1956; Marcus & Marcus, 1959) and probably bulloid gastropods. Small sandy-bottom worms may selectively utilize Foraminifera, which are recorded among gut contents of young errant polychaetes (Perkins, 1958). Furthermore, sand-dwelling Foraminifera will be ingested by generalized deposit feeding animals such as holothurians, but their place in the diets of these larger organisms is unknown.

Rocky-bottom communities

Many rocky -bottom communities are associated with turbulent environ- ments so that there tends to be relatively little fine detritus present. Never- theless, organic detritus does collect in the holdfasts and mats of megascopic algae. Bacteria, diatoms and other unicellular algae thrive in these places. In addition, the fronds of larger algae, particularly certain coralline species,

282 JERE H. LIPPS AND JAMES W. VALENTINE

support large standing crops of attached bacteria and diatoms (Lee & al., 1966; DeLaca & Lipps, in preparation), and algal ‘slimes’ on rock surfaces commonly contain bacteria. In all these microhabitats, Foraminifera are locally diverse and common. For example, in highly turbulent rocky-shore intertidal areas on Bodega Head, California, nearly 20 species of Foramini- fera live among algae or are attached to firm substrates (unpublished data, paleobiology group, Bodega Marine Laboratory). Their densities on some of the matted algae are on the order of several hundred, per 10 cc. of algae, while a hundred individual Foraminifera have been observed attached to a single small frond of the coralline alga Corallina (DeLaca & Lipps, in pre- paration). Many of these rocky-shore species of Foraminifera have been maintained in cultures where they have been fed small diatoms and bacteria.

We do not know of any rocky-bottom predators that feed exclusively on Foraminifera, but it is likely that small grazing metazoans feeding on epiphytes and epizoonts regularly ingest Foraminifera, which are recorded in the gut contents of gastropods such as Patella (Pelseneer, 1935) and Tricola (Marcus & Marcus, 1960).

Abyssal benthonic communities

Although the trophic structure of abyssal communities is poorly known, the diversity of life now recorded from abyssal depths (Hessler & Sanders, 1967) testifies to a dependable food source there. Probably a significant amount of regeneration occurs on abyssal bottoms. I t seems probable, by analogy with other communities, that abyssal Foraminifera consume bacteria and extremely minute organic particles (and perhaps larger food items as well) and if so, their trophic role in these communities may be of even more importance than elsewhere. For the abyssal zone there are records of apparently rather selective predation of Foraminifera by scaphopods (Wolf, 1961), of the inclusion of Foraminifera as a probably important item in a somewhat varied diet by pectinids (Knudsen, 1967), and of incidental ingestion of abyssal Foraminifera together with major food items by decapods (Sokolova, 1957).

Pelagic communities

The biology of planktonic Foraminifera is essentially unknown, so that their widespread use as biostratigraphic guides and ecological indicators is entirely empirical. Ryther (1969) has summarized pelagic food chains. As he points out, it has been increasingly apparent that the bulk of primary productivity of truly oceanic waters is due to the nannoplankton, which range in size only between about 5 and 25 p. In general, the nannoplanktonic organisms are too small to be captured by most metazoan herbivores. Before the energy they represent can be utilized it must be assimilated by small herbi- vores, and these are chiefly the planktonic protozoans, including radiolarians

FORAMINIFERA AND TROPHIC STRUCTURE 283

and Foraminifera. The nannoherbivores are preyed upon in turn by small carnivorous zooplankters, including chaetognaths (Croce, 1963), thecosome pteropods (Boas, 1886), and others. Thus the planktonic Foraminifera play a significant role in a key trophic level in pelagic communities by assimilating energy from minute photosynthetic organisms.

In coastal waters, the phytoplankton is dominated by ‘larger’ micro- plankton, chiefly diatoms, which range to over 100 in size. These phyto- plankton can be directly preyed upon by copepods, planktotrophic larvae, numerous other pelagic forms, and even a wide variety of suspension feeding benthonic forms. The intermediate microherbivore level is not required, although it may be present, and this may account in part for the lack of endemic species of planktonic Foraminifera in coastal waters. Some metazoa that feed on radiolarians and Foraminifera in offshore waters, such as the pelagic crab Pleuroncodes, switch to larger diatoms in coastal upwelling waters (Longhurst, Lorenzen, & Thomas, 1967).

Summary and conclusions

It is clear from the foregoing account that our knowledge of foraminifera1 diets and predators is still very fragmentary. Foraminifera must consume a greater range of food than is yet recorded, and quite a variety of small carnivores for which feeding records do not yet exist, such as small gastro- pods, crustaceans and worms, probably utilize Foraminifera as regular diet items. Nevertheless the fundamental and probably primitive role of Fora- minifera seems to be as consumers of minute organisms and probably detritus; when they have assimilated part of the abundant energy available at this level, it can be passed on to larger organisms on higher trophic levels. This is a particularly critical level in the energetics of communities on two counts. First, the number of organisms that regularly feed upon the very small microflora and nannoflora appears to be moderately limited. This is especially true in pelagic communities and in bethonic communities on hard substrates ; on sediment substrates, numbers of large deposit feeders evidently can and do utilize these minute organisms. Secondly, this level represents a very late stage in the degradation of organic debris and the concomitant regeneration of inorganic nutrients, which must thereafter be taken up by photosynthesizers. When bacteria are eaten by Foraminifera and other groups, energy not otherwise available is retrieved to support a variety of organisms.

The organisms exploiting Foraminifera as food range all the way from specialized microcarnivores to forms that utilize Foraminifera as important items in mixed diets and to those that include relatively small numbers of Foraminifera in generalized diets. This trophic model is summarized in Fig. 1.

If this model proves to be rather general, then the utilization of larger food particles by some Foraminifera may well represent a secondary speciali-

284 JERE H. LIPPS AND JAMES w. VALENTINE

zation. It will be of great interest to test our conclusions, for the evolutionary pathways of Foraminifera may to some extent be amenable to interpretation in terms of specialization or elaboration of their trophic roles. Furthermore, increasing knowledge of their trophic positions may eventually permit the evaluation of their contributions to the evolution of ancient ecosystems.

NUTRIENTS

I

INannop lonk ton - - - - - -- - - - 7 (Mlcroplankton in coasta l wa te rs )

N o n n o h e r b i v o r e s o r M i c r o h e r b i vores [LO RA MlNlFE RA] in open ocean

~ 1 Microcar;ivores

1 ~

(Chlef ly smaller - - - zaopla n k ton )

C o r n i v o r e s -. (Larger Zooplankton

and Nektan)

Benthonic Diatoms

I I I I I I 1 I I I I I

M i c r o h e r b i v o r e s

M i c r o c a r n i v o r e s _ _

.1 M o c r o f o u n o

Permanent Detr i tus

Fig. 1 . Generalized diagram showing the position of foraminifera in the trophic structure of marine communities. Data chiefly from Mare (1942) and Ryther (1969), together with other sources cited in text.

FORAMINIFERA AND TROPHIC STRUCTURE 285

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