A Spineless Column by Ronald L. Shimek, Ph.D.

Foraminiferans


Over the last several years I have spent a considerable amount of time trying to convince marine reef aquarists that one of the most useful and important components of a coral reef aquarium system is the deep sand bed. With over thirty years of experience as a marine ecologist studying the interactions in sediment ecosystems, I have acquired a tremendous urge to discuss the importance of such beds in great and wondrous detail, and I have been fortunate enough to have been able to do so at numerous conferences and aquarium societies. Often, however, this has had the interesting side effect of causing most people to drift gently into dreamland. While such events are indeed a cause for puzzlement, I have decided that exploring its cause would be less than enlightening. Rather in this month's column, I decided to forego my usual quarterly discussion of reef aquarium sand beds.

Instead, I thought I would take this opportunity to acquaint you with some of the most unusual organisms that make their way into coral reef aquaria, the Foraminifera. Forams, as they are commonly called, are marine creatures found in a wide variety of habitats. They are not animals; they lack not only a number of animal characteristics, but also the photosynthetic capabilities of organisms such as plants or algae. So, biologists consider they are neither plants nor animals, and they are taxonomically placed in a separate kingdom, with a number of other groups of bizarre creatures. This kingdom is called the Protista. Even though they are not animals, some protists, such as forams and some other protozoans, act somewhat like animals.

While many protozoans are not clearly visible to the unaided eye, forams are often evident and common in many marine environments, and those found in aquaria are often large enough to be observed easily with a hand lens or magnifying glass. Even so, though, they tend not to show too much detail. This is due to two reasons, first the detail that is there is often very tiny, below the range of normal visual acuity, and secondly, due in part to the type of body these organisms have there is often not much detail to see. They simply don't have a body divided into separate parts or structures to see any detail.

Figure 1. A foraminiferan collected from my aquarium.

Many of the forams found in aquaria are best observed with a hand lens. These are available on-line from biological or geological supply houses and will magnify ten to twenty times. Using such a lens, an aquarist will be able to clearly see foraminiferans and many other small organisms if they are near the aquarium walls. Magnifying glasses will also work, but they typically don't magnify the organisms sufficiently.

As the typical aquarist discovers, our hobby is rife with unusual organisms. Coral reef organisms, in general, are not that familiar to most folks. We are terrestrial animals, and the other animals we are familiar with are also terrestrial organisms. Oceanic environments, such as coral reefs and the deep sea contain strange and often wonderful creatures. Our aquaria are proof of that, but even amongst the strange and wonderful organisms of coral reefs, foraminiferans classify as a "wee bit weirder" yet. Foraminiferans are truly amongst the most unusual creatures in our systems.

Forams and their relatives are organisms that are simply constructed; they may be described as an amoeba in a shell. Probably the most basic and primitive type of animal-like living creatures that many people ever see are the amoebas often used in introductory biology or even a general science course to show a "primitive" single cell. However, that so-called primitive characteristic is misleading. Even a common amoeba is many thousands of times larger and more complex than a bacterium, an organism that is a much more basic and primitive form of life. To some extent, then, the apparent simplicity of an amoeba or foraminiferan is misleading. On the other hand, the level of intracellular structure seen in these organisms is quite low compared to such complicated protists as ciliates.

Figure 2. Scanning electron micrograph of a test or shell
of the foraminiferan, Cribrononion lene. The small pores,
or "foramina," found in the test or shell are the basis of the
name for the group of organisms.

The amoeba that most people have seen is the common Amoeba proteus or the delightfully named Chaos chaos. However, these particular species are only a couple of the many kinds of related organisms at this level of body structure. Many people consider that amoebas and other protozoans are organisms that are made of only one cell. Another, equally valid way of looking at them, however, is as organisms without any cells at all. How we consider these organisms, as having one cell or being without cells, significantly colors our appreciation of them. We are organisms constructed of many trillions of cells, and we tend to, with more than a little bit of hubris, look upon ourselves as the pinnacle of life. From this point of view, a lowly little one-celled blob is hardly worth any consideration at all. On the other hand, if we consider both ourselves and amoebas simply as organisms, we can see that these little blobs are more than they might otherwise seem, for both humans and amoebas are organisms, and must face some conceptually similar problems. All organisms must meet and successfully pass certain tests. They must obtain nutrition, grow, reproduce, sense the environment, and avoid being eaten. It may well be that amoebas are primitive. It may also be that they are very well adapted to a wholly different environment than we are, and are in fact, within that context not any less successful than any other widespread organism.

Nonetheless, the amoebas are not large complex multicellular animals. They are minute blobs of protoplasmic goo that are adapted to slither around on wet surfaces, either under water, in wet soil, or inside of other organisms. They have no defined shape or orientation. Front is simply the direction they are moving at the moment. Their body is almost infinitely deformable. They are small enough that they have no need for any special system to eliminate wastes, send nervous impulses or eat. They eat by simply enfolding their body surface to enclose a tasty food item in a bubble of cell membrane material. Once encased inside their body, digestive enzymes are secreted into the bubble surrounding the food item and it is dissolved. Indigestible food is simply expelled from the body. Respiration or other gas exchange simply occurs across their body surface.

Foraminiferans have been called the "the most common group of non-bacterial organisms in the world." They are in uncountable numbers in and on all ocean bottoms and in the marine plankton. I have worked with some foraminiferan predators called scaphopods. In some of the areas where the scaphopods are abundant and I have sampled foraminiferans, there are more than 70,000 forams per square yard of ocean bottom. These abundances appear to be typical or even on the low side for some marine environments. In some places, skeletons from dead planktonic foraminiferans have settled to the ocean bottoms to form layers of "foraminiferan ooze" more than 6,600 feet thick. They are also quite abundant in most natural coral reefs and in reef aquarium systems, yet most aquarists remain unfamiliar with them.

Here is an image of the test or shell of the pelagic foram Globigerina sp.

Many fantastic images of forams, living and dead, can be found by following this link.

Although foraminifera are often thought of as simply being amoebas possessing an outside shell, there is more to them than that. Not the least of the problems with such a simplistic approach is that the shell is actually interior to the outer cell membrane that constitutes the outer surface of the organism. Nonetheless, these shells act as support and protection for the majority of the protoplasm that constitutes the foram's body. Three basic shelled foram types may be recognized, defined on the basis of differences in their shell, and recently a few naked forams have been found as well. The naked forams are unusual for a second reason, that being they are found in fresh water. All other forams are marine. Foraminifera with the first skeletal type are called agglutinated or arenaceous forams. They glue sand and other materials together to form an irregular, often star- or tree- shaped structure. These organisms are very common in some coral reefs, particularly in areas where sponges are common. In these areas they may form "spicule trees;" three-dimensional structures made of sponge spicules glued together extending up into the water column. However, these irregular, or agglutinated, forams really come into dominance in the deep seas. Here some species may get large, about the size of dinner plates, perhaps larger. Some species extend up off the bottom as a tree-like shape and have been documented to snare and eat fish or small shrimps. Others form networks of root-like growths that may cover large areas. None of this group has, to the best of my knowledge, been seen in aquaria, and in fact, only a few individuals of these deep- sea groups have ever been seen alive.

Here are links to some pictures of arborescent forams from Antarctica plus information on their biology.
http://scilib.ucsd.edu/sio/nsf/fguide/protoctista10.html
http://scilib.ucsd.edu/sio/nsf/gallery/sam6.jpg

Another type of foraminiferan secretes its shell wholly out of organic materials, chiefly protein. One common variety of this group looks like shiny brown spheres, about one-twentieth of an inch or so in diameter. In nature, they move slowly up and down algal stalks or across the substrate collecting and eating particulate material. Their food is mostly bacteria and microalgae. I have seen a few of these in some aquaria, and they may actually be pretty common in some hobbyist's tanks, but their small size and unspectacular color tends to camouflage them.

The final kind of shelled foram secretes a shell, totally or mostly, out of calcium carbonate. These shells may be spherical, discoidal, tubular, or some other odd shapes. They range in size from about one tenth of a millimeter in diameter to giants, referred to as mermaid's pennies, well over a inch in diameter. They are very abundant and quite common around reefs tropics as well as in our aquaria. These organisms move very slowly. Extended around their bodies are meshes of fine strands of protoplasm referred to as "reticulopodia." They use these to ingest the bacteria and other small organic particulate material that is their main food.

A beautiful photo of a calcareous test may be found by following this link.

Here is a link to some calcareous forams living on a limpet in Antarctica.

Here is a link to a tropical foram with its feeding filaments extended. This species is common in reef aquaria.

Shelless or "naked" fresh-water (!) foraminiferans have recently been described, primarily on the basic of body form, the presence of reticulopodia, and cellular chemistry. Very little is known about their biology.

Some information about the fresh water forms, including an image, may be found by following this link.

In Indo-Pacific coral reef areas, the calcareous-shelled forams may be exceptionally abundant. In fact, the beach sands around some atolls, such as some of the islets in Palau, may be almost entirely made from foram shells. Such abundance is not limited to the Pacific; the pink sands of Bermuda get their color from pink foram skeletons; primarily from Homotrema rubrum, a foram that grows abundantly in some aquaria. It should not be surprising then, that foraminiferans may become common in our systems. Presumably they enter our systems on live rock, live sand, or coral and thrive.

Cells are considered to be the basic unit of life. Some cells, those found in bacteria and archaeans (a form of life that is somewhat similar to bacteria) are very tiny and lack much in the way of visually evident internal structure. The cells of animals, plants, fungi and most protists are much larger and complex, and contain a lot of microscopically visible intracellular machinery referred to as organelles. The one type of organelle found in almost all larger cells is the nucleus. This is the site of "cellular control" and contains the genetic material that defines the cell and cellular functions. If people think of cells at all, or if they think of the cells that larger organisms are composed of, they generally assume that most cells have only one nucleus. Most cell types in multicellular animals, indeed, do have only one nucleus. In mammals, some exceptions are striated (or skeletal) muscle cells which have many nuclei, and mature red blood cells which don't have a nucleus.

One feature that sets foraminiferans apart from many other protozoans is the fact that they may be multinucleate. Smaller forams often have one nucleus, but larger forams may have several thousand nuclei within their body. Nevertheless, forams do not have bodies divided up into cells. The lack of discrete cells is one reason they are not considered to be animals. In the large agglutinated forams, the nuclei seem to be more-or-less distributed throughout the protoplasmic mass. In the shelled forams, the main mass of the body, including most of the nuclei, is found inside the shell, but a large amount extends outward into or over the surrounding substrate in a mesh-like network of fine fibers, the reticulopodia. These fibers are their site of food collection. An image of a giant foram from Antarctica showing feeding pseudopods, plus lots of neat information may be found by following this link.

Most forams are presumed to eat bacteria, other protozoans, or fine particulate material by ingesting them when they come in contact with the fiber network. However, the larger forams are predators on just about anything they can catch. A large foraminiferan, with a shell about a tenth of an inch in diameter, may have fibers that extend outwards over a half an inch from the shell. Food items are ingested and eaten, and as the foram clears an area of acceptable food, it slowly moves across or through the sediments.

In a deep sand bed, feeding foraminiferans perform several vital functions for the aquarist. First, they clear small particulate material from between the sediment grains, allowing water movement, preventing stagnation. Second, such feeding opens space on individual sediment grains, in a manner analogous to forest fires opening spots in a forest. This allows more bacterial population growth to occur, and as the metabolism leading to this growth IS the biological filter, this clearing of space is necessary for continual biological filtration. Finally, when the forams metabolize their ingested material, soluble mineral nutrients such as phosphate and ammonium, ions are formed and excreted as waste. In turn, these materials may be utilized by algae and converted into a form that may be exported from the system simply by subsequent harvesting of the algae. So, foraminiferans are a vital link in the process leading to the removal of excess nutrients caused by the necessity of feeding all the animals in the system.

Some of the most abundant forams that are found in our aquaria are spectacular. They are large and obvious and are often exceptionally abundant. And, unlike the remainder of the forams discussed in this article, they are not found in the sediments. As they don't look like anything else in our systems, they are often misidentified as small sponges, hydrocorals or stony corals. These foraminiferans belong to a peculiar foram species called Homotrema rubrum and it has a shell that may be orange, but is more typically hot pink or bright cherry red. The red coloration is due to an iron salt that is incorporated into the skeleton. Found growing on hard surfaces such as rocks, the calcareous shell looks like a small hydrocoral or a hard, spiky crystal with angular projections. Homotrema seldom get larger than an eighth or quarter of an inch in height, but their brilliant color renders them very obvious. They feed on particulate material in the tank's water, probably mostly bacterial aggregates they catch in fine filamentous protoplasmic strands which extend from the tips of the angular projections. There are similar white foraminiferan species found in aquaria. Their bodies look like small "spiky" versions of a stony coral, rather like nano-sized versions of bird's nest coral, Seriatopora hystrix. These foraminiferans have not been identified to species.

Figure 3. A Homotrema rubrum; about one-third of an inch high.
The rhizopodia are feeding structures.

The other forams found in our aquaria are less evident, but more typical in shape. Some individuals may actually be about as large as Homotrema and they are often far more abundant. In some aquaria, these are actually the most abundant "animal-like" organisms. And they generally are completely overlooked. They are usually colored some shade of white, beige or tan, although some common species are pink. These species are typically spherical, ovoid, or discoidal and can't be identified to species without specialized references. Sometimes they may be seen crawling on rocks, algae, or tank walls, but most of the time they are found in the sediments. Many of them are about the size of a sesame seed.

Figure 4. A large aquarium foram attached to sand grains by
its rhizopodial feeding network.

An easy way to see if your system has an abundant foram population is to sample a bit of the sand bed. Remove a small amount of sediment from the surface of your sand bed using a turkey baster or some other implement. Put it into a clean clear glass bowl or dish, making sure it is covered with water. You don't need much sediment for this evaluation, just enough to make a layer one sand grain deep, and there should be plenty of open area on the bottom of the bowl. Then examine the sediments with a hand lens or magnifying glass, and look for clumps of sand grains that are attached to other sand grains by "mucous" masses. On close examination, many of these masses will be seen to have a large discoidal or spherical "grain" in them. This will likely be a foram.

Figure 5. Some forams collected in about 10 minutes from one of my aquaria.

It takes microscopic examination of the sediments to confirm the presence of foraminiferans. But if you are one of those hobbyists with access to a microscope, you should examine the "suspect" sand grain for the appearance of fine dots on the surface. The name Foraminifera is derived from a combination of Latin and Greek terms meaning "bearing pores or holes" and the surface of most foram shells are covered with microscopic holes visible at about 40x magnifications. If you are lucky, you may find larger greenish or grayish-green foraminiferans about a quarter of an inch in diameter. These are forams that have zooxanthellae. This is surely one of the odder biological associations, that of a one "unicellular" organism with other, symbiotic, unicellular organisms living it. Zooxanthellate forams are quite commonly found in natural reefs, but are less abundant in our systems, possibly because the light levels are lower than is normally found in many shallow water communities.

Figure 6. Foram containing zooxanthellae collected from my aquarium.

Many forams are themselves food for other aquarium denizens. Hermit crabs will eat them as will many snails and some bristle worms. There are microscopic predators, as well; some nematodes (roundworms) and flatworms will eat them. The sand-sifting fishes are likely eating forams, among other things, that they extract from the sand. Such predation pressure, of course, will depress the foram populations, but is not likely to have significant effects as long as there are not too many predators. Like most amoebas, forams may reproduce by binary fission, or splitting into two. Forams, however, may at other times reproduce sexually producing many hundreds of offspring. If conditions are good, they will rapidly spread throughout the sand bed.

Conclusion

Beauty is not limited to larger things. On a microscopic scale, foraminiferans often possess a sculptured symmetry and architecture that is incomparable. They are fascinating, if minute, organisms found in many of our aquaria. Their small size belies their importance at helping us with our aquarium maintenance. As with many of the other small organisms found in sand beds, many of the larger, more decorative of our reef aquarium species would simply be impossible to keep without the contribution of foraminiferans. If you want to learn more about foraminiferans, I would suggest you check out invertebrate zoology textbooks at your local library, or do online searches using the following terms: foraminifera, or foraminiferida. There is a wealth of information on this ecologically very important group.



If you have any questions about this article, please visit my author forum on Reef Central.

Useful References:

Kozloff, E. N. 1990. Invertebrates. Saunders College Publishing. Philadelphia. 866 pp.

Ruppert, E. E. and R. D. Barnes. 1994. Invertebrate Zoology. Saunders College Publishing. Philadelphia. 1056 pp.

A Scientific Journal Devoted To Foraminiferans:

Journal of Foraminiferal Research

Selected References From The Primary Literature Which May Be Of Interest (Articles of Special Interest Are Starred =):

Bernard, J. M. and S. S. Bowser. 1992. Bacterial biofilms as a trophic resource for certain benthic foraminifera. Marine Ecology Progress Series. 83:263-272.

Bornmalm, L., B. H. Corliss and K. Tedesco. 1997. Laboratory observations of rates and patterns of movement of continental margin benthic foraminifera. Marine Micropaleontology. 29:175-184.

Bowser, S. S. and J. M. Bernhard. 1993. Structure, bioadhesive distribution and elastic properties of the agglutinated test of Astrammina rara (Protozoa: Foraminiferida). Journal of Eukaryotic Microbiology. 40:121-131.

Cedhagen, T. and S. Mattson. 1991. Globipelorhiza sublittoralis, new genus new species a komokiacean (Protozoa: Foraminiferida) from the Scandinavian sublittoral. Sarsia. 76:209-213.

Chevillon, C. 1996. Skeletal composition of modern lagoon sediments in New Caledonia: coral, a minor constituent. Coral Reefs. 15:199-207.

Goldstein, S. T. and B. H. Corliss. 1994. Deposit feeding in selected deep-sea and shallow-water benthic foraminifera. Deep-Sea Research. 41:229-241.

Gooday, A. J. 1991. Xenophyophores (Protista, Rhizopoda) in box-core samples from the abyssal northeast Atlantic Ocean (BIOTRANS area): Their taxonomy, morphology, and ecology. Journal of Foraminiferal Research. 21:197-212.

Gooday, A. J., B. J. Bett and D. N. Pratt. 1993. Direct observation of episodic growth in an abyssal xenophyophore (Protista). Deep-Sea Research. 40:2131-2143.

Gooday, A. J., L. A. Levin, C. L. Thomas and B. Hecker. 1992. The distribution and ecology of Bathysiphon filiformis Sars and Bathysiphon major De Folin (Protista, Foraminiferida) on the continental slope off North Carolina. Journal of Foraminiferal Research. 22:129-146.

Gooday, A. J., S. S. Bowser and J. M. Bernhard. 1996. Benthic foraminiferal assemblages in Explorers Cove, Antarctica: A shallow-water site with deep-sea characteristics. Progress in Oceanography. 37:117-166.

Hemleben, C. and H. Kitazato. 1995. Deep-sea foraminifera under long time observation in the laboratory. Deep-Sea Research. 42:827-832.

Langer, M. R. and C. A. Gehring. 1993. Bacteria farming: a possible feeding strategy of some smaller, motile foraminifera. Journal of Foraminiferal Research. 23:40-46.

Langer, M. W. and C. I. Bell. 1995. Toxic foraminifera: Innocent until proven guilty. Marine Micropaleontology. 24:205-214.

Lee, J. J., C. G. Wray and C. Lawrence. 1995. Could foraminiferal zooxanthellae be derived from environmental pools contributed to by different coelenterate hosts? Acta Protozoologica. 34:75-85.

Lee, J. J., J. Morales, S. Bacus, A. Diamont, P. Hallock, J. Pawlowski and J. Thorpe. 1997. Progress in characterizing the endosymbiotic dinoflagellates of soritid foraminifera and related studies on some stages in the life cycle of Marginopora vertebralis. Journal of Foraminiferal Research. 27:254-263.

Morales, R. A. and M. M. Murillo. 1996. Distribution, abundance and composition of coral reef zooplankton, Cahuita National Park, Limon, Costa Rica. Revista De Biologia Tropical. 44:619-630.

Pawlowski, J., M. Holzman, J. F. Fahri, X. Pochon and J. J. Lee. 2001. Molecular identification of algal endosymbionts in large miliolid foraminifera: 2. Dinoflagellates. Journal of Eukaryotic Microbiology. 48:368-373.

Roettger, R. and R. Krueger. 1990. Observations on the biology of Calcarinidae (Foraminiferida). Marine Biology (Berlin). 106:419-426.

Ruetzler, K. and S. Richardson. 1996. The Caribbean spicule tree: A sponge-imitating foraminifer (Astrorhizidae). Bulletin de l'Institut Royal des Sciences Naturelles de Belgique Biologie. 66:143-151.

Shires, R., A. J. Gooday and A. R. Jones. 1994. A new large agglutinated foraminifer (Arboramminidae N. Fam.) from an oligotrophic site in the abyssal northeast Atlantic. Journal of Foraminiferal Research. 24:149-157.

Shires, R., A. J. Gooday and A. R. Jones. 1994. The morphology and ecology of an abundant new Komokiacean mudball (Komokiacea, Foraminiferida) from the Bathyal and Abyssal NE Atlantic. Journal of Foraminiferal Research. 24:214-225.

Sliter, W. V. 1971. Predation on benthic foraminifers. Journal of Foraminiferan Research. 1:20-29.

Travis, J. L., S. S. Bowser, J. G. Calvin and J. J. Lee. 1988. Pseudopodial tension in Amphisorus hemprichii, a Giant Red Sea Foraminifer. Protoplasma. (1988) (Suppl. 1):64-71.

Yanko, V., J. Kronfeld and A. Flexer. 1994. Response of benthic foraminifera to various pollution sources: Implications for pollution monitoring. Journal of Foraminiferal Research. 24:1-17.




Reefkeeping Magazine™ Reef Central, LLC-Copyright © 2008

Foraminiferans by Ronald L. Shimek, Ph.D. - Reefkeeping.com