Coralmania by Eric Borneman

From the Food of Reefs to the Food of Corals

Last month, I discussed the topic of food sources to coral reefs, and this month I will narrow the subject down to food sources for corals. Coral feeding is part of a well-orchestrated “three-part harmony,” because corals are supremely adapted to utilizing all manner of the available food sources on coral reefs. The three parts to this story, or harmony, are light, prey capture, and direct absorption. This month, I will cover only the first part, the nutritive aspects of light.

The Energy of Light

Before becoming concerned about a repetition of a bevy of other articles on the subject by many authors, this will not be a discussion of aspects of lighting, qualities of light, suggestions for lighting, or anything of that nature. Perhaps such subjects are interesting; they certainly have been well discussed, and presumably because of the vital importance of light to many corals. Rather, it is my intention here to have the readers understand exactly why lighting is an important subject in reef aquaria.

As I mentioned in the last article, there are two basic types of organisms: autotrophs (mostly photosynthetic organisms) and heterotrophs. Corals are heterotrophs, with a big caveat. Most reef building corals, or hermatypes, and many non-reef building corals, or ahermatypes, maintain symbioses with various dinoflagellate algae called zooxanthellae. While the coral polyp itself is not autotrophic, its nearly obligate association with these dinoflagellates provides polyps with a built-in autotroph that it can, to some degree, control. Therefore, reef corals with polyps maintaining symbionts have characteristics of both autotrophs and heterotrophs. Lighting provides the energy for zooxanthellae to photosynthesize. It may or may not come as some surprise that light, to corals, is simply food.

Also mentioned in the last article was the fact that the waters around coral reefs usually have extremely low levels of various nutrient sources, largely because of fierce competition for those same nutrients amongst the vast numbers of species found there. A common and successful strategy to allow successful competition for habitat space in such an environment is to utilize an energy resource that is not generally limited in tropical waters... sunlight. Corals are not the only organisms to utilize this strategy, as clams, sponges, hydroids, foraminiferans, nudibranchs, and many other organisms also host photosynthetic algal or bacterial cells in their tissues for a similar purpose. As it turns out, sunlight is such a valuable commodity that means to attain as much of it as possible are built into the life history strategies and behaviors of organisms harboring such symbionts. For corals, regulation of the zooxanthellae population is possible, they expand or contract their tissues to expose more or less zooxanthellae to sunlight, and they modify their growth forms to those ideally suited to their “place in the sun.” Accessory animal pigments are also produced to further modify the light environment to which corals are exposed.

Zooxanthellate and Azooxanthellate Corals

Corals far outside tropical areas, or those in very deep water, do not contain zooxanthellae. Oddly enough, perhaps, is that there are a great many azooxanthellate corals existing on coral reefs alongside or nearby their brethren with symbionts. If harboring zooxanthellae is such a successful strategy, why don’t all corals have these symbionts? Part of the answer lies in evolution. Perhaps it has not been advantageous for some species to adopt them, or perhaps not all species have recently invaded the shallow water zones and have not had enough evolutionary time to do so.

A transmission electron micrograph of a zooxanthella. The areas with parallel bands are stacked thylakoid membranes of the chloroplasts where light-harvesting takes place.


In fact, there are corals that are facultatively zooxanthellate; these corals, some from the tropics and some from sub-tropical regions can exist either with, or without, zooxanthellae. Commonly researched corals of this type include some species of Madracis, Astrangia, and Oculina. In fact, one of the nemeses of aquarists, Aiptasia pallida, the glass anemone, is also facultatively zooxanthellate. As it happens, these corals tend to exist with zooxanthellae in warm, clear, shallow waters and without them in turbid, cold, or deep waters.

What this means, among other things, is that if it doesn’t provide much of an advantage to host zooxanthellae in certain areas, why have them present at all? It could be argued that some photosynthesis is better than none at all, even in deep or temperate water. But, perhaps this is not the case… if there is a cost involved. And, indeed there is a cost to the organism to maintain zooxanthellae within their cells. Apparently, there is no such thing as a “free lunch” for corals, either. These facultative hosts must make a metabolic choice as to whether the benefits of hosting zooxanthellae outweigh the costs. In most coral reef environments, the symbiosis is not so optional, and is usually considered to be nearly an obligate association. I say nearly, because bleaching is a prime example of when the costs of maintaining the symbiosis outweigh the benefits, although the bleaching response is complex and such a statement represents something of a simplification.  

This somewhat answers the question of why some corals maintain zooxanthellae: they retain benefits of photosynthesis where prevailing conditions are advantageous over the costs of maintaining them, such as on coral reefs. This group includes most of the hermatypic stony corals, most of the shallow water Caribbean gorgonians, a couple of shallow water Pacific gorgonians, more than half of the soft corals, about half of the number of species of zoanthids (although the vast majority in terms of numbers of organisms), most of the corallimorphs, and a single genus of hydrocoral (although this single genus, Millepora, contains the majority in terms of numbers of organisms on coral reefs).  

It may seem logical that zooxanthellate species must exist in shallow water to take advantage of sunlight, but we are still left with one pressing question. How do some azooxanthellate species seem to compete so well amongst zooxanthellate species, in particular, some Pacific soft corals like Dendronephthya species and Tubastraea micranthus? The answer lies in the fact that most probably compete well with their rapid growth, prolific asexual reproduction, and other behaviors. For the most part, zooxanthellate corals do indeed compete their azooxanthellate kin for sunlight-drenched areas, often resigning those without algal partners to recesses, caves, nooks, crannies, and seemingly less desirable real estate. Lest it be thought that azooxanthellate corals are “inferior,” it is more accurately stated that, like many specialists that exist on reefs because of their specialization, they compete well where others cannot. In other words, every organism finds its place where it tends to be successful. As testimony to the fact that zooxanthellae are not necessarily the penultimate adaptation to shallow coral reef waters, at one time in history, all corals were azooxanthellate and did not compete for the space to catch sunlight at all. 

Types of Zooxanthellae

So successful is the symbiosis between corals and their zooxanthellae that multiple relationships have developed. At one time, and not long ago at all, coral researchers were convinced that all corals held but one type of symbiont within them. These single celled algae were called, despite numerous synonymous names, Symbiodinium microadriaticum. Eventually, several other dinoflagellate zooxanthellae were found in the fire coral, Millepora, and in some zoanthids. However, it was still largely assumed that all other corals harbored a single species of algae. About twenty years ago, the walls around such a notion began to crumble, and it is now recognized that there are many clades (groups of biological taxa that includes all descendants of a common ancestor), such as species, types, and subtypes of zooxanthellae that inhabit coral tissue. In fact, so widespread is the diversity beginning to appear that a complete rewriting of coral symbiosis is beginning, with only a few introductory chapters written as of today. The diversity and nature of the various relationships is now hardly known. What is known is that not only may there be a variety of one coral/one symbiont relationships, but that various corals may harbor more than one symbiont, may potentially be able to harbor more than one symbiont even if it is not usually found to do so, and that even single corals may harbor more than one symbiont at the same time. I would refer the reader to more information in my article here, even though much of that information has already changed, so rapid are the advances in this field. There is a very large body of science regarding this subject, and to cover it in much more depth without many additional pages, I am afraid, would be doing the subject an injustice.

What The Symbiosis Provides And How Much

Given the general background above, I can now delve into the crux of this relationship and describe just what it means to house autotrophs in a heterotrophic body. Zooxanthellae are initially acquired either from the water column (in broadcast spawning corals), or are given a starter culture from the parent polyp (in brooding corals). Over the course of their lives, coral polyps maintain various densities of zooxanthellae in their tissues according to environmental and metabolic conditions. Polyps periodically release or lose some, require more from the water column, and control their growth and reproduction within their tissues quite effectively. For a description of when the symbiosis does not go quite as smoothly, a process known as coral bleaching, see this article. The algae are maintained mostly in the underlying tissue layer, the gastrodermis, and within the tentacles of some species, in small containment vesicles called vacuoles. These vacuoles are formed within the gut cavity of corals after the dinoflagellates have been swallowed, and they can even migrate across tissue layers.   

Once in place, the zooxanthellae reproduce until they form a mostly single layer within the tissue; an arrangement that maximizes light capture as a photosynthetic umbrella, or antenna, while minimizing shading of adjacent algal cells.

The upper layer of the Acropora sp. is the epidermis. The lower layer is the gastrodermis. Within the cells are round to oval golden spheres. These are the zooxanthellae.

The zooxanthellae are then carefully controlled by their coral host by being subjected to nitrogen limitation. As mentioned in last month’s article, nitrogen levels in coral reef waters are typically extraordinarily low, with most being found as ammonia. This is in contrast to aquaria where the dominant nitrogen species is usually nitrate. Nitrogen is the end all-be all for zooxanthellae growth and reproduction. By limiting nitrogen in the form of excretion products, the polyp keeps the zooxanthellae in the numbers and density that maximize photosynthetic efficiency for its own use. Using several released compounds, most of which are still unidentified, the polyp stimulates the zooxanthellae to release virtually all of the products of its photosynthesis, and these are then used by the polyp for its own needs. If nitrogen was made readily available to the zooxanthellae (for example, if high levels were present in the water and the dissolved nitrogen “diffused” into the coral tissue), it could then be accessed by the algae without limitation by the polyp, and zooxanthellae could begin to grow and reproduce like a “phytoplankton culture.” In this case, the symbiosis becomes less advantageous to the coral, and it will expel some of the symbionts to try and re-establish maximal benefit from its algal partners. As a practical note, when very high densities of zooxanthellae exist in coral tissue, the resultant coloration of the coral is usually a rich or dark brown color.

This relationship may not sound altogether “symbiotic.” It may even sound parasitic, since the coral is clearly taking advantage of the zooxanthellae, and seemingly without much “giving.” Yet, nitrogen is so limiting on coral reefs that even the limited excretion of the coral provides a relatively stable supply, as well as a protected stable environment, to the zooxanthellae.

Given that corals are “squeezing” their symbionts for all they are worth, what exactly are they worth? As it turns out, the symbionts provide a constant “sugar fix.” The high carbon products of photosynthesis are mostly sugars, and the coral squeezes out almost 100% of the algal production, allowing just enough to maintain the algae’s carbon needs for its survival. In shallow clear water, efficient corals can get over 100% of their daily carbon needs from their zooxanthellae. These photosynthetically-derived sugars are then used by the coral for metabolic functions that require energy, and much of them are lost in the copious production of mucus. Coral mucus, in turn, and as was shown in the previous article, is itself a food source to the reef. The production of mucus by corals is also very important for their protection, food acquisition, competition, and other functions.

Unfortunately, zooxanthellae don’t make much else besides sugar. The coral squeezes out what it can, but not much more ever results. In particular, nitrogen, once again, is a problem. It seems everyone on the reef is always scrambling for nitrogen, the substance needed to produce protein; proteins required for nematocysts, vitamins, tissue maintenance, injury repair, cell division, growth, gamete production, even the very toxins used to paralyze prey. Proteins are the ticket to growth and reproduction in zooxanthellae, as well as for coral polyps. Thus, it may come as little surprise that this great sugar fix provided by symbiotic algae comes up rather nutritionally short in the course of coral nutrition. To survive and, hopefully, thrive, corals need more than light. They need to swallow more than their symbiotic zooxanthellae. And this will be the subject of next month’s article.

Links to Part 1, Part 3, Part 4, Part 5, Part 6, Part 7

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

Suggested Reading:

Baghdasarian, G. and L. Muscatine (2000). "Preferential expulsion of dividing algal cells as a mechanism for regulating algal-cnidarian symbiosis." Biological Bulletin 199(December): 278-286.

Baker, A. C. and R. Rowan (1997).Diversity of symbiotic dinoflagellates (zooxanthellae) in Scleractinian corals of the and eastern Pacific. Proceedings of the 8th International Coral Reef Symposium, Panama

Benayahu, Y. (1992). Onset of zooxanthellae acquisition in course of ontogenesis of broadcasting and brooding soft corals. Proceedings of the Seventh International Coral Reef Symposium, Guam, University of Guam Press.

Bil', K. Y., P. V. Kolmakov, et al. (1985). Photosynthetic Products of Zooxanthellae of the Reef-Building Corals Stylophora pistillata and Seriatopora coliendrum from Different Depths of the Seychelles Islands. The Ecology of Reefs, NOAA.

Blank, R. J. and R. K. Trench (1985). "Speciation and symbiotic dinoflagellates." Science 229(16 August 1985): 656-658.

Blank, R. J. and R. K. Trench (1986). "Nomenclature of endosymbiotic dinoflagellates." Taxon 35(2): 286-294.

Bythell, J. C. (1988). A total nitrogen and carbon budget for the elkhorn coral Acropora palmata (Lamarck). Proceedings of the 6th International Coral Reef Symposium, Australia.

Colley, N. J. and R. K. Trench (1985). "Cellular events in the reestablishment of a symbiosis between a marine dinoflagellate and a coelenterate." Cell and Tissue Research: 100-103.

Cook, C. B. and C. F. D'Elia (1987). "Are natural populations of zooxanthellae ever nutrient-limited?" Symbiosis 4: 199-212.

Davies, P. S. (1984). "The role of zooxanthellae in the nutritional energy requirements of Pocillopora eydouxi." Coral Reefs 2: 181-186.

Drew, E. A. (1972). "The biology and physiology of alga-invertebrate symbioses. II. The density of symbiotic algal cells in a number of hermatypic hard corals and alcyonarians from various depths." Journal of Experimental Marine Biology and Ecology 9: 71-75.

Dubinsky, Z. and P. L. Jokiel (1994). "Ratio of energy and nutrient fluxes regulates symbiosis between zooxanthellae and corals." Pacific Science 48(3): 313-324.

Falkowski, P. G., Z. Dubinsky, et al. (1993). "Population control in symbiotic corals: ammonium ions and organic molecules maintain the density of zooxanthellae." BioScience 43(9): 606-611.

Falkowski, P. G. and J. A. Raven (1997). Making Cells. Zooxanthellae: a case study in unbalanced growth. Aquatic Photosynthesis, Blackwell Science: 257.

Farrant, P. A., M. A. Borowitzka, et al. (1987). "Nutrition of the temperate Australian soft coral Capnella gaboensis II. The role of zooxanthellae and feeding." Marine Biology 95: 575-581.

Gattuso, J.-P., D. Yellowlees, et al. (1993). "Depth- and light-dependent variation of carbon partitioning and utilization in the zooxanthellate scleractinian coral Stylophora pistillata." Marine Ecology Progress Series 92: 267-276.

Goreau, T. F., N. I. Goreau, et al. (1971). "Reef corals: autotrophs or heterotrophs?" Biological Bulletin 141(October): 247-260.

Goulet, T. L. and M. A. Coffroth (1997). A within colony comparison of zooxanthella genotypes in the Caribbean gorgonian Plexaura kuna. Proceedings of the 8th International Coral Reef Symposium, Panama.

Grant, A. J., M. Remond, et al. (1998). "Low molecular-weight release factor from Plesiastrea versipora (Scleractinia) that modifies release and glycerol metabolism of isolated symbiotic algae." Marine Biology 130: 553-557.

Hinde, R. (1988). Factors produced by symbiotic marine invertebrates which affect translocation between the symbionts. Cell to Cell Signals in Plant, Animal and Microbial Symbioses. S. Scannerini, D. Smith, P. Bonfante-Fasolo and V. Gianinazzi-Pearson. Berlin, Springer-Verlag. H17: 311-346.

Hoegh-Guldberg, O. (1994). "Population dynamics of symbiotic zooxanthellae in the coral Pocillopora damicornis exposed to elevated ammonium [(NH4)2SO4] concentration." Pacific Science 48(3): 263-272.

Hoegh-Guldberg, O. and G. J. Smith (1989). "Influence of the population density of zooxanthellae and supply of ammonia on the biomass and metabolic characteristics of the reef corals Seriatopora hystrix and Stylophora pistillata." Marine Ecology Progress Series 57: 173-186.

Hoegh-Guldberg, O. and J. Williamson (1999). "Availability of two forms of dissolved nitrogen to the coral Pocillopora damicornis and its symbiotic zooxanthellae." Marine Biology 133: 561-570.

Taguchi, S. and R. A. I. Kinzie (2001). "Growth of zooxanthellae in culture with two nitrogen sources." Marine Biology 138: 149-155.

Taylor, D. L. (1983). The coral-algal symbiosis. Algal Symbiosis: A continuum of interaction strategies. L. J. Godd. Cambridge, Cambridge University Press: 19-35.

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From the Food of Reefs to the Food of Corals by Eric Borneman -