"There remains the undoubted, well demonstrated, fact that corals are most highly
adapted for the capture and extremely rapid digestion of exclusively animal prey and
that, in relation to the bulk of the tissues, they have a literally enormous feeding surface,
in most species only exposed at night when zooplankton is abundant."

Yonge, 1963

Thus far in this somewhat interrupted series of articles, I have discussed the food of coral reefs, the role of zooxanthellae and light in supplying corals with nutrition, and the role of phytoplankton in coral nutrition. In this article, I will discuss the contributions of zooplankton. Future articles in this series will treat the contributions of bacterioplankton, dissolved material, and particulate material and their roles as a food resource to corals.

As a brief review of my earlier articles, corals are polytrophic (or mixotrophic) in that they are able to acquire energy from multiple sources. They are able to provide themselves with nutrition from the photosynthetic products (photosynthate) of their zooxanthellae, although the majority of this material is carbon rich and nitrogen poor. As such, it has been described as "junk food," providing the quick energy needed for their respiration and much of the excess carbon lost as mucus. Most studies of corals refer to carbon in terms of animal metabolism or respiration. However, nitrogen is what is required for protein synthesis, growth and reproduction. While calcification, or skeletal growth, is dramatically increased because of the energy provided by zooxanthellae, other aspects of the coral's needs, such as tissue growth, ability to successfully compete and repair injuries, and sexual reproduction is highly dependent on protein production. As photosynthate does not provide enough nitrogen to meet their daily needs, feeding on various sources of material, such as zooplankton, is needed by corals to make up for this deficit. Additionally, feeding provides the source for any required trace elements, essential amino acids which are not able to be synthesized by the coral, vitamins, phosphate, and other elements. In other words, feeding is absolutely essential for the survival of corals. The notion that corals are able to exist without feeding, or by light only, is incorrect in all cases, with different species relying to varying degrees on energy acquisition from multiple sources (light, zooplankton, etc.). The relative amounts of energy provided by a given source will depend on the relative levels of those things at any one time, the specific qualities of the species (some naturally depend more on one thing than another), and various other environmental and behavioral influences and adaptations.

Introduction

Zooplankton are defined as small (often microscopic) aquatic animals and nonphotosynthetic protists suspended or weakly swimming in water. Zooplankton form an important food (trophic) resource to many groups of animals, are part of a complex food web, and are themselves significant consumers of phytoplankton, bacterioplankton and other zooplankton. There are numerous ways to describe zooplankton; they can be grouped according to their size, taxonomy, habitat, and other characteristics (Figure 1).

The Occurrence and Types of Zooplankton on Coral Reefs

Zooplankton, tending to be quite numerous, albeit small, also accumulate where there is sufficient food to allow for their growth and reproduction. It is correct to assume that areas of higher nutrients tend to foster higher populations of zooplankton, as well. Although certain types of zooplankton are found in sometimes quite specific areas, the relative contributions of each group are quite similar. This is especially true given the overwhelming contributions of some groups to the plankton (Table 1). Copepods comprise by far the largest fraction of total zooplankton - more than all the other groups combined. On coral reefs, demersal copepods can form dense swarms more than 5 cubic meters in size and with between 500,000 and 1,500,000 copepods per cubic meter (Hamner and Carleton 1979). Even with such great densities, and with demersal zooplankton comprising such a large portion of the total zooplankton availability on reefs, the amount of pelagic zooplankton is still astonishingly large. Hamner et al. (1988) measured zooplankton in the water column flowing over the reef crest by using a one meter wide trap. During one day, 0.5kg of plankton was collected across that one meter strip. Given that most tanks are about one meter wide, the pelagic fraction of zooplankton alone (not counting the much greater contribution of demersal zooplankton) would mean an aquarist would have to dump over a pound of food in their tank each day to simulate just the small fraction of plankton available to a reef crest community.

It is probably reasonably well known that coral reef zooplankton are more abundant at night. Much of the zooplankton on reefs is not pelagic, and is not washed into the reef environment from the open ocean where levels are comparatively lower. The majority of reef zooplankton is demersal, and rises into the water column from the benthos at night when levels of predation are lower. But, perhaps the degree to which variations in the relative amounts of zooplankton occur at night by comparison with levels during the day might be surprising (Table 2). While some corals feed during the day, and some feed day and night, the majority feed at night. This corresponds to when zooplankton is most abundant. In this way, corals can gain energy from light during the daytime and feed at night when zooplankton is most abundant. This is the most energy efficient way for corals to maximize their energy intake. Of course, exceptions arise over time, and even night feeding corals may feed during the day, although it is likely they will only do this if there is sufficient prey to warrant the considerable energy expense of prey capture. In aquariums, since there is such a relative paucity of zooplankton and a concurrent lack of nightly migration, coupled with the normal daytime feeding of the tank, many normally night-feeding corals extend to feed during the day. Tentacle extension, it should be noted, is not always related to food capture, and may also be indicative of competition or to expose corals with zooxanthellae in the tentacles to light. Generally, corals with transparent tentacles (tentacles lacking zooxanthellae), are night feeders.

Because it is not known what the energy budgets of corals in aquariums are, it is difficult to say whether or not there is an advantage or disadvantage to the often abnormal feeding behaviors in aquariums. If corals meet their energy needs through various combinations available at various times of the day, there is probably little disadvantage. Nor am I comfortable suggesting the feeding at night is "better" than feeding during the day. However, it is more natural, and it may be stressful for those corals that feed almost exclusively at night in the wild to feed during the day. The possible deleterious effects of strong lighting on normally withdrawn tentacles may also be injurious since they probably lack the photoprotective pigments of the rest of the tissue and the zooxanthellae.

The Contribution of Zooplankton to Coral Nutrition

In 1995, Sorokin wrote, "The polyps of scleractinian corals have the largest ratio of
catching area of the body to its biomass among all other aquatic animals." The debate over the contribution of zooplankton to coral energy is far from new. C.M. Yonge was the first to demonstrate that zooxanthellate corals (many diverse species) could survive "indefinitely" if provided with adequate zooplankton, even if totally deprived of light. In contrast, corals provided light and deprived of zooplankton did not survive. However, in light of increasing study of the zooxanthellae, it became known that many shallow-water corals could meet above 100% of their carbon requirements from light alone. Depending on the study, results indicated often conflicting data on the relative contributions of light and zooplankton to coral energy budgets. Some suggested that the zooplankton contribution was negligible, others suggested it was extensive, while still others suggested it depending on factors such as the depth (light availability) or polyp size (large polyped corals relied more on feeding that small polyped corals). It is now fairly well established that different species gain different amounts of energy from the various sources, depending on many factors that include species-specific differences, habitat and environment, and the dynamic changes in the availability of the various resources. However, it is all but conclusively demonstrated that feeding is required for survival in amounts that vary from slight to total dependence.

One of the greatest myths among reefkeepers is that "SPS" corals depend mostly on light, and require less food than "LPS" corals. This is entirely untrue. As an example, consider the data from Sebens (1997) below (Figure 2). This graph shows the capture rate of an equivalent biomass of two corals, the large-polyped Montastraea cavernosa and the very small-polyped Madracis mirabilis. For those unfamiliar with Madracis, it is related to and somewhat resembles Pocillopora and Stylophora. The capture rate of the small polyped coral was 36 times greater than the large-polyped coral! Furthermore, M. cavernosa has been shown in other studies to be a voracious zooplanktivore.

Figure 2.	Number of zooplankton captured by equivalent biomass of coral (100 polyps of M. cavernosa, 9000 polyps of M. mirabilis). Adapted from Sebens (1997).

Many other studies confirm the predatory abilities and requirements of "SPS" corals. It should not be surprising given the fast growth rate and fecundity of many small polyped species. In other words, more growth and reproduction requires more energy, especially nitrogen for tissue growth. The difference, if one exists between "SPS" and "LPS" corals, lies primarily in the size of the food captured. Most of the prey of small polyped corals may just be too small to see. Aquarists have a tendency to be strongly visual, and so if gross observations don't indicate that a coral is consuming food offered to it, they wrongfully assume the coral must not need to be fed. To further illustrate the roles of zooplankton capture by stony corals, consider the data below (Table 3).

Three corals were used in this study: Manacina areolata which is a very large-polyped coral that resembles the open brain coral, Trachphyllia geoffroyi; the large-polyped Montastraea cavernosa; and the very small-polyped Porites porites. The first column represents an approximation of the metabolic rate of the three species. Porites respires the most calories, and thus has the highest metabolism. As might be expected, it also has the highest caloric ingestion rate. It is notable that all three corals take in roughly three times what their basic metabolic rate requires. The additional calories can be used for injury repair, competition, growth and reproduction, and excess is generally lost as waste material and mucus. Lest any readers suggest that these are Caribbean species, and that the situation might be different in the Pacific, I offer the following data set (Table 4).

From the original data, I have totaled the energy inputs to provide a comparison with the Caribbean species in Table 3. This study is notable in that it considers only carbon, and not nitrogen. Carbon is typically thought to be mostly provided by the zooxanthellae photosynthesis. Despite the fact that most of the corals listed are able to theoretically meet 100% or more of their daily carbon needs by light, the zooplankton column shows that an even larger percentage can be met by feeding on this resource alone - for all but three of the species, none of which are "SPS" corals. Notice also how similar most of the species are to those in Table 3 in that they take in much more than they require for their daily metabolic needs. I have also given a ratio of heterotrophy (feeding) to autotrophy (photosynthesis). The higher the number, the more the coral depends on nutrient acquisition from feeding by comparison to energy provided by photosynthesis. Note how there are no noticeable patterns, but rather the ratios seem to vary simply according to species and not polyp-size, habitat, or other obvious variable. In all cases except for Galaxea and Symphyllia, more energy is acquired by feeding than by photosynthesis, and for the typical "SPS" species, the ratios tend to be higher. Finally, I have provided a column that shows the percentage of feeding on zooplankton compared to feeding on bacteria or dissolved organic material. Once again, there are no obvious trends except that some species rely more on zooplankton than others and that, if anything, the "SPS" corals feed on zooplankton a lot. In fact, most corals show linear feeding saturation dynamics under all but extremely high particle concentrations. What this means is that corals have a hard time "getting full." They continue to capture prey and do not get satiated until prey densities become so great that such levels are almost never possible. To put it another way, even if you were to pour a pound of food per day into an average sized reef aquarium, the corals would still "be hungry." I have so many papers on zooplankton abundances, composition, and the role of feeding in corals that to list them all and discuss them would require an entire book. I have chosen the studies above because they are typical, useful, and exemplify what could be shown again and again were I to list and describe other works.

I will finish this very brief coverage of zooplankton with several recent findings. In a September 2002 coral reef conference in Cambridge, several papers were presented that should give an idea of not only the very latest information, but also emphasize what is written above. Many years ago, one of the only complete energy budgets for a coral was done for what might be considered the ultimate shallow-water "SPS" coral, Acropora palmata (Bythell 1988, 1990). The study showed, basically, that 70% of this coral's nitrogen needs were met by feeding and that 91% of its carbon needs were met by light. At the 2002 conference, Bythell et al. examined three more corals, the larger polyped Montastraea cavernosa, M. annularis and Menadrina meandrites. They found zooplankton to provide 20-80 times the carbon and 112-460 times the nitrogen previously shown for Acropora palmata. Finally, Fanny et al. (2002) investigated the role of zooplankton consumption on the metabolism of the small-polyped coral, Stylophora pistillata under 3 different conditions of light (80, 200, 300 µmoles m-2 s-1) and 2 feeding regimes (Artemia and natural plankton). They found that regardless of light, fed corals had higher chlorophyll a concentrations, higher protein levels, and had photosynthesis rates 2-10 times higher than those deprived of food. This group also measured calcification rates, both in the dark and in light, and found that calcification, as is well known to be the case, is enhanced by light. However, for the first time it was shown that feeding results in calcification rates 50-75% higher than in control corals (not fed). It was also found that feeding does not affect the light-enhancement process of photosynthesis on calcification. To make these results completely understandable, if corals can feed on zooplankton, they will calcify 50-75% faster irrespective of light levels provided.

Conclusion

It has always surprised me the lengths aquarists go to devise various simulations of natural reef processes. The amount of ingenuity, effort, and expense spent on various aquarium devices and products is almost beyond belief. Aquarists hinge their belief that some bottle of trace elements or some new color temperature light bulb will increase the health and growth of their corals, despite scanty or non-existent evidence of it being true. Of all the many things that can potentially increase respiration, photosynthesis, and calcification - and have been show again and again to do so absolutely- feeding and water flow are the major players. Light, of course, is critically important as well, but aquarists by and large can and do provide enough quantity and quality of light for corals. Period. Phytoplankton, while a very beneficial addition to aquaria, does not feed most corals (Borneman 2002). Something as significant as zooplankton to both coral and coral reefs would seem worthy of the highest efforts in trying to produce, add, grow, substitute or in some way provide to tanks. I cannot think of a single greater accomplishment and advance for aquarists than to provide by whatever means (higher export and higher input, larger refugia, purchase, plankton tow, culture, etc.) significantly greater levels of zooplankton or zooplankton substitutes to their corals. I hope I am being dramatic enough by writing this, for this is among the most important steps that must be made to realize the majority of those lofty goals and ideals that are so often stated and desired by those keeping corals in aquariums. Similarly, I very much hope that the information in this article, and provided in additional works in the bibliography below, gives the slightest inkling of the predatory capabilities and importance of feeding in all corals.

"The quality and fates of coral primary production imply that zooxanthellae provide "junk food" to their hosts, and beg the question of nutrient limitation of coral growth rates under conditions of adequate light…On present evidence it seems clear that all corals need to supplement their diet (with food) from outside the symbiosis (heterotrophy) in order to meet these requirements."

Hatcher, 1988

Links to Part 1, Part 2, Part 3, Part 5, Part 6, Part 7

Ayukai, Y. 1991. Standing stock of microzooplankton on coral reefs: a preliminary study. J Plankton Research 13: 895-899.

Borneman, E.H. 2002. The Food of Reefs, Part 3: Phytoplankton. Reefkeeping. November issue.

Bythell J.C., Thomason J.C., Heidelberg K.B., Sebens, K. P. 2002. Is zooplankton capture an important trophic pathway in reef corals? Proc ISRS Eur Meeting - Cambridge 4-7th September 2002. Abstracts.

Bythell, J.C. 1990. Nutrient uptake in the reef-building coral Acropora palmata at natural environmental concentrations.Mar Ecol Prog Ser 68: 65-69.

Bythell, J.C. 1988. A total nitrogen and carbon budget for the elkhorn coral Acropora palmata (Lamarck) Proc 6th Int Coral Reef Symp 2: 535-540.

Coles, Stephen L.. 1997. Quantitative estimates of feeding and respiration for three scleractinian corals. Limnol Oceanogr 14: 949-953

Emery A.R. 1968. Preliminary observations on coral reef plankton. Limnol Oceanogr 13: 293-303.

Fanny H., Tambutte E., Ferrier-Pages C. 2002. Effect of zooplankton availability on the metabolism of the scleractinian coral Stylophora pistilllata (Esper, 1797). Proc ISRS Eur Meeting - Cambridge 4-7th September 2002. Abstracts.

Ferraris J.D. 1982. Surface zooplankton at Carrie Bow Cay, Belize. In: the Atlantic Barrier Reef Ecosystem at Carrie Bow Cay, Belize, I. Structure and Communities (Rutzler K, Macintyre I.G., eds.) Smithsonian Institution Press, Washington: 143-152.

Ferrier-Pages C., Allemand D., Gattuso J.-P., Rassoulzadegan F. 1998. Microheterotrophy in the zooxanthellate coral Stylophora pistillata: effects of light and ciliate density. Limnol Oceanogr 43: 1639-1648.

Grottoli A.G., Wellington G.M. 1999. Effect of light and zooplankton on skeletal ?13C values in the eastern Pacific corals Pavona clavus and Pavona gigantea. Coral Reefs 18: 29-41.

Hamner, W.M., Jones, M. S., Carleton, J. H., Hauri, I. R., Williams, D. M..1988. Zooplankton, planktivorous fish and water currents on a windward reef face: Great Barrier Reef, Australia. Bull Mar Sci 42(3): 459-479

Hamner, W.M. and Carleton, J.H. 1979. Copepod swarms: attributes and role in coral reef ecosystems. Limnol Oceanogr 24(1): 1-14.

Hatcher, Bruce Gordon. 1988. Coral reef primary productivity: a beggar's banquet. TREE 3(5): 106-111.

Johannes R. E., Coles S.L., Kuenzel N.T. 1970. The role of zooplankton in the nutrition of some scleractinian corals. Limnology and Oceanography 15: 579-586.

Lewis, J.B. 1976. Experimental tests of suspension feeding in Atlantic reef corals. Mar Biol 36: 147-150

Lewis, J. B. and Price W.S. 1975. Feeding mechanisms and feeding strategies of Atlantic reef corals. J. Zool Soc Lond 176: 527-544.

Lewis, J. B. 1974. The importance of light and food upon the early growth of the reef coral Favia fragum (Esper). J Exp Mar Biol Ecol 13: 299-304.

Porter, J. W., Porter J. G. 1977. Quantitative sampling of demersal plankton migrating from different coral reef substrate. Limnol Oceanogr 22: 553-555.

Porter, J. W. 1976. Autotrophy, heterotrophy and resource partitioning in Caribbean reef-building corals Amer Nat 110 (975): 731-742.

Sebens, K. P. 1997. Zooplankton capture by reef corals: corals are not plants! Reef Encounter 21: 10-15.

Sebens K.P., Grace, S.P., Helmuth B., Maney E.J., Miles J.S.1998. Water flow and prey capture by three scleractinian corals, Madracis mirabilis, Montastrea cavernosa, and Porites porites in a field enclosure. Mar Biol 131: 347-360.

Sebens, Kenneth P. 1977. Autotrophic and heterotrophic nutrition of coral reef zoanthids. Proc 3rd Int Coral Reef Symp: 397-404.

Sorokin, Y.I. 1980. Experimental investigation of heterotrophic nutrition of abundant species of reef building corals. Dokl Biol Sci 246 (1-6) 1323-1325.

Sorokin, Y.I. 1981. Aspects of the biomass, feeding, and metabolism of common corals of the Great Barrier Reef, Australia. Proc 4th Int Coral Reef Symp 2: 27-31.

Wellington, G. M. 1982. An experimental analysis of the effects of light and zooplankton on coral zonation. Oecologia (Berl) 52: 311-320.

Wilkinson, C. R. 1986. The nutritional spectrum of coral reef benthos; or Sponging off one another for dinner. Oceanus 29 (2): 68-75.

Yonge, C.M. and Nicholls, A.G. 1931. Studies on the physiology of corals. V. The effects of starvation in light and darkness on the relationship between corals and zooxanthellae. Sci Rep Gr Barrier Reef Exped 1929-29 1: 213-251.