Chemical Warfare on Coral Reefs: Revealing secrets of seaweed defenses and herbivore attacks

Grazers, including such diverse organisms as fish, sea urchins, crabs, and snails, play a crucial role in coral reef ecology. However, the preferred prey of grazers - seaweeds - are not passive victims: they often defend themselves against being eaten by producing a variety of noxious chemicals. These chemicals can taste bad or affect the digestion of grazers in such a way that they avoid eating certain species, or they will take only a bite or two before looking for something else to eat. This confers substantial advantages to seaweeds that produce these chemicals, since swimming away from or hiding from grazers are not options. The results of repeated interactions among grazers and defended seaweeds ultimately shapes the way coral reefs look and function.

Over the past 20 years, understanding of the ecology of seaweed defenses has grown dramatically. For example, chemicals that often make seaweeds resistant to fish grazing do not provide protection from some other grazers, such as certain crabs, worms, ascoglossans (snails without shells), or amphipods (small crustaceans). Further, some seaweeds additionally defend themselves by producing calcium carbonate, a mineral that hardens some algae until they become almost rock-like, reducing the ability of some grazers to bite into the alga. Other grazers avoid these seaweeds because their stomachs cannot process the calcium carbonate without releasing tremendous quantities of CO2 gas - these fish have a lot of acid in their stomachs and for them eating these seaweeds would be like dropping a Tums tablet into a coke. Seaweeds with calcium carbonate (known as calcified algae including for example, Halimeda and Penicillus are often among the most common species on coral reefs. In some instances, the combination of chemicals and mineral defenses work together to deter multiple grazer groups, or to deter in combination grazers that are not effectively deterred by either trait alone. Preliminary work conducted by Dr. Hay suggests that common parrotfish in the Florida Keys might be avoiding chemically-rich seaweeds but are capable of feeding on calcified seaweeds, while common surgeonfishes might be avoiding calcified species, but not chemical-rich seaweeds. The implications of these results are significant because it is well known that seaweeds are abundant at many reef relocations in the Florida Keys and seaweeds are known to overgrow corals.

One objective of this month's Aquarius mission is to evaluate how different species of herbivores affect ecosystem function, and if maintaining greater diversity of consumers is critical for controlling seaweeds on coral reefs. That is, experiments will be conducted to determine if certain species of herbivorous fishes are disproportionately important in removing certain types of seaweeds from reef habitats, or if certain mixes of herbivore species are critical to prevent seaweeds from overgrowing corals. In addition to improving our basic understanding of coral reef ecology, this investigation may offer new options for coral reef management and restoration. Most reef conservation and management is presently based on protecting reefs from human disturbances (for example, pollution and overfishing), under the assumption that damaged reefs will recover if local stresses are removed. However, this assumption may be flawed because it's possible that disturbances have pushed reef communities so far towards seaweed-dominated systems (because corals have died and algae have taken over) that they won't recover unless key components of the system are replaced. The idea is that once reefs become largely covered by algae they support fewer fish because fish depend on corals for habitat, and fewer new corals grow because all available space is occupied by algae. In the Keys and many Caribbean locations this situation is made worse by the fact that a major grazer - the black sea urchin - was largely killed off by a disease epidemic in the 1980s.

If this study determines that certain species, or certain mixes, of herbivorous fishes are disproportionately important in removing common seaweeds from the reef, then this understanding may suggest new opportunities and approaches for reef management. Disproportionately important species could be used as "biological fulcrums" to leverage reefs back to desired states of ecosystem function. However, we know little about how specific species of grazing fish affect community structure, how effects of many species sum to produce an overall effect, or whether a particular mix of species (biodiversity) is critical, or of minimal importance, for reef function. If most reef herbivores are ecologically redundant, then one species may be an adequate substitute for another. However, if ecologically important herbivores differ considerably in their responses to seaweed defenses, then particular herbivores, or mixes of herbivores, could be crucial to maintaining ecosystem function by preventing seaweeds from overgrowing corals.

This hypothesis will be evaluated in a series of experiments that use large (2 meters long by 2 meters wide by 0.6 meters tall) cages attached to hard bottom communities in the vicinity of the Aquarius underwater laboratory. The cages will be used to enclose specific fish species, and mixes of fish species, to determine: 1) their long-term effects on community structure; 2) how small mobile species (for example, juvenile fishes, crabs, and amphipods) that can move through the mesh (mesh size equals 2.5 centimeters) of the cages respond to these community changes; and 3) how algal chemical and mineral defenses generate the mechanisms that drive these changes, possibly affecting the overgrowth of corals. Some cages will be established that keep out all large herbivores, while others will include either two small redband parrotfish (Sparisoma aurofrenatum), two small ocean surgeonfish (Acanthurus bahainus), or one redband parrotfish and one ocean surgeonfish. These two fish species are among the most abundant species found on reefs in Florida.

Cage experiments have a long tradition in marine experimental ecology. They are not perfect in the sense that they do not rigorously mimic specific field conditions such as natural fish densities and enclosed fish may be forced (due to limited mobility and choices) to feed on less palatable species. However, cage experiments are extremely useful in identifying major mechanisms that affect ecosystem function. For example, it is possible that the dramatic patterns observed in the preliminary results described above are conservative - that is, some species will not feed on some seaweeds regardless of limited other options. This field investigation using Aquarius for the lengthy setup times of the cages and initial sampling represents the first attempt ever to identify how differences in fish feeding behavior and seaweed chemical defenses affect community structure on reefs in Florida.