WHEN LIFE IS ON THE ROCKS: CHEMICAL DEFENSES IN SESSILE MARINE ORGANISMS

Introduction

The key limiting resource in marine hard-bottom communities is space. Nowhere is this more evident than on the shallow coral reefs of the tropics. Partly because living space is so valuable, a large proportion of reef inhabitants exist as sessile (non-mobile permanently attached) individuals. The reef-building corals are attached to the fossil limestone skeletons of earlier inhabitants of a site. Sponges, sea fans, sea whips, bryozoans, tunicates, macroalgae, and other organisms also live attached to this non-living hard substrate, and on the living coral as well.

Most of the sessile reef inhabitants occur as free-living larval forms or propagules, but take up a permanently attached benthic (botton-associated) existence when they later settled onto the reef.

Better Living Through Chemistry

Living as sessile organisms, reef inhabitants overcome the severe real estate shortage by simply not leaving a good patch of habitat once they find one. But, an immobile existence gives rise to its own problems. Chief among these is the need to keep from being eaten, the need to keep from being fouled or overgrown, the need to successfully reproduce, and the need to ward off microbial infections.

Though each of these challenges is a primary concern, the solution to the problems is often secondary. That is to say, these organisms often rely on secondary metabolites, or biochemical 'natural products' to overcome many of the difficulties of life on the rocks. The study of how these organisms use natuaral products to meet environmental challenges is known as marine chemical ecology.

Select among the challenges presented below to see how various reef inhabitants utilize natural chemical products they produce to meet each challenge.

How Can Natural Products Keep Marine Organisms From Being Eaten?

Natural products can be toxic or noxious (bad tasting/smelling) to would-be consumers of sessile organisms. Various marine macroalgae, sponges, and other organisms avoid being eaten because they produce and sequester these products. Sometimes a fish will take a bite out of such organisms only to discover that it is unpalatable or toxic. Sponges, algae, etc., usually survive these encounters, and the co-occurring fish species learn to avoid preying on these species in the future.

Effective as they are, chemical feeding deterrents do not stop all animals from trying to make a meal out of the natural product-producing organisms. Just as these organisms have evolved their chemical defenses, so have a handful of specialist consumers evolved the ability to detoxify or safely sequester these nasty compounds, and thus they are not deterred from preying on these species as are most animals.

Perhaps even more remarkable, some of these predators have evolved the ability to retain the defensive chemicals they ingest and use them for their own defense. Among the better-known examples are sea slugs like the Indo-Pacific Elysiella pusilla. This gastropod mollusc preferentially feeds on green macroalgae with high concentrations of toxic compounds (diterpenoids), and converts and retains the compounds for its own defense against predatory fish. Similarly, the South Pacific sea slug Glossodoris pallida utilizes diet-derived metabolites from the sponges it eats for its own defense. In the Caribbean, the tiger flatworm (Martigrella crozieri) similarly exploits defensive compounds it obtains from its prey, the sea squirt Ecteinascidia turbinata. This sea squirt is the source of the anti-cancer agent ecteinascidin 743.

How Can Natural Products Allow Marine Organisms to Maintain Space?

Sessile reef organisms are potentially susceptible to overgrowth, undercutting, or crowding out by competitors. For filter feeding species like sponges, crowding by competitors often leads to preemption of the planktonic food resources they need to survive. For photosynthetic organisms like macroalgae (seaweed), crowding by other organisms is detrimental because it can shade the algae.

To reduce such competition, some seaweeds, sponges, and other sessile organisms use a chemical defensive strategy called allelopathy. Allelopathy is the suppression of growth of one species by another due to the release of toxic substances. Examples of allelopathic interactions on the reef include the sponge chemicals to kill that uses secondary metabolites to kill living tissues of the corals they colonize to free up living space for itself.

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How Can Natural Products Help Ensure Reproductive Success?

The vast majority of sessile, permanently attached reef invertebrates produce free-living, planktonic larvae. A planktonic larval stage is certainly an effective means of broadcast-dispersal of larvae, but at the time of settlement, the larvae must be able to successfully locate habitats meeting their specific juvenile and adult survival needs.

Since the ability to correctly recognize and settle into suitable habitat is literally a matter of life and death, it is not surprising that many marine invertebrate larvae possess a remarkable ability to 'smell their way' onto appropriate settlement sites. This revolves around the ability of larvae to sense and home in on waterborne chemical cues originating from adult conspecifics, favored adult prey items, or reliable co-occurring organisms.

Almost as important, chemical cues can also elicit an avoidance behavior in larvae, e.g., if the cues in question indicate the presence of large numbers of potential predators.

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How Can Natural Products Protect Marine Organisms Against Infections?

Researchers do not understand how all of the marine natural products thus far discovered function to benefit the source organisms in their natural environment. But, we can make some inferences based on what has been discovered from laboratory bioassays on the extracted compounds. The fact that a large number of marine natural products demonstrate pronounced antibiotic, antiviral, or antifungal properties suggests that these compounds may well play a similar role in nature.

As ubiquitous as marine microbes are now known to be (as many as 1 million bacterial cells in a single milliliter of seawater), what would be truly surprising is if sessile organisms in the marine environment didn't have a way to naturally defend themselves against potential infection and disease.

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