FEATURE CHEMICAL ECOLOGY AND MARINE BIODIVERSITY: INSIGHTS AND PRODUCTS FROM THE SEA By Mark E. Hay and William Fenical TREMENDOUS ATTENTIONhas been focused on the 1987). As examples, kelps form a structural matrix loss oK and threats to, terrestrial biodiversity. Until that is critical for nearshore temperate communi- very recently (Norse, 1993), much less attention ties, and corals play this same role on tropical was devoted to marine biodiversity despite the fact reefs. When kelps are removed by storms, El Nifio that marine systems are larger, older, have a huge events, overgrazing by sea urchins, or due to an- impact on global climate, and support nearly twice thropogenic stresses, normal ecological processes as many phyla of animals as do terrestrial systems are altered and the composition and organization of (see Table 2-2 in Norse, 1993). Our reduced atten- the entire nearshore community can change dra- tion to marine biodiversity reflects our relative ig- matically (Simenstad et al., 1978: Tegner and Day- norance of marine systems rather than their lack of ton, 1987: Duggins et ell., 1989). In a similar way, importance to humans or to the ecosystem func- destruction of tropical corals due to overfishing, tions on which virtually all terrestrial life depends. storms, and general habitat degradation (e.g., sedi- Humans have spent thousands of years in intimate mentation) lessens topographic complexity and association with terrestrial biota, but only a few turns species-rich coral reefs into algal beds with decades using SCUBA and submersibles to ex- reduced biodiversity (Hughes, 1994). Biologically plore the world's oceans. In this article we discuss produced chemical diversity may play a similar, how chemically mediated interactions affect ma- but unappreciated, role in structuring marine com- fine biodiversity and consider the insights that can munities and affecting marine biodiversity. • . secondary be gained from understanding the mechanisms in- volved in these interactions. Distribution and Diversity of Novel Secondary metabolites . , . can Biodiversity is often used incorrectly as a syn- Metabolites have important com- onym of species diversity; however, biodiversity Secondary metabolites (i.e., unusual compounds also encompasses genetic and ecosystem diversity that are not involved in primary metabolism) ap- plex or indirect (Norse, 1993). The factors that produce and main- pear to be most common among tropical benthic effects that alter tain patterns of biodiversity at these different lev- organisms that are subject to high rates of attack by els are complex and poorly understood. In this re- consumers on coral reefs (Hay and Steinberg, marine biodiversity view, we argue that secondary metabolites 1992: Paul, 1992; Pawlik, 1993: Bolser and Hay, in on the genetic, produced by a variety of marine organisms as de- press). However, secondary metabolites also play fenses against consumers, pathogens, and competi- important roles in temperate (Steinberg, 1992) and species, and ecosys- tors {Hay and Steinberg, 1992: Paul, 1992) can Antarctic benthic communities (McClintock, 1994), have important complex or indirect efl'ects that and possibly in pelagic communities worldwide tem levels. alter marine biodiversity on the genetic, species, (Huntley et ell., 1986; Paerl, 1988). and ecosystem levels. Seaweeds, sponges, ascidians, soft corals, and The role of biogenic structural complexity in af- other sessile organisms produce a diverse array of fecting species diversity has been extensively stud- novel secondary metabolites (Figs. 1-6) including ied and is broadly appreciated in both marine and terpenes, acetogenins, alkaloids, and polypheno- terrestrial communities (Ehrlich and Roughgarden, lics. Some of these compounds differ fundamen- tally from terrestrial secondary metabolites in that Mark E. Hay, University of North Carolina at Chapel Hill, they are halogenated (Fig. 1, elatol from the red Institute of Marine Sciences, Morehead City. NC 28557. USA; seaweed Laurencia) and often possess chemical Phone: 919-726-6841: FAX: 919-726-2426: lnternet: sea- structures that are unprecedented among terrestrial [email protected]; William Fenical, Scripps Institution of Oceanography. University of Calilbrnia at San Diego, La Jolla, organisms (Faulkner, 1994 and reviews cited CA 92093, USA; Phone: 619-534-2133; FAX: 619-558-3702: therein). To date, several thousand marine sec- Internet: [email protected] ondary metabolites have been described, with 10 OCEANOGRAPHY-VoI.9, No. 1-1996 can avoid their own consumers by association with these chemically noxious hosts. Some examples of how defended organisms enhance the evolution or maintenance of species diversity by producing lo- calized sites of lowered consumer activity or by serving as a source of chemical defenses for other organisms are outlined below. Associational Refuges: Turning Competitors into Accomplices Palatable seaweeds that are usually driven to local extinction by grazers can persist in herbi- vore-rich communities if they grow on or beneath their herbivore resistant competitors (reviewed by Hay, 1992). The brown seaweed Stypopodium zonale produces cytotoxic compounds that deter feeding by Caribbean reef fishes and urchins. Nu- merous species of palatable seaweeds are significantly more common near the base of Sty- popodium plants than several centimeters away; if the deterrent plant is removed, these more palat- able species are rapidly eaten (Littler et al., 1986), • . defended organ- lowering local species diversity. When plastic isms enhance the mimics of Stypopodium are placed in the field, they also provide a partial refuge for palatable evolution or mainte- Fig. 1: Examples of marine secondary metabo- species, but they are less effective than the real nance of species lites. plants, suggesting that associational refuges are generated in part by the physical presence of a diversity by produc- nonfood plant, but that the plant's chemical repug- more being discovered daily. As one example of ing localized sites of the chemical variety to be found in marine organ- nance makes the associational refuge more effec- isms, members of the red algal genus Laurencia tive. lowered consumer produce an amazing array of complex terpenoids In temperate communities, palatable seaweeds activity... and acetogenins--possibly making it the world's can minimize losses to herbivorous fishes and most chemically complex genus. The genus pro- urchins by growing on or near unpalatable sea- duces over 500 different terpenes representing at weeds such as Sargassum filipendula (Hay, 1986; least 26 different structural classes, more than 16 Pfister and Hay, 1988). Growing in close associa- of which are novel and found only in Laurencia tion with these unpalatable competitors depresses (Faulkner, 1994 and previous reviews). This type the growth of palatable species by as much as of rich chemical diversity can function as a habitat 85%, but the associational benefits, in terms of re- duced herbivory, can more than offset this compet- gradient that promotes the evolution and mainte- itive cost (Hay, 1986). Thus, palatable species can nance of biodiversity through resource or habitat partitioning, specialization of consumers or com- be dependent on their unpalatable competitors to mensals, and selection for genetic or phenotypic prevent their exclusion from the community due to herbivory. Correlative and manipulative studies in diversity among consumers associated with popu- lations or species that differ chemically. Plant sec- both field and mesocosm systems indicate that re- ondary metabolites appear to play this role in ter- moval of common unpalatable competitors like can cause extinction, rather than com- restrial systems where they are hypothesized to Sargassum petitive release, of associated competitors that are have promoted the tremendous species diversity of more palatable (Hay, 1986). These associational herbivorous insects (Strong et al., 1984). refuges were initially interpreted as arising from Chemically Mediated Effects on Species simple visual crypsis (Hay, 1986), but more de- Diversity tailed investigations suggest that chemistry plays a The ecology and evolution of marine chemical significant role (Pfister and Hay, 1988; Wahl and defenses have been studied most thoroughly for Hay, 1995). benthic organisms on reefs, with the majority of As a final benthic example, up to 18% of the attention being devoted to defenses against gener- dry mass of algae in the genus Desmarestia can be alist consumers like fishes and urchins (Hay and sulfuric acid; this concentration is sufficient to Steinberg, 1992; Paul, 1992; Bolser and Hay, in quickly kill seaweeds and dissolve barnacles from press)• Once organisms become well defended the rocks when this kelp is deposited in the inter- chemically, they may then become targets of evo- tidal by waves (Hay and Fenical, 1988). In lutionary opportunity for other potential prey that Chilean kelp beds heavily grazed by sea urchins, OCEANOGRAPHY*VoI.9, NO. 1"1996 1 1 the palatable kelp Macrocvstis cannot successfully chaetes, and crabs (collectively called mesograzers) colonize unless it invades an area encircled by would have low fitness if they lived on plants that Desmarestia plants, which appear to act as "'acid were preferred by fishes because they would be- brooms" that prevent urchins from entering the come fecal pellets more often than reproductive area (Dayton, 1985). Although planktonic systems adults. It was, therefore, hypothesized that