The Natural Function of Seaweed Secondary Metabolites
Mark E. Hay
Institute of Marine Sciences
University of North Carolina at Chapel Hill
Many seaweed secondary metabolites deter feeding by marine herbivores. However, the deterrent effects of a compound may vary greatly against different herbivores, and structurally similar metabolites may have very different effects against the same herbivore Understanding the ecological and evolutionary forces selecting for this variance and the mechanisms of action producing it will advance both pure and applied aspects of marine ecology and marine biotechnology.
More than 600 secondary metabolites have been isolated from marine algae (Faulkner 1984, 1986). The large majority of these (about 60%) are terpenes, but fatty acids are also common (comprising about 20% of the metabolites), with nitrogenous compounds and compounds of mixed biosynthesis each making up only about 10% (Van Alstyne and Paul 1988). Many of these compounds are bioactive and have been extensively studied using laboratory and pharmacological assays (Faulkner 1984, 1986; Paul and Fenical 1987). However, their natural functions under ecologically realistic conditions have been investigated only recently (Steinberg 1985, 1988; Targett et al. 1986; Hay et al. 1987a, b, 1988a, b, c; PauI 1987; Paul et al. 1987; Paul and Van Alstyne 1988a; Hay and Fenicall988; Van Alstyne 1988).
Numerous seaweed metabolites have now been assayed in both field and laboratory tests to determine their effectiveness as feeding deterrents against herbivorous fishes, sea urchins, gastropods, amphipods, and polychaetes (see Hay and Fenical 1988). Although many seaweed
metabolites are effective general deterrents against the most common marine herbivores (fishes, sea urchins, shelled gastropods), the defensive value of a compound has been demonstrated to be a specific function of both compound structure and the particular herbivore species attacking
the plant. Structurally similar compounds can differ dramatically in their effect on herbivore food choice, and compounds that deter one herbivore can have very different effects on another (Hay et al. 1987a, b, 1988a; Paul and Fenical 1987; Paul et al., 1987; Steinberg 1988). As examples, isolaurinterol and aplysin (Hay et al. 1987b), pachydictyolh and dictyol-E (Hay et al. 1987a), and ochtodene and condrocole-C (Paul et al. 1987) are structurally similar terpenes that vary significantly in how they affect feeding by herbivores. Since the function of a compound cannot be predicted by structural class, it is inappropriate to classify terpenes as toxins and phlorotannins as digestibility reducers, as has occasionally been done.
Small herbivore size, limited mobility, and certain life-history characteristics that might diminish dispersal and promote local adaptation appear to be correlated with herbivore resistance to seaweed chemical defenses (Hay and Fenical 1988). Small relatively sedentary herbivores (mesograzers) like ascoglossans, tube-building amphipods, and polychaetes often selectively live on and consume seaweeds that are low preference foods for fishes and larger invertebrates. Metabolites from these seaweeds deter feeding by larger herbivores but stimulate, or do not affect, feeding by mesograzers (Hay et al. 1987a, 1988a, c; Paul et al. 1987; Paul and Van
Alstyne 1988b).
Many of these mesograzers are not restrictively specialized to particular host plants and several appear to be resistant to a broad range of unrelated seaweed metabolites that significantly deter feeding by fishes (Hay et al. 1987a, 1988a, c; Paul et al. 1987). Several mesograzers appear to have evolved feeding preferences for chemically-defended seaweeds because these plants provide them with living sites that serve as escapes from fish predation (see Hay et al. 1987a and Hay and Fenical 1988). In these respects, many marine mesograzers are ecologically similar to herbivorous terrestrial insects (Bernays and Graham 1988 and references therein), and their
resistance to plant defenses may result from a mechanism similar to the mixed-function oxidase (MFO) system, which is thought to explain the resistance of insect pests to many agrochemicals (see Futuyma 1983 and Hay et al. 1988~).
A few seaweed metabolites significantly deter feeding by crustacean mesograzers but do not affect feeding by fishes or larger invertebrates. If these compounds selectively target mechanisms of detoxication that are common to both crustacean mesograzers and insects, they might be useful as agrochemicals since they show selective instead of broad-scale activity and since they are marine compounds with which terrestrial insects would have had no evolutionary experience. To date, most of the applications for marine natural products, and often the natural products themselves, have been found by conducting largescale screening programs. Since these programs are not based on a compelling biological rationale, they are often costly and inefficient. Many inactive organisms are screened and many active compounds are not detected because they degrade during collection, storage, and extraction, or because they are not tested against appropriate target organisms. An enhanced understanding of the natural functions, effects, and mechanisms of action of secondary metabolites would provide a biologicallybased rationale for the productive development of products based on marine natural products. Work with seaweed defensive chemicals offers one example of how ecological understanding may fwilitate the integration of marine chemical ecology and biotechnology.
LITERATURE CITED
Bernays, E., and M. Graham. 1988. On the
