Constraints on chemically mediated coevolution: multiple functions for seaweed secondary metabolites

Diterpene alcohols produced by the brown seaweed Dictyota menstrualis deter feeding by numerous species of abundant herbivores. Here we show that these same compounds also may prevent fouling organisms from colonizing the surface of this alga. In the field, Dictyota menstrualis plants were less frequently and less heavily fouled than any of the other common seaweed species investigated. In laboratory assays, larvae of the common fouling bryozoan Bugula neritina failed to settle on Dictyota even though they contacted its surface as often as they contacted the surface of a preferred host alga. Rejection occurred only after direct contact with the alga's surface. Rejection of Dictyota was not mediated by water-borne chemical cues or by surface wettability (a physical property of the surface that can affect fouling). The lipid-soluble extract from surface rubbings of Dictyota inhibited larval settlement when placed on other surfaces and contained the diterpene alcohols pachydictyol A and dictyol E. Larvae exposed to these compounds experienced mortality, abnormal development, or reduced rates of development. Although the potential for chemically mediated coevolution between plants and herbivores has been the focus of scores of previous investigations, such coevolution will depend on selection altering the chemical defenses of the plant following the evolution of resistance by herbivores. Such a reciprocal response will be constrained if compounds play multiple roles that are ecologically important. Dictyota produces secondary metabolites that are broadly defensive against a wide variety of consumers and fouling organisms. Although certain consumers may evolve resistance to these metabolites, it is unclear that feeding by these consumers will result in reciprocal responses from the plant. We suggest that coevolved interactions may be uncommon, and that many interactions that appear to be coevolved may result from fortuitous and opportunistic preadaptations