THE H. T. ODUM SYNTHESIS ESSAY New Trends in Marine Chemical Ecology

This essay is the outcome of a colloquium convened in November 2005 at the Benthos Laboratory of the Stazione Zoologica Anton Dohrn in Ischia, Italy, on chemical ecology and the role of secondary metabolites in the structuring and functioning of marine biodiversity. The participants of the workshop are part of the European Network of Excellence MarBEF (Marine Biodiversity and Ecosystem Function), a consortium of 56 European marine institutes to integrate and disseminate knowledge and expertise on marine biodiversity. Here we review some of the new trends and emerging topics in marine chemical ecology. The first section deals with microbial chemical interactions. Microbes communicate with each other using diffusible molecules such as N-acylhomoserine lactones (AHL). These are regulators in cell-density-dependent gene regulation (quorum sensing) controlling microbial processes. In chemical interactions with higher organisms, microbes can act either as harmful pathogens that are repelled by the host’s chemical defense or as beneficial symbionts. These symbionts are sometimes the true producers of the host’s secondary metabolites that have defensive and protective functions for their hosts. We also describe how allelochemicals can shape phytoplankton communities by regulating competition for available resources, and also interactions among individuals of the same species. Compounds such as the diatom-derived unsaturated aldehydes have been demonstrated to act as infochemicals, and they possibly function as a diffusible bloom-termination signal that triggers an active cell death and bloom termination at sea. The same molecules have also been shown to interfere with the reproductive capacity of grazing animals deterring future generations of potential predators. Such compounds differ from those that act as feeding deterrents since they do not target the predator but its offspring. Many of the neurotoxins produced by dinoflagellates act as feeding deterrents, and laboratory experiments have shown that ingestion of these algae by some microzooplankton and macrozooplankton can cause acute responses such as death, incapacitation, altered swimming behavior, and reduced fecundity and egg-hatching success. These effects may rarely occur in nature because of low individual grazing rates on dinoflagellate cells and grazing on other food sources such as microflagellates and diatoms. We also consider the nutritional component of marine plant-herbivore interactions, especially in the plankton, and the information available on the effects of growing conditions of algae on the production of toxic metabolites. Species producing saxitoxins seem to consistently produce the highest amounts of toxins (on a per cell basis) in the exponential phase of growth, and there is a decrease in their production under nitrogen, but not under phosphorus stress, where the production actually increases. We try to explain the circumstances under which organisms defend themselves chemically and argue that the most likely explanatory model for the production of secondary metabolites used for defense in planktonic organisms is the carbon nutrient balance hypothesis, which predicts that most algae produce their toxins mainly under conditions where carbon is in excess and nitrogen (or other nutrients) is limiting. We also discuss chemically mediated macroalgal-herbivore interactions in the benthos and the large variation in concentration of seaweed defense metabolites at different spatial and temporal scales. Seaweeds have been shown to produce a large variety of secondary metabolites with highly variable chemical structures such as terpenoids, acetogenins, amino acid derivates, and polyphenols. Many of these compounds probably have multiple simultaneous functions for the seaweeds and can act as allelopathic, antimicrobial, and antifouling or ultraviolet-screening agents, as well as herbivore deterrents. We also provide examples of interactions between marine benthic invertebrates, especially sponges, molluscs, and cnidarians, that are mediated by specific secondary metabolites and discuss the role of these in shaping benthic communities.