SYNERGISMS IN PLANT DEFENSES AGAINST HERBIVORES - INTERACTIONS OF CHEMISTRY, CALCIFICATION, AND PLANT-QUALITY

Many tropical seaweeds and benthic invertebrates produce both secondary metabolites and calcium carbonate (CaCO3) particles or spicules that serve as possible defenses against consumers. To evaluate the relative defensive value of CaCO3, secondary metabolites, and the potential synergistic or additive effects of the two, we made artificial agar-based ''seaweeds'' in which we manipulated algal organic content, CaCO3, and the secondary metabolites produced by the calcified green seaweeds Rhipocephalus phoenix, Udotea cyathiformis, and Halimeda goreauii, all of which are relatively resistant to herbivores. The effects of these manipulations on herbivore feeding were evaluated using three different types of herbivores, the sea urchin Diadema antillarum, the amphipod Cymadusa filosa, and a mixed-species group of small parrotfishes. Addition of finely powdered CaCO3 as 69% of food dry mass had no effect on feeding by parrotfishes, deterred feeding by Cymadusa, and deterred Diadema when food organic content was low but not when it was higher. Although calcification of algal tissues has generally been considered a structural defense that hardens seaweed thalli and makes them more resistant to attack, the decreased feeding on CaCO3-containing foods in our assays occurred without any measurable alteration of food toughness. At natural concentrations, semipurified secondary metabolites from Rhipocephalus or Udotea deterred feeding by all three herbivores. In most assays, feeding was depressed more by the addition of metabolites from Rhipocephalus or Udotea than by the addition of CaCO3 even though CaCO3 was added at 1.3-2.2 times the natural concentration for these plants. In contrast, the major metabolite from Halimeda goreauii, when tested alone, did not affect feeding by any of the herbivores. In two of our nine assays, the synchronous combination of CaCO3 and secondary metabolites acted synergistically and deterred feeding significantly more than the sum of the effects of each tested separately. Mechanisms producing these synergisms are unknown, but it is possible that calcification could also be acting as a chemical defense by altering gut pH in ways that increase the potency of the secondary metabolites. It is common for chemical, structural, morphological, and nutritional deterrents to co-occur in individual prey species. For some plant-herbivore interactions, the combined effects of these characteristics can be much more than the sum of their separate effects.