Publications

Relationships among food choice, compensatory feeding, and the consequences for consumer fitness rarely have been quantified. We created foods of varying nutritional quality and evaluated the consequences of compensatory feeding for three sympatric species of amphipods by analyzing food choices, feeding rates, and long-term effects on fitness. Nutritional quality was manipulated by creating low-quality diets from algae (low in protein, nitrogen, and total organic carbon), high-quality diets from commercial fish food (high in protein, nitrogen, and total organic carbon), and intermediate-quality diets from mixtures of those two foods. When high- and low-quality diets were simultaneously offered, the more mobile, non-tube-building amphipods, Gammarus mucronatus and Elasmopus levis, both fed preferentially on the high-quality diet. The more sedentary, tube-building amphipod Ampithoe longimana did not discriminate between these foods. When confined to a single food type, all three species exhibited compensatory feeding on the low-quality diet. Despite compensatory feeding, when Elasmopus levis were cultured on the low-quality food, they experienced reduced survivorship, growth, and fecundity during two successive ovulations, compared to individuals feeding on more nutrient-rich foods. Low-nutrient foods caused similar declines in growth and female gonad size for Gammarus mucronatus. In contrast, the survivorship, growth, and fecundity of Ampithoe longimana was not affected by any of the diets tested. Thus, compensatory feeding allowed the more sedentary species, Ampithoe longimana, to completely circumvent the effects of low nutritional quality, but the same behavior was ineffective for both of the more mobile species, Gammarus mucronatus and Elasmopus levis. The ability of A. longimana to achieve equal fitness by substituting food quantity for food quality may allow this sedentary species to form longer associations with individual host plants, minimize movement among hosts, and thus lower its risk of being detected by predators.

To determine the direct effects of microcystin on the fitness of herbivorous zooplankton, we experimentally added microcystin‐LR to freeze‐dried cells of palatable Chlorella and fed these compound‐treated cells to two clones of Daphnia pulicaria that had shown differing responses to a diet containing a strain of Microcystis aeruginosa that produces microcystin. The Daphnia that performed better on a diet containing live Microcystis showed reduced population growth when exposed to microcystin‐LR‐treated Chlorella , whereas the Daphnia that performed poorly on the diet containing live Microcystis was not affected by the experimental diet containing microcystin‐LR. This is the first study to unambiguously show that some Daphnia strains are and some strains are not harmed by the consumption of microcystin‐LR. These surprising results were not generated by interference from lipophilic secondary metabolites in Microcystis . When the crude lipophilic extract of Microcystis was added to dried Chlorella cells, it enhanced the fitness of both Daphnia clones. We hypothesize that the Daphnia clone more tolerant to live cells may upregulate resistance when cued by the presence of the live Microcystis cells, but not by microcystin‐LR alone. Alternatively, the Daphnia clone that grew well on a diet containing live Microcystis may sequester compounds from Microcystis that defend the cyanobacteria from autotoxicity; these compounds would have been unavailable to Daphnia consuming freeze‐dried Chlorella treated with microcystin‐LR alone. Thus, microcystin‐LR can suppress Daphnia fitness when consumed; however, the effects of microcystin vary across clones of herbivorous zooplankton and the consequences of this variance should not be overlooked when considering zooplankton‐cyanobacteria interactions.

Grazing by the generalist amphipod Ampithoe longimana induced increased concentrations of defensive secondary metabolites in the brown alga Dictyota menstrualis and made the seaweed less susceptible to further attack by the amphipod. Although A. longimana preferentially consumes D. menstrualis, its feeding rates can be reduced significantly by high concentrations of diterpenoid dictyols produced by the alga. In 1991, D. menstrualis from sites with high numbers of A. longimana had higher levels of grazing scars, higher concentrations of dictyols, and were less palatable to A. longimana than plants from sites with few amphipods. Among-site differences in palatability to amphipods did not correlate with plant differences in protein, nitrogen, or carbon content. Within a site, plants that had apparent amphipod grazing scars were significantly less palatable to A. longimana than neighboring undamaged plants. Controlled field experiments manipulating A. longimana densities supported the hypothesis that feeding by this amphipod induced elevated chemical defenses in the alga. Compared to undamaged control plants, amphipod-damaged plants had 19-34% more of three diterpenoid secondary metabolites and were 50% less palatable to amphipods. Soluble protein and thallus toughness were unaffected by amphipod grazing and thus could not have caused the differences in palatability. High-pressure liquid chromatography evaluation of adventitious branches growing from blade margins at sites of amphipod grazing scars showed that these branches had significantly elevated levels of two diterpenoids relative to normal blade apices or middles. Thus, the amphipod-induced resistance to further attack occurs through an increase in chemical defenses, and these defenses are, to some extent, localized within the plant thallus. Among-site differences in amphipod densities, grazing scars, seaweed defensive chemistry, and plant palatability that we documented in 1991 varied considerably during 1992 and 1993, suggesting that these interrelationships may be complex. In 1992, A. longimana densities did not differ between sites, and there were no between-site differences in palatability or concentrations of deterrent secondary metabolites. In 1993, however, A. longimana densities did differ between sites, but between-site differences were less dramatic than in 1991. Some secondary metabolites were slightly, but significantly, increased at the site with higher densities of A. longimana, but this had no effect on A. longimana feeding. It has been long recognized that marine herbivores are active participants in seaweed-herbivore interactions and can greatly influence the structure of benthic algal communities. Our findings suggest that seaweeds are not passive participants in these interactions, but can actively alter their susceptibility to herbivores in ecological time. Induced responses to herbivory help explain both spatial (i.e., within-thallus, within-site, and among-site) and temporal variation in the chemical defenses of D. menstrualis.

Herbivores often specialize on particular hosts that provide both food and shelter from natural enemies. It is thus often unclear whether a plant's value as a food or its value as a safe shelter has played a larger role in selecting for specialization. Decorator crabs offer a novel opportunity to investigate the relative effects of diet vs. natural enemies in selecting for specialization because these crabs place plant shelter on their backs as camouflage but need not use these plants as food, thus decoupling the plant's value as a food from its value as a shelter. In this study, we show that juveniles of the decorator crab Libinia dubia selectively decorate with the chemically defended brown alga Dictyota menstrualis but treat this plant as a low-preference food. Common omnivorous fishes that are potential predators of Libinia avoid consuming Dictyota due to the alga's potent chemical defenses. In the field, juvenile crabs decorated with Dictyota experience significantly less predation than crabs decorated with an alga that is not chemically noxious to local fishes, and the Dictyota metabolite that most strongly deters feeding by fishes is the specific metabolite that determines decoration choice by this crab. Thus, by behaviorally sequestering defenses from this chemically noxious plant, these small crabs reduce their susceptibility to predation. In the presence of predators, juvenile crabs reduce their rate of feeding, but not of decorating, suggesting that antipredator behavior such as decorating takes precedence over feeding. In addition, only juvenile crabs that are of a size that can be consumed by local fishes decorate at all. Adult crabs that have carapace widths exceeding the gape size of co-occurring fishes do not decorate in either the field or the laboratory. Apparently predation, rather than diet selection, drives decoration specialization in Libinia, highlighting how indirect effects of plant secondary chemistry can impact herbivore behavior, ecology, and evolution.

Previous investigations have shown that the sedentary amphipod Ampithoe longimana escapes consumers by selectively living on and eating chemically defended seaweeds in the genus Dictyota. However, A. longimana and Dictyota overlap only in the southern portion of the amphipod's range; Dictyota is not available to amphipods from more northerly regions. We used this disjunction in distribution to test the hypothesis that A. longimana populations co-occurring with Dictyota would have greater tolerance for the seaweed's chemical defenses and would display higher feeding preference for, and fitness on, the seaweed than would more northerly populations. We also evaluated the genetic vs. phenotypic basis of these patterns and attempted to detect trade-offs between tolerance for Dictyota and ability to use other plants as foods. Such geographic studies of herbivory have been conducted using terrestrial insects, but few studies have focused on other herbivores, and this is especially true for marine systems. In multiple-choice feeding assays with both field-collected and laboratory-reared adults, a North Carolina population of A. longimana sympatric with Dictyota more readily fed on Dictyota and was more resistant to Dictyota's deterrent chemistry than was a Connecticut population from outside of Dictyota's geographic range. When raised on Dictyota menstrualis and D. ciliolata, A. longimana juveniles from North Carolina grew faster, matured faster, and produced more reproductive females than did Connecticut juveniles. The differential tolerance for Dictyota has a genetic basis, as it was maintained through two generations grown to maturity in a common environment. When several northern and southern populations were assayed, they displayed similar regional differences in feeding preferences. Though southern juveniles had higher fitness on Dictyota than northern juveniles, southern juveniles performed as well as northern juveniles when raised on seven other seaweeds, including seaweeds (e.g., Fucus vesiculosus and Sargassum filipendula) that produce secondary metabolites in a different class from those found in Dictyota. Thus, tolerating Dictyota did not incur detectable performance trade-offs when juveniles were confined to feeding on alternative seaweeds. Our results suggest that the evolution of host preferences may depend more on the host value as a refuge from enemies than on minimizing the costs of tolerating plant secondary metabolites.

Five secondary metabolites from tropical marine algae and one related compound from an herbivorous sea—hare (Aplysidae) were coated, at approximately natural concentrations, onto the palatable seagrass Thalassia testudinum and placed on coral reefs where they could be eaten by the diverse group of herbivorous fishes that occur there. Laboratory feeding assays with the herbivorous sea urchin Diadema antillarum were also conducted. When compared to appropriate controls, the following terpenoid compounds significantly reduced the amount of Thalassia eaten by both Diadema and reef fishes: stypotriol, from the brown seaweed Stypopodium zonale; pachydictyol—A, which is produced by several genera of tropical (Dictyota and Dilophus) and warm—temperate (Pachydictyon and Glossophora) brown seaweeds; elatol, from the tropical red alga Laurencia obtusa; and isolaurinterol, which is produced by several tropical and warm—temperate species of Laurencia. Under very mild acid conditions, isolaurinterol is converted to a structurally similar compound, aplysin, found in high concentrations in sea—hares that feed on isolaurinterol—containing Laurencia species. Aplysin did not deter feeding by either type of herbivore. Cymopol, a terpenoid bromohydroquinone from the green alga Cymopolia barbata, significantly reduced feeding by reef fishes but significantly stimulated feeding by Diadema. Pharmacological and crude bioactivity tests suggest that several of these compounds function as generalized toxins. However, these generalized laboratory assays are not necessarily good predictors of how compounds will affect feeding by herbivores. For example, pachydictyol—A and stypotroil were equally effective at deterring fishes and Diadema, even though pachydictyol—A shows almost no bioactivity in laboratory assays while stypotriol and its oxidation product, stypoldione, are very bioactive. Herbivory on coral reefs is more intense than in any other habitat studied and the diversity of herbivore types is high. It appears that this intense grazing has provided strong selection for seaweeds that synthesize unique secondary metabolites that significantly reduce the consumption of plants exposed to attack by a diverse group of reef herbivores.