Lee A. Dyer

Host specificity of Lepidoptera in tropical and temperate forests

For numerous taxa, species richness is much higher in tropical than in temperate zone habitats. A major challenge in community ecology and evolutionary biogeography is to reveal the mechanisms underlying these differences. For herbivorous insects, one such mechanism leading to an increased number of species in a given locale could be increased ecological specialization, resulting in a greater proportion of insect species occupying narrow niches within a community. We tested this hypothesis by comparing host specialization in larval Lepidoptera (moths and butterflies) at eight different New World forest sites ranging in latitude from 15° S to 55° N. Here we show that larval diets of tropical Lepidoptera are more specialized than those of their temperate forest counterparts: tropical species on average feed on fewer plant species, genera and families than do temperate caterpillars. This result holds true whether calculated per lepidopteran family or for a caterpillar assemblage as a whole. As a result, there is greater turnover in caterpillar species composition (greater β diversity) between tree species in tropical faunas than in temperate faunas. We suggest that greater specialization in tropical faunas is the result of differences in trophic interactions; for example, there are more distinct plant secondary chemical profiles from one tree species to the next in tropical forests than in temperate forests as well as more diverse and chronic pressures from natural enemy communities.

Tasty Generalists and Nasty Specialists? Antipredator Mechanisms in Tropical Lepidopteran Larvae

To examine the effectiveness of larval antipredator mechanisms and to test the assumption that diet breadth and chemistry are important predictors of predation responses. I offered 70 species of lepidopteran larvae to the predatory ant Paraponera clavata (Hymenoptera: Formicidae). Prey chemistry and diet breadth were significant predictors of rejection, as was plant chemistry but to a lesser degree. Specialist caterpillars were better protected than generalists, and prey with unpalatable extracts were frequently rejected by P. clavata, while prey with palatable extracts were rarely rejected. Specialists with unpalatable host plant extracts were more likely to be rejected than specialists that had host plants with more palatable extracts. Other significant predictors included morphology, behavior, and interactions between developmental stage and prey chemistry and between developmental stage and diet breadth. I concluded that predation could be a substantial selective force in the evolution of narrow diet breadth and that plant chemistry could be the mechanism whereby specialists are better defended.

ON THE CONDITIONAL NATURE OF NEOTROPICAL CATERPILLAR DEFENSES AGAINST THEIR NATURAL ENEMIES

Lepidopteran larvae possess multiple defenses against a diverse group of predators and parasitoids. Many studies of larval defenses have determined whether a defense works against a particular enemy, but the question of which types of defenses are most effective against which types of enemy has not been examined closely. We assessed the efficacy of different caterpillar defenses against parasitoid wasps, flies, and nematodes, and compared the results to earlier work with predatory invertebrates. Third to fifth instar caterpillars from 266 species and 30 families were collected in a lowland wet forest in Costa Rica during wet and dry seasons from 1996 through 1999, scored for various behavioral and morphological defenses, and then reared in the laboratory. Defense categories were used as predictor variables in logit models with parasitism as the response variable. Whether or not a particular caterpillar defense was effective depended on the taxon of parasitoid that attacked. Caterpillars attacked by flies benefited from a solitary, exophytic feeding habit; wasps were most deterred by biting, dropping, and regurgitating; and larvae attacked by nematodes benefited from both a solitary habit and behavioral defenses. Mortality caused by parasitoids was high for caterpillars that are normally protected from predators. In particular, chemically defended herbivores that are undesirable meals for predators are safe hosts for parasitoids.

The global distribution of diet breadth in insect herbivores

Significance Dietary specialization determines an organism’s resource base as well as impacts on host or prey species. There are important basic and applied reasons to ask why some animals have narrow diets and others are more generalized, and if different regions of the Earth support more specialized interactions. We investigated site-specific host records for more than 7,500 species of insect herbivores. Although host specialists predominate, the proportion of specialists is affected by the diversity of hosts and shifts globally, supporting predictions of more exclusive tropical interactions. These results not only affect our understanding of the ecology of food webs, but also have implications for how they respond to environmental change, as well as for ecosystem management and restoration. Understanding variation in resource specialization is important for progress on issues that include coevolution, community assembly, ecosystem processes, and the latitudinal gradient of species richness. Herbivorous insects are useful models for studying resource specialization, and the interaction between plants and herbivorous insects is one of the most common and consequential ecological associations on the planet. However, uncertainty persists regarding fundamental features of herbivore diet breadth, including its relationship to latitude and plant species richness. Here, we use a global dataset to investigate host range for over 7,500 insect herbivore species covering a wide taxonomic breadth and interacting with more than 2,000 species of plants in 165 families. We ask whether relatively specialized and generalized herbivores represent a dichotomy rather than a continuum from few to many host families and species attacked and whether diet breadth changes with increasing plant species richness toward the tropics. Across geographic regions and taxonomic subsets of the data, we find that the distribution of diet breadth is fit well by a discrete, truncated Pareto power law characterized by the predominance of specialized herbivores and a long, thin tail of more generalized species. Both the taxonomic and phylogenetic distributions of diet breadth shift globally with latitude, consistent with a higher frequency of specialized insects in tropical regions. We also find that more diverse lineages of plants support assemblages of relatively more specialized herbivores and that the global distribution of plant diversity contributes to but does not fully explain the latitudinal gradient in insect herbivore specialization.

Revisiting the evolution of ecological specialization, with emphasis on insect–plant interactions

Ecological specialization is a fundamental and well-studied concept, yet its great reach and complexity limit current understanding in important ways. More than 20 years after the publication of D. J. Futuyma and G. Morenos oft-cited, major review of the topic, we synthesize new developments in the evolution of ecological specialization. Using insect-plant interactions as a model, we focus on important developments in four critical areas: genetic architecture, behavior, interaction complexity, and macroevolution. We find that theory based on simple genetic trade-offs in host use is being replaced by more subtle and complex pictures of genetic architecture, and multitrophic interactions have risen as a necessary framework for understanding specialization. A wealth of phylogenetic data has made possible a more detailed consideration of the macroevolutionary dimension of specialization, revealing (among other things) bidirectionality in transitions between generalist and specialist lineages. Technological advances, including genomic sequencing and analytical techniques at the community level, raise the possibility that the next decade will see research on specialization spanning multiple levels of biological organization in non-model organisms, from genes to populations to networks of interactions in natural communities. Finally, we offer a set of research questions that we find to be particularly pressing and fruitful for future research on ecological specialization.

Synergistic Effects of Three Piper Amides on Generalist and Specialist Herbivores

The tropical rainforest shrub Piper cenocladum, which is normally defended against herbivores by a mutualistic ant, contains three amides that have various defensive functions. While the ants are effective primarily against specialist herbivores, we hypothesized that these secondary compounds would be effective against a wider range of insects, thus providing a broad array of defenses against herbivores. We also tested whether a mixture of amides would be more effective against herbivores than individual amides. Diets spiked with amides were offered to five herbivores: a naïve generalist caterpillar (Spodoptera frugiperda), two caterpillar species that are monophagous on P. cenocladum (Eois spp.), leaf-cutting ants (Atta cephalotes), and an omnivorous ant (Paraponera clavata). Amides had negative effects on all insects, whether they were naïve, experienced, generalized, or specialized feeders. For Spodoptera, amide mixtures caused decreased pupal weights and survivorship and increased development times. Eois pupal weights, larval mass gain, and development times were affected by additions of individual amides, but increased parasitism and lower survivorship were caused only by the amide mixture. Amide mixtures also deterred feeding by the two ant species, and crude plant extracts were strongly deterrent to P. clavata. The mixture of all three amides had the most dramatic deterrent and toxic effects across experiments, with the effects usually surpassing expected additive responses, indicating that these compounds can act synergistically against a wide array of herbivores.

Immunological cost of chemical defence and the evolution of herbivore diet breadth

Selective pressures from host plant chemistry and natural enemies may contribute independently to driving insect herbivores towards narrow diet breadths. We used the specialist caterpillar, Junonia coenia (Nymphalidae), which sequesters defensive compounds, iridoid glycosides, from its host plants to assess the effects of plant chemistry and sequestration on the larval immune response. A series of experiments using implanted glass beads to challenge immune function showed that larvae feeding on diets with high concentrations of iridoid glycosides are more likely to have their immune response compromised than those feeding on diets low in these compounds. These results indicate that larvae feeding on plants with high concentrations of toxins might be more poorly defended against parasitoids, while at the same time being better defended against predators, suggesting that predators and parasitoids can exert different selective pressures on the evolution of herbivore diet breadth.

Relative strengths of top-down and bottom-up forces in a tropical forest community

Abstract We tested integrative bottom-up and top-down trophic cascade hypotheses with manipulative experiments in a tropical wet forest, using the ant-plant Piper cenocladum and its associated arthropod community. We examined enhanced nutrients and light along with predator and herbivore exclusions as sources of variation in the relative biomass of plants, their herbivores (via rates of herbivory), and resident predaceous ants. The combined manipulations of secondary consumers, primary consumers, and plant resources allowed us to examine some of the direct and indirect effects on each trophic level and to determine the relative contributions of bottom-up and top-down cascades to the structure of the community. We found that enhanced plant resources (nutrients and light) had direct positive effects on plant biomass. However, we found no evidence of indirect (cascading through the herbivores) effects of plant biomass on predators or top predators. In contrast, ants had indirect effects on plant biomass by decreasing herbivory on the plants. This top-down cascade occurred whether or not plant resources were enriched, conditions which are expected to modify top-down forces.

Trade-offs in Antiherbivore Defenses in Piper cenocladum: Ant Mutualists Versus Plant Secondary Metabolites

Ant–plant mutualisms may provide indirect evidence for costs of antiherbivore defenses when plants demonstrate trade-offs between allocating resources and energy into ant attractants versus chemical defenses. We tested the hypothesis that ecological trade-offs in defenses are present in Piper cenocladum. This plant possesses two distinct defenses: food bodies that attract predatory ants that destory herbivore eggs and amides that deter herbivores. Previous studies have demonstrated that the food bodies in P. cenocladum are an effective defense because the ants deter herbivory by specialist herbivores. Amides in other Piper species have been shown to have toxic qualities, but we tested the additional hypothesis that these amides have an actual defensive function in P. cenocladum. To test for ecological trade-offs between the two putative defenses, fragments of P. cenocladum were examined for the presence of amides both when the plant was producing food bodies and when it was not producing food bodies. Plants with active ant colonies had redundant defenses, producing food bodies and high levels of amides at the same time, but we detected a trade-off in that they had significantly lower levels of amides than did plants with no ants. To test for the defensive value of P. cenocladum amides, we used an ant bioassay and we examined herbivory results from previous experiments with plants that had variable levels of amides. These tests demonstrated that amides are deterrent to omnivorous ants, leaf cutting ants, and orthopterans. In contrast, the resident Pheidole bicornis ants are effective at deterring herbivory by specialist herbivores that oviposit eggs on the plant but not at deterring herbivory by nonresident omnivores. We concluded that although both amides and food body production appear to be costly, redundancy in defenses is necessary to avoid damage by a complex suit of herbivores.

The insect immune response and other putative defenses as effective predictors of parasitism

Parasitic wasps and flies (parasitoids) exert high mortality on caterpillars, and previous studies have demonstrated that most primary and secondary defenses do not protect caterpillars against parasitoids. We investigated the efficacy of tertiary defenses (i.e., immune responses) against parasitoids. Using a bead injection technique to measure the immune response and a 15-year database to measure parasitism, we compared the immune response for 16 species of caterpillars in nine different families. We found that caterpillar species with a strong immune response had the lowest incidence of parasitism, and when statistically compared to other defensive traits, the immune response was the best predictor of parasitism. Parasitoids either avoid attacking caterpillar species with a capacity for high levels of melanization or are killed once they have parasitized. In either case, the immune response is clearly one of the most effective defenses that caterpillars have against parasitism, and elucidating consistent predictors of variation in encapsulation could improve understanding of parasitism patterns in time and space and could enhance biological control efforts.