Ecological theory predicts that the high local diversity observed in tropical forests is maintained by negative density–dependent interactions within and between closely related plant species. By using long-term data on tree growth and survival for coexisting Inga (Fabaceae, Mimosoideae) congeners, we tested two mechanisms thought to underlie negative density dependence (NDD): competition for resources and attack by herbivores. We quantified the similarity of neighbors in terms of key ecological traits that mediate these interactions, as well as the similarity of herbivore communities. We show that phytochemical similarity and shared herbivore communities are associated with decreased growth and survival at the sapling stage, a key bottleneck in the life cycle of tropical trees. None of the traits associated with resource acquisition affect plant performance, indicating that competition between neighbors may not shape local tree diversity. These results suggest that herbivore pressure is the primary mechanism driving NDD at the sapling stage.
Nicole M. van Dam and Roberto Salguero-Gómez joint last authorship.
Selective pressures imposed by herbivores are often positively correlated with investments that plants make in defense. Research based on the framework of an evolutionary arms race has improved our understanding of why the amount and types of defenses differ between plant species. However, plant species are exposed to different selective pressures during the life of a leaf, such that expanding leaves suffer more damage from herbivores and pathogens than mature leaves. We hypothesize that this differential selective pressure may result in contrasting quantitative and qualitative defense investment in plants exposed to natural selective pressures in the field. To characterize shifts in chemical defenses, we chose six species of Inga, a speciose Neotropical tree genus. Focal species represent diverse chemical, morphological, and developmental defense traits and were collected from a single site in the Amazonian rainforest. Chemical defenses were measured gravimetrically and by characterizing the metabolome of expanding and mature leaves. Quantitative investment in phenolics plus saponins, the major classes of chemical defenses identified in Inga, was greater for expanding than mature leaves (46% and 24% of dry weight, respectively). This supports the theory that, because expanding leaves are under greater selective pressure from herbivores, they rely more upon chemical defense as an antiherbivore strategy than do mature leaves. Qualitatively, mature and expanding leaves were distinct and mature leaves contained more total and unique metabolites. Intraspecific variation was greater for mature leaves than expanding leaves, suggesting that leaf development is canalized. This study provides a snapshot of chemical defense investment in a speciose genus of tropical trees during the short, few‐week period of leaf development. Exploring the metabolome through quantitative and qualitative profiling enables a more comprehensive examination of foliar chemical defense investment.
1. The outstanding diversity of Amazonian forests is predicted to be the result of several processes. While tree lineages have dispersed repeatedly across the Amazon, interactions between plants and insects may be the principal mechanism structuring the communities at local scales.2. Using metabolomic and phylogenetic approaches, we investigated the patterns of historical assembly of plant communities across the Amazon based on the Neotropical genus of trees Inga (Leguminosae) at four, widely separated sites.3. Our results show a low degree of phylogenetic structure and a mixing of chemotypes across the whole Amazon basin, suggesting that although biogeography may play a role, the metacommunity for any local community in the Amazon is the entire basin. Yet, local communities are assembled by ecological processes, with the suite of Inga at a given site more divergent in chemical defences than expected by chance 4. Synthesis. To our knowledge, this is the first study to present metabolomic data for nearly 100 species in a diverse Neotropical plant clade across the whole Amazonia.Our results demonstrate a role for plant-herbivore interactions in shaping the clade's community assembly at a local scale, and suggest that the high alpha diversity in Amazonian tree communities must be due in part to the interactions of diverse tree lineages with their natural enemies providing a high number of niche dimensions.
Coevolutionary theory has long predicted that the arms race between plants and herbivores is a major driver of host selection and diversification. At a local scale, plant defenses contribute significantly to the structure of herbivore assemblages and the high alpha diversity of plants in tropical rain forests. However, the general importance of plant defenses in host associations and divergence at regional scales remains unclear. Here, we examine the role of plant defensive traits and phylogeny in the evolution of host range and species divergence in leaf-feeding sawflies of the family Argidae associated with Neotropical trees in the genus Inga throughout the Amazon, the Guiana Shield and Panama. Our analyses show that the phylogenies of both the sawfly herbivores and their Inga hosts are congruent, and that sawflies radiated at approximately the same time, or more recently than their Inga hosts. Analyses controlling for phylogenetic effects show that the evolution of host use in the sawflies associated with Inga is better correlated with Inga chemistry than with Inga phylogeny, suggesting a pattern of delayed host tracking closely tied to host chemistry. Finally, phylogenetic analyses show that sister species of Inga-sawflies are dispersed across the Neotropics, suggesting a role for allopatric divergence and vicariance in Inga diversification. These results are consistent with the idea that host defensive traits play a key role not only in structuring the herbivore assemblages at a single site, but also in the processes shaping host association and species divergence at a regional scale.
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