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Introduction Plants and their insect herbivores represent a large fraction of the species in Amazonian forests and are often directly implicated in the origin and maintenance of biodiversity at local and regional scales. How these interactions may change over geographic distance is unknown because very few studies have investigated the herbivore fauna and defense chemicals of any host plant species at multiple sites in tropical forests. One hypothesis, the Geographic Mosaic Theory of Coevolution, predicts that if herbivore assemblages turn over in different parts of a plant’s range, then plant defense chemicals should also change, reflecting local selection pressures. Methods We tested this theory by studying 12 species of Protium (Burseraceae) trees that occur in both Iquitos, Peru, and Manaus, Brazil, in rainforests separated by 1500 km. We surveyed all insects observed directly feeding on the plants in both locations for 48 weeks in Manaus and 64 weeks in Iquitos. We analyzed the secondary metabolites in the leaves of all species in both locations using GC/MS and HPLC. Results and Discussion Although in both locations we found that Protium herbivores were dominated by insects from the orders Hemiptera, Coleoptera and Lepidoptera, we found almost complete turnover in the herbivore species composition in the two sites, and each host plant species had a different assemblage of herbivores in each location. Comparing the phylogenetic beta-diversity, we found low similarity in herbivore phylogenetic relatedness between host plant species in the two locations. However, the secondary metabolites found within a Protium species were similar across the two locations. We found no strong evidence that individuals from a host plant species in Iquitos or Manaus expressed locally-adapted defense chemicals, as individuals from geographic locations did not form clusters when looking at patterns of chemical similarity. These results are not consistent with the Geographic Mosaic Theory of Coevolution. The most intriguing pattern we found was a strong correlation between the diversity of herbivores per host plant species in both locations. We also found that plants with high chemical richness had lower numbers of herbivore species and numbers of total herbivores in both locations. We conclude that high chemical diversity is the most effective strategy for Protium trees to reduce insect herbivore attacks. We speculate that each secondary metabolite is effective at repelling only a few insect herbivores, and that different chemicals are likely effective in different parts of a plants’ geographic range. Future studies should investigate additional locations and additional natural enemies (i.e., fungal pathogens) to test the hypothesis that chemical diversity reduces attack from natural enemies and may explain the ecological and evolutionary success of rainforest trees over time and space.
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Natural Enemies and the Maintenance of Tropical Tree Diversity: Recent Insights and Implications for the Future of Biodiversity in a Changing World
Over the past five decades, many studies have examined the Janzen-Connell hypothesis, which posits that host-specific natural enemies, such as insect herbivores and fungal pathogens, promote plant species coexistence by providing a recruitment advantage to rare plant species. Recently, researchers have been exploring new and exciting angles on plant-enemy interactions that have yielded novel insights into this long-standing hypothesis. Here, we highlight some empirical advances in our understanding of plant-enemy interactions in tropical forests, including improved understanding of variation in plant species’ susceptibility to enemy effects, as well as insect and pathogen host ranges. We then review recent advances in related ecological theory. These theoretical studies have confirmed that specialist natural enemies can promote tree diversity. However, they have also shown that the impact of natural enemies may be weakened, or that natural enemies could even cause species exclusion, depending on enemy host range, the spatial extent of enemy effects, and variation among plant species in seed dispersal or enemy susceptibility. Finally, we end by discussing how human impacts on tropical forests, such as fragmentation, hunting, and climate change, may alter the plant-enemy interactions that contribute to tropical forest diversity.
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- Award ID(s):
- 1845403
- PAR ID:
- 10213120
- Date Published:
- Journal Name:
- Annals of the Missouri Botanical Garden
- Volume:
- 105
- Issue:
- 3
- ISSN:
- 0026-6493
- Page Range / eLocation ID:
- 377 to 392
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Endara, María José (Ed.)Introduction: Plants and their insect herbivores represent a large fraction of the species in Amazonian forests and are often directly implicated in the origin and maintenance of biodiversity at local and regional scales. How these interactions may change over geographic distance is unknown because very few studies have investigated the herbivore fauna and defense chemicals of any host plant species at multiple sites in tropical forests. One hypothesis, the Geographic Mosaic Theory of Coevolution, predicts that if herbivore assemblages turn over in different parts of a plant’s range, then plant defense chemicals should also change, reflecting local selection pressures. Methods: We tested this theory by studying 12 species of Protium (Burseraceae) trees that occur in both Iquitos, Peru, and Manaus, Brazil, in rainforests separated by 1500 km. We surveyed all insects observed directly feeding on the plants in both locations for 48 weeks in Manaus and 64 weeks in Iquitos. We analyzed the secondary metabolites in the leaves of all species in both locations using GC/MS and HPLC. Results and Discussion: Although in both locations we found that Protium herbivores were dominated by insects from the orders Hemiptera, Coleoptera and Lepidoptera, we found almost complete turnover in the herbivore species composition in the two sites, and each host plant species had a different assemblage of herbivores in each location. Comparing the phylogenetic beta-diversity, we found low similarity in herbivore phylogenetic relatedness between host plant species in the two locations. However, the secondary metabolites found within a Protium species were similar across the two locations. We found no strong evidence that individuals from a host plant species in Iquitos or Manaus expressed locally-adapted defense chemicals, as individuals from geographic locations did not form clusters when looking at patterns of chemical similarity. These results are not consistent with the Geographic Mosaic Theory of Coevolution. The most intriguing pattern we found was a strong correlation between the diversity of herbivores per host plant species in both locations. We also found that plants with high chemical richness had lower numbers of herbivore species and numbers of total herbivores in both locations. We conclude that high chemical diversity is the most effective strategy for Protium trees to reduce insect herbivore attacks. We speculate that each secondary metabolite is effective at repelling only a few insect herbivores, and that different chemicals are likely effective in different parts of a plants’ geographic range. Future studies should investigate additional locations and additional natural enemies (i.e., fungal pathogens) to test the hypothesis that chemical diversity reduces attack from natural enemies and may explain the ecological and evolutionary success of rainforest trees over time and space.more » « less
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The evolution of diverse and novel morphological traits is poorly understood, especially how symbiotic interactions can drive these adaptations. The extreme diversity of external traits in insect-induced galls is currently explained by the Enemy Hypothesis, in which these traits have selective advantage in deterring parasitism. While previous tests of this hypothesis used only taxonomic identity, we argue that ecologically functional traits of enemies (i.e. mode of parasitism, larval development strategy) are a crucial addition. Here, we characterize parasitoid guild composition across four disparate gall systems and find consistent patterns of association between enemy guild and gall morphology. Specifically, galls with a longer average larva-to-surface distance host a significantly higher proportion of enemies with a distinct combination of functional traits (i.e. ectoparasitic, idiobiont, elongate ovipositor). Our results support the Enemy Hypothesis and highlight the importance of species ecology in examining insect communities and the evolution of novel defensive characters.more » « less
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Pre-dispersal seed mortality caused by premature fruit drop is a potentially important source of plant mortality, but one which has rarely been studied in the context of tropical forest plants. Of particular interest is premature fruit drop triggered by enemies, which – if density-dependent – could contribute to species co-existence in tropical forest plant communities. We used a long-term (31 year) dataset on seed and fruit fall obtained through weekly collections from a network of seed traps in a lowland tropical forest (Barro Colorado Island, Panama) to estimate the proportion of seeds prematurely abscised for 201 woody plant species. To determine whether enemy attack might contribute to premature fruit drop we tested whether plant species abscise more of their fruit prematurely if they: (1) have attributes hypothesised to be associated with high levels of enemy attack, and (2) are known to be attacked by one enemy-group (insect seed predators). We also tested (3) whether mean rates of premature fruit drop for plant species are phylogenetically conserved. Overall rates of premature fruit drop were high in the plant community. Across all species, 39% of seeds were abscised before completing their development. Rates of premature seed abscission varied considerably among species and could not be explained by phylogeny. Premature seed abscission rates were higher in species which are known to host pre-dispersal insect seed predators and species with attributes that were hypothesised to make them more susceptible to attack by pre-dispersal enemies, namely species which (1) have larger seeds, (2) have a greater average height, (3) have temporally predictable fruiting patterns, and (4) are more abundant at the study site. Synthesis. Premature fruit drop is likely to be a major source of seed mortality for many plant species on Barro Colorado Island. It is plausible that pre-dispersal seed enemies, such as insect seed predators, contribute to community-level patterns of premature fruit drop and have the potential to mediate species co-existence through stabilising negative density dependence. Our study suggests that the role of pre-dispersal enemies in structuring tropical plant communities should be considered alongside the more commonly studied post-dispersal seed and seedling enemies.more » « less
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The tree diversity-productivity relationship is key to effective forest restoration and management; however, it remains unclear what role foliar chemical diversity and interactions between trees and their enemies play in driving this relationship. Trees produce chemical metabolites in their leaves that impact herbivory and pathogen infection. If trees alter the diversity of metabolites they produce when grown in more diverse communities, this could impact interactions with herbivores and pathogens. Ultimately, these tropic interactions with plant enemies, mediated by chemical diversity, could be important drivers of diversity-productivity relationships. Using a large-scale tree diversity experiment, we used a focal tree sampling design from 14 species across a gradient of tree species richness to assess the role of foliar chemicals and trophic interactions in the diversity-productivity relationship. We used untargeted metabolomics to measure foliar phytochemical diversity, monitored tree-enemy interactions, including foliar fungal pathogens, caterpillar communities, and deer browsing, and modelled their relationship to tree growth using path analysis. We unraveled significant evidence for top-down mediation of the diversity-productivity relationship driven primarily by herbivores rather than foliar pathogens, and contrasting effects of foliar chemical diversity on different enemy types. Individual trees growing in more diverse communities had higher phytochemical diversity and higher caterpillar richness, but lower leaf fungal pathogen richness. Leaf phytochemical diversity was positively associated with caterpillar richness and fungal pathogen richness, but negatively associated with browsing by white-tailed deer (Odocoileus virginianus). Path analysis revealed that phytochemical diversity, caterpillar richness, insect damage, and deer damage – but not foliar pathogens – all mediated positive indirect effects of tree richness on tree growth rate. Synthesis: We highlight the significant mediation of diversity-productivity relationships via contrasting effects of phytochemical diversity on plant-enemy interactions. Ultimately, our study underscores the importance of incorporating trophic interactions into biodiversity-ecosystem function studies.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.3417/2020591
