- 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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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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Abstract The enemy release hypothesis (ERH) attributes the success of some exotic plant species to reduced top‐down effects of natural enemies in the non‐native range relative to the native range. Many studies have tested this idea, but very few have considered the simultaneous effects of multiple kinds of enemies on more than one invasive species in both the native and non‐native ranges. Here, we examined the effects of two important groups of natural enemies–insect herbivores and soil biota–on the performance of
Tanacetum vulgare (native to Europe but invasive in the USA) andSolidago canadensis (native to the USA but invasive in Europe) in their native and non‐native ranges, and in the presence and absence of competition.In the field, we replicated full‐factorial experiments that crossed insecticide,
T. vulgare–S. canadensis competition, and biogeographic range (Europe vs. USA) treatments. In greenhouses, we replicated full‐factorial experiments that crossed soil sterilization, plant–soil feedback, and biogeographic range treatments. We evaluated the effects of experimental treatments onT. vulgare andS. canadensis biomass.The effects of natural enemies were idiosyncratic. In the non‐native range and relative to populations in the native range,
T. vulgare escaped the negative effects of insect herbivores but not soil biota, depending upon the presence ofS. canadensis ; andS. canadensis escaped the negative effects of soil biota but not insect herbivores, regardless of competition. Thus, biogeographic escape from natural enemies depended upon the enemies, the invader, and competition.Synthesis: By explicitly testing the ERH in terms of more than one kind of enemy, more than one invader, and more than one continent, this study enhances our nuanced perspective of how natural enemies can influence the performance of invasive species in their native and non‐native ranges. -
Abstract Natural pest control is an alternative to pesticide use in agriculture, and may help to curb insect declines and promote crop production. Nonconsumptive interactions in natural pest control that historically have received far less attention than consumptive interactions, may have distinct impacts on pest damage suppression and may also mediate positive multipredator interactions. Additionally, when nonconsumptive effects are driven by natural enemy aggression, variation in alternative resources for enemies may impact the strength of pest control. Here we study control of the coffee berry borer (CBB),
Hypothenemus hampei , by a keystone arboreal ant species,Azteca sericeasur , which exhibits a nonconsumptive effect on CBB by throwing them off coffee plants. We conducted two experiments to investigate: (1) if the strength of this behavior is driven by spatial or temporal variability in scale insect density (an alternative resource thatAzteca tends for honeydew), (2) if this behavior mediates positive interactions betweenAzteca and other ground‐foraging ants, and (3) the effect this behavior has on the overall suppression of CBB damage in multipredator scenarios. Our behavioral experiment showed that nearly all interactions betweenAzteca and CBB are nonconsumptive and that this behavior occurs more frequently in the dry season and with higher densities of scale insects on coffee branches. Our multipredator experiment revealed that borers thrown off coffee plants byAzteca can survive and potentially damage other nearby plants but may be suppressed by ground‐foraging ants. Although we found no non‐additive effects betweenAzteca and ground‐foraging ants on overall CBB damage, together, both species resulted in the lowest level of plant damage with the subsequent reduction in “spillover” damage caused by thrown CBB, indicating spatial complementarity between predators. These results present a unique case of natural pest control, in which damage suppression is driven almost exclusively by nonconsumptive natural enemy aggression, as opposed to consumption or prey behavioral changes. Furthermore, our results demonstrate the variability that may occur in nonconsumptive pest control interactions when natural enemy aggressive behavior is impacted by alternative resources, and also show how these nonconsumptive effects can mediate positive interactions between natural enemies to enhance overall crop damage reduction. -
Abstract Species richness in tropical forests is correlated with other dimensions of diversity, including the diversity of plant–herbivore interactions and the phytochemical diversity that influences those interactions. Understanding the complexity of plant chemistry and the importance of phytochemical diversity for plant–insect interactions and overall forest richness has been enhanced significantly by the application of metabolomics to natural systems. The present work used proton nuclear magnetic resonance spectroscopy (1H‐NMR) profiling of crude leaf extracts to study phytochemical similarity and diversity among
Piper plants growing naturally in the Atlantic Rainforest of Brazil. Spectral profile similarity and chemical diversity were quantified to examine the relationship between metrics of phytochemical diversity, specialist and generalist herbivory, and understory plant richness. Herbivory increased with understory species richness, while generalist herbivory increased and specialist herbivory decreased with the diversity ofPiper leaf material available. Specialist herbivory increased when conspecific host plants were more spectroscopically dissimilar. Spectral similarity was lower among individuals of common species, and they were also more spectrally diverse, indicating phytochemical diversity is beneficial to plants. Canopy openness and soil nutrients also influenced chemistry and herbivory. The complex relationships uncovered in this study add information to our growing understanding of the importance of phytochemical diversity for plant–insect interactions and tropical plant species richness.