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
- NSF-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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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. -
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Abstract The enemy release hypothesis (ERH) posits that introduced species often leave their enemies behind when introduced to a new range. This release from enemies may allow introduced species to achieve higher growth and reproduction and may explain why some invaders flourish in new locations. Red mangroves (
Rhizophora mangle ) were introduced to Hawaiʻi from Florida over a century ago. Because Hawaiʻi has no native mangroves, the arrival ofR. mangle fundamentally changed the structure and function of estuarine shorelines. While numerous enemies affect red mangroves in their native range (tropical America), in Hawaiʻi, mangroves apparently experience little herbivory, which may explain why introduced mangroves are so productive, fecund, and continue to spread. In this study, we compared the effects of enemies in native and introduced populations of brackish red mangroves (R. mangle ) in 8–10 sites in the native range (Florida, Belize, and Panama) and introduced range of mangroves (Hawaiʻi). At each site, we measured the (1) occurrence of enemies using timed visual surveys, (2) occurrence of damage to different mangrove structures (leaves, apical buds, dead twigs, roots, propagules, and seedlings), and (3) rate of propagule herbivory using tethering experiments. Consistent with the ERH, we found an order of magnitude less damage and fewer enemies in introduced than native mangrove sites. While introduced mangroves harbored few enemies and minimal damage, native mangroves were affected by numerous enemies, including leaf‐eating crabs, specialist bud moths, wood‐boring insects and isopods, and propagule predators. These patterns were consistent across all plant structures (roots to leaves), among marine and terrestrial enemies, and across functional groups (browsers, borers, pathogens, etc.), which demonstrates enemy escape occurs consistently among different functional groups and via trophic (e.g., herbivores) and non‐trophic (e.g., root borers) interactions. Our study is among the first biogeographical enemy release studies to take a comprehensive approach to quantifying the occurrence of damage from a broad suite of marine and terrestrial taxa across an array of wetland plant structures. Understanding how natural enemies alter this key foundation species will become increasingly relevant globally as mangroves continue to invade new regions through intentional plantings or range expansion driven by climate change. -
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The present study investigated the preference–performance relationship and tritrophic interactions involving the hornworm
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Potatoe ,Nicotiana , andDatura compared withCapsicum ,Physalis , and the otherSolanum subgenera. However, larval parasitism byC. congregata Potatoe /Datura and notNicotiana (i.e. 33% vs. 12% vs. 4% parasitism onPotatoe ,Datura , andNicotiana , respectively). Experimental laboratory rearing confirmed that wasp survival is lower onNicotiana sp. thanSolanum lycopersicum The data obtained in the present study show that the negative preference‐performance relationship in hornworms across solanaceous plants is maintained in part because by utilising noxious food plants
M. sexta gains protection against parasitism. -
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We examined how host species identity, relatedness and seed viability influence the composition of fungal communities associated with seeds of four co‐occurring pioneer trees (
Cecropia insignis ,C. longipes ,C. peltata andJacaranda copaia ). Seeds were buried in mesh bags in five common gardens in the understorey of a lowland tropical forest in Panama and retrieved at intervals from 1 to 30 months. A subset of the seeds in each bag was used to determine germination success. One half of each remaining seed was tested for viability; and the other half was used to culture and identify seed‐infecting fungi.Seeds were infected by fungi after burial. Although fungal communities differed in viable versus dead seeds, and across burial locations, community composition primarily varied as a function of plant species identity (30.7% of variation in community composition vs. 4.5% for viability and location together), even for congeneric
Cecropia species. Phylogenetic reconstruction showed that relatedness of fungi mostly reflected differences betweenJacaranda (Bignoniaceae) andCecropia (Urticaceae).Although the proportion of germinable seeds decreased gradually over time for all species, intraspecific variation in survival was high at the same location (e.g. ranging from 0% to 100% for
C. peltata ) suggesting variable exposure or susceptibility to seed pathogens.Synthesis . Our study provides evidence under field conditions that congeneric tree species with similar life history traits differ markedly in seed‐associated fungal communities when exposed to the same soil‐borne fungi. This is a critical first step supporting pathogen‐mediated coexistence of closely related tree species.
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.3417/2020591
