- 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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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 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 Many studies identify fungal and oomycete phytopathogens as natural enemies capable of influencing plant species composition and promoting diversity in plant communities. However, little is known about how plant‐pathogen interactions vary along regional abiotic gradients or with tree species characteristics, which limits our understanding of the causes of variation in tree species richness.
We surveyed 10,756 seedlings from 272 tree species for disease symptoms along a mean annual precipitation gradient in the tropical wet forests of Central Panama for 3 months in the early wet season (June–August) and 2 months in the following dry season (March–April). Over 99% of observed disease symptoms were caused by necrotrophic foliar pathogens, while less than 1% of symptoms were attributed to soilborne pathogens. Foliar disease incidence was inversely related to mean annual precipitation, a pattern which may be due to greater disease susceptibility among dry forest species.
Foliar disease incidence increased with conspecific seedling density but did not respond to the proximity of conspecific adults. Although foliar disease incidence decreased as mean annual precipitation increased, the strength of conspecific density‐ or distance‐dependence was independent of the precipitation gradient.
Seedlings of common tree species and species dispersed by non‐flying mammals had a higher risk of foliar pathogen incidence. Increased disease in common species may help reduce their dominance.
Synthesis . The increases in foliar pathogen incidence with conspecific seedling density, species abundance, and dispersal mechanism indicate that foliar disease incidence is non‐random and may contribute to the regulation of tropical plant communities and species coexistence. Furthermore, the relationships between foliar disease incidence, dispersal mechanism and precipitation suggest plant‐pathogen interactions could shift as a response to climate change and disruption of the disperser community. -
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. -
Host plants that promote development of insect herbivores are sometimes less preferred to more toxic plants, which are co‐opted for protection from natural enemies, resulting in higher fitness in communities with strong top‐down control. However, the degree to which variation in growth rate and risk of natural enemy attack drive insect plant preferences is an open question, with little field data available across diverse plant families.
The present study investigated the preference–performance relationship and tritrophic interactions involving the hornworm
Manduca sexta , its natural enemies, and plants in the nightshade family (Solanaceae) using a 2‐year common garden containing 18 wild and domesticated species. The degree to which natural enemy pressure explained field patterns in the laboratory was then tested using targeted assays involving parasitism by the waspCotesia congregata .In the field, the most preferred plants for female oviposition tended to be inversely correlated with the species providing optimal larval growth. Hawkmoths preferred plants in the subgenus
Potatoe ,Nicotiana , andDatura compared withCapsicum ,Physalis , and the otherSolanum subgenera. However, larval parasitism by was only significant for hornworms onC. 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. than , which could be driven by nicotine.Solanum 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.