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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.
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The impact of habitat fragmentation on domatia-dwelling mites and a mite-plant-fungus tritrophic interaction
Abstract Context Habitat fragmentation is a leading threat to biodiversity, yet the impacts of fragmentation on most taxa, let alone interactions among those taxa, remain largely unknown. Objectives We studied how three consequences of fragmentation—reduced patch connectivity, altered patch shape, and edge proximity—impact plant-dwelling mite communities and mite-plant-fungus interactions within a large-scale habitat fragmentation experiment. Methods We sampled mite communities from the leaves of Quercus nigra (a plant species that has foliar domatia which harbor fungivorous and predacious mites) near and far from edge within fragments of varying edge-to-area ratio (shape) and connectivity via corridors. We also performed a mite-exclusion experiment across these fragmentation treatments to test the effects of mite presence and fungal hyphal abundance on leaf surfaces. Results Habitat edges influenced the abundance and richness of leaf-dwelling mites; plants closer to the edge had higher mite abundance and species richness. Likewise, hyphal counts were higher on leaves near patch edges. Despite both mite and fungal abundance being higher at patch edges, leaf hyphal counts were not impacted by mite abundance on those leaves. Neither patch shape nor connectivity influenced mite abundance, mite species richness, or the influence of mites on leaf surface fungal abundance. Conclusion Our results suggest that mites and foliar fungi may be independently affected by edge-structured environmental gradients, like temperature, rather than trophic effects. We demonstrate that large-scale habitat fragmentation and particularly edge effects can have impacts on multiple levels of microscopic communities, even in the absence of cascading trophic effects.
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- PAR ID:
- 10418292
- Date Published:
- Journal Name:
- Landscape Ecology
- Volume:
- 37
- Issue:
- 12
- ISSN:
- 0921-2973
- Page Range / eLocation ID:
- 3029 to 3041
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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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 unravelled 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
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ABSTRACT Many plants engage in indirect defense via tri‐trophic interactions whereby plants provide resources such as food or shelter to mutualists in exchange for protection against herbivores and pathogens, increasing plant fitness. As temperature regimes shift under climate change, understanding the influence of temperature on tri‐trophic defensive interactions is increasingly important. However, where plant species host multiple tri‐trophic defensive interactions, we still lack an understanding of if each interaction, even within the same system, responds in the same way to temperature. In this study, we monitored black cherry (Prunus serotina)seedlings for 10 weeks under ambient and increased temperatures to explore the effects of temperature on two different tri‐trophic defensive interactions between black cherry and: (1) mutualistic leaf domatia‐dwelling mites and leaf fungi; and (2) arthropod predators and herbivores. We found that the positive association between mite abundance and domatia size increased by 8.7% on warmed plants, while warming weakened the positive relationship between mite abundance and the abundance of foliar fungi by 14%, though warmer conditions alone did not affect the abundances of any of these groups. Further, warming increased the abundance of arthropod predators by 116% and decreased the amount of herbivory plants experienced by 42%, but did not modify the impact predators had on herbivory. Ultimately, the differences among interacting species with warming did not translate to differences in plant growth, indicating black cherry can be robust to at least some of the variation in species interactions caused by changing temperatures in the short term. These findings illustrate that warming can modify the abundance of, and relationships between, some but not all tri‐trophic defensive interactions in a given system, further confirming that temperature does not impact plant interactions uniformly.more » « less
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- Free Publicly Accessible Full Text
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1007/s10980-022-01529-2
