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Tree species richness attenuates the positive relationship between mutualistic ant-hemipteran interactions and leaf chewer herbivory.

ABSTRACT: Interactions across trophic levels influence plant diversity effects on ecosystem functions, but the complexity of these interactions remains poorly explored. For example, the interplay between different interactions (e.g. mutualism, predation) might be an important moderator of biodiversity-ecosystem function relationships. We tested for relationships between trophobioses (facultative ant-hemipteran mutualism) and leaf chewer herbivory in a subtropical forest biodiversity experiment. We analysed trophobiosis and herbivory data of more than 10 000 trees along a tree species richness gradient. Against expectations, chewing damage was higher on trees with trophobioses. However, the net positive relationship between trophobioses and overall herbivory depended on tree species richness, being most pronounced at low richness. Our results point to indirect, positive effects of ant-tended sap suckers on leaf chewers, potentially by altering plant defences. Direct antagonistic relationships of trophobiotic ants and leaf-chewing herbivores-frequently reported to drive community-wide effects of trophobioses in other ecosystems-seemed less relevant. However, antagonistic interactions likely contributed to the attenuating effect of tree species richness, because trophobiotic ant and herbivore communities changed from monocultures to species-rich mixtures. Our findings, therefore, suggest that biodiversity loss might lead to complex changes in higher trophic level effects on ecosystem functions, mediated by both trophic and non-trophic interactions.

SUBMITTER: Schuldt A

PROVIDER: S-EPMC5597841 | biostudies-literature | 2017 Sep

REPOSITORIES: biostudies-literature

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Tree species richness attenuates the positive relationship between mutualistic ant-hemipteran interactions and leaf chewer herbivory.

Schuldt Andreas A Fornoff Felix F Bruelheide Helge H Klein Alexandra-Maria AM Staab Michael M

Proceedings. Biological sciences 20170901 1862

Interactions across trophic levels influence plant diversity effects on ecosystem functions, but the complexity of these interactions remains poorly explored. For example, the interplay between different interactions (e.g. mutualism, predation) might be an important moderator of biodiversity-ecosystem function relationships. We tested for relationships between trophobioses (facultative ant-hemipteran mutualism) and leaf chewer herbivory in a subtropical forest biodiversity experiment. We analyse ...[more]

PMID: 28878067

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Project description:Despite the importance of herbivory for the structure and functioning of species-rich forests, little is known about how herbivory is affected by tree species richness, and more specifically by random vs. non-random species loss. We assessed herbivore damage and its effects on tree growth in the early stage of a large-scale forest biodiversity experiment in subtropical China that features random and non-random extinction scenarios of tree mixtures numbering between one and 24 species. In contrast to random species loss, the non-random extinction scenarios were based on the tree species' local rarity and specific leaf area - traits that may strongly influence the way herbivory is affected by plant species richness. Herbivory increased with tree species richness across all scenarios and was unaffected by the different species compositions in the random and non-random extinction scenarios. Whereas tree growth rates were positively related to herbivory on plots with smaller trees, growth rates significantly declined with increasing herbivory on plots with larger trees. Our results suggest that the effects of herbivory on growth rates increase from monocultures to the most species-rich plant communities and that negative effects with increasing tree species richness become more pronounced with time as trees grow larger. Synthesis. Our results indicate that key trophic interactions can be quick to become established in forest plantations (i.e. already 2.5 years after tree planting). Stronger herbivory effects on tree growth with increasing tree species richness suggest a potentially important role of herbivory in regulating ecosystem functions and the structural development of species-rich forests from the very start of secondary forest succession. The lack of significant differences between the extinction scenarios, however, contrasts with findings from natural forests of higher successional age, where rarity had negative effects on herbivory. This indicates that the effects of non-random species loss could change with forest succession.

Project description:The diversity of plant neighbors commonly results in direct, bottom-up effects on herbivore ability to locate their host, and in indirect effects on herbivores involving changes in plant traits and a top-down control by their enemies. Yet, the relative contribution of bottom-up and top-down forces remains poorly understood. We also lack knowledge on the effect of abiotic constraints such as summer drought on the strength and direction of these effects. We measured leaf damage on pedunculate oak (Quercus robur), alone or associated with birch, pine or both in a long-term tree diversity experiment (ORPHEE), where half of the plots were irrigated while the other half remained without irrigation and received only rainfall. We tested three mechanisms likely to explain the effects of oak neighbors on herbivory: (1) Direct bottom-up effects of heterospecific neighbors on oak accessibility to herbivores, (2) indirect bottom-up effects of neighbors on the expression of leaf traits, and (3) top-down control of herbivores by predators. Insect herbivory increased during the growth season but was independent of neighbor identity and irrigation. Specific leaf area, leaf toughness, and thickness varied with neighbor identity while leaf dry matter content or C:N ratio did not. When summarized in a principal component analysis (PCA), neighbor identity explained 87% of variability in leaf traits. PCA axes partially predicted herbivory. Despite greater rates of attack on dummy caterpillars in irrigated plots, avian predation, and insect herbivory remained unrelated. Our study suggests that neighbor identity can indirectly influence insect herbivory in mixed forests by modifying leaf traits. However, we found only partial evidence for these trait-mediated effects and suggest that more attention should be paid to some unmeasured plant traits such as secondary metabolites, including volatile organic compounds, to better anticipate the effects of climate change on plant-insect interactions in the future.

Dataset Information

Tree species richness attenuates the positive relationship between mutualistic ant-hemipteran interactions and leaf chewer herbivory.

Publications

Tree species richness attenuates the positive relationship between mutualistic ant-hemipteran interactions and leaf chewer herbivory.

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