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.

A tale of scale: Plot but not neighbourhood tree diversity increases leaf litter ant diversity

“…Considering that ant diversity correlates with the diversity of many taxa (Agosti et al, ) and that the brown food web is tightly connected to the green food web (Zou, Thebault, Lacroix, & Barot, ), similar recoveries for other organisms are likely. The positive association between plot tree diversity and litter ant diversity indicates that diverse tree mixtures increase ant abundance and diversity, which may have far‐reaching consequences, for example by enhancing ant‐mediated ecosystem functions including nutrient cycling (Folgarait, ; Griffiths et al, ) and by stabilizing trophic interactions (Schuldt et al, ; Staab et al, ). As trees are actively planted in reforestation and plantation forestry (as in BEF experiments), our results suggest that diversifying tree mixtures in young forests can promote species diversity and positive diversity effects across trophic levels without reducing carbon stocks (Liu et al, ) or lowering potential future harvest (Huang, Chen, et al, ).…”

“…If competitive species benefit from high‐quality habitats, then high neighbourhood‐scale tree diversity may decrease PD. To examine this thought, we correlated the presence of T. wroughtonii (9% of all specimens), the most dominant species whose influence on trophic and non‐trophic interactions of other species is largest when local tree diversity is high (Schuldt, Fornoff, Bruelheide, Klein, & Staab, ) with ant abundance, richness, FD and PD. As expected, the presence of T. wroughtonii reduced PD (Figure S2), indicating competitive exclusion of phylogenetically distinct species.…”

“…The positive association between plot tree diversity and litter ant diversity indicates that diverse tree mixtures increase ant abundance and diversity, which may have far-reaching consequences, for example by enhancing ant-mediated ecosystem functions including nutrient cycling (Folgarait, 1998;Griffiths et al, 2018) and by stabilizing trophic interactions (Schuldt et al, 2017;Staab et al, 2015). As trees are actively planted in reforestation and plantation forestry (as in BEF experiments), our results suggest that diversifying tree mixtures in young forests can promote species diversity and positive diversity effects across trophic levels without reducing carbon stocks to see whether the effects revealed by our study remain in more mature forest stands.…”

Tree diversity increases robustness of multi-trophic interactions

“…Therefore, the functional relationship of both mutualistic partners may be stabilized under high tree diversity, and, in the future, experimental manipulations of higher trophic levels will help to validate causality. Besides protecting mutualistic Hemiptera, ants could reduce chewing herbivore occurrence and indirectly benefit plant primary production and growth in more diverse environments [57,58].…”

Landscape-level bird loss increases the prevalence of honeydew-producing insects and non-native ants

“…Negative impacts on native vegetation due to non-native ant–HPI associations have been documented from numerous island systems, including the Seychelles (Hill et al 2003), Christmas Island (O’Dowd et al 2003), and Mauritius (Hansen and Müller 2009). In addition to direct damage through their feeding, HPIs can potentially increase damage by chewing herbivores (Schuldt et al 2017) and act as vectors for numerous plant diseases (Weintraub and Beanland 2006), and their attending ants can disrupt pollination (Lach 2007; Hansen and Müller 2009) and seed dispersal (Davis et al 2010; Hansen and Müller 2009). Finally, because nearly all of the ants and HPIs on Guam are recent introductions, limestone forest trees may lack traits that protect against the negative impacts of these ant–HPI associations (e.g., Junker et al 2011).…”