Keystone mutualism strengthens top–down effects by recruiting large-bodied ants

Abstract

Determining the impacts of mutualistic interactions and predator diversity on food webs are two important goals in community ecology. In this study, we examined how predator community variation mediates the strength of top-down effects in the presence and absence of mutualistic interactions. We examined the impacts of predatory ant species that simultaneously prey on leaf-chewing herbivores (Lepidoptera) and engage in food-for-protection mutualisms with sap-feeding herbivores (Hemiptera) in the lower canopy of Connecticut forests. In this 2-year study, we examined three hypothetical mechanisms by which mutualisms can alter the top-down effects of ants: (1) sap feeders increase ant abundance, thus strengthening predatory effects; (2) sap feeders increase the relative abundance of a species that has stronger predatory effects; and (3) changes to predator diversity (species richness) are caused by sap feeders mediating top-down effects of the ant community. Experiments revealed that host plants occupied by sap feeders favored large-bodied ant species in the genus Camponotus, but there were no changes to community-wide ant abundance or ant species richness. Fitting predictions of predation strength based on the functional trait of body size, large-bodied Camponotus suppressed caterpillars and reduced leaf herbivory. This work shows that the ant-hemipteran mutualism, which has been characterized as a keystone interaction, can generate strong top-down effects on leaf-chewing herbivores and herbivory via increasing the relative abundance of species with functional traits relevant to predation, such as body size. Therefore, the emergence of specific ants as keystone predators in a community can be contingent upon their mutualism with sap-feeding Hemiptera.

Keystone mutualism influences forest tree growth at a landscape scale

“…Nevertheless, focused experimental work on hickory trees showed how the ant/sap‐feeder mutualism generated cascading effects in this community. The presence of sap‐feeders specifically increased the local abundance of large‐bodied Camponotus ants, which are more behaviourally aggressive predators than other predaceous ants in the same habitat (Clark & Singer ), and suppressed a relatively large size range of caterpillars, thus sparing hickory branches from severe defoliation (Clark & Singer ).…”

“…We studied the growth of hickory trees in the Eucarya group ( Carya glabra , C. ovata and C. tomentosa ) in central Connecticut, USA, where they host several species of sap‐feeding herbivores tended by ants (Clark et al ; Clark & Singer ). Sap‐feeder herbivores on Carya include an assemblage of Membracidae and Coccidae (Hemiptera), with a hickory specialist, Carynota mera (Membracidae), dominating in this system and Eulecanium caryae (Coccidae) occurring in relatively small aggregations of one to three individuals (Clark & Singer , personal observations). Several ant species in the genera Camponotus and Formica are the most common participants in this interaction in this region, and large Camponotus spp.…”

“…To assess effects of ant‐exclusion and other environmental variables on herbivores, we censused caterpillars and sap‐feeders on the manipulated and control trees. Based on timing of peak caterpillar abundance and ant/sap‐feeder interactions in past work (Clark et al ; Clark & Singer ), we quantified the abundance of sap‐feeders (phloem‐feeding hemipterans) on entire host trees by carefully searching shoots where treehoppers (Membracidae) and scale insects (Coccidae) fed in May of 2014, 2015 and 2016 (species reported in Clark & Singer ). Thirty‐nine % of trees sampled were occupied by ant‐tended, phloem‐feeding Hemipteran species.…”

Generalising indirect defence and resistance of plants

“…For instance, in diverse systems, EFNs, domatia and honeydew‐producing herbivores all increase the abundance of ant species on plants (Janzen 1966; Kaplan & Eubanks 2005; Mooney & Agrawal 2008; but see Heil et al 2005 as an example of EFN‐ant specificity), often at the expense of other predatory arthropods that are also preyed upon by ants (Eubanks 2001; Styrsky & Eubanks 2007). In some cases, interactions disproportionately promote the abundance of the most effective predators, such as large‐bodied ants in ant–aphid–plant interactions (Clark & Singer 2018). In other cases, it is less clear whether the most effective predators are those most favoured by an indirect defence trait.…”

Ant-mealybug mutualism modulates the performance of co-occurring herbivores

“…Early work has exposed the positive and reciprocal effects of mutualism on the colonization and development of both species involved in the mutual interaction 8,9 . Currently, some studies have illuminated the ecological influence of ant-hemipteran mutualism on other co-occurring community members 6,10,11 . Ant diversity and aggressiveness can directly modulate the effects of the mutualism on the surrounding community 12 , affecting the ambient feed groups composed by predators and other arthropod specie 6 , in which of the abundance of arthropod species significantly decrease on trees with ant-hemipteran mutualism 13 .…”