Predatory birds and ants partition caterpillar prey by body size and diet breadth.

The effects of predator assemblages on herbivores are predicted to depend critically on predator-predator interactions and the extent to which predators partition prey resources. The role of prey heterogeneity in generating such multiple predator effects has received limited attention. Vertebrate and arthropod insectivores constitute two co-dominant predatory taxa in many ecosystems, and the emergent properties of their joint effects on insect herbivores inform theory on multiple predator effects as well as biological control of insect herbivores. Here we use a large-scale factorial manipulation to assess the extent to which birds and ants engage in antagonistic predator-predator interactions and the consequences of heterogeneity in herbivore body size and diet breadth (i.e. the diversity of host plants used) for prey partitioning. We excluded birds and reduced ant density (by 60%) in the canopies of eight northeastern USA deciduous tree species during two consecutive years and measured the community composition and traits of lepidopteran larvae (caterpillars). Birds did not affect ant density, implying limited intraguild predation between these taxa in this system. Birds preyed selectively upon large-bodied caterpillars (reducing mean caterpillar length by 12%) and ants preyed selectively upon small-bodied caterpillars (increasing mean caterpillar length by 6%). Birds and ants also partitioned caterpillar prey by diet breadth. Birds reduced the frequency dietary generalist caterpillars by 24%, while ants had no effect. In contrast, ants reduced the frequency of dietary specialists by 20%, while birds had no effect, but these effects were non-additive; under bird exclusion, ants had no detectable effect, while in the presence of birds, they reduced the frequency of specialists by 40%. As a likely result of prey partitioning by body size and diet breadth, the combined effects of birds and ants on total caterpillar density were additive, with birds and ants reducing caterpillar density by 44% and 20% respectively. These results show evidence for the role of prey heterogeneity in driving functional complementarity among predators and enhanced top-down control. Heterogeneity in herbivore body size and diet breadth, as well as other prey traits, may represent key predictors of the strength of top-down control from predator communities.

Singer MS ，Clark RE ，Lichter-Marck IH ，Johnson ER ，Mooney KA ... -  《-》

Ant-caterpillar antagonism at the community level: interhabitat variation of tritrophic interactions in a neotropical savanna.

Ant foraging on foliage can substantially affect how phytophagous insects use host plants and represents a high predation risk for caterpillars, which are important folivores. Ant-plant-herbivore interactions are especially pervasive in cerrado savanna due to continuous ant visitation to liquid food sources on foliage (extrafloral nectaries, insect honeydew). While searching for liquid rewards on plants, aggressive ants frequently attack or kill insect herbivores, decreasing their numbers. Because ants vary in diet and aggressiveness, their effect on herbivores also varies. Additionally, the differential occurrence of ant attractants (plant and insect exudates) on foliage produces variable levels of ant foraging within local floras and among localities. Here, we investigate how variation of ant communities and of traits among host plant species (presence or absence of ant attractants) can change the effect of carnivores (predatory ants) on herbivore communities (caterpillars) in a cerrado savanna landscape. We sampled caterpillars and foliage-foraging ants in four cerrado localities (70-460 km apart). We found that: (i) caterpillar infestation was negatively related with ant visitation to plants; (ii) this relationship depended on local ant abundance and species composition, and on local preference by ants for plants with liquid attractants; (iii) this was not related to local plant richness or plant size; (iv) the relationship between the presence of ant attractants and caterpillar abundance varied among sites from negative to neutral; and (v) caterpillars feeding on plants with ant attractants are more resistant to ant predation than those feeding on plants lacking attractants. Liquid food on foliage mediates host plant quality for lepidopterans by promoting generalized ant-caterpillar antagonism. Our study in cerrado shows that the negative effects of generalist predatory ants on herbivores are detectable at a community level, affecting patterns of abundance and host plant use by lepidopterans. The magnitude of ant-induced effects on caterpillar occurrence across the cerrado landscape may depend on how ants use plants locally and how they respond to liquid food on plants at different habitats. This study enhances the relevance of plant-ant and ant-herbivore interactions in cerrado and highlights the importance of a tritrophic perspective in this ant-rich environment.

Sendoya SF ，Oliveira PS 《-》

Multiple interaction types determine the impact of ant predation of caterpillars in a forest community.

Direct and indirect effects of predators are highly variable in complex communities, and understanding the sources of this variation is a research priority in community ecology. Recent evidence indicates that herbivore community structure is a primary determinant of predation strength and its cascading impacts on plants. In this study, we use variation in herbivore community structure among plant species to experimentally test two hypotheses in a temperate forest food web. First, variation in the strength of predator effects, such as ant predation of caterpillars, is predicted to be density dependent, exhibiting stronger effects when prey abundance is high (density-dependent predation hypothesis). Second, mutualistic interactions between ants and sap-feeding herbivores are expected to increase the abundance of predatory ants, strengthening predation effects on herbivores with cascading effects on host plants (keystone mutualism hypothesis). Using a large-scale predator exclusion experiment across eight dominant tree species, we tracked changes in insect density on 862 plants across two years, recording 2,322 ants, 1,062 sap-feeders, 5,322 caterpillars, and quantifying herbivory on 199, 338 leaves. In this experiment, density-dependent predation did not explain variation in the direct or indirect effects of ants on caterpillars and herbivory. In partial support of the keystone mutualism hypothesis, sap-feeders strengthened top-down effects of ants on caterpillars under some conditions. However, stronger ant predation of caterpillars did not lead to measurable trophic cascades on trees occupied by sap-feeders. Instead, the presence of sap-feeders was associated with increased per capita feeding damage by caterpillars, and this bottom-up effect attenuated the indirect effects of ants on host plants. These findings demonstrate that examining the multi-trophic impacts of mutualisms and predation in the context of the broader community can reveal patterns otherwise masked by compensatory interactions.

Clark RE ，Farkas TE ，Lichter-Marck I ，Johnson ER ，Singer MS ... -  《ECOLOGY》

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

Clark RE ，Singer MS 《-》

Dietary specialization is conditionally associated with increased ant predation risk in a temperate forest caterpillar community.

The enemy-free space hypothesis (EFSH) contends that generalist predators select for dietary specialization in insect herbivores. At a community level, the EFSH predicts that dietary specialization reduces predation risk, and this pattern has been found in several studies addressing the impact of individual predator taxa or guilds. However, predation at a community level is also subject to combinatorial effects of multiple-predator types, raising the question of how so-called multiple-predator effects relate to dietary specialization in insect herbivores. Here, we test the EFSH with a field experiment quantifying ant predation risk to insect herbivores (caterpillars) with and without the combined predation effects of birds. Assessing a community of 20 caterpillar species, we use model selection in a phylogenetic comparative framework to identify the caterpillar traits that best predict the risk of ant predation. A caterpillar species' abundance, dietary specialization, and behavioral defenses were important predictors of its ant predation risk. Abundant caterpillar species had increased risk of ant predation irrespective of bird predation. Caterpillar species with broad diet breadth and behavioral responsiveness to attack had reduced ant predation risk, but these ant effects only occurred when birds also had access to the caterpillar community. These findings suggest that ant predation of caterpillar species is density- or frequency-dependent, that ants and birds may impose countervailing selection on dietary specialization within the same herbivore community, and that contingent effects of multiple predators may generate behaviorally mediated life-history trade-offs associated with herbivore diet breadth.

Singer MS ，Clark RE ，Johnson ER ，Lichter-Marck IH ，Mooney KA ，Whitney KD ... -  《-》