Scared Sick? Predator-pathogen facilitation enhances the exploitation of a shared resource

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Resource use generally increases with greater consumer diversity, an effect often attributed to resource partitioning. Pathogens and predators are two classes of consumer that exhibit differences in ecologically important traits (e.g., size, resource acquisition strategy, foraging location) that could lead to complementary effects on shared prey/hosts. To examine this possibility, we manipulated diversity among a community of predators and pathogens that together attack an herbivorous beetle, Leptinotarsa decemlineata, and measured resulting effects on herbivore suppression and resulting plant damage. We found that herbivore mortality increased, and plant damage decreased, when more natural enemy species were present. However, closer examination revealed that it was the pairing of predator with pathogen species, rather than greater biodiversity per se, that strengthened herbivore suppression. In this community, predators occur aboveground, attacking herbivore juvenile stages feeding on plant foliage, whereas pathogens occur belowground and attack herbivores pupating in the soil. In a subsequent field experiment, we tracked the emergence of predator-pathogen complementarity throughout the course of beetle development. We found that herbivores exposed to predators aboveground were more susceptible to subsequent pathogen infection belowground, consistent with our observation in the laboratory that predator exposure weakens beetles' immune response. Thus, predators facilitated resource capture by pathogens, perhaps reflecting an inherent conflict for the herbivore in allocating energetic resources toward anti-predator vs. anti-pathogen defenses. Our results suggest that predator-pathogen combinations were particularly taxing not because the consumer species partitioned resources among themselves, but instead because they enforced the partitioning of resources internal to prey/host individuals.

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