Scared Sick? Predator-pathogen facilitation strengthens Colorado potato beetle (Leptinotarsa decemlineata) control

Herbivore suppression often strengthens with increasing predator biodiversity, but little is known about the role of entomopathogens in these relationships. Entomopathogens and predators are two classes of natural enemy 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. We manipulated species richness among a community of predators and entomopathogens that together attack the Colorado potato beetle, Leptinotarsa decemlineata, and measured resulting effects on beetle suppression and resulting plant damage. We found that beetle 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 entomopathogen species, rather than greater biodiversity per se, that strengthened herbivore suppression. In this community predators (Hippodamia convergens, Nabis alternatus, and Pterostichus melanarius) occur aboveground, attacking beetle stages feeding on plant foliage, whereas entomopathogens (Steinernema carpocapsae, Heterorhabditis marelatus, and Beauvaria bassiana) occur belowground and attack beetles 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 beetles exposed to predators aboveground were more susceptible to subsequent entomopathogen infection belowground, consistent with our observation in the laboratory that predator exposure weakens beetles’ immune response. Thus, predators facilitated resource capture by entomopathogens, perhaps due to conflicting energetic demands for anti-predator versus anti-pathogen defenses. Our results suggest that predator-pathogen combinations were particularly taxing not because the natural enemy species partitioned resources among themselves, but instead because they enforced the partitioning of resources internal to beetle individuals.