Huffaker revisited: spatial heterogeneity and the coupling of ineffective agents in biological control.

In a classic study, Huffaker demonstrated that abiotic forms of spatial heterogeneity could induce stability in predator-prey interactions. Recent theories suggest that space can also act to destabilize predator-prey systems and that stability can arise from coupling of unstable units. Here, using Huffaker's classic experimental design refitted with modern empirical and statistical techniques, we reassess the effect of space on predator-prey interactions when the prey are pests of agriculture, and when predators must compete with pathogens for shared prey resources. Using an empirical system including aphids, ladybird beetles and entomopathogenic fungi, we show that while two different control agents were ineffective at controlling pests in insolation, coupling them together not only improved control of the pest, but also reduced the occurrence of large, spatially-clustered pest outbreaks. Our results suggest that as agriculture becomes increasingly isolated and consolidated across landscapes, endogenous forms of spatial heterogeneity, which arise from interactions between diverse assemblages of control agents, may break down. We suggest that improving connectivity across landscapes is important for maintaining effective biological control in agroecosystems.