Learning predator promotes coexistence of prey species in host-parasitoid systems

Ecological theory suggests that frequency-dependent predation, in which more common prey types are disproportionately favored, promotes the coexistence of competing prey species. However, many of the earlier empirical studies that investigated the effect of frequency-dependent predation were short-term and ignored predator-prey dynamics and system persistence. Therefore, we used long-term observation of population dynamics to test how frequency-dependent predation influences the dynamics and coexistence of competing prey species using insect laboratory populations. We established two-host-one-parasitoid populations with two bruchid beetles, Callosobruchus chinensis and C. maculatus, as the hosts and the pteromalid wasp Anisopteromalus calandrae as their common parasitoid. When the parasitoid was absent, C. chinensis was competitively excluded in ∼20 wk. Introducing the parasitoid greatly enhanced the coexistence time to a maximum of 118 wk. In the replicates of long-lasting coexistence, the two host species C. maculatus and C. chinensis exhibited periodic antiphase oscillations. Behavioral experiments showed frequency-dependent predation of A. calandrae that was caused by learning. Females of A. calandrae learned host-related olfactory cues during oviposition and increased their preference for the common host species. Numerical simulations showed that parasitoid learning was the essential mechanism that promoted persistence in this host-parasitoid system. Our study is an empirical demonstration that frequency-dependent predation has an important role in greatly enhancing the coexistence of prey populations, suggesting that predator learning affects predator-prey population dynamics and shapes biological communities in nature.