Density-Dependence and agricultural intensity affect host-parasite-parasitoid interactions in a bird-insect trophic system

Abstract

Agricultural intensification is a major cause of population declines in farmland birds and insects worldwide. While these declines are expected to disrupt trophic interactions through density-dependent cascading effects, examples outside of crop pest control or involving more than two trophic levels remain poorly documented. Here we quantify such cascading effects across three trophic levels involving a declining aerial insectivore, the Tree Swallow (Tachycineta bicolor), which breeding success decreases with agricultural intensity, Protocalliphora bird blowflies (Diptera: Calliphoridae) that parasitize its nestlings, and Nasonia parasitoid jewel wasps (Hymenoptera: Pteromalidae) that feed upon blowfly pupae within swallow nests. Agriculture intensity may affect each of these actors either directly via, for instance, toxicological effects from pesticide use, or indirectly through density-dependent trophic interactions, which can exacerbate or mitigate one another. Using Bayesian models within a causal inference framework, we quantified how nestling host density, meteorological conditions, and agricultural landscape context affect Nasonia parasitoid infestation of Protocalliphora pupae, and estimated Protocalliphora emergence success. Analyses were based on 3,340 Protocalliphora puparia collected from 248 Tree Swallow nests over a 16-year period (2004-2019) across a 10,200-km2 agricultural intensity gradient in Southern Quebec, Canada. Model predictions indicated that Protocalliphora emergence probability increased steeply with nestling host availability (i.e., nestling-days). Whereas Nasonia parasitoid infestation occurrence at the nest level increased with Protocalliphora host availability, the proportion of infested Protocalliphora pupae within nest decreased and led to a dilution effect at the individual level. Although Protocalliphora abundance within nests decreased with agricultural intensity, their emergence probability peaked in agrointensive landscapes. This increase was associated with reduced Nasonia infestation rates, suggesting that agricultural intensity indirectly mitigated parasitoid pressure on Protocalliphora host populations. Our results highlight how agricultural intensification can shape multitrophic interactions and life-history traits (emergence success and infestation rates) by simultaneously reducing host availability and weakening top-down control by parasitoids.