Hierarchical fear: parental behaviour and corticosterone release mediate nestling growth in response to predation risk

Abstract

Nestling development, a critical life-stage for altricial songbirds, is highly vulnerable to predation, particularly for open-cup nesting species. Since nest predation risk increases cumulatively with time, rapid growth may be an adaptive response that promotes early fledging. However, greater predation risk can reduce parental provisioning rate as a risk aversion strategy and subsequently constrain nestling growth, or directly elicit a physiological response in nestlings with adaptive or detrimental effects on development rate. Despite extensive theory, evidence for the relative strength of these effects on nestling development in response to prevailing predation risk and the underlying mechanisms remain unclear. For an alpine population of horned lark (Eremophila alpestris), we elevated perceived predation risk (decoys/playback) during the nestling stage to assess the influence of predator cues and parental care on nestling wing growth and the glucocorticoid hormone corticosterone. We used piecewise path analysis to test a hypothesized causal response structure composed of direct and indirect pathways. Nestlings under greater perceived predation risk reduced corticosterone and increased wing growth, resulting in an earlier age at fledge. This represented both a direct response that was predator-specific, and an indirect response dependent on parental provisioning rate. Parents that reduced provisioning rate most severely in response to predator cues had smaller nestlings with greater corticosterone. Model comparisons indicated the strongest support for a directed, causal influence of corticosterone on nestling wing growth, highlighting corticosterone as a potential physiological mediator of the nestling growth response to predation risk. Finally, cold temperatures prior to the experiment constrained wing growth closer to fledge, illustrating the importance of considering the combined influence of weather and predation risk across developmental stages. We present the first study to separate the direct and indirect effects of predation risk on nestling development in a causal, hierarchical framework that incorporates corticosterone as an underlying mechanism and provides experimental evidence for an adaptive developmental response to predation risk in ground-nesting songbirds.