Stress and Aversive Learning in a Wild Vertebrate: The Role of Corticosterone in Mediating Escape from a Novel Stressor

Abstract

Elevated plasma corticosterone during stressful events is linked to rapid changes in behavior in vertebrates and can mediate learning and memory consolidation. We tested the importance of acute corticosterone elevation in aversive learning of a novel stressor by wild male eastern fence lizards (Sceloporus undulatus). We found that inhibiting corticosterone elevation (using metyrapone, a corticosterone synthesis blocker) during an encounter with a novel attacker impaired immediate escape responses and limited learning and recall during future encounters. In the wild and in outdoor enclosures, lizards whose acute corticosterone response was blocked by an earlier metyrapone injection did not alter their escape behavior during repeated encounters with the attacker. Control-injected (unblocked) lizards, however, progressively increased flight initiation distance and decreased hiding duration during subsequent encounters. Aversive responses were also initially higher for control lizards exposed to a higher intensity first attack. Further, we demonstrate a role of corticosterone elevation in recollection, since unblocked lizards had heightened antipredator responses 24-28 h later. Exogenously restoring corticosterone levels in metyrapone-injected lizards maintained aversive behaviors and learning at control (unblocked) levels. We suggest that the corticosterone mediation of antipredator behaviors and aversive learning is a critical and general mechanism for the behavioral flexibility of vertebrate prey.