Ontogeny of escape-hatching decisions: vibrational cue use changes as predicted from costs of sampling and false alarms

Abstract

As animals develop, their abilities and needs change, altering cost/benefit trade-offs and optimal behavior responses to cues. We tested if ontogenetic changes in information use and environmentally cued hatching decisions of embryos match adaptive predictions, using red-eyed treefrogs, Agalychnis callidryas. These arboreal embryos hatch rapidly and prematurely to escape egg predators, cued by physical disturbance in attacks. Hatching early increases tadpole mortality, and premature embryos use multiple frequency and temporal properties of vibrations to assess risk, avoiding false alarms in benign disturbances such as rain. Because development increases hatchling survival, we hypothesized embryos approaching spontaneous hatching would reduce vibration sampling to reduce egg-predation risk, accepting more false alarms if cues are time-consuming to assess. We designed stimuli to elicit high or low hatching of younger embryos, with the property that reduces hatching either rapidly evident (frequency spectrum or fast temporal pattern) or time-consuming to assess (slow temporal pattern). We developed a new egg-tray vibration playback system to present motion-only cues with minimal disturbance in setup, then used it to compare responses of younger and previously untestable older embryos. The playback duration embryos experienced before or without hatching decreased with age, suggesting reduced vibration sampling. At both stages, hatching responses differed between frequencies, and among temporal patterns; nearly full-term embryos still showed selective hatching responses to cues. Hatching increased developmentally in a stimulus-dependent manner, with the greatest change in response to the slow pattern, as predicted. Developmental changes in discrimination appear well-matched to changing trade-offs, consistent with ontogenetic adaptation of embryo behavior.

Significance statement

Animal behavior changes ontogenetically for many reasons, including developing capacities to sense and assess cues and perform actions, adaptive responses to changing costs and benefits, and learning. Hatching is a critical behavior, subject to selection from pre- and post-hatching environments, that is performed during a period of rapid development. Environmentally cued hatching is widespread, and many embryos use vibrations to inform behavior. The egg-tray system we developed enables vibration playbacks to red-eyed treefrog embryos across a broader range of stages than previously possible, facilitating tests of how and why development changes behavior. Playbacks revealed that embryos at different stages assess cues and make decisions differently, with stage-specific responses matching adaptive predictions. This reveals a new level of complexity in embryo information use, motivating and enabling further research assessing the role of adaptive ontogeny and developmental constraint in early behavioral development.