Escape-hatching decisions show adaptive ontogenetic changes in how embryos manage ambiguity in predation risk cues

Abstract

As animals develop, their capacities to sense cues, assess threats, and perform actions change, as do the relative costs and benefits that underlie behavioural decisions. We presented ambiguous cues to test if hatching decisions of red-eyed treefrogs, Agalychnis callidryas, change developmentally following adaptive predictions based on changing costs of decision errors. These arboreal embryos hatch prematurely to escape from egg predators, cued by vibrations in attacks. Young embryos modulate hatching based on the frequency and temporal properties of cues, reducing false alarms that unnecessarily expose them to risk in the water. Since the cost of false alarms decreases developmentally, we hypothesized that hatching responses to ambiguous cues would increase. We tested this using vibration playbacks at two ages, with two sets of 3 stimuli. We matched sampling costs and varied ambiguity in either temporal or frequency properties, so one stimulus elicited high hatching (positive control) and two elicited low hatching but differed in ambiguity, based on prior results with younger embryos. Older embryos hatched faster, indicating reduced cue sampling. They responded strongly to both clear threat cues and ambiguous stimuli but little when either property clearly indicated low risk. In both experiments, we saw the greatest ontogenetic change in response to the more ambiguous stimulus. These playback experiments improve our understanding of how embryos facing risk tradeoffs make adaptive decisions based on incidental cues from predators. Ambiguity in incidental cues is ubiquitous and developmental changes in behaviour due to ontogenetic adaptation of decision processes are likely to be widespread.

Significance statement

Animals must use imperfect information to guide their behavior, and the costs of decision errors often change with development. We found the decision rules that embryos apply to ambiguous cues to deploy escape behavior change developmentally, matching adaptive predictions based on changing cost–benefit tradeoffs. Our results, consistent across two different forms of ambiguity, suggest selection has shaped behavioral development to improve how embryos use ambiguous incidental cues for defense. This work both extends and generalizes earlier experiments varying the cost of information. It cautions against oversimplifying assumptions about embryo information use—at least for species and in contexts where a history of strong selective tradeoffs may have honed their capacity to make a key decision well—and demonstrates the value of vibration playbacks and embryo hatching behavior for research in animal cognition.