Developmental changes in red-eyed treefrog embryo behavior increase escape-hatching success in wasp attacks

Abstract

The arboreal embryos of red-eyed treefrogs (Agalychnis callidryas) hatch prematurely to escape from egg predators, and escape success increases with age. We assessed developmental changes in the behavior and hatching performance of embryos attacked by wasps (Polybia rejecta) and their contributions to improved embryo survival. We recorded videos of 4- and 5-day-old embryos exposed to wasp attacks and determined each embryo’s fate. For a stratified random sample of embryos that escaped and died, we determined the occurrence, sequence, and timing of events during wasp-embryo interactions. We constructed path diagrams of event sequences, tested for age effects on transition probabilities, and measured the durations of periods between key events. Overall, escape success was 38% higher in older embryos. They were more likely to hatch pre-emptively than younger ones, thus less likely to experience direct attacks, suggesting that developmental gains in mechanosensory sensitivity may increase hatching responses to indirect cues. During direct attacks, embryos were equally likely to be captured by wasps at both ages, and hatching speed was similar, suggesting no relevant difference in escape-hatching performance. After a wasp ruptured their egg capsule, older embryos were more likely to exit, and they did so much sooner; younger embryos remained in ruptured capsules for longer and were more likely to be attacked again. This developmental change in embryo behavior indicates decreased tolerance for egg-stage risk as the chance of tadpole survival increases, suggesting that ontogenetic adaptation to changing risk trade-offs contributes strongly to the developmental increase in escape success.

Significance statement

As animals develop, both their abilities and the optimal strategies for antipredator defense change, and some show ontogenetic adaptation of defensive behavior. This is documented in the larval and juvenile stages but rarely examined during the embryonic period, when development is fastest. We document substantial changes in embryo behavior across a 1-day period following the onset of predator-induced hatching in red-eyed treefrogs, with rapidly decreasing tolerance of egg-stage risk contributing to higher survival under wasp predation as the costs of hatching decrease. This provides evidence for ontogenetic adaptation of defensive behavior in a natural predation context and across an earlier developmental period than previously known, thereby strengthening results from prior work with vibration playbacks across later developmental stages. It suggests that even during periods of rapid development of morphology and abilities, understanding behavioral decisions may be crucial to explaining changes in survival.