The ghost of predation future: threat-sensitive and temporal assessment of risk by embryonic woodfrogs

Amphibians are able to learn to recognize their future predators during their embryonic development (the ghost of predation future). Here, we investigate whether amphibian embryos can also acquire additional information about their future predators, such as the level of threat associated with them and the time of day at which they would be the most dangerous. We exposed woodfrog embryos (Rana sylvatica) to different concentrations of injured tadpole cues paired with the odor of a tiger salamander (Ambystoma tigrinum) between 1500 and 1700 hours for five consecutive days and raised them for 9 days after hatching. First, we showed that embryos exposed to predator odor paired with increasing concentrations of injured cues during their embryonic development subsequently display stronger antipredator responses to the salamander as tadpoles, thereby demonstrating threat-sensitive learning by embryonic amphibians. Second, we showed that the learned responses of tadpoles were stronger when the tadpoles were exposed to salamander odor between 1500 and 1700 hours, the time at which the embryos were exposed to the salamander, than during earlier (1100–1300 hours) or later (1900–2100 hours) periods. Our results highlight the amazing sophistication of learned predator recognition by prey and emphasize the importance of temporal considerations in experiments examining risk assessment by prey.