Our results demonstrate that amphibians can learn both the identity and the temporal foraging pattern of their predators prior to hatching. They subsequently use this information as tadpoles to adjust the time at which they display high intensities of responses to predators. This represents a high level of sophistication of risk assessment by young prey animals, but the exact mechanism that they use to acquire temporal information is unclear, as field conditions do not allow us to distinguish between an internal clock, light intensity or sun position. What we do know, however, is that this temporal learning takes place over a short time period (over a 4 or 5 day period), as the embryos did not have a fully formed neural tube before day 2 or 3. Water temperature during conditioning bouts was highly variable from day to day (over a range of 12°C), which makes it unlikely that the responses are elicited by temperature-specific conditions.
Theoretical models suggest that learning is advantageous in highly variable environments (Ferrari et al. 2007
; Stephens 2009
). Such would be the case when prey animals, like amphibians, find themselves in environments where predation pressure may vary from extremely low to extremely high (i.e. the variability between years is high). Hence, learning should allow prey to collect information about their environment that will help them make better-informed decisions. However, gathering information about the environment is often costly in terms of both time and energy (Dukas 1998
). The temporal learning that we observed implies that the cost of being cautious during a predator's foraging time may be small compared with the probable benefit of reducing mortality. Interestingly, the response to the salamanders disappeared when the exposure time did not match the time when the predator was active. These results imply that individual tadpoles experience predators with highly predictable cycles.
In our experiment, we tested woodfrog larvae two weeks following hatching, and found that the information the tadpoles learned as embryos was used to adjust the intensity of their antipredator responses throughout the day. However, could this temporal information have been used by the embryos themselves? In most cases, embryos cannot display active antipredator behaviour (swimming away from predators), because they are anchored at a specific location. However, embryos may be able to better time their conspicuousness (wriggling movements related to hatching), limiting them, for example, to periods where predators are not foraging. Indeed, numerous species of amphibians show considerable variation in their timing of hatching related to the presence of egg and larval predators (Chivers et al. 2001
). Thus, it is possible that temporal learning of information about predation risk is used at an earlier stage than the one we documented.
The window of memory for which learned information is available is often related to the expected value of the information later in life. The information should be available for a longer time if the environment has a low variability (depending on the probability of the information being useful after a given period). If the environment is rapidly changing, the information will be erroneous and potentially costly; thus, the memory window should be shorter (Stephens 2009
). In our study, the cues used to mediate learning were crushed tadpole cues paired with salamander cues. It is likely that tadpole-specific predators that tadpoles experienced as embryos will also be present when the embryos in turn reach their larval stage (i.e. the variability within a year is low). Hence, the information still has a high informative potential. This begs the question: would embryos experiencing embryo-specific predators (e.g. leeches feeding on eggs) remember predator-related information as tadpoles? Likewise, it would be fruitful to provide embryos conflicting information about the time at which predators forage and test how such an increase in environmental variability influences learning and memory of predator cues. The field of embryonic learning is at its infancy; further research would bring insights into the evolutionary ecology of learning and forgetting.