Learning by embryos and the ghost of predation future

Abstract

Most research on the effects of exposure to stressful stimuli during embryonic development has focused on post-embryonic behaviour that appears to be abnormal or maladaptive. Here, we tested whether exposure to some stressful stimuli (predatory cues) can lead to post-embryonic behaviour that is adaptive. When eggs of ringed salamanders (Ambystoma annulatum) were exposed to chemical cues from predators, post-hatching larvae showed reduced activity and greater shelter-seeking behaviour; larvae that had been exposed to control cues did not show these behaviours. In addition, wood frog (Rana sylvatica)tadpoles learned to respond to chemical cues from unfamiliar predators with danger based on embryonic conditioning. Therefore, if embryonic experience is a good predictor of future risk, learning associated with exposure to negative stimuli during development may be adaptive.

Figure 1

Post-hatching behaviour of Ambystoma annulatum larvae that had been exposed as embryos to chemical stimuli from predators (cannibalistic conspecifics), non-predators (tadpoles of R. catesbeiana) or to a blank control. (a) Activity measured as total number of lines crossed in 5 min (mean±1 s.e.). Statistical analysis was an ANOVA followed by Tukey's post hoc comparisons; different letters indicate significant differences. (b) Habitat choice measured as proportion of larvae found in the plants after 5 hours. Statistical analysis was the Fisher's exact probability test; ^*p=0.011; n.s., p>0.15.

Figure 2

Activity measured as proportional change in line crosses (mean±1 s.e.) for wood frog tadpoles that had been exposed to tadpole alarm cues paired with newt odour (TP+NO), well water paired with newt odour (WW+NO) or well water only (WW) in the egg. Different shading patterns represent the responses of tadpoles from different clutches.