Embryonic learning and developmental carry-over effects in an invasive anuran

Tiffany S. Garcia, Jenny C. Urbina, Evan M. Bredeweg, Maud C. O. Ferrari

Carry-over effects influence trait responses in later life stages as a result of early experience with environmental cues. Predation risk is an influential stressor and selection exists for early recognition of threats. In particular, invasive species may benefit from carry-over effects by preemptively recognizing and responding to novel predators via latent developmental changes and embryonic learning. In a factorial experiment, we conditioned invasive American bullfrog embryos (Lithobates catesbeianus) to the odor of a novel fish predator, largemouth bass (Micropterus salmoides) alone or in combination with injured conspecific cues. We quantified developmental carryover in the larval life stage and found that individuals conditioned to the highest risk (fish and injured conspecific cues) grew into longer bodied larvae relative to larvae from lower risk treatments. We also assessed embryonic learning, a behavioral carry-over effect, and found an interaction between embryonic conditioning and larval exposure. Behavioral responses were only found in scenarios when predation risk varied in intensity across life history stages, thus requiring a more flexible antipredator strategy. This indicates a potential trade-off between the two strategies in larval growth and development rates, and time until metamorphosis. Our results suggest that early predator exposure and carry-over effects have significant impacts on life history trajectories for American bullfrogs. This research contributes to our understanding of a potentially important invasion mechanism in an anuran species of conservation concern.