Behavioral changes in tadpoles after multigenerational exposure to an invasive intraguild predator

Prey subject to intraguild predation may face conflicting selective pressure on behavior, with competition favoring increased activity and predation favoring activity reduction. To discover how this evolutionary conflict might be resolved, we compared the behavior of tadpoles (i.e., larvae) from 4 families drawn from different populations that had potentially coevolved with an introduced intraguild predator for up to 90 years with the behavior of tadpoles from 4 families from unexposed populations. Intraguild prey were tadpoles of the declining California Red-legged Frog (Rana draytonii) and the intraguild predator was the invasive American Bullfrog (Lithobates catesbeianus), a voracious predator and strong competitor of other anurans. Limited evidence suggests that some native amphibians that have co-occurred with invasive predators for generations show adaptive behavioral responses to predator chemical cues. We tested whether R. draytonii larvae from families either allotopic or syntopic with bullfrogs would show responses to cues from over-wintered bullfrog larvae. In the presence of cues, early-stage syntopic larvae decreased movement, consistent with an evolved innate defense, while allotopic larvae did not show behavioral changes. Later-stage syntopic larvae were generally more active than allotopic larvae, especially in the absence of cues, indicating a potential adaptive response to competition from bullfrog larvae. Increased activity appeared to be timed for when tadpoles became more resistant to predation. This is the first study to show changes in behavior across development consistent with complex selective pressure from an introduced intraguild predator. These findings have important implications for management of an endangered amphibian and a widely introduced, invasive intraguild predator.