Long-term anti-predator learning and memory N. canaliculata

Anti-predator behaviours in response to predator cues can be innate, or they can be learned through prior experience and remembered over time. The duration and strength of continued anti-predator behaviour after predator cues are no longer present and the potential for an enhanced response when re-exposed to predator cues later are less known but could account for observed variation in anti-predator responses. We measured the carryover effects of past predation exposure and the potential for anti-predator learning and memory in the marine snail Nucella canaliculata from six populations distributed over 1,000km of coastline. We exposed lab-reared snails to cues associated with a common crab predator or seawater control in two serial experiments separated by over 7 months. Responses were population and sex dependent with some populations retaining anti-predator behaviours while others showed a capacity for learning and memory. Male snails showed a strong carryover of risk-aversion while females were able to return to normal feeding rates and grow more quickly. These behavioural differences culminated in strong impacts on feeding and growth rates demonstrating that this variation has implications for the strength of trait-mediated indirect interactions, which can impact entire ecosystems.

Methods
We ran a fully crossed, factorial experiment that exposed Nucella canaliculata snails to either control or predator cue treatments (rock crabs with crushed conspecific snail cues) in an initial experiment (Trial 1) followed seven months later by another experimental exposure (Trial 2) to either a seawater control or predator cues (rock crabs, no crushed conspecific). During both of these exposures, we tracked each individual snail’s behaviour in containers that provided areas of refuge and risk. This design allowed us to assess 1) how prior exposure to predator cues influenced the behaviour of snails months later (fear retention), 2) how prior experience influenced the behaviour of snails in a subsequent exposure to predator cues (fear memory), and 3) how these capabilities varied depending on source population or sex. We also collected size data (length, weight, and weight-to-length ratio) to determine if size impacted behavioural patterns.