Adaptive forgetting in Iberian green frog tadpoles (Pelophylax perezi): learned irrelevance and latent inhibition may avoid predator misidentification.

Predator recognition often requires learning by prey individuals. Iberian green frog tadpoles (Pelophylax perezi) have the ability to learn to recognize new potential predators when their chemical cues are found paired with conspecific alarm cues. However, a random pairing of alarm cues and chemical stimuli of a nonpredator might later induce costly antipredator responses to nondangerous species. Here, we studied the potential existence in this frog species of two phenomena (learned irrelevance and latent inhibition) that could help tadpoles to avoid these nonadaptive responses to chemical cues of nonpredator species. Our results showed that, when tadpoles experienced a random pattern of presence of alarm cues alone or predator cues alone over the 4 days before or after the simultaneous detection of these two cues paired, no learned association was formed. These results showed the existence of an effect of learned irrelevance on learning in Iberian green frog tadpoles. Also, tadpoles clearly inhibited the formation of a learning association between predator and alarm cues after a 4-day period during which they had been exposed to the predator cues alone. This result showed the existence of an effect of latent inhibition on learning about cues related to increased predation risk. Thus, both learned irrelevance and latent inhibition, rather than being considered to be failed predator recognition, can rather be seen as adaptive ways for dealing with conflicting information and as strategies to avoid learning irrelevant information and costly antipredatory responses to nonpredatory stimuli.

Learning, memorizing and apparent forgetting of chemical cues from new predators by Iberian green frog tadpoles.

Many antipredator adaptations are induced by the prey's ability to recognize chemical cues from predators. However, predator recognition often requires learning by prey individuals. Iberian green frog tadpoles (Pelophylax perezi) have the ability to learn new potential predators. Here, we tested the memory capabilities of Iberian green frog tadpoles. We conditioned tadpoles with chemicals cues from a non-predatory fish in conjunction with conspecific alarm cues, and examined whether tadpoles retained their conditioned response (reduction of activity level). We found that conditioned tadpoles reduced their activity levels in subsequent exposures to the non-predatory fish cues alone. Tadpoles were able to remember this association and reduced movement rate at least for 9 days after. The ability to learn and memorize potential predators may be especially important for the survivorship of prey species that are likely to find a high variety of predators. However, after those 9 days, there was a lack of response to the non-predatory fish cues alone in the absence of reinforcement. This could be explained if tadpoles behave according to the threat-sensitive predator avoidance hypothesis, and the perceived risk to the learning cue diminished over time, or it could be due to an apparent forgetting process to avoid non-adaptative responses to chemical cues of non-dangerous species that were randomly paired with alarm cues. Thus, this study demonstrates that green frog tadpoles in the absence of reinforcement remember the chemical cues of a learned predator only for a limited time that may be adaptative in a threat-sensitive context.

Generalization of learned predator recognition: an experimental test and framework for future studies.

While some prey species possess an innate recognition of their predators, others require learning to recognize their predators. The specific characteristics of the predators that prey learn and whether prey can generalize this learning to similar predatory threats have been virtually ignored. Here, we investigated whether fathead minnows that learned to chemically recognize a specific predator species as a threat has the ability to generalize their recognition to closely related predators. We found that minnows trained to recognize the odour of a lake trout as a threat (the reference predator) generalized their responses to brook trout (same genus as lake trout) and rainbow trout (same family), but did not generalize to a distantly related predatory pike or non-predatory suckers. We also found that the intensity of antipredator responses to the other species was correlated with the phylogenetic distance to the reference predator; minnows responded with a higher intensity response to brook trout than rainbow trout. This is the first study showing that prey have the ability to exhibit generalization of predator odour recognition. We discuss these results and provide a theoretical framework for future studies of generalization of predator recognition.

Detection and discrimination of conspecific scents by the anguid slow-worm Anguis fragilis.

We tested the ability of male slow-worms, Anguis fragilis, a limbless anguid lizard with secretive, semifossorial habits, to detect chemical associated with conspecifics by using a T-maze in the laboratory. Male slow-worms discriminated conspecific male and female scent deposits. Males selected the arm with female scent, suggesting that scent deposits may be used to locate potential mates. Also, male slow-worms did not avoid the chemicals of other males, suggesting that they are not territorial. However, males discriminated their own scent from those of other males, and spent more time exploring the arm with other male scent, which suggests that scent marks may bear information that could be used in future intrasexual social contexts. We conclude that discrimination of conspecifics based on scents may be more widespread than previously expected among lizards inhabiting visually restricted environments.