Widespread learned predator recognition to an alien predator across populations in an amphibian species.

Alien predators are a major cause of decline and extinction of species worldwide, since native organisms are rarely equipped with specific antipredatory strategies to cope with them. However, phenotypic plasticity and learned predator recognition may help prey populations to survive novel predators. Here we examine geographical variation in the learning ability of larval spadefoot toads (Pelobates cultripes) to recognize invasive predatory crayfish (Procambarus clarkii). We compare the learning-mediated behavioural responses of tadpoles from six populations across two regions in Spain (central and southern), with different histories of exposure to the presence of the invasive species. Two of the populations showed innate recognition of chemical cues from the invasive crayfish, whereas three of them learned to recognize such cues as a threat after conditioning with conspecific alarm cues. Learning abilities did not differ among southern populations, but they did among central populations. We assessed patterns of genetic variation within and among these two regions through microsatellite markers and found low genetic divergence among the southern populations but greater differentiation among the central ones. We hypothesize that similar responses to the invasive crayfish in southern populations may have arisen from a combination of extended historical exposure to this introduced predator (~ 50 y) and higher levels of gene flow, as they inhabit a highly interconnected pond network. In contrast, populations from central Spain show lower connectivity, have been exposed to the invasive crayfish for a shorter period of time, and are more divergent in their plastic responses.

Assessment of predation risk through conspecific cues by anuran larvae.

Accurate assessment of predation risk is critical for prey survival during predator-prey interactions. Prey can assess predation risk by the presence of cues dropped by predators themselves, but they can also gather information about risk level through cues released by other prey, avoiding the hazard of being in close proximity to predators. In this study, we examine the ability of anuran larvae (Pelobates cultripes) to detect predation risk indirectly when they are in contact with conspecifics that have been recently exposed to chemical stimuli from natural predators (larvae of aquatic beetles). In a first experiment, we confirmed that larvae exposed to predator cues exhibited innate defensive behavior, indicating that they perceived the risk of predation and, thus, could potentially act as risk indicators for naïve conspecifics. In a second experiment, we observed that unexposed larvae paired with a startled conspecific adjusted their antipredator behavior, presumably by mirroring conspecifics' behavior and/or using chemical cues from their partners as a risk information source. This cognitive ability of tadpoles to assess predation risk through conspecific cues might play an important role in their interaction with predators, facilitating the early detection of potential threats to elicit appropriate antipredator responses and increase the chances of survival.

Stable Isotopes Reveal Trophic Partitioning and Trophic Plasticity of a Larval Amphibian Guild.

Temporary ponds are highly variable systems where resource availability and community structure change extensively over time, and consequently the food web is highly dynamic. Amphibians play a critical role both as consumers and prey in aquatic communities and yet there is still little information on the trophic status of most amphibians. More importantly, little is known about the extent to which they can alter their trophic ecology in response to changing conditions. We experimentally investigated the effects of increased amphibian density, presence of intraguild competitors, and presence of native and invasive predators (either free or caged) on the trophic status of a Mediterranean amphibian guild, using stable isotopes. We observed variations in δ13C and δ15N isotopic values among amphibian species and treatments and differences in their food sources. Macrophytes were the most important food resource for spadefoot toad tadpoles (Pelobates cultripes) and relatively important for all anurans within the guild. High density and presence of P. cultripes tadpoles markedly reduced macrophyte biomass, forcing tadpoles to increase their feeding on detritus, algae and zooplankton, resulting in lower δ13C values. Native dytiscid predators only changed the isotopic signature of newts whereas invasive red swamp crayfish had an enormous impact on environmental conditions and greatly affected the isotopic values of amphibians. Crayfish forced tadpoles to increase detritus ingestion or other resources depleted in δ13C. We found that the opportunistic amphibian feeding was greatly conditioned by intra- and interspecific competition whereas non-consumptive predator effects were negligible. Determining the trophic plasticity of amphibians can help us understand natural and anthropogenic changes in aquatic ecosystems and assess amphibians' ability to adjust to different environmental conditions.