Prior Experience Alters the Behavioral Response of Prey to a Nonnative Predator

—Anuran larvae (tadpoles) can alter their behavior and morphology in response to predators with which they have coevolved. Furthermore, tadpoles of a few species are capable of learning, which can elicit or reinforce predator-avoidance behaviors. However, it remains unclear how widespread this capacity for learning is among anurans and whether it is biased in favor of evolutionarily familiar predators. Here, we test whether prior experiences will modify the behavioral response of Lowland Leopard Frog Lithobates (Rana) yavapaiensis tadpoles to Green Sunfish Lepomis cyanellus, a recently introduced predator. We exposed focal tadpoles for 10 days to the chemical and visual cues of one of three conditioning treatments: a cricket-fed Green Sunfish, a tadpole-fed Green Sunfish, or a control tank without predator. Subsequently, we measured the swimming activity of focal tadpoles in response to a neutral cue (water) and the chemical cues of Green Sunfish. No difference between conditioning treatments was observed in response to the water cue. In contrast, tadpoles that had previously experienced either of the sunfish conditioning treatments displayed significantly higher swimming activity than control tadpoles for 2–4 min after exposure to the sunfish chemical cues. Our results indicate that the behavior of tadpoles can be altered by prior experiences, even in the absence of alarm cues. In addition to providing another example of learning in tadpoles, our results suggest that tadpoles may have a broad learning template that can be applied to organisms with which they have recently come into contact. Anuran larvae (tadpoles) have evolved a number of morphological and behavioral traits to cope with unpredictable levels of predation. For example, in the presence of predators with which they have coevolved, tadpoles can accelerate their development (Warkentin, 2000) or reduce their foraging activity (Relyea, 2001). In addition, they can develop larger tail fins and muscles, which may increase their swimming speed (although see Van Buskirk and McCollum, 2000; Van Buskirk, 2002) or deflect attacks away from the head (Van Buskirk et al., 2003, 2004). Predator-induced phenotypes presumably represent adaptive trade-offs in the presence of predation (Lima and Dill, 1990; Relyea, 2001; Van Buskirk, 2002; Álvarez and Nicieza, 2006) despite their energetic or developmental costs (Lawler, 1989; Skelly, 1992; Van Buskirk, 2000; Relyea and Auld, 2004). The behavioral responses of prey to predators can be constitutive or phenotypically plastic. A constitutive response implies that tadpoles will display an innate predator avoidance behavior in response to evolutionarily familiar predators (Kats et al., 1988; Griffiths et al., 1998). In addition, some species of tadpoles are capable of learning (a form of phenotypic plasticity). For example, tadpoles will display more pronounced predator-avoidance behavior after having witnessed predation events (Murray et al., 2004; Mandrillon and Saglio, 2005) or simulations thereof (Ferrari et al., 2005; Mirza et al., 2006; Gonzalo et al., 2007). The altered behavior in response to prior exposure to predators is likely to increase survival in the presence of predators (Griffin, 2004; Álvarez and Nicieza, 2006). In aquatic taxa such as amphibians and fish, learning of predators is frequently facilitated when predators are tagged, or associated, with alarm cues—the organic compounds released from injured conspecific prey (Semlitsch and Reyer, 1992; Chivers and Smith, 1998; Kats and Dill, 1998; Summey and Mathis, 1998). For example, Mirza et al. (2006) showed that chemical alarm cues from injured conspecifics facilitate recognition of an evolutionarily familiar odonate predator in American Toad Bufo americanus tadpoles and that the strength of the predator-avoidance behavior correlated with the concentration of alarm cues. But learning is not universal among tadpoles (e.g., Laurila et al., 1997). For most anuran species, it is not known whether tadpoles can learn and, in instances where they do, whether they rely on alarm cues, predator-specific cues, or a combi3 Corresponding Author. E-mail: mschlaepfer@ esf.edu Journal of Herpetology, Vol. 44, No. 2, pp. 185–192, 2010 Copyright 2010 Society for the Study of Amphibians and Reptiles