Learning to find food: evidence for embryonic sensitization and juvenile social learning in a salamander Adam L. Crane a, * , Emilee J. Helton b , Maud C. O. Ferrari c , Alicia Mathis d a Department of Biology, University of Saskatchewan, SK, Canada b National Park Service, Moose, WY, U.S.A. c Veterinary Biomedical Sciences, WCVM, University of Saskatchewan, Saskatoon, SK, Canada d Biology Department, Missouri State University, Springfield, MO, U.S.A. article info Article history: Received 9 November 2017 Initial acceptance 26 February 2018 Final acceptance 25 May 2018 MS. number: A17-00888R2 Keywords: generalization imprinting local enhancement olfaction social facilitation For many species, learning is an essential mechanism for dealing with the environment correctly and efficiently. Animals that quickly learn important information, and learn at a young age, can gain a competitive advantage in exploiting resources. Moreover, animals that learn indirectly through social observations can avoid the fitness costs of directly learning about potential dangers. Here we tested such learning capabilities in ringed salamanders, Ambystoma annulatum, a species where adults are primarily solitary and do not provide parental care. Adults lay eggs in ponds where embryos have the opportunity to learn from chemical cues in their environment before hatching, whereupon the high density of larvae provides an opportunity to learn from social information. In this study, we found that these salamanders can learn an attraction to novel food stimuli as embryos and that naïve observer larvae can learn from conspecifics that show attraction to stimuli. Embryonic exposure to a novel food stimulus (shrimp odour) caused attraction to that stimulus posthatching, and this response appeared to be generalized to another potential prey stimulus (mussel odour) but not to a novel plant stimulus. In a test of social learning, only observers that were paired with models corralled near a novel food stimulus were subsequently attracted to the stimulus. This study is the first to report embryonic learning of food or social learning by salamanders, providing more evidence for generalized learning by embryos and social learning by species lacking more complex social behaviours. © 2018 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. Correctly responding to environmental stimuli is essential to maximizing fitness, but fluctuations in the environment can pose challenges to decision making (Dall, 2010; Kacelnik & Bateson, 1996; Lima & Dill, 1990). For instance, changes in food availability or predation pressure may lead to a failure to accurately assess such information. Learning is generally viewed as the act of acquiring new information or the modification or reinforcement of existing information based on experience, resulting in behavioural changes (Brown & Chivers, 2005; Papaj & Prokopy, 1989; Stephens, 1991). According to learning theory, stable environments facilitate the evolution of innate responses to stimuli, whereas variable and complex environments can promote learned responses (Stephens, 1991, 1993). In a changing environment, individuals that learn can better exploit resources and have an increased probability of sur- vival and reproductive success (Brown & Chivers, 2005). Such learning capabilities may be particularly important during early life periods where mortality rates are generally high (Pianka, 1970; Sogard, 1997), and indeed, young animals often show a high ca- pacity for learning (Bornstein, 1989; Fawcett & Frankenhuis, 2015). In classic research by Lorenz (1935), geese, Anser anser , during a sensitive period in early development would instinctively bond with other moving stimuli in place of their parents. This phenom- enon, known as imprinting, allows goslings to quickly learn to recognize their parents. Imprinting (or a learning process akin to imprinting) is not restricted to social stimuli however (Immelmann, 1975). For instance, several studies have explored imprinting of food stimuli during sensitive learning periods (e.g. Burghardt & Hess, 1966; Guib e, Poirel, Houd e, & Dickel, 2012; Punzo, 2002). Even as embryos, animals are capable of learning how to maximize their probability of survival in their postnatal environ- ment via a variety of sensory modalities (e.g. Darmaillacq, Lesimple, & Dickel, 2008; Hepper & Waldman, 1992; Lickliter & Hellewell, 1992). Chemosensory cues, for instance, are relatively long last- ing, can move around barriers, and are available when visibility is * Correspondence: A. L. Crane, Department of Biology, University of Saskatch- ewan, 112 Science Place, Saskatoon, SK S7N 5E2, Canada. E-mail address: adam.crane@usask.ca (A. L. Crane). Contents lists available at ScienceDirect Animal Behaviour journal homepage: www.elsevier.com/locate/anbehav https://doi.org/10.1016/j.anbehav.2018.06.021 0003-3472/© 2018 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. Animal Behaviour 142 (2018) 199e206