Reef fishes innately distinguish predators based on olfactory cues associated with recent prey items rather than individual species Danielle L. Dixson a, b, c, * , Morgan S. Pratchett b , Philip L. Munday a, b a School of Marine & Tropical Biology, James Cook University, Townsville, Australia b ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Australia c School of Biology, Georgia Institute of Technology, Atlanta, GA, U.S.A. article info Article history: Received 26 September 2011 Initial acceptance 24 October 2011 Final acceptance 27 March 2012 Available online 5 May 2012 MS. number: A11-00737R Keywords: Amphiprion percula anemonefish chemical ecology coral reef fish diet larvae olfaction predation An individual’s ability to identify and respond accurately to a predator greatly affects its probability of survival. Chemosensory cues are an important mechanism for predator detection in aquatic environ- ments. Whether fish are aware of the risks posed by distinct fish species, or whether a common che- mosensory cue distinguishes predatory fishes, is unknown. One possibility is that fish distinguish predatory fishes based on their diet. To test this, we manipulated the diet of three nominally non- piscivorous species and examined behavioural responses of juvenile anemonefish, Amphiprion percula, to chemical cues of nonpredators fed a diet rich in fish product. In pairwise choice trials, naïve A. percula showed indifference to chemosensory cues from nonpiscivorous fishes fed their usual diet, but signifi- cantly avoided chemical cues from piscivorous and nonpiscivorous fishes fed a diet containing fish product. These results indicate that A. percula larvae innately distinguish between piscivorous and nonpiscivorous fishes based on chemosensory cues in the diet. To test for an effect of piscivorous diet in nature, we constructed patch reefs that emitted scents of dietary cues in natural concentrations. Patches that emitted scent of a piscivorous diet received on average 22% less settlement than control patches or than patches that emitted scent of an herbivore or invertivore. Chemosensory detection of recent prey provides a robust cue to assess predation risk associated with a diverse range of fishes (especially during settlement) and may be reinforced through additional sensory (e.g. visual) and learned recognition of individual species consistently associated with these distinctive chemosensory cues. Ó 2012 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. Early detection and avoidance of predators greatly enhances individual survival. Consequently, a range of morphological and behavioural adaptations have evolved to help individuals identify potential predators (Blanchard & Blanchard 1989; Kats & Dill 1998; Apfelbach et al. 2005; Kindermann et al. 2009). Many taxa innately recognize potential predators (fishes: Hawkins et al. 2004; Dixson et al. 2010; Vail & McCormick 2011; crustaceans: Wahle 1992; reptiles: Amo et al. 2005; Balderas-Valdivia & Ramírez-Baustista 2005; birds: Gŏth 2004; rodents: Apfelbach et al. 2005; primates: Brown et al. 1992). This innate predator recognition is even main- tained in laboratory strains of rats and mice that have not been exposed to selection pressure from predators for several hundred generations (Blanchard & Blanchard 1990; Wallace & Rosen 2000; Yang et al. 2004; Fendt 2006). Innate recognition of potential predators is highly advantageous, particularly when organisms are young or are transitioning to new environments. However, it is unclear what cues are used to detect predation risk associated with each new species encountered, especially given the large number of species that may be encountered in highly diverse ecosystems such as tropical rainforests and coral reefs. Visual and chemosensory cues are important in the recognition of potential predators, but their relative importance appears to differ between terrestrial and aquatic environments. Although birds rely heavily on visual cues to recognize potential predators, experimental studies have shown that birds respond to subtle behavioural traits to distinguish potential predators rather than distinguishing specific species of predators. Most notably, birds respond in a consistent fashion (producing alarm calls and aggressive behaviour) to known predators and model species that mimic predators (Curio 1975; Veen et al. 2000). Chemosensory cues are also important for terrestrial prey species that can identify predator-rich areas based on territorial markings (Dickman & Doncaster 1984; Dickman 1992; Kats & Dill 1998; Stapley 2003; Labra & Niemeyer 2004; Amo et al. 2005; Apfelbach et al. 2005). Predator-naïve, laboratory-reared rats show innate chemical predator recognition by performing species-specific defence behaviours in response to urine samples of feline and canid * Correspondence: D. L. Dixson, School of Biology, Georgia Institute of Tech- nology, 310 Ferst Drive, Atlanta, GA 33035, U.S.A. E-mail addresses: danielle.dixson@gmail.com (D. L. Dixson), morgan.pratchett@ jcu.edu.au (M. S. Pratchett), philip.munday@jcu.edu.au (P. L. Munday). Contents lists available at SciVerse ScienceDirect Animal Behaviour journal homepage: www.elsevier.com/locate/anbehav 0003-3472/$38.00 Ó 2012 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.anbehav.2012.04.001 Animal Behaviour 84 (2012) 45e51