Cultural transmission of predator recognition in fishes: intraspecific and interspecific learning

Individuals that live in groups may have the opportunity to learn to recognize unfamiliar predators by observing the fright responses of experienced individuals in the group. In intraspecific trials, naive fathead minnows, Pimephales promelas, gave fright responses to chemical stimuli from predatory northern pike, Esox lucius, when paired with pike-experienced conspecifics but not when paired with pike-naive conspecifics. These pike-conditioned minnows retained the fright responses to pike odour when tested alone, indicating that learning had occurred, and transmitted their fright responses to pike-naive minnows in subsequent trials. Brook stickleback, Culaea inconstans, are found in mixed-species aggregations with fathead minnows and are also vulnerable to predation by northern pike. In a series of interspecific tests, pike-naive brook stickleback gave fright responses to chemical stimuli from northern pike when paired with pike-experienced minnows but not when paired with pike-naive minnows. Pike-conditioned stickleback also retained the fright responses when tested alone and subsequently also transmitted the fright responses to pike-naive minnows. Individuals may benefit from observations of the fright responses of conspecifics or heterospecifics by (1) being alerted to the immediate presence of unfamiliar predators and (2) learning to recognize unfamiliar predators as a potential threat. ? 1996 The Association for the Study of Animal Behaviour Individuals in either monospecific or mixedspecies groups may experience a number of advantages compared with solitary individuals. One advantage may be the opportunity for cultural transmission of beneficial behaviour patterns from experienced group members to younger or less experienced individuals (reviewed in Mainardi 1980; Curio 1988; Mineka & Cook 1988). Cultural transmission of information used in predator recognition has been reported for a number of species. For example, predator-naive individuals of several species of birds learn to recognize predators by observing the mobbing responses of conspecifics (jackdaws, Corvus monedula: Lorenz 1952; European blackbirds, Turdus merula: Curio et al. 1978; zebra finches, Taeniopygia guttata: Vieth et al. 1980). Cultural transmission of predator recognition has also been reported for ducks (Klopfer 1957) and for several species of primates (Herzog & Hopf 1984; review in Mineka & Cook 1988), and has been suggested for gastropod molluscs (Wood 1968; Morgan 1972). For some fishes, predator-naive individuals may be alerted to the presence of potential predators via their associations with either experienced conspecifics (Verheijen 1956; Magurran & Higham 1988) or heterospecifics (Krause 1993). The short-term consequence of such information transfer may be an increased probability of survival of the current encounter with an unfamiliar predator. There may also be long-term benefits if naive individuals become conditioned to recognize the predator as dangerous in future encounters. ‘Conditioned’ individuals may subsequently transmit the learned information to naive individuals. Only one study has reported such cultural transmission of learned fright responses for fishes. Zebra danios, Brachydanio rerio, in one tank transmitted the recognition of a synthetic chemical (morpholine) to naive conspecifics in an adjacent tank (Suboski et al. 1990). Correspondence: A. Mathis, Department of Biology, Southwest Missouri State University, Springfield, MO 65804-0095, U.S.A. D. P. Chivers and R. J. F. Smith are at the Department of Biology, University of Saskatchewan, 112 Science Place, Saskatoon, Saskatchewan S7N 5E2, Canada. 0003–3472/96/010185+17 $12.00/0 ? 1996 The Association for the Study of Animal Behaviour