WHO DARES, WINS: THE FUNCTION AND EVOLUTION OF PREDATOR INSPECTION BEHAVIOUR IN SHOALING FISH

by TONY PITCHER (RenewableResources Assessment Group, Imperial College, Londen, UK*)

ABSTRACT

This paper examines the experimental evidence which underpins our current under- standing of inspection behaviour in fish shoals, and reviews ideas about how predator inspection behaviour could have evolved. For fish which are vulnerable to attack in the presence of a predator, inspection is critical in the recognition of danger and in the precise assessment of risk on a second-to-second time scale. Up to a threshold, inspec- tion rates increase with danger, partly because new fish in the shoal begin to inspect. Inspection appears to have a genetic basis, although experience with predators during development can fine-tune it. Inspection is evidently a risky business, as shown indirectly by attack-cone avoidance and directly by predator strikes in experiments. An appraisal of the current state of a predator is transferred from inspectors to other individuals in the group: we do not know whether such information transfer is active or passive, or whether it involves an element of manipulation. In multispecies groups, some species seem to benefit from the inspection of others. There are large individual differences in inspection, so groups probably comprise two types of individuals with differing trade-offs between risk and information. A key question is how such apparently altruistic behaviour can have evolved. Among putative functions which have been examined, inspection seems to facilitate anticipa- tion of attack, but hypotheses of attack inhibition, attack invitation, and approach conditional on danger have not been supported unequivocally by experimental results. The tit-for-tat strategy of alternating cooperation between pairs of fish is a strong candidate explanation for inspection, but frequent observations of singletons and large groups inspecting are not easily compatible with tit-for-tat. The reason for the anomaly may be that inspection is opportunistic: depending on the circumstances, inspecting individuals may choose from a range of mechanisms that mitigate risk of attack. Risk dilution (safety in numbers) operates to form large inspecting groups when perceived risk is high, and cannot be entirely ruled out as an explanation for behaviour in other sizes of shoals. Singletons may bear the costs of inspection alone in order to manipulate the rest of the group to their advantage. Through rapid serial repetition of a standard act at a rate proportional to perceived danger, inspection may itself be an easily detected, discriminated and remembered signal. Its unhurried form may reflect the evolution of deception and self-deception in shoaling fish. KEY WORDS:evolution; fish shoals; fish schools; predator inspection; tit-for-tat; risk dilution; signals; minnows; sticklebacks; antipredator behaviour.

*) current address: Fisheries Centre, 2204 Main Mall, University of British Columbia, Vancouver, British Columbia, V6T 1Z4, Canada. 372

INTRODUCTION

'Who dares wins' is the motto of the special forces who operate in danger areas behind enemy lines. Their basic function is to improve chances of military success by transmitting information about enemy movements and inferences about the intention to attack. Individual fish that perform predator inspection behaviour carry out an analo- gous function: they appear to put themselves at risk to acquire infor- mation about the predator. This information is transmitted to others and enhances the survival of other members of the shoal. Human soldiers act altruistically under military orders, reflecting a cutural trait which must date back to at least the hunter-gatherer stage in human evolution (TRIVERS, 1971; HUNTINGFORD & TURNER, 1987), and may be present in some primates (DE WAAL, 1982). Primate behaviour depends on individual recognition and is centred on the gameplays of reciprocal altruism. But in contrast, shoaling fish have not evolved such complex social behaviour. Fish must be acting under a simpler behaviour pattern which has been shaped by evolution without indi- vidual recognition. Why then do they seem to act altruistically when inspecting a predator? This paper examines the experimental evidence which underpins our current understanding of inspection behaviour, and reviews the ideas about how predator inspection behaviour could have evolved. Predator inspection behaviour has been reported from many species of fish (mosquitofish, GEORGE, 1960; sticklebacks, REIST, 1983; bluegill sunfish, G. S. HELFMAN, pers. comm.; gobies, SMITH & SMITH, 1989; cichlids, PITCHER et al., unpublished). Inspection is one of a repertoire of antipredator defences which may be employed by shoaling fish (e.g. minnows, PITCHER, 1979). Similar behaviours occur ion mammals (HIRSCH & BOLLES, 1980) and birds (KRUUK, 1976). In many early experiments such behaviour was often scored as an 'approach' (e.g. GEORGE, 1960; GILES & HUNTINGFORD, 1984). The significance of these approaches as predator inspection was first recognised in experiments in which minnows (Phoxinus phoxinus) were under attack by pike (Esox lucius) (PITCHER et al., 1986a), since when the behaviour has attracted much attention. Typically, an individual or small group leaves the shoal and swims towards the predator, pauses, turns, and returns to the shoal (see ALLAN & PITCHER, 1986), although there are minor differences in the mode and speed of performance in different species.