By-product mutualism, Tit-for-Tat reciprocity and cooperative predator inspection: a reply to Connor

When a shoal of small fish is at risk of being attacked by a pike, an individual or a small group of fish may leave the safety of the shoal and approach the predator to inspect it to obtain information about the pending risk (Magurran et al. 1985; Pitcher 1992). A pair of fish that jointly carries out a predator inspection visit is probably in a Prisoner’s Dilemma (Milinski 1987, 1990, 1992). Both fish share the risk of being eaten. As one fish proceeds, however, it must rely on the other one’s following, although this other fish may be tempted to rush back and watch the leading fish’s fate from a safe distance. Assuming a Prisoner’s Dilemma, I have interpreted my experimental results with sticklebacks, Gasterosteus aculeatus (Milinski 1987), as evidence for a Titfor-Tat-like cooperation strategy that is based on reciprocity (Axelrod & Hamilton 1981; Nowak & Sigmund 1992). This interpretation was corroborated by further experiments and observations both with sticklebacks (Milinski et al. 1990a, b; Külling & Milinski 1992; Huntingford et al. 1994) and guppies, Poecilia reticulata (Dugatkin 1988, 1991; Dugatkin & Alfieri 1991a, b). A challenging alternative interpretation has been proposed by Connor (1996): ‘a model of by-product mutualism that includes partner preferences can account for all those phenomena during predator inspection in fish that have previously been attributed to a cooperative strategy, Tit for Tat, based on the Prisoner’s Dilemma’ (page 451). West-Eberhard (1975) defined byproduct mutualism as mutualism that is maintained by ordinary selfish behaviour incidentally benefiting neighbours. Individuals may increase the by-product benefits they receive by coordinating their actions (Connor 1996), for example, by jointly inspecting a predator. How can we test which hypothesis better explains the results? Theoretically, this is easily done because the two hypotheses are mutually exclusive. By-product mutualism is not feasible if the inspecting fish are in a Prisoner’s Dilemma, whereas Tit-for-Tat reciprocity does not make sense outside a Prisoner’s Dilemma. Connor (1996) is right when he says that unequivocal evidence has not been provided for the Prisoner’s Dilemma in this situation. I have always argued that a Prisoner’s Dilemma is possible in predator inspection and that there is some evidence for it (Milinski 1987, 1990, 1992), such as the two following facts. (1) Usually small groups or single fish inspect the predator (e.g. Magurran 1990; Pitcher 1992), although joining an inspector or a group should become increasingly attractive with each additional inspector because of the risk dilution (‘safety in numbers’) and the confusion effect. This observation seems to fit the Prisoner’s Dilemma paradigm, because Tit-for-Tat cooperation in an iterated Prisoner’s Dilemma is only stable in small groups, especially in pairs (Boyd & Richerson 1988). (2) In a Prisoner’s Dilemma, the highest payoff is gained by an individual that defects when the partner cooperates. Does a fish that avoids the risk and stays behind obtain enough information to have a higher net benefit (i.e. the fitness increase from information gained minus the fitness reduction from potential risk) than the fish that proceeds on its own? Supporting evidence is provided by experimental studies with minnows, Phoxinus phoxinus (Pitcher et al. 1986; Magurran & Higham 1988). Thus, it seems more likely than not that the Prisoner’s Dilemma is fulfilled. It is a Correspondence: M. Milinski, Abteilung Verhaltensökologie, Zoologisches Institut, Universität Bern, CH-3032 Hinterkappelen, Switzerland (email: milinski@esh.unibe.ch).