Connor 1996

Anim. Behav., 1996, 51, 451–454

COMMENTARIES Partner preferences in by-product mutualisms and the case of predator inspection in fish RICHARD C. CONNOR Division of Biological Sciences & the Michigan Society of Fellows, Museum of Zoology, University of Michigan (Received 28 November 1994; initial acceptance 25 January 1995; final acceptance 7 March 1995; MS. number: -1152)

In this paper I will make two points. First, partner preferences are expected and found in by-product mutualisms (Brown 1983) where individuals vary in their ability to provide or use by-product benefits (Wrangham 1982). Second, 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 (Axelrod & Hamilton 1981). While grazing, cattle may stir up insects on which cattle egrets, Bubulcus ibis, feed (Thompson et al. 1982). The cattle egrets thus receive by-product benefits (Rothstein & Pierotti 1988) from the cattle’s foraging efforts; i.e. benefits that are a by-product of the cattle’s selfish behaviour. In the cattle–egret scenario, only the egrets receive by-product benefits. Selection may also favour associations where both parties receive by-product benefits, resulting in a by-product mutualism. For example, if both the cattle and egrets receive by-product benefits from their association (e.g. if the cattle benefit incidentally from alarm calls given by and for egrets) then the association would be a by-product mutualism. By-product mutualism was recognized by West-Eberhard (1975) as mutualism ‘maintained by ordinary selfish behavior incidentally benefiting neighbors’ (page 19). Similarly, Brown (1983) viewed by-product mutualism as involving, ‘typically behaviors that a solitary animal must do regardless of the presence or behavior of others’ Correspondence: R. C. Connor, Museum of Zoology, University of Michigan, Ann Arbor, MI 48109, U.S.A. (email: [email protected]). 0003–3472/96/020451+04 $12.00/0

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(page 30). In many cases, however, individuals may increase the by-product benefits they receive by coordinating their actions (e.g. McDonald & Potts 1994). Connor (1995) recognized a continuum of by-product mutualisms, from those involving behaviour patterns performed irrespective of the presence of other individuals, to behaviour patterns that require coordination among individuals such as the synchronous schooling movements of fish threatened by a predator (Pitcher & Parrish 1993). By-product mutualisms are common in intraand interspecific interactions. Examples include mixed- or single-species flocks, schools or herds where members enjoy reduced predation risk (e.g. Ehrlich & Ehrlich 1973; FitzGibbon 1990; Pitcher & Parrish 1993). Strangler figs (Ficus spp.) provide an unusual example. The figs grow up around a host tree, ensheathing and often killing it, leaving a hollow, freestanding strangler fig. Young strangler figs with different genotypes growing up around the same host tree may fuse, providing each individual with better structural support and possibly more light and soil resources if, by fusing, the figs hasten the demise of the host tree (Thomson et al. 1991). The benefits of by-product mutualism may come at the expense of conspecifics, as when individuals cooperate to exclude others from a food source. Wrangham (1982) pointed out that kin should be preferred partners in such ‘interference mutualisms’. Partner preferences may also be found in by-product mutualisms where the benefits are not produced at the expense of conspecifics. In ‘non-interference mutualisms’, preferences should vary in accordance with variation among individuals in their ability to produce 1996 The Association for the Study of Animal Behaviour

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by-product benefits or their ability to use them (Wrangham 1982). If choice is possible, individuals should choose associates that provide them with the greatest benefit. The optimum mutualist for one individual may not be the optimum mutualist for another. For example, hermit crabs may trade shells if both individuals obtain a better fitting shell in the exchange (Hazlett 1983, 1987). Individuals may encounter and explore the shells of a number of others before an exchange takes place (Hazlett 1987). Shell exchange is a by-product mutualism based on highly selective associations. Partner preferences may be stable in by-product mutualisms where individuals interact repeatedly. Male savanna baboons, Papio cynocephalus, solicit other males to participate in attacks on males consorting with oestrous females. The soliciting and the joining male each participate in the coalition because they have a better chance of acquiring the female if they act in concert than if they act alone (Bercovitch 1988; Noë 1992). However, coalitions are not formed at random from among the available males. Middle-ranking males often form coalitions with the same middleranking partners (Noë 1986), possibly selecting on the basis of their fighting ability (Noë 1994). Milinski (1987) argued for Tit-for-Tat reciprocity between sticklebacks engaged in predator inspection. I follow others (e.g. Lazarus & Metcalfe 1990; Masters & Waite 1990; Reboreda & Kacelnik 1990; Turner & Robinson 1992) in suggesting that cooperative predator inspection is a by-product mutualism that can be fully described without reference to the Prisoner’s Dilemma. However, describing the alternative as simply the ‘shoaling’, ‘proximity seeking’ or ‘safety in numbers’ hypothesis (e.g. Milinski 1990, 1992; Dugatkin 1991; Dugatkin & Alfieri 1991a; Huntingford et al. 1994) is incomplete. If fish benefit from predator inspection, an alternative model must include predator inspection and shoaling, as well as the tension between these often opposing tendencies (see also Dugatkin 1988, 1991; Lazarus & Metcalfe 1990; Turner & Robinson 1992). Consider two inspecting fish that leave the shoal to approach a predator together, one taking the lead before stopping. The following fish may then decide to seek more information about the predator and move forward to a point past the lead fish until the shoaling response causes it to slow or

stop. The stopping point may reflect a compromise between the inspecting motive, which favours moving forward, and the shoaling response, which favours retreat. The other fish may then decide that it needs more information and moves forward; again to a point in front of the other fish where tension between the shoaling and inspecting responses brings it to a halt. In this simple model, two fish, making separate but selfish decisions regarding the benefits of shoaling versus further inspection, can leap-frog towards a predator. Milinski (1987), Milinski et al. (1990a, b) and Dugatkin (1991) claimed that such a pair of inspecting fish are in a Prisoner’s Dilemma, because when one fish moves forward beyond the other, the fish behind obtains the benefit without paying the cost. It is not clear, however, how much benefit the trailing fish obtains (Murphy & Pitcher 1991). At any rate, in many by-product mutualisms, the mutualistic behaviour patterns are performed asynchronously, so at different times individuals perform costly acts that benefit not only themselves but also other individuals nearby (Connor, 1995). Unable to provide unequivocal evidence for a Prisoner’s Dilemma or to reject shoaling hypotheses conclusively in favour of Tit for Tat, various authors have argued that consistent patterns of partner preference support the hypothesis that the dynamics of joint predator inspection are governed by Tit for Tat (Milinski et al. 1990a, b; Dugatkin 1991; see also Huntingford et al. 1994). This conclusion implicitly assumes that partner preferences are not expected in by-product mutualisms. As I have argued above, theory predicts and data indicate that such preferences exist. For partner preferences to occur in predator inspection, it is only necessary that individuals vary in either their shoaling or inspecting response and that other fish can respond to this variability. Variation in either trait will produce individuals that vary in their ‘stopping’ point, the point where the perceived costs and benefits of advancing are equal. We can imagine a continuum from cautious to bold fish (for a review of this phenomenon, see Wilson et al. 1994). Murphy & Pitcher (1991) found consistent differences in the behaviour of individual minnows, Phoxinus phoxinus. ‘Bold’ minnows were among the first to enter a feeding tank, and inspected predators frequently. At the other extreme were more cautious individuals who were the last to enter the feeding tank and

Commentaries inspected less often. Partner preference in the by-product mutualism model requires that individuals recognize whether other individuals are bold or cautious, but it is also compatible with individual recognition. If we include partner preference in the by-product mutualism model presented above, we can account for any of the behaviour patterns reported thus far, including cases in which one fish tends to follow the other (Huntingford et al. 1994), the tendency for a lead fish to turn back more often than a trailing fish, or for a lead fish that has turned back to be the second to swim forward again compared to a trailing fish that has turned back (Dugatkin 1991). In the latter case, for example, if a lead fish has acquired more information about the predator than the trailing fish, then it is not surprising that the trailing fish is the next to move forward. Below I reconsider the patterns of partner preferences in predator inspection that have been offered as support for Tit for Tat. I substitute the terms ‘bold’ and ‘cautious’ where the authors used ‘cooperative’ and ‘non-cooperative’. Consistent Pair Formation during Predator Inspection Milinski et al. (1990b) found a weak trend for pairs of fish from groups of four to be each other’s nearest neighbour during predator inspection. They suggest that similar cost/benefit ratios for predator inspection may be the basis upon which pairs are formed. This hypothesis is consistent with the by-product mutualism model. Preference for Previously Cooperative Individuals It is easy to predict a priori that bold fish will prefer to inspect with bold fish. The situation is less clear for cautious fish; another cautious fish might make a better shoaling partner, but it may also be advantageous to have a bold fish as an inspecting partner. Dugatkin & Alfieri (1991b) experimentally demonstrated a preference in guppies to swim nearer to a bold guppy that had previously remained closer (on average) to a predator during inspection than to a cautious guppy that had remained further back. Their result is consistent with the by-product mutualism model in which individuals prefer to associate with bold guppies.

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More Cooperation with a Defecting Partner that had Previously Cooperated Milinski et al. (1990a) claimed to demonstrate ‘trust’ between ‘cooperating’ fish. If a fish that previously cooperated was made to defect (by having it vanish behind an opaque partition) the test fish swam further towards the predator than it did on a run with a fish that had defected the first time. Trust makes more sense in the by-product mutualism model where the fish are not in a Prisoner’s Dilemma and cheating is not profitable. If ‘boldness’ is a consistent individual trait and a fish had determined that another fish was bold before, then it could ‘trust’ it to be bold during subsequent inspections. A fish playing Tit for Tat should be more careful. In conclusion, partner preferences are expected in by-product mutualisms when individuals vary in the amount of by-product benefits they produce, and when individuals vary in their ability to use by-product benefits from particular individuals. Evidence of partner preferences alone cannot be used as evidence for cooperative strategies based on the Prisoner’s Dilemma. I thank C. Ray Chandler, Paul W. Sherman and three anonymous referees for helpful comments.

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