reciprocal allogrooming in impala, aepyceros melampus

Anim. Behav.,1992,44,1073-1083

Reciprocal allogrooming in impala, Aepyceros melampus

B E N J A M I N L. H A R T * ~ & L Y N E T T E A. HARTS" *Department of Physiological Sciences, and t Department of Epidemiology and Preventive Medicine,

School of Veterinary Medicine, University of California, Davis, CA 95616, U.S.A. and

Department of Animal Physiology, University of Nairobi, Nairobi, Kenya

(Received 29 August 1991; initial acceptance 10 January 1992; final acceptance 12 March 1992; MS. number: A6146)

Abstract. Adult female and male impala engage in a type of allogrooming in which partners alternately deliver bouts of oral grooming to the head and neck. These grooming encounters comprise typically six to 12 tit-for-tat-like exchanges of bouts and are highly reciprocal among adult females, adult bachelor males and subadult males. Although allogrooming among females could be between related individuals, that occurring among adult males would appear to be between unrelated individuals. Unlike allogrooming reported for some primate species and other ungulates, the dominant impala received no more grooming than the subordinate. It is proposed that one function of impala allogrooming is to reduce the ectoparasite load on body areas an animal cannot reach with its own mouth. The impala reciprocal aUogrooming system is unique among free-ranging antelope and other ungulates and may be a candidate for the tit-for- tat strategy of evolved cooperation.

Allogrooming in impala (Aepyceros melampus), in which the partners alternately exchange grooming bouts, has been reported as occurring between adult females, adult bachelor males and subadult males (Hart & Hart 1988; Hart et al. 1992) and between two fawns as well as between fawns and unrelated adult females (Mooring & Hart 1992). The pattern of allogrooming, which appears to be highly reciprocal, is unique among ungulates. In impala the allogrooming occurs in a different context than that typical of other species that allogroom as adults in that it is routinely observed in loosely structured social groups. Jarman (1979) claimed that in the Serengeti there was no fixed membership in female impala groups and no evidence of social bonds between females. Murray (1981) found the estimated level of relatedness of female impala in Zimbabwe was small, ranging from 0.04 to 0' 12 among peers. Males in bachelor groups are reportedly unrelated since they disperse from their natal clans (Jarman 1979; Murray 1982). Allogrooming in primates has been studied the most extensively, and in adults is usually reported as occurring between related individuals (Sade

:~Address for correspondence: Benjamin L. Hart, Depart- ment of Physiological Sciences, School of Veterinary Medicine, University of California, Davis, CA 95616, U.S.A.

1965; Kaufmann 1967; Missakian 1974; Massey 1977; Silk 1982). When allogrooming occurs in ruminants it is also reported to be among related individuals (Newson et al. 1973; Clutton-Brock et al. 1976; Reinhardt & Reinhardt 1980). In primates allogrooming is often attributed to maintenance of social bonds, diversion of aggressive attacks (Silk 1982; de Waal & Luttrell 1986) and reinforcement of alliances (Silk 1982; Seyfarth & Cheney 1984). During an allogrooming session or encounter, grooming is often disproportionally directed to the most dominant of the pair (Seyfarth 1976, 1980; Fairbanks 1980).

The purpose of the present study was to conduct observations on the impala allogrooming system and to address the following questions. (1) How are allogrooming exchanges initiated? (2) What is the role of dominance, if any, in the distribution of grooming bouts and episodes? Although the role of dominance cannot be easily estimated by observing female herds, in bachelor herds there is a clear dominance of mature males over younger males and juveniles (Jarman 1979). Thus, the distribution of grooming in an encounter between the adult male and a subaduit male would provide information concerning whether dominance plays a role in the grooming behaviour. We were also interested in examining the degree of reciprocity of bouts and

0003-3472/92/121073+11 $08.00/0 �9 1992 The Association for the Study of Animal Behaviour 1073

1074 Animal Behaviour, 44, 6

grooming episodes exchanged with a large data base of allogrooming encounters among females and bachelor males. Because the goal was to accumulate as many observations on allogrooming encounters as possible in free-ranging wild impala, no attempt was made to identify individuals. Attempts were made, in fact, to avoid sampling the same animals more than once, except when one subject allogroomed consecutively with different partners. Obviously some questions about allogrooming interactions can only be answered by knowing individuals and their relationship to grooming partners, but the goal of this study was to formulate generalizations about impala allogrooming which might then form a basis for studies of questions requiring identification of individuals.

M E T H O D S

Impala were studied during June and July of 1986 and 1987 in the vicinities of the Masai Mara Reserve, Lake Naivasha and Lake Nakuru areas of Kenya. Observations were made from a vehicle 50--200 m away from the subjects. The technique involved observing a group of impala and when one animal approached or turned towards another, these animals were focused upon continuously until it was clear that an allogrooming encounter would or would not occur. When allogrooming occurred, the exchange was observed until it ended with one or both animals turning or walking away. For the recording system, one person observed through binoculars or a spotting scope, and one person recorded. Efforts were made to note the occurrence of any behaviour, such as putting the head down, that could be interpreted as solicitation of, or presentation for, grooming. Allogrooming, like self oral grooming, occurs in bouts of upward sweeping movements of the lower incisors or tongue against the pelage of the head or neck of the partners. The upward sweeping movements, occurring at the rate of about one per second, were called episodes. Bouts of such episodes were generally exchanged back and forth until one partner did not return a bout. An encounter was defined as an exchange of bouts from the delivery of a bout by one partner until the partners stopped exchanging bouts and engaged in non-allogrooming behaviour. The sequence of delivery of bouts, number of grooming episodes per bout and parts of the body groomed were noted. Notation was made as to whether the tongue or the lower incisors were being used when

this could be clearly seen, which was about 50% of the time. The designation of the termination of a bout was obvious when one animal stopped grooming and the partner then delivered a bout. When one partner delivered two or more bouts consecutively, the designation of a new bout was indicated by the delivery of episodes to a different part of the body (right head and left neck for example) or the engagement in a non-grooming behaviour such as visual scanning of the environ- ment between episodes. Alternatively, a pause of at least 5 s between episodes indicated a new bout. The number of animals in the group and the estimated inter-individual distance (in body lengths) were also noted when an allogrooming encounter was recorded.

Two types of impala groups were observed. Female groups consisting of females, fawns, juveniles and (usually) one territorial male, were observed for allogrooming among adult females, among fawns and between the territorial male and a female. Bachelor male groups were observed for the occurrence of allogrooming among adult males, among subadult males and between one adult male and one subadult male.

R E S U L T S

Allogrooming was observed between the following combinations of animals: two adult females, an adult female and a fawn, an adult female and the territorial male, two adult bachelor males, two bachelor subadult males, and an adult bachelor male and a subadult bachelor male. In all instances the form of the allogrooming encounters was basi- cally the same. Encounters typically started with one partner turning to an animal adjacent to it and initiating the exchange by delivering a bout of usually six to 12 grooming episodes to the partner's head or neck. On some occasions one animal walked a few metres to another animal and initiated an encounter. The recipient of the initial bout usually immediately returned a bout of episodes to the first animal's head or neck and then the first animal delivered another bout to the partner which was again immediately reciprocated, and so forth until there was an exchange of typically six to 12 bouts, or three to six bouts per partner (Fig. 1). Episodes within a bout were delivered at the rate of about one per second. No more than 5 s generally elapsed between bouts that were exchanged between partners. The longest recorded encounter

Hart & Hart: Allogrooming in impala 1075

Figure 1. A typical allogrooming sequence (a, b, c, d) showing an exchange of bouts between two adult female impala. Each photograph represents a bout of several grooming episodes.

involved two adult females and comprised 44 exchanges with one partner receiving 21 bouts and the other 23 bouts. There were several instances of allogrooming between adult females and fawns estimated to be about 1-2 months old, as well as between fawns. These allogrooming encounters were of the same reciprocal nature as allogrooming between two adult females and the fawns delivered as many bouts to the female as they received from her. Encounters involving fawns were not systematically recorded; it was usually not possible to determine a fawn's dam since nursing was seldom observed.

It was only with adult females that a sufficient number of allogrooming encounters were recorded to allow a consideration of details such as the frequency with which an animal attempted to initiate an encounter without a partner responding, proportion of times the animal initiating an encounter also gave the final bout, and the frequency with which animals gave two or more bouts sequentially (gratuitous bouts) before a partner returned a bout.

AIIogrooming in Adult Female Impala A total of 55 allogrooming encounters were

recorded between two adult females in observations on 49 groups. The mean group size of

females was 26 and the estimated mean ( _+ SE) inter- individual distance was 2.9+0.28 body lengths. Although allogrooming usually started with one animal turning to an adjacent partner, on two occasions one partner was observed walking a short distance to the partner before beginning to groom. The exchange of bouts ended when one partner walked away or simply did not return a grooming bout. Butting at the end of the encounter, as seen between males (see below), was not observed. There were three encounters where each partner delivered only one bout. In 41% of encounters which lasted for at least two exchanges, the animal that delivered the first bout also delivered the last bout. Thirteen of the 55 encounters contained at least one instance, within the encounter, of two or more bouts being delivered sequentially by one animal before the partner returned a bout. In four of these instances three or four bouts were given sequentially before the partner returned a bout. Altogether, gratuitous bouts comprised only 5 % of the 551 bouts that were observed to be exchanged.

When the number of bouts and total episodes received and delivered by one partner of a pair were plotted it became evident that the allogrooming encounters were highly reciprocal (Table I and Fig. 2). The Spearman rank correlation coefficient for bouts delivered and bouts received by the


Table I. Flow chart of grooming episodes delivered between four pairs of allogrooming females illustrating typical reciprocal encounters

Females

Pair 1 Pair 2 Pair 3 Pair 4 Bout A B A B A B A B

I 6 ~ 1 ~ 3 ~ 1 5 ~ 2 1 / 1 5 8 3 3 4 ~ 1 0 ~ / 1 2 / 1 0 4 / 8 "~.15 3 ~ 8 ~ 2 5 1 2 ~ 6 j 13 ~ ' -" 6 6 / I 0 8 ~ 1 0 ~ 1 2 7 1 6 ~ . 11 / 8 / 1 4 8"~10~ ~ 9 9 9 /

10 5 ~ 5 ~ 2 ~ 1 0 11 3 / Total episodes delivered 43 52 33 45 42 42 27 18

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Figure 2. The reciprocal nature of allogrooming between adult females as evidenced in the bouts delivered and received by one of the partners. The 45 ~ line represents ideal reciprocity. Some points are for more than one pair of animals where pairs corresponded in the bouts delivered and received.

partner who delivered the first bout was 0.93 ( t= 18"09, P<0.001). For episodes delivered and received the coefficient was 0.88 (t=13.55, P < 0.001). The animal delivering the first bout delivered a mean (+ SE) of 5'5 4- 0"72 bouts comprising 49_+ 10"67 total episodes, while receiving a mean of 4.8_ 0.73 bouts comprising 43 _+ 10.48 episodes.

Thus, the approximate number of episodes per bout delivered or received was nine. When the actual grooming activity could be observed, it was apparent that while some grooming was performed with the tongue, most grooming involved scraping the lower incisors against the direction of the hair of the recipient. This tooth scraping with the lateral


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Figure 3. Frequency histogram of number of encounters recorded as a function of the number of total bouts exchanged once an initial bout was reciprocated (N= 44).

dental comb (see Discussion) was even performed on the face of the recipient and around the eyes.

There was no clear-cut indication of atlogrooming encounters being preceded by behaviour suggestive of solicitation. Rather, allogrooming encounters were initiated by one animal starting to groom the partner. Once an encounter was underway, we observed postural movements such as lowering, raising, or turning the head to expose certain skin areas to the groomer. These postural adjustments (Fig. 1) would have been interpreted as solicitations or presentations had they occurred prior to either animal delivering the first bout.

The initiation of allogrooming by delivering rather than soliciting grooming is illustrated by our records of four occasions when a third female impala was observed to approach an allogrooming pair and begin grooming with one of the pair. In all instances the third animal delivered the first bout. This was then reciprocated by the animal which received this bout and the grooming then continued with this new set of partners. Never was any sign of threat (head butting), or other indication of agonistic behaviour, displayed by an animal which interrupted a grooming pair. On some occasions one adult female would approach another, as if to start grooming, but the two would appear to stare at each other for a few moments and then one or

the other would walk away with no allogrooming occurring.

There appeared to be a degree of social facilitation acting on the tendency to allogroom within a group, although data were not systematically collected to document this point. Several times a group of females was observed for 15-30 min with no occurrences of allogrooming and then as many as three simultaneous allogrooming encounters would occur over the next 5-15 min.

Most of the time when allogrooming was initiated by one animal, the prospective partner returned a grooming bout, however, on 10 occasions (18%) these initial bouts were not reciprocated. When the prospective partners did return bouts, the total number of bouts exchanged varied from two to 44. The probability that a subsequent bout would occur once the initial bout was reciprocated was estimated to be 0,91, excluding the few outlying encounters with 38 or more total bouts. Thus, there were progressively fewer encounters with an increasing number of bouts (Fig. 3).

Although allogrooming encounters were highly reciprocal in bouts exchanged, some were skewed in the favour of one partner in terms of episodes per bout. For example, there were seven encounters in which one partner delivered more than twice as


Figure 4. A typical allogrooming sequence (a, b, c, d) of bouts exchanged between adult male impala. Each photograph represents a bout of several grooming episodes.

many episodes as the other. The initiator in these seven non-reciprocal encounters received the most episodes in only three of the encounters, a finding that is not consistent with the concept that the most skewed encounters resulted from some sort of 'cheating' by the initiator.

On five occasions adult females were observed to allogroom with the territorial male. In all five encounters the territorial male delivered the initial bout. In two instances females did not return any bouts. Males delivered a mean of 2.5 bouts with 15.8 episodes and females delivered a mean of 1.4 bouts with 7-8 episodes. Although the data are too few for statistical testing, it is clear that males did not characteristically receive more allogrooming than the female partner.

Allogrooming in Adult Bachelor Males

A total of 23 allogrooming encounters were recorded in observations on 14 groups. The mean group size was 16 and the estimated mean (+_ sE) inter-individual distance was 6.6_+ 1.4 body lengths. It was more common for males to walk a short distance to engage in aUogrooming than for females; this was noted on 10 occasions. The pattern of allogrooming was the same as with adult females (Fig. 4), except that most encounters

(83 %) ended with the animals pressing their horns together or sparring. In no instance did the allogrooming encounters in males lead to what would be considered serious fighting. In five instances additional allogrooming followed the sparring. Serious threatening and fighting was observed occasionally among adult males in bachelor herds, but no allogrooming was ever seen in association with threatening or fighting. As with allogrooming among females, the exchange of total bouts and episodes was highly reciprocal (Fig. 5). The Spearman rank correlation coefficient for bouts delivered and received by the animal delivering the first bout was 0.94 ( t= 12.43, P<0.001), and for episodes 0.93 ( t= 11.35, P < 0-001).

The initiators of the grooming encounters delivered a mean (+SE) of 3'8_+0-74 bouts comprising 18+4.56 episodes while the partners delivered a mean of 3.4_+0.75 bouts comprising 20_+6.83 episodes. Thus, bachelor males delivered approxi- mately five episodes per bout or half that of females. However, none of the measures for males were significantly different than females (Mann- Whitney U-test). Grooming was usually with the lower incisors as in females, although licking was also observed. In four instances a male delivered an initial grooming bout without the partner reci- procating. In only two of the 19 encounters, did


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Bouts received Figure 5. The reciprocal nature of allogrooming between adult males as evidenced in the bouts delivered and received by one of the partners. The 45~ represents ideal reciprocity. Some points are for more than one pair of animals where pairs corresponded in the bouts delivered and received.

one partner receive more than twice as many grooms as the partner. As with females, there were no occasions where an animal displayed a posture suggestive of solicitation prior to the first allogrooming bout. However, such postural adjustments were made during encounters. Social facilitation seemed to play a role in allogrooming and it was common to watch a herd for 30 rain and see no allogrooming and then in a subsequent comparable period see several simultaneous encounters.

AIIogrooming in Subadult Males

Subadult male impala in bachelor herds were observed to allogroom with other subadults and with adult males. A total of 14 allogrooming encounters was observed in 14 groups where one of the partners was a subadult. The mean group size was 15 and the mean (• estimated inter- individual distance was 7.3+0-76 body lengths. The pattern of allogrooming where a subadult was involved was the same as that between adult males, and bouts delivered and received in an exchange were highly reciprocal (Fig. 6). The Spearman rank correlation coefficient for bouts delivered and received by the animal delivering the first bout was 0.97 (t=13.7, P<0.001) and for episodes 0-95

( t= 10-4, P<0.001). As with bachelor males most encounters ended with sparring or the males pressing their horns together. The animal initiating the exchange delivered a mean of 5.5___ 1-23 bouts comprising 32 ___ 8-10 episodes and received a mean of 4-7 _+ 1.23 bouts comprising 28 • 8.12 episodes. The number of episodes per bout was approxi- mately six, which was similar to adult males. There were no differences in the measures of allogrooming between the subadult males and bachelor males or females. There was one instance of a bout being delivered with no reciprocation and one instance of one partner receiving more than twice as many grooms as the partner.

There were eight of these recorded instances where, by virtue of size, we judged one partner to be dominant (see Jarman 1979). These were instances where one partner was an adult male and the other partner was a subadult, or where a subadult male had larger and more fully developed horns than its subadult partner. Allogrooming did not favour the presumably dominant animal inasmuch as the dis- tributions of grooming bouts and episodes were close to the same for both partners, and the larger animal delivered the first bout as many times as the smaller animal (Table II). We observed five instances where a larger and presumably dominant


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Figure 6. The reciprocal nature ofallogrooming between subadult males as evidenced in the bouts delivered and received by one of the partners. The 45 ~ line represents ideal reciprocity. Some points are for more than one pair of animals where pairs corresponded in bouts delivered and received.

Table II. Allogrooming behaviour in male impala where one member of pair was judged to be dominant

Delivers first bout No. bouts delivered Total episodes delivered Grooming pair Dominant Subordinate Dominant Subordinate Dominant Subordinate

1 x 9 8 85 72 2 x 8 8 45 50 3 • 18 18 188 160 4 x 3 2 30 27 5 • 2 1 7 3 6 x 2 2 7 11 7 x 0 1 0 3 8 x 4 3 10 10 Mean 0.5 0.5 5.8 5.4 46.5 42.0

male broke into an ongoing grooming exchange between a pair of subadults. The animal interrupt- ing always delivered the first bout when initiating allogrooming with one of the subadults.

D I S C U S S I O N

In impala females, bachelor males and subadult males, the basic pattern o f al logrooming was virtually identical. Two individuals would turn

towards each other or come together and exchange, in a tit-for-tat-like fashion, a number of oral- grooming bouts to the head and neck. The number of bouts and total grooming episodes exchanged between the two partners were highly reciprocal whether the exchange involved two or 42 bouts. Postural adjustments, interpreted as presenting part of the body to be groomed (lifting the head, exposing the neck or lowering the neck, exposing the top of the head), occurred after an encounter had started. Presentation or solicitation for


grooming was not seen prior to the initiation of allogrooming, and an animal seeking allogrooming delivered the first bout to the prospective partner. That the animal seeking allogrooming would deliver the first bout was particularly evident when one animal walked to another and delivered the first bout or when one animal interrupted grooming between two others and delivered a bout to one of the grooming partners, initiating a new encounter. Males more frequently than females walked a short distance to initiate a grooming encounter, perhaps reflecting the greater inter-individual distance for males, which was, on average, twice that of females. Both adult and subadult bachelor males usually ended an encounter with sparring or pressing their horns together. Allogrooming was never associated with serious fighting. This sparring was never seen in female grooming encounters. On the five occasions during which females were observed briefly allogrooming with the territorial male, these encounters were all initiated by the male, and it was the male who delivered most of the grooming episodes.

The distribution of grooming between the two partners did not appear to favour either partner, even if one was apparently dominant. Larger males delivered the first bout as often as smaller males and the number of total bouts and episodes were almost equally divided between the two partners. Since allogrooming was commonly seen among males in bachelor herds, it clearly occurs between non- related individuals. Thus, in impala, partner choice and distribution of grooming do not seem to be necessarily influenced by dominant-subordinate relationships or genetic relatedness. The impala atlogrooming pattern thus contrasts with allogrooming observations of most primate species (see Introduction) although there is at least one note- worthy exception as reported for blue monkeys, Cereopitheeus mitis stuhlmanni (Rowell 1991), which share these similarities with impala.

Observations on a population of 35 free-ranging captive impala living in a naturalistic setting at the San Diego Wild Animal Park reveal that impala fawns have an early predisposition to engage in the adult-style allogrooming behaviour. Fawns engaged in reciprocoal allogrooming with other fawns in the first week after birth. By the second week fawns allogroomed with mothers and non- mother adult females, and beyond 3 weeks after birth allogrooming encounters with non-mother adults were more frequent than with mothers. The

fawns initiated and delivered as many allogrooming encounters per hour as adults. Fawns hand- reared away from their mothers, and raised in a pen with orphan impala fawns and fawns of other species of antelope, initiated grooming with both impala fawns and heterospecific fawns. Hetero- specific fawns rarely returned grooming, but impala fawns continued to deliver grooming bouts to these heterospecific fawns (Mooring & Hart 1992).

It is likely that allogrooming in impala, like self oral grooming, functions to remove ectoparasites, especially ticks, from parts of the body the animal cannot reach with its own mouth. In cattle, Bos taurus, prevention of oral grooming has been shown to increase parasite load by at least four-fold (Snowball 1956; Bennett 1969). Prevention of grooming in cattle also allows lice to increase six- fold (Lewis et al. 1967). Cattle groom with their tongues, whereas antelope such as impala usually use an upward scraping motion with the lower incisors for both self grooming and allogrooming. In impala the lateral incisors and canine teeth comprise the lateral dental grooming apparatus, a dental modification that serves no function in grazing or browsing, but appears to be especially developed for grooming (McKenzie 1990). In older impala or with excessive grooming, there is attrition of the lateral dental elements which in turn reduces the efficiency of grooming in removing ectoparasites (McKenzie 1990). A recent exper- iment by McKenzie (unpublished), in which the dental grooming apparatus was blocked on one side by dental cement, resulted in eight times more adult ticks on the blocked than the unblocked side.

Impala inhabit woodland areas which are reported to have more ticks than the grassland areas (Londt & Whitehead 1972; Norval 1977). Impala are frequented by oxpeckers, whereas these tick birds are never seen on savanna- dwelling gazelles, Gazella grantii and G. thomsonii, topi, Damaliscus lunatus, and Coke's hartebeest, Aleelaphus buscelaphus (Hart et al. 1989). In a study of comparative self oral grooming rates among East African antelope, body size was found to be inversely related to grooming rates. However, impala were found to deliver more self oral grooming than the size-matched, plains-dwelling antelope Grant 's gazelle (Hart et al. 1992). In females allogrooming appears to deliver as much as half the grooming coverage to the head and neck that is delivered to the rest of the body by self oral


grooming. Correspondingly, scratch grooming of the head and neck in impala is significantly reduced in comparison to other antelope (Hart et al. 1992), suggesting that allogrooming reduces the need for scratch grooming.

That grooming and the removal ofectoparasites may be critical in protecting an animal's resources is emphasized by the costs of ticks in body resources. Several studies have documented that in growing calves the equivalent of one engorging tick produces a growth decrement of at least 0.6 kg on an annualized basis (Little 1963; Seebeck et al. 1971; Turner & Short 1972; Williams et al. 1978). Extrapolating this information to slender impala, just a few engorging ticks may present a substantial cost in terms of intraspecific competition among females in rearing fawns or escaping from predators, and in males in competition for territory and females (Hart 1990). The benefit of ectoparasite removal through allogrooming would appear to be gained through the modest cost to each partner of energy expended in grooming, loss of water and electrolytes from saliva expended, distraction from vigilance for predators and attrition of the lateral dental elements.

In a paper on self grooming in antelopes (Hart et al. 1992), evidence was presented that self grooming is driven by a central timing or programming mechanism much as it is in rodents (Fentress 1973, 1988). Such grooming would serve to remove ticks before they attach for feeding. Thus, even in the San Diego Wild Animal Park where ectoparasites are rare, self grooming occurs, albeit at a reduced rate in comparison with Kenya. Allogrooming also occurs at the Wild Animal Park among impala females, possibly also as a function of the hypothetical central programming mechanism.

Assuming there is a benefit to being groomed on the head and neck by another impala, and that there is some cost entailed by the groomer, impala reciprocal allogrooming may be a candidate for the TFT model of evolved cooperation among non- relatives (Axelrod & Hamilton 1981; Axelrod & Dion 1988). Originally developed as repeated simultaneous play of the prisoner's dilemma game, the rules and principles of TFT also hold for sequential play (Axelrod & Dion 1988). TFT strategy involves cooperating on the first move and then doing whatever the other player did on the preced- ing move (if partner grooms you, groom back, when it does not groom you, do not groom back).

Not only is impala allogrooming highly reciprocal in bouts delivered and received, but apparently the partner seeking grooming delivers the first bout to a prospective partner, a strategy that would reduce the likelihood of cheating. TFT and other models of cooperation imply repeated interactions between the same individuals spread out over days, weeks or months, but one could assume that one allogrooming encounter between two impala com- prises the total history of cooperative interactions between two individuals. Thus, the requirement of models of cooperation where players must be able to recognize and locate each other in the future is not necessary.

Regardless of the accuracy or inaccuracy in correctly modelling allogrooming in impala, the system would appear to be an evolutionarily stable system. The behaviour has been observed in groups of impala throughout Africa, from Kenya through the southern part of the continent, as well as in captive herds. Impala have the longest paleonto- logical tenure of all extant antelope species (Kingdon 1982; Vrba 1984). Given that the behaviour seems to have survived for millions of years, impala allogrooming may be worthy of further exploration as an example of evolved cooperation.

A C K N O W L E D G M E N T S

Financial support was provided by the University Research Expeditions Program, University of California, Berkeley. We appreciate the cooperation of the Kenyan Wildlife Conservation and Management Department in the Ministry of Tourism and Wildlife. Further assistance was provided by John Wright of Oserian and Cesare Bellingeri of Kongoni Farms.

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reciprocal allogrooming in impala, aepyceros melampus

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