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Food exchange strategies in an infant chimpanzee
Louis Lefebvre* Department of Biology, McGill University, Montrgal, Qugbec, Canada
Received 29 January 1981 and accepted 1 September 1981 Keywords: chimpanzee, food
exchange, food sharing.
Food Exchange Strategies in an Infant Chimpanzee There is anecdotal evidence that exchange can be used by chimpanzees in food-sharing interactions. This research examines the foodexchange strategies of a four-year old nursery-raised female chimpanzee. When food type is varied, the chimpanzee's behavior is flexible and depends on the value of each food type offered and requested in the exchange. When only the most preferred food type is involved, the chimpanzee uses a single behavior, offering only a piece of the food it is given first; this strategy reaches an optimal level after a few sessions, when the smallest permissible amount of food is offered in exchange by the chimpanzee. Chimpanzees thus have the cognitive capacities for qualitatively adaptive and quantitatively optimal resource exchange; why these capacities are not used in the wild is discussed as a function of hypotheses bearing on foraging patterns and socialstructure. 1. I n t r o d u c t i o n
Food-sharing in chimpanzees has been well studied both in the field (Goodall, 1968; Teleki, 1973; McGrew, 1975 ; Silk, 1978) and in captivity (Silk, 1979). A m o n g adult chimpanzees, sharing ks infrequent.and seems to be restricted to animal prey; mothers, however, often share a large variety of plant foods with their infants (Goodall, 1968; Silk, 1978). When analysed in the light of recent theories on the evolution of behavior, sharing of plant foods seems to follow general predictions based on the principles 0fkin selection, parent-offspring conflict and optimal foraging: it occurs mostly between mothers and their infants, maternal resistance increases as the infant becomes older and the types Of food solicited and shared are most often those that are difficult to procure or process (Silk, 1978, 1979). Soliciting by an infant is usually done by begging gestures and whimpering, although it m a y sometimes be reduced to outright snatching. Begging and snatching are. not the only Ways to obtain food, however: Nissen & Crawford (1936), Elder (1977), Silk (1979) and Premack (1976) give anecdotal evidence of food-sharing that involves e x c h a n g e . In Premack's example, a caged female offered monkey chow in soliciting coffee from a h u m a n visitor; Premack calls the offer a "spontaneous invention". I n Silk's example, a juvenile relinquished possession of a lock an adult was trying to obtain from it when the adult shared food with the juvenile. I f sharing does occur on a Significant basis through exchange, this could have important evolutionary repercussions, since it makes selection of sharing by reciprocal altruism more likely (Trivers, 1971). O n a cognitive level, this behavior is of great interest in comparing chimpanzees and humans; intelligent resource exchange has usually been thought of as a strictly h u m a n phenomenon. T h e present study focuses on quantitative aspects of food exchange in a nursery-raised infant chimpanzee. T h e study was devised following a spontaneous occurrence of exchange witnessed by the author. Sophie, an infant female aged about two years at the time, offered a piece of apple when whimpering and begging for yoghurt proved unsuccessful; this was done by bringing the a p p l e directly into contact with the observer's mouth. This behavior was seen only once at the time and was not repeated by the chimpanzee when prompted to do so. I t is not claimed that the incident was anything more than accidental at the time. W h e n the present study was initiated, however, almost two years after the spontaneous occurrence of exchange, the chimpanzee showed complete mastery of the rusk in the first trials. A detailed analysis of exchange could thus be started, to see Journal of Human Evolution (1982) 11, 195-204
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what behavioral strategies an infant chimpanzee would use in food exchange (Experiment 1) and if and how these strategies represented optimal quantitative solutions to the exchange problem (Experiment 2). 2. G e n e r a l P r o c e d u r e
Procedures common to both experiments will first be described. The subject of the study, Sophie, was aged 47 months at the start of the experiments and 51 months at the end. She was received a week after birth from the Institute for Primate Studies in Norman, Oklahoma and housed in nursery conditions at the Laboratoire de Psychologic Compar& of the Universitfi de Montr6al. Housed with her from reception was her half-brother, Spock, born within a week of Sophie; both were given stable substitute h u m a n mothers for 189 years, after which care was given by a rotating staff of keepers and students. Although it is impossible to be certain of the degree of direct or indirect experience with exchange tasks the chimpanzee had before the study, no instances of food exchange as such were recorded except the one described above. Exchange not involving food return by the chimpanzee was used to some extent by caretakers for dealing with aspects of feeding or cleaning up; typical examples of this are the chimp's bringing back a drinking cup to the caretaker in order to obtain more juice or giving back a play object in exchange for food. No claim is made here that the present experiments represent Sophie's first contact with exchange of any type; what can be stated with some certainty, however, is that there is no reason to believe that quantitative aspects of the experiments described below were affected by indirect prior experience. All experiments were done with Sophie and the experimenter alone in a room of the Laboratoire; during some sessions of Experiment 1, note-taking and, in some instances, exchanging itself was done by a student (D.P.). The procedure common to Experiments 1 and 2 involved: (1) sitting down face to face with Sophie; (2) showing her the items involved in the exchange by holding them up in each hand simultaneously; (3) giving her the first item, with random variation of the hand used for offering; (4) holding out the empty hand while showing the second food item and saying the Quebec slang equivalent of "will you give me a n y ? " ; (5) giving her the second item if any part, however small, of the first item was given back or (6) not giving the second item if no food was returned.
Experiment 1 The first experiment was designed to see how the chimpanzee's behavior varied according to what food items were offered and requested in an exchange. Procedure. Three food types were used: commercial monkey chow, small pieces of apple (1/16 of one apple) and squares of sweet biscuit (approx. 3 • 3 • 1 cm). Choice experiments showed that the biscuit was always preferred to the apple and the appl e to the monkey chow; although this latter food type seemed to hold little attraction in the context of the experiment, it was readily eaten by Sophie as a staple food. The three food items were presented in all possible nine combinations of first given-second offered, each paired
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presentation occurring at r a n d o m in the experimental session. Seven sessions of three nine-trial series were given over 16 days. Results. Five types of behavior were observed: (A) no exchange, in which Sophie took the item given first and gave nothing back, usually movifig away from the experimenter in the process, with occasional threat behavior; (B) immediate exchange, in which the chimpanzee took the first item and gave it back untouched to obtain and eat the second item offered; (C) double exchange, in which Sophie took the first item, gave it back uneaten, took the second item and also gave that one back uneaten; (D) giving back a piece, however small, of the first item taken and eating the second item obtained; (E) exchange gesture, in which Sophie gave back saliva or touched her lips to the experimenter's empty hand without giving back any food, a behavior which disappeared after the first two sessions for lack of reinforcement Category (E) does not seem to represent an error caused by incomplete learning of the exchange rules; it appeared after the chimpanzee clearly shov)ed it understood the task and w a s accompanied by very alert looking at the experimenter's face, which probably served to obtain cues about the strategy's chances to Succeed. Behaviors (A) to (E) represent an exhaustive sample of the acts observed in t h e e x p e r i m e n t . By classifying these behaviors on a rough ordinal scale, it is possible to summarize the results as shown in Table 1. Behaviors resulting in a return of the complete item were given a score of 2, behaviors resulting in the return of a piece of the item first given were assigned a score of 1 and behaviors resulting in no food return at all were given a score of 0; since 21 trials were given for each paired wesentation, the m a x i m u m amount of the first item Table 1
Amount of food given back as a function of the type of food offered (Rough ordinal scale)
Type of food offered Monkey Chow Apple Biscuit Total (without diagonal)
Type of food given back Monkey chow Apple
Biscuit
Total (without diagonal) 11 56 61
(11 ) 42 42
11 (21 ) 19
0 14 (16)
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given back for any given cell of the matrix in Table 1 is 42. This value is reached when the monkey chow is gi~zen first ~ind requested back for either the apple or the biscuit. Since double exchange 0ccurfed or/ly when monkey chow was given first and also offered second and Was impossible t o distinguish quantitatively from immediate exchange, the marginal totals o f Table: I: d o n6t include the diagonal values involving identical items within a
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pair. These marginal totals can be interpreted as average values given to each food item by the chimpanzee, either as first item given back or second item desired, over all other food types it is paired with. Thus, the marginal totals for columns represent the value of the food types as items to be given back, with the monkey chow being given back six times as readily as the biscuit (84 to 14). The row totals measure the attractiveness of the food types as second items offered, with the monkey chow appearing five times less attractive than the apple (11 to 56) or the biscuit (11 to 61). These proportions can serve as indicators of the tendency to give back an item when first offered and of the attractiveness of the second item. Thus, the tendency to give back the monkey chow, the apple and the biscuit can respectively be estimated as proportions of 6 : 2 : 1 ; conversely, the attractiveness of these same items varies in proportions of 1 : 5 : 5, with apple and biscuit being approximately equal to the latter value. This scale of proportions can be used to express each trial in terms of subjective value for the chimpanzee. For example, a trial where monkey chow is given first and biscuit offered second represents a tendency to give back the first item estimated at 6 and a desire for the second item at 5; a trial in which apple is given first and monkey chow offered second represents a tendency to give back of 2 and a desire to obtain the second item of 1. Since each trial can be given two values of this type, each behavior can be expressed in a two-dimensional space defined by co-ordinates consisting of the mean values on the scale o f the trials in which it appears. I f double exchange is seen only in trials involving monkey chow/monkey chow, its position on the graph is (6,1), respectively the values for giving back this item and its attractiveness as second item. I f giving back only a piece of the first item occurs in trials consisting of apple/biscuit and biscuit/apple, then the position o f this behavior is defined by an average of trials estimated at (2,5) and (1,5). Intuitively, one would expect that trials in which the tendency to give back the first item and the attractiveness of the second item are both low should result in no exchange. It could also be predicted that trials in which tendency to give back and attractiveness of the second item are both high should result in immediate exchange. Figure 1 shows how Figure 1. Strategy space of the chimpanzee, in terms of value given to the food items when given first and requested back (tendency to give back) and when offered second (attractiveness). Abcissa and ordinate are in rough proportional scale as determined in Table 1. (B) biscuit; (A) apple; (M) monkey chow.
6 '"~5
Immediate exchange Piece
~
4 Exchange gesture
2 9 No exchange
(M)I I 1 (B)
[ 2 (A)
I 5
Double exchange 9 I 4
I 5
I 6 (M)
Tendency to give
these obvious (and other, less obvious) cases are positioned in the chimpanzee's strategy space. Immediate exchange and no exchange fall on the predicted extremes, while exchange gestures and giving back a piece are of intermediate value. The two-dimensional space is thus a convenient way of expressing behavioral alternatives on a scale of subjective value for food types as items to be given back or items desired in exchange; this approach
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could also serve to predict the behavioral outcome of trials involving food types other t h a n the ones used here, whose value for the chimpanzee could be estimated in relation tO known food types. Experiment 2 This experiment focuses on one of the behaviors seen in the previous experiment and examines how it changes with time. The behavior chosen is that of giving back only a piece of the first item offered, which was seen in cases where the tendency tO give back is relatively low and the attractiveness of the second item is relatively high. Procedure. In this experiment, food type was held constant (sweet biscuit only). Six sessions of ten trials each were given over 25 days. In all of the sessions, five small pieces of biscuit (approx. 1 • 1 • 0"5 cm) were given first and then requested back while a single, large piece of biscuit (approx. 4 • 4 • 1 cm, e.g. more than the five small pieces put together) was offered in exchange. The amount of small pieces given back was quantified in the following way: each uneaten small piece was counted as one item returned, while partially eaten small pieces were given values of 89188or ~t according to the size of the piece involved; /t or 0.125 was the smallest value possible and covered pieces as small as the chimpanzee could bite off and return, usually by spitting out the piece onto the experimenter's hand. Results. As quantified above, the mean amount of biscuit given back over the six sessions (with all trials averaged) and over the ten trials (with all sessions averaged) is shown in Figure 2 (a) and (b). In both cases, this amount is seen to decrease over time. Since the data in Figure 2 (a) can be interpreted either in terms of a negative linear trend or as a set of two distinct response phases (sessions 1 to 3 and sessions 4 to 6), the trial data are split up into two halves and plotted separately in Figure 2(c). Both curves show that the Figure 2. A m o u n t of food given back as a f u n c t i o n of: (a) session n u m b e r a v e r a g e d over all trials; (b) trial n u m b e r a v e r a g e d over sessions; (c) trial n u m b e r a v e r a g e d over sessions 1 to 3 ((2)) a n d sessions 4 to 6 ( [ ] ) . Sessions a
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chimpanzee reaches an asymptote around trial 3, while the amount given back on trial 1 of the first three sessions is much larger. In the last three sessions, a larger amount of biscuit is also given back on trial 1, even if this is much less than what is given back in the initial sessions. Trial 1 can thus be considered a sampling trial even in later sessions, where the chimpanzee checks to see if the exchange rules are still the same as before; once this has been verified, the chimpanzee adopts the optimal strategy of giving back as little as possible (~ to ~ of a piece). A control session consisting of five trials was given on the day after session 6, with the same exchange rules but run by a different experimenter in a different locale (on the grass outside the laboratory) and using a different container for the biscuits. In this situation, the average amount of pieces given back over the five trials returned to the same value it had at the start of the three first sessions, i.e. approximately three whole pieces (range 2"5 to 4.5). The change in context, though it involved no modification of the exchange rules (and this was understood by Sophie, judging from the very small latency of giving back in these trials), thus led to the adoption of a more conservative strategy, such as that employed on the sampling trial of the initial sessions. Sophie's behavior gave every indication that her change in strategy was not caused by a lack of comprehension of the task, but by factors related to the change in experimental conditions. 3. D i s c u s s i o n
The results obtained in this study and since confirmed on three other chimpanzees (Lefebvre & Hewitt, in preparation) can be summarized in four points: (1) a four-year-old chimpanzee can withhold immediate consumption of highly valued food and give part of it back to obtain another food item; (2) this behavior is systematic and adapted to the value of the foods involved in the exchange; (3) one of the behaviors used by the chimpanzee, giving back a piece of the first item, becomes optimal after a few sessions; (4) use of this strategy becomes more conservative if experimental conditions are changed in the direction of an increased uncertainty of outcome. Seen from the point of view of feeding behavior, these results confirm broad predictions of optimal foraging theory (Krebs, 1978). In Experiment 2, food gain is maximized when the chimpanzee gives back as little as possible, as it does from session 4 on. In sessions 1 to 3, the amount of food returned decreases progressively, as if the chimpanzee was testing in small decremental steps how little it can give back and still get the second item. This is somewhat analogous to the sampling behavior known to occur in birds (Krebs et al., 1978), where the animal forgoes instantaneous maximization of food intake in order to gain information about the situation. The sampling involved here applies both to alternative strategies and to the amount of food given back. In the first sessions, the chimpanzee may be sampling exchange rules by giving back saliva and going through the motions of food return; this is no accidental clumsiness, since such errors cease to occur when they are not reinforced. Itis also conceivable that this behavior represents a form of cheating, where the animal attempts to benefit by violating the rules. The term "cheating" need not imply conscious planning, as it is often used in a purely evolutionary sense (Dawkins & Krebs, 1978); it is hard, however, not to postulate some kind of knowledge by the chimpanzee
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that giving back saliva is of less value and less likely to be successful than giving back a piece of actual food. The method used in Figure 1 to express the relationship between behavioral outcome and the value of the food types given and offered requires some explanation. It is a variant of McFarland & Sibly's (1972) "state space" approach, where the factors determining a behavioral outcome are plotted as axes in an n-dimensional space. Any tendency (MeFarland & Sibly deal with motivation) or behavioral decision (as in the present case) that depends on multiple factors can be expressed as a point in this n-dimensional space. Since the chimpanzee's behavior depends on only two factors, the data from Experiment 1 can be easily visualized in the two-dimensional space of Figure 1. However, the method could be generalized to include more factors, such as the animal's position in relation to that of the exchange partner in the dominance hierarchy, if this factor were investigated in future experiments. The "state space" method could prove very useful in the study of multi-determined decision making. Seen from the point of view of intelligent behavior, the results indicate that a four-yearold chimpanzee can make "more!' and "less" value judgements and use these in a social interaction. This implies both social and non-social intelligence. Although Sophie could understand numerical concepts without spatial cues at the time of the experiment (Smilga & Mathieu, unpublished), the situation studied here did not require such advanced capacities. In experiment 2, Sophie could rely on the fact that three small pieces of biscuit took up more surface and volume than a single small piece; numerical judgements of a non-perceptual nature may well have been used, but it is impossible to be sure of this for lack of adequate controls. The possible presence of cheating and the flexibility in the strategies used attest to the high level of social intelligence shown by the chimpanzee. One of the pressures that may have oriented the evolution of intelligence in apes and hominids is the advantages an individual can gain in being able to predict social outcomes and manipulate the behavior of other individuals for its own benefit (Humphrey, 1976). The behavior shown by Sophie is highly attuned to the probabilities of social outcome, as shown especially b y the changes in amount given back produced by a modification of exchange conditions: increased uncertainty of outcome in session 7 leads to a return to early levels of amount given back, where a higher uncertainty of outcome was also present. Food exchange can thus be added to the growing list of sophisticated abilities great apes show in captivity but do not use in the wild. This list includes tool use in gorillas and orang-utans (Parker & Gibson, 1979), symbolic communication (Gardner & Gardner, !969) and symbolic request and cooperative usage of tools (Savage-Rumbaugh et al., 1979) in chimpanzees. Although some elements of iconic gestural communication are known to occur in wild chimpanzees and gorillas (Chevalier-Skolnikoff, 1979), the magnitude of the discrepancy between competence and performance remains puzzling: why aren't these abilities used if they are available? In some cases, what seems to be missing are the social and ecological conditions necessary for the occurrence in the wild of abilities seen in captivity, even though the cognitive prerequisites for them are present. A close examination of the literature on chimpanzee feeding ecology suggests, however, that this explanation may not be adequate to account for the absence of reported food exchange in wild chimpanzees. Four sets of conditions are necessary for the occurrence of food exchange: (1) that individuals need different food types; (2) that different individuals actually control access to different food types, so that one cannot simply take what one needs without interacting
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with others; (3) that individuals possess the cognitive elements necessary for understanding exchange and (4) that conditions favoring the evolution of reciprocal sharing exist in those species. These four conditions appear to apply to P. troglodytes. Chimpanzees need a variety of food types to assure a balanced diet, given the nutrient content of the food types they eat (Hladik, 1977). In an average day, 14.6 different food types are eaten in the Combe population (Wrangham, 1977) and 20-0 in the Ipassa, Gabon, population (Hladik, 1977). Although different groups of food types show different daily feeding peaks, there is a significant overlap in the time at which these foods are eaten. Different food types can be eaten in the same meal. They are sometimes combined simultaneously, in meat and foliage wads for example (Goodall, 1968; Teleki, 1973). Although evidence for consistent individual differences in diet, food preference and specific hungers is scarce in the wild (i.e. only Hugo ate more plant foods than others in Wrangham's 1977 study), individual differences are clearly seen in captivity. Restricted access to different food types also applies to chimpanzees. Individuals forage in subgroups, which can be split up or reformed for, during or after feeding (Goodall, 1968; Wrangham, 1977). Although individuals in a subgroup usually feed on the same food type, it is "not uncommon" (Goodall, 1968) for them to feed on different foods. Chimpanzees compete for feeding sites and may exclude others from these sites (Wrangham, 1977). Individuals feeding intensively at a site may deplete it, so that others visiting the site a day later will obtain a significantly reduced amount of food (Wrangham, 1977). Restricted access to a food item and the need to get a piece of the item immediately because of rapid depletion is even more dramatic in the case of animal prey (Teleki, 1973). Individuals foraging separately may meet at common feeding locations either by chance, by convergence on known food sites or by attraction to a site in response to the vocalizations of others (Goodall, 1968; Teleki, 1973; Wrangham, 1977). Although it is not extensive, food transport does occur even over relatively long distances (one-half mile, Goodall, 1968). Transport is done with or in the mouth (including half-chewed wads kept for relatively long periods), in the hands, around the neck or in the angle of the thigh and hip, and it occurs with both animal and vegetable foods. The cognitive elements necessary for exchange are present in wild populations. Chimpanzees can communicate their desire for food controlled by another individual; begging is well known and has a success rate of approximately 50 % (Nishida, 1970; Teleki, 1973; in capitivity, Nissen & Crawford, 1936). A chimpanzee can also withhold consumption of a highly valued food and voluntarily offer a piece of it to another individual (Teleki, 1973) ; such active sharing is less frequent than tolerated scrounging, but is nevertheless significant. The readiness to share a food item, whether actively or passively is partly a function of the value of that item (Nishida, 1970; in captivity, Nissen & Crawford, 1936). Since olive baboons are known to be able to evaluate each other as reciprocators (Packer, 1977), we can easily assume that chimpanzees are also capable of this. Food exchange can be seen as a form of immediate reciprocal altruism. Chimpanzees have all of the characteristics considered by Trivers (1971) to favor the evolution of reciprocity: a long lifespan, repeated occasions to interact, a strong degree of mutual interdependence, a sufficient mnemonic capacity and discriminative ability to remember and identify acts and individuals. The dominance hierarchy of chimpanzees is not of the type where food can be preempted by a dominant at all times (Trivers, 1971; Goodall, 1968); even high ranking males have to beg for meat once others control a piece of carcass
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(Teleki, 1973). Reciprocity is known to exist in aggressive coalitions and to contribute to status (Riss & Goodall, 1977; de Waal, 1978). If the potential initial disadvantage of non-reciprocated altruism needs to be compensated by the advantage of kin-selected altruism for reciprocity to evolve (Rothstein, 1980), the high incidence of sharing within kin groups shows that chimpanzees have this prerequisite to pure reciprocity (McGrew, 1975; Silk, 1978). In any case, some sharing of meat among adult P. troglodytes appears to be kin-independent (Teleki, 1973). I f these social, ecological, cognitive and evolutionary conditions for the appearance of food exchange appear to be sufficient, they underline the fact that some of the factors thought to be responsible for the evolution of exchange in hominids m a y not be strictly necessary. Differences in individual foraging patterns need not have been compartmentalized along age and sex class lines. The ability to construct food transport tools and the daily or periodic meeting and concentration at a "base camp" (Isaac, 1976; 1978) also do not appear to be necessary conditions, although they might very well have favored exchange. The same reasoning applies to cooperative hunting of large animal prey (Teleki, 1975). Logically sufficient conditions do not make a phenomenon appear. Each of the factors outlined above may represent a real but infrequent event, so that the combined probability of these conditions working together may be extremely low. In addition, the selective advantage of that very rare occurrence may be slight in relation to alternatives. Finally, chimpanzee social interactions may be too tense for exchange of valued resources to be stable, in the sense that the frequent recourse to physical aggression may interfere with mutually beneficial sharing. We can nevertheless conclude that the cognitive capacity for exchange is not restricted to man and that any future reports &isolated cases of exchange in wild chimpanzees should not really come as a total surprise.
I am grateful to Mireille Mathieu for the opportunity to work at the Laboratoire de Psychologic compar4e, to Diane P4russe and Jean-Marie Bonnet for their help with the experiments, to Don Kramer and Dominique Spahn for comments on the manuscript and to Bernard Chapais for suggestions concerning the discussion.
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Krebs, J. (1978). Optimal fol*aging: decision rules for predators. In (J. Krebs & N. B. Davies, Eds) Behavioural Ecology: an Evolutionary Approach, pp. 23-63. Oxford: Blackwell. Krebs, J., Kacelnik, A. & Taylor, P. J. (1978). Test of optimal sampling by foraging great tits. Nature (London) 275, 27-31. McFarland, D . J . & Sibly, R. (1972). "Unitary drives" revisited. Animal Behaviour 20~ 548-564. McGrew, W. C. (1975). Patterns of plant food sharing in wild chimpanzees. In (S. Kondo, M. Kawai & A . Ehara, Eds) Contemporary Primatology, pp. 304-309. Basel: Larger. Nishida, T. (1970). Social behaviour and relationship among wild chimpanzees of the 1VIahali lklountains. Primates I1~ 47-87. Nissen, H. W. & Crawford, M. P. (1936). A preliminary study of food-sharing behavior in young chimpanzees. Journal of Comparative Psychology22~ 383-419. Packer, C. (1977). Reciprocal altruism in Papio anubis. Nature 265, 441-443. Parker, S. Taylor & Gibson , K. R. (1979). A developmental model for the evolution of language and intelligence in ear!y hominids. Behavioral and Brain Sciences 2, 367-408. Premaek, D: (1976). Language and intelligence in ape and man. American Scientist 64, 674-683, Riss, D. & Goodall, J. (1977). The recent rise to tile alpha rank in a population of free-living chimpanzees. Folia Primatologlca 27~ 134-151. Rothstein, S. I. (1980). Reciprocal altruism and kin selection are not cleariy separable phenomena. Journal of Theoretical Biology 87, 255-262. Savage-Rumbaugh, S., Boysen, S.: & Rumbaugh, D. (1979). Linguistically-mediated tool use and exchange by chimpanzees (Pan troglodytes). Behavioral and Brain Sciences 4, 539-554. Silk, J. B. (1978). Patterns of food-sharing among mother and infant chimpanzees at Gombe National Park, Tanzania. Folia Primatologica 29, 129-141. Silk, J i B; (1979). Feeding, foraging and food-sharing behavior of immature chimpanzees. Folla Primatologiea 31~ 125-142. Teleki, G. (1973). The predatory behavior of wild chimpanzees. Lewisburg, Pa. : Bucknell University Press. Teleki, G. (1975). Primate subsistence patterns: collector-predators and gatherer-hunters. Journal of Human Evolution 4~ 125-184. Trivers, R. L. (197 !). The evolution of reciprocal altruism. Quarterly Review of Biology 46, 35-57. van LawickGoodall J. (1968). The behaviour offree-living chimpanzees in the Gombe Stream Reserve. Animal Behaviour Monographs 1~ 161-311. Wrangham, R. (1977). Feeding behaviour of chimpanzees in Gombe National Park, Tanzania. In (T. H. Clutton-Brock, Ed.) Primate Ecology: studies of feeding and ranging behaviour in lemurs, monkeys and apes, pp. 503-538. London: Academic Press.
Received 29 January 1981 and accepted 1 September 1981 Keywords: chimpanzee, food
exchange, food sharing.
Food Exchange Strategies in an Infant Chimpanzee There is anecdotal evidence that exchange can be used by chimpanzees in food-sharing interactions. This research examines the foodexchange strategies of a four-year old nursery-raised female chimpanzee. When food type is varied, the chimpanzee's behavior is flexible and depends on the value of each food type offered and requested in the exchange. When only the most preferred food type is involved, the chimpanzee uses a single behavior, offering only a piece of the food it is given first; this strategy reaches an optimal level after a few sessions, when the smallest permissible amount of food is offered in exchange by the chimpanzee. Chimpanzees thus have the cognitive capacities for qualitatively adaptive and quantitatively optimal resource exchange; why these capacities are not used in the wild is discussed as a function of hypotheses bearing on foraging patterns and socialstructure. 1. I n t r o d u c t i o n
Food-sharing in chimpanzees has been well studied both in the field (Goodall, 1968; Teleki, 1973; McGrew, 1975 ; Silk, 1978) and in captivity (Silk, 1979). A m o n g adult chimpanzees, sharing ks infrequent.and seems to be restricted to animal prey; mothers, however, often share a large variety of plant foods with their infants (Goodall, 1968; Silk, 1978). When analysed in the light of recent theories on the evolution of behavior, sharing of plant foods seems to follow general predictions based on the principles 0fkin selection, parent-offspring conflict and optimal foraging: it occurs mostly between mothers and their infants, maternal resistance increases as the infant becomes older and the types Of food solicited and shared are most often those that are difficult to procure or process (Silk, 1978, 1979). Soliciting by an infant is usually done by begging gestures and whimpering, although it m a y sometimes be reduced to outright snatching. Begging and snatching are. not the only Ways to obtain food, however: Nissen & Crawford (1936), Elder (1977), Silk (1979) and Premack (1976) give anecdotal evidence of food-sharing that involves e x c h a n g e . In Premack's example, a caged female offered monkey chow in soliciting coffee from a h u m a n visitor; Premack calls the offer a "spontaneous invention". I n Silk's example, a juvenile relinquished possession of a lock an adult was trying to obtain from it when the adult shared food with the juvenile. I f sharing does occur on a Significant basis through exchange, this could have important evolutionary repercussions, since it makes selection of sharing by reciprocal altruism more likely (Trivers, 1971). O n a cognitive level, this behavior is of great interest in comparing chimpanzees and humans; intelligent resource exchange has usually been thought of as a strictly h u m a n phenomenon. T h e present study focuses on quantitative aspects of food exchange in a nursery-raised infant chimpanzee. T h e study was devised following a spontaneous occurrence of exchange witnessed by the author. Sophie, an infant female aged about two years at the time, offered a piece of apple when whimpering and begging for yoghurt proved unsuccessful; this was done by bringing the a p p l e directly into contact with the observer's mouth. This behavior was seen only once at the time and was not repeated by the chimpanzee when prompted to do so. I t is not claimed that the incident was anything more than accidental at the time. W h e n the present study was initiated, however, almost two years after the spontaneous occurrence of exchange, the chimpanzee showed complete mastery of the rusk in the first trials. A detailed analysis of exchange could thus be started, to see Journal of Human Evolution (1982) 11, 195-204
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what behavioral strategies an infant chimpanzee would use in food exchange (Experiment 1) and if and how these strategies represented optimal quantitative solutions to the exchange problem (Experiment 2). 2. G e n e r a l P r o c e d u r e
Procedures common to both experiments will first be described. The subject of the study, Sophie, was aged 47 months at the start of the experiments and 51 months at the end. She was received a week after birth from the Institute for Primate Studies in Norman, Oklahoma and housed in nursery conditions at the Laboratoire de Psychologic Compar& of the Universitfi de Montr6al. Housed with her from reception was her half-brother, Spock, born within a week of Sophie; both were given stable substitute h u m a n mothers for 189 years, after which care was given by a rotating staff of keepers and students. Although it is impossible to be certain of the degree of direct or indirect experience with exchange tasks the chimpanzee had before the study, no instances of food exchange as such were recorded except the one described above. Exchange not involving food return by the chimpanzee was used to some extent by caretakers for dealing with aspects of feeding or cleaning up; typical examples of this are the chimp's bringing back a drinking cup to the caretaker in order to obtain more juice or giving back a play object in exchange for food. No claim is made here that the present experiments represent Sophie's first contact with exchange of any type; what can be stated with some certainty, however, is that there is no reason to believe that quantitative aspects of the experiments described below were affected by indirect prior experience. All experiments were done with Sophie and the experimenter alone in a room of the Laboratoire; during some sessions of Experiment 1, note-taking and, in some instances, exchanging itself was done by a student (D.P.). The procedure common to Experiments 1 and 2 involved: (1) sitting down face to face with Sophie; (2) showing her the items involved in the exchange by holding them up in each hand simultaneously; (3) giving her the first item, with random variation of the hand used for offering; (4) holding out the empty hand while showing the second food item and saying the Quebec slang equivalent of "will you give me a n y ? " ; (5) giving her the second item if any part, however small, of the first item was given back or (6) not giving the second item if no food was returned.
Experiment 1 The first experiment was designed to see how the chimpanzee's behavior varied according to what food items were offered and requested in an exchange. Procedure. Three food types were used: commercial monkey chow, small pieces of apple (1/16 of one apple) and squares of sweet biscuit (approx. 3 • 3 • 1 cm). Choice experiments showed that the biscuit was always preferred to the apple and the appl e to the monkey chow; although this latter food type seemed to hold little attraction in the context of the experiment, it was readily eaten by Sophie as a staple food. The three food items were presented in all possible nine combinations of first given-second offered, each paired
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presentation occurring at r a n d o m in the experimental session. Seven sessions of three nine-trial series were given over 16 days. Results. Five types of behavior were observed: (A) no exchange, in which Sophie took the item given first and gave nothing back, usually movifig away from the experimenter in the process, with occasional threat behavior; (B) immediate exchange, in which the chimpanzee took the first item and gave it back untouched to obtain and eat the second item offered; (C) double exchange, in which Sophie took the first item, gave it back uneaten, took the second item and also gave that one back uneaten; (D) giving back a piece, however small, of the first item taken and eating the second item obtained; (E) exchange gesture, in which Sophie gave back saliva or touched her lips to the experimenter's empty hand without giving back any food, a behavior which disappeared after the first two sessions for lack of reinforcement Category (E) does not seem to represent an error caused by incomplete learning of the exchange rules; it appeared after the chimpanzee clearly shov)ed it understood the task and w a s accompanied by very alert looking at the experimenter's face, which probably served to obtain cues about the strategy's chances to Succeed. Behaviors (A) to (E) represent an exhaustive sample of the acts observed in t h e e x p e r i m e n t . By classifying these behaviors on a rough ordinal scale, it is possible to summarize the results as shown in Table 1. Behaviors resulting in a return of the complete item were given a score of 2, behaviors resulting in the return of a piece of the item first given were assigned a score of 1 and behaviors resulting in no food return at all were given a score of 0; since 21 trials were given for each paired wesentation, the m a x i m u m amount of the first item Table 1
Amount of food given back as a function of the type of food offered (Rough ordinal scale)
Type of food offered Monkey Chow Apple Biscuit Total (without diagonal)
Type of food given back Monkey chow Apple
Biscuit
Total (without diagonal) 11 56 61
(11 ) 42 42
11 (21 ) 19
0 14 (16)
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given back for any given cell of the matrix in Table 1 is 42. This value is reached when the monkey chow is gi~zen first ~ind requested back for either the apple or the biscuit. Since double exchange 0ccurfed or/ly when monkey chow was given first and also offered second and Was impossible t o distinguish quantitatively from immediate exchange, the marginal totals o f Table: I: d o n6t include the diagonal values involving identical items within a
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pair. These marginal totals can be interpreted as average values given to each food item by the chimpanzee, either as first item given back or second item desired, over all other food types it is paired with. Thus, the marginal totals for columns represent the value of the food types as items to be given back, with the monkey chow being given back six times as readily as the biscuit (84 to 14). The row totals measure the attractiveness of the food types as second items offered, with the monkey chow appearing five times less attractive than the apple (11 to 56) or the biscuit (11 to 61). These proportions can serve as indicators of the tendency to give back an item when first offered and of the attractiveness of the second item. Thus, the tendency to give back the monkey chow, the apple and the biscuit can respectively be estimated as proportions of 6 : 2 : 1 ; conversely, the attractiveness of these same items varies in proportions of 1 : 5 : 5, with apple and biscuit being approximately equal to the latter value. This scale of proportions can be used to express each trial in terms of subjective value for the chimpanzee. For example, a trial where monkey chow is given first and biscuit offered second represents a tendency to give back the first item estimated at 6 and a desire for the second item at 5; a trial in which apple is given first and monkey chow offered second represents a tendency to give back of 2 and a desire to obtain the second item of 1. Since each trial can be given two values of this type, each behavior can be expressed in a two-dimensional space defined by co-ordinates consisting of the mean values on the scale o f the trials in which it appears. I f double exchange is seen only in trials involving monkey chow/monkey chow, its position on the graph is (6,1), respectively the values for giving back this item and its attractiveness as second item. I f giving back only a piece of the first item occurs in trials consisting of apple/biscuit and biscuit/apple, then the position o f this behavior is defined by an average of trials estimated at (2,5) and (1,5). Intuitively, one would expect that trials in which the tendency to give back the first item and the attractiveness of the second item are both low should result in no exchange. It could also be predicted that trials in which tendency to give back and attractiveness of the second item are both high should result in immediate exchange. Figure 1 shows how Figure 1. Strategy space of the chimpanzee, in terms of value given to the food items when given first and requested back (tendency to give back) and when offered second (attractiveness). Abcissa and ordinate are in rough proportional scale as determined in Table 1. (B) biscuit; (A) apple; (M) monkey chow.
6 '"~5
Immediate exchange Piece
~
4 Exchange gesture
2 9 No exchange
(M)I I 1 (B)
[ 2 (A)
I 5
Double exchange 9 I 4
I 5
I 6 (M)
Tendency to give
these obvious (and other, less obvious) cases are positioned in the chimpanzee's strategy space. Immediate exchange and no exchange fall on the predicted extremes, while exchange gestures and giving back a piece are of intermediate value. The two-dimensional space is thus a convenient way of expressing behavioral alternatives on a scale of subjective value for food types as items to be given back or items desired in exchange; this approach
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could also serve to predict the behavioral outcome of trials involving food types other t h a n the ones used here, whose value for the chimpanzee could be estimated in relation tO known food types. Experiment 2 This experiment focuses on one of the behaviors seen in the previous experiment and examines how it changes with time. The behavior chosen is that of giving back only a piece of the first item offered, which was seen in cases where the tendency tO give back is relatively low and the attractiveness of the second item is relatively high. Procedure. In this experiment, food type was held constant (sweet biscuit only). Six sessions of ten trials each were given over 25 days. In all of the sessions, five small pieces of biscuit (approx. 1 • 1 • 0"5 cm) were given first and then requested back while a single, large piece of biscuit (approx. 4 • 4 • 1 cm, e.g. more than the five small pieces put together) was offered in exchange. The amount of small pieces given back was quantified in the following way: each uneaten small piece was counted as one item returned, while partially eaten small pieces were given values of 89188or ~t according to the size of the piece involved; /t or 0.125 was the smallest value possible and covered pieces as small as the chimpanzee could bite off and return, usually by spitting out the piece onto the experimenter's hand. Results. As quantified above, the mean amount of biscuit given back over the six sessions (with all trials averaged) and over the ten trials (with all sessions averaged) is shown in Figure 2 (a) and (b). In both cases, this amount is seen to decrease over time. Since the data in Figure 2 (a) can be interpreted either in terms of a negative linear trend or as a set of two distinct response phases (sessions 1 to 3 and sessions 4 to 6), the trial data are split up into two halves and plotted separately in Figure 2(c). Both curves show that the Figure 2. A m o u n t of food given back as a f u n c t i o n of: (a) session n u m b e r a v e r a g e d over all trials; (b) trial n u m b e r a v e r a g e d over sessions; (c) trial n u m b e r a v e r a g e d over sessions 1 to 3 ((2)) a n d sessions 4 to 6 ( [ ] ) . Sessions a
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chimpanzee reaches an asymptote around trial 3, while the amount given back on trial 1 of the first three sessions is much larger. In the last three sessions, a larger amount of biscuit is also given back on trial 1, even if this is much less than what is given back in the initial sessions. Trial 1 can thus be considered a sampling trial even in later sessions, where the chimpanzee checks to see if the exchange rules are still the same as before; once this has been verified, the chimpanzee adopts the optimal strategy of giving back as little as possible (~ to ~ of a piece). A control session consisting of five trials was given on the day after session 6, with the same exchange rules but run by a different experimenter in a different locale (on the grass outside the laboratory) and using a different container for the biscuits. In this situation, the average amount of pieces given back over the five trials returned to the same value it had at the start of the three first sessions, i.e. approximately three whole pieces (range 2"5 to 4.5). The change in context, though it involved no modification of the exchange rules (and this was understood by Sophie, judging from the very small latency of giving back in these trials), thus led to the adoption of a more conservative strategy, such as that employed on the sampling trial of the initial sessions. Sophie's behavior gave every indication that her change in strategy was not caused by a lack of comprehension of the task, but by factors related to the change in experimental conditions. 3. D i s c u s s i o n
The results obtained in this study and since confirmed on three other chimpanzees (Lefebvre & Hewitt, in preparation) can be summarized in four points: (1) a four-year-old chimpanzee can withhold immediate consumption of highly valued food and give part of it back to obtain another food item; (2) this behavior is systematic and adapted to the value of the foods involved in the exchange; (3) one of the behaviors used by the chimpanzee, giving back a piece of the first item, becomes optimal after a few sessions; (4) use of this strategy becomes more conservative if experimental conditions are changed in the direction of an increased uncertainty of outcome. Seen from the point of view of feeding behavior, these results confirm broad predictions of optimal foraging theory (Krebs, 1978). In Experiment 2, food gain is maximized when the chimpanzee gives back as little as possible, as it does from session 4 on. In sessions 1 to 3, the amount of food returned decreases progressively, as if the chimpanzee was testing in small decremental steps how little it can give back and still get the second item. This is somewhat analogous to the sampling behavior known to occur in birds (Krebs et al., 1978), where the animal forgoes instantaneous maximization of food intake in order to gain information about the situation. The sampling involved here applies both to alternative strategies and to the amount of food given back. In the first sessions, the chimpanzee may be sampling exchange rules by giving back saliva and going through the motions of food return; this is no accidental clumsiness, since such errors cease to occur when they are not reinforced. Itis also conceivable that this behavior represents a form of cheating, where the animal attempts to benefit by violating the rules. The term "cheating" need not imply conscious planning, as it is often used in a purely evolutionary sense (Dawkins & Krebs, 1978); it is hard, however, not to postulate some kind of knowledge by the chimpanzee
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that giving back saliva is of less value and less likely to be successful than giving back a piece of actual food. The method used in Figure 1 to express the relationship between behavioral outcome and the value of the food types given and offered requires some explanation. It is a variant of McFarland & Sibly's (1972) "state space" approach, where the factors determining a behavioral outcome are plotted as axes in an n-dimensional space. Any tendency (MeFarland & Sibly deal with motivation) or behavioral decision (as in the present case) that depends on multiple factors can be expressed as a point in this n-dimensional space. Since the chimpanzee's behavior depends on only two factors, the data from Experiment 1 can be easily visualized in the two-dimensional space of Figure 1. However, the method could be generalized to include more factors, such as the animal's position in relation to that of the exchange partner in the dominance hierarchy, if this factor were investigated in future experiments. The "state space" method could prove very useful in the study of multi-determined decision making. Seen from the point of view of intelligent behavior, the results indicate that a four-yearold chimpanzee can make "more!' and "less" value judgements and use these in a social interaction. This implies both social and non-social intelligence. Although Sophie could understand numerical concepts without spatial cues at the time of the experiment (Smilga & Mathieu, unpublished), the situation studied here did not require such advanced capacities. In experiment 2, Sophie could rely on the fact that three small pieces of biscuit took up more surface and volume than a single small piece; numerical judgements of a non-perceptual nature may well have been used, but it is impossible to be sure of this for lack of adequate controls. The possible presence of cheating and the flexibility in the strategies used attest to the high level of social intelligence shown by the chimpanzee. One of the pressures that may have oriented the evolution of intelligence in apes and hominids is the advantages an individual can gain in being able to predict social outcomes and manipulate the behavior of other individuals for its own benefit (Humphrey, 1976). The behavior shown by Sophie is highly attuned to the probabilities of social outcome, as shown especially b y the changes in amount given back produced by a modification of exchange conditions: increased uncertainty of outcome in session 7 leads to a return to early levels of amount given back, where a higher uncertainty of outcome was also present. Food exchange can thus be added to the growing list of sophisticated abilities great apes show in captivity but do not use in the wild. This list includes tool use in gorillas and orang-utans (Parker & Gibson, 1979), symbolic communication (Gardner & Gardner, !969) and symbolic request and cooperative usage of tools (Savage-Rumbaugh et al., 1979) in chimpanzees. Although some elements of iconic gestural communication are known to occur in wild chimpanzees and gorillas (Chevalier-Skolnikoff, 1979), the magnitude of the discrepancy between competence and performance remains puzzling: why aren't these abilities used if they are available? In some cases, what seems to be missing are the social and ecological conditions necessary for the occurrence in the wild of abilities seen in captivity, even though the cognitive prerequisites for them are present. A close examination of the literature on chimpanzee feeding ecology suggests, however, that this explanation may not be adequate to account for the absence of reported food exchange in wild chimpanzees. Four sets of conditions are necessary for the occurrence of food exchange: (1) that individuals need different food types; (2) that different individuals actually control access to different food types, so that one cannot simply take what one needs without interacting
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with others; (3) that individuals possess the cognitive elements necessary for understanding exchange and (4) that conditions favoring the evolution of reciprocal sharing exist in those species. These four conditions appear to apply to P. troglodytes. Chimpanzees need a variety of food types to assure a balanced diet, given the nutrient content of the food types they eat (Hladik, 1977). In an average day, 14.6 different food types are eaten in the Combe population (Wrangham, 1977) and 20-0 in the Ipassa, Gabon, population (Hladik, 1977). Although different groups of food types show different daily feeding peaks, there is a significant overlap in the time at which these foods are eaten. Different food types can be eaten in the same meal. They are sometimes combined simultaneously, in meat and foliage wads for example (Goodall, 1968; Teleki, 1973). Although evidence for consistent individual differences in diet, food preference and specific hungers is scarce in the wild (i.e. only Hugo ate more plant foods than others in Wrangham's 1977 study), individual differences are clearly seen in captivity. Restricted access to different food types also applies to chimpanzees. Individuals forage in subgroups, which can be split up or reformed for, during or after feeding (Goodall, 1968; Wrangham, 1977). Although individuals in a subgroup usually feed on the same food type, it is "not uncommon" (Goodall, 1968) for them to feed on different foods. Chimpanzees compete for feeding sites and may exclude others from these sites (Wrangham, 1977). Individuals feeding intensively at a site may deplete it, so that others visiting the site a day later will obtain a significantly reduced amount of food (Wrangham, 1977). Restricted access to a food item and the need to get a piece of the item immediately because of rapid depletion is even more dramatic in the case of animal prey (Teleki, 1973). Individuals foraging separately may meet at common feeding locations either by chance, by convergence on known food sites or by attraction to a site in response to the vocalizations of others (Goodall, 1968; Teleki, 1973; Wrangham, 1977). Although it is not extensive, food transport does occur even over relatively long distances (one-half mile, Goodall, 1968). Transport is done with or in the mouth (including half-chewed wads kept for relatively long periods), in the hands, around the neck or in the angle of the thigh and hip, and it occurs with both animal and vegetable foods. The cognitive elements necessary for exchange are present in wild populations. Chimpanzees can communicate their desire for food controlled by another individual; begging is well known and has a success rate of approximately 50 % (Nishida, 1970; Teleki, 1973; in capitivity, Nissen & Crawford, 1936). A chimpanzee can also withhold consumption of a highly valued food and voluntarily offer a piece of it to another individual (Teleki, 1973) ; such active sharing is less frequent than tolerated scrounging, but is nevertheless significant. The readiness to share a food item, whether actively or passively is partly a function of the value of that item (Nishida, 1970; in captivity, Nissen & Crawford, 1936). Since olive baboons are known to be able to evaluate each other as reciprocators (Packer, 1977), we can easily assume that chimpanzees are also capable of this. Food exchange can be seen as a form of immediate reciprocal altruism. Chimpanzees have all of the characteristics considered by Trivers (1971) to favor the evolution of reciprocity: a long lifespan, repeated occasions to interact, a strong degree of mutual interdependence, a sufficient mnemonic capacity and discriminative ability to remember and identify acts and individuals. The dominance hierarchy of chimpanzees is not of the type where food can be preempted by a dominant at all times (Trivers, 1971; Goodall, 1968); even high ranking males have to beg for meat once others control a piece of carcass
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(Teleki, 1973). Reciprocity is known to exist in aggressive coalitions and to contribute to status (Riss & Goodall, 1977; de Waal, 1978). If the potential initial disadvantage of non-reciprocated altruism needs to be compensated by the advantage of kin-selected altruism for reciprocity to evolve (Rothstein, 1980), the high incidence of sharing within kin groups shows that chimpanzees have this prerequisite to pure reciprocity (McGrew, 1975; Silk, 1978). In any case, some sharing of meat among adult P. troglodytes appears to be kin-independent (Teleki, 1973). I f these social, ecological, cognitive and evolutionary conditions for the appearance of food exchange appear to be sufficient, they underline the fact that some of the factors thought to be responsible for the evolution of exchange in hominids m a y not be strictly necessary. Differences in individual foraging patterns need not have been compartmentalized along age and sex class lines. The ability to construct food transport tools and the daily or periodic meeting and concentration at a "base camp" (Isaac, 1976; 1978) also do not appear to be necessary conditions, although they might very well have favored exchange. The same reasoning applies to cooperative hunting of large animal prey (Teleki, 1975). Logically sufficient conditions do not make a phenomenon appear. Each of the factors outlined above may represent a real but infrequent event, so that the combined probability of these conditions working together may be extremely low. In addition, the selective advantage of that very rare occurrence may be slight in relation to alternatives. Finally, chimpanzee social interactions may be too tense for exchange of valued resources to be stable, in the sense that the frequent recourse to physical aggression may interfere with mutually beneficial sharing. We can nevertheless conclude that the cognitive capacity for exchange is not restricted to man and that any future reports &isolated cases of exchange in wild chimpanzees should not really come as a total surprise.
I am grateful to Mireille Mathieu for the opportunity to work at the Laboratoire de Psychologic compar4e, to Diane P4russe and Jean-Marie Bonnet for their help with the experiments, to Don Kramer and Dominique Spahn for comments on the manuscript and to Bernard Chapais for suggestions concerning the discussion.
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