Behavioral Ecology Vol. 14 No. 6: 887-891
© 2003 International Society for Behavioral Ecology
Grooming among female Japanese macaques: distinguishing between reciprocation and interchange
a Istituto di Scienze e Tecnologie della Cognizione, Consiglio Nazionale delle Ricerche, Rome 00197, Italy b School of Social and Health Sciences, Division of Psychology, University of Abertay Dundee, DD1 1HG, UK c Cattedra di Psichiatria, Università Tor Vergata, 00136 Rome, Italy
Address correspondence to G. Schino. E-mail: gschino{at}casaccia.enea.it.
Received 15 April 2002; revised 7 November 2002; accepted 27 January 2003.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Grooming among female Japanese macaques (Macaca fuscata) was studied to test some predictions derived from the application of biological market theory. Contrary to expectations, Japanese macaques did not time match the duration of grooming episodes, their degree of reciprocation was not related to rank distance, and they did not distribute their immediately reciprocated and nonreciprocated grooming in different ways. However, they did reciprocate total amount of grooming received. These results suggest that the use of the temporal patterning of grooming (immediately reciprocated versus nonreciprocated grooming) to distinguish the different classes of traders predicted by the theory (reciprocal versus interchange traders) is unsuccessful.
Key words: biological market theory, grooming, macaques, reciprocation.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Modeling has a long history as a theoretical device to further the understanding of complex phenomena in several biological disciplines, most notably ecology and evolutionary biology (see Axelrod and Hamilton, 1981
; MacArthur and Wilson, 1967; Maynard Smith, 1982). Far less common has been the use of modeling to further the understanding of the patterning and distribution of animal social behavior. A notable exception is primate allogrooming that, possibly because it is easily observed and quantified, has been the subject of popular modeling attempts. Seyfarth (1977) was the first to propose a model of social grooming (hereafter, grooming) among female primates. His model has been enormously influential and is indeed quite successful in predicting overall grooming distribution in a variety of species and settings (for a recent meta-analysis, see Schino, 2001).
Further development of the modeling of grooming behavior has been allowed by the explicit application of principles deriving from the biological market theory (Noë and Hammerstein, 1994, 1995; Noë et al., 2001). Grooming in a variety of species has been interpreted in light of biological market principles (Bshari, 2001; Stopka and Macdonald, 1999). Barrett et al. (1999; see also Barrett and Henzi, 2001; Henzi et al., 1997) provided the most thorough treatment. They conceived grooming as a tradable commodity and individuals within a primate group as traders that compete with each other in the marketplace exchanging grooming for itself (reciprocal traders) or for other goods (interchange traders). Such market model assumes that when grooming is exchanged for itself, females will use immediate reciprocation (time matching) in order to avoid being cheated and to obtain equivalent value for their services. In making such assumption, Barrett et al. (1999) implicitly equated immediately reciprocated grooming (grooming episodes that are temporally linked) with functionally reciprocated grooming (grooming episodes that are exchanged with other grooming). In other words, they assumed that the temporal patterning of grooming could be used to distinguish reciprocal from interchange traders.
Because the market model also assumes that closely ranking females will be primarily reciprocal traders and that distantly ranking females will be primarily interchange traders, it predicts that immediately reciprocated grooming will be directed primarily to closely ranking females, whereas nonreciprocal grooming will be directed primarily to high-ranking females (that can exchange it for tolerance or agonistic support).
In this article, we attempt an evaluation of some specific predictions of the model that derive from the assumption that reciprocal and interchange traders can be distinguished on the basis of the temporal patterning of grooming. The following predictions were tested:
- among immedately reciprocated grooming bouts, there will be a positive correlation (time matching) between the amount of grooming given and received;
- there will be a negative relation between rank distance and degree of reciprocation;
- high-ranking females will receive more nonreciprocal grooming than do low-ranking females, whereas received reciprocal grooming will not be dependent on social rank;
- each female will direct more of her nonreciprocal grooming up than down in the hierarchy, whereas reciprocal grooming will be directed evenly to higher- and to lower-ranking females;
- reciprocal grooming will be directed primarily to closely ranking females, whereas nonreciprocal grooming will not; and
- overall, females will distribute their reciprocal and nonreciprocal grooming in different ways.
The testing of predictions 1 and 2 replicated and extended the analyses presented by Barrett et al. (1999), whereas testing of predictions 3–6 examined whether macaques distributed reciprocal and nonreciprocal grooming according to different criteria. Specifically, nonreciprocal grooming should be characteristic of interchange traders and thus be strongly influenced by rank of the recipient (similar to what is predicted by Seyfarth's original model), whereas reciprocal grooming should be characteristic of reciprocal traders and should be directed to closely ranking animals and essentially governed by time matching of grooming duration.
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METHODS |
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Subjects and housing
The subjects of the present study was a captive group of Japanese macaques (Macaca fuscata) housed in the Rome zoo (Bioparco) in a 700-m2 outdoor enclosure fitted with climbing structures, ropes, and a pool. The group numbered 71 animals at the beginning of the study, including 22 adult females (5 years or older) that were the subjects of the observations.
The group had been captured as a whole in Takasakiyama, Japan, in 1977 and has been under continuous observation until 1999. Maternal genealogies were thus known for all animals born after 1977. Further information on the group history and housing condition can be found in a study by Schino et al. (1995).
Behavioral observations
The 22 female subjects were the focus of 9–12 focal-animal 60-min observation sessions by using the "all occurrences" sampling technique (Altmann, 1974). A total of 263 h of observation was made. The timing and duration of every episode of allogrooming were recorded, along with the identity of the interactants. Data were collected from April–November 1996, thus avoiding the mating season in order to minimize the confounding influences of sexual activity (D'Amato et al., 1982; Mehlman and Chapais, 1988). For analytical purposes, grooming was considered to be reciprocal if two grooming episodes involving the same two females in opposite directions were separated by less than 60 s. Thus defined, about 28% of time spent grooming was reciprocal. Use of slightly different operational definitions of reciprocal grooming (30 s or 3 min) did not alter the results.
Data analysis
To replicate the analyses of Barrett et al. (1999), we randomly selected one immediately reciprocated grooming bout for each dyad of females in the group (the first bout observed for that dyad) and used the duration of those episodes to test for time matching and for the correlation between degree of time matching and rank distance.
An alternative approach to avoid pseudoreplication is the use of matrix correlations (de Vries, 1993; Hemelrijk, 1990). We therefore used the Kr test and the Mantel test to examine the relation between rank distance and degree of reciprocation (using the ratio of reciprocal to total grooming as an index of degree of reciprocation), and to compare the distributions of reciprocal and nonreciprocal grooming. Standard nonparametric statistics were used for other analyses.
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RESULTS |
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Occurrence and distribution of immediate grooming reciprocation
We first replicated the analyses of Barrett et al. (1999)
. Contrary to their finding, female macaques did not match the duration of immediately reciprocated grooming bouts (Spearman correlation: rs =.072, N = 25, p = ns) (Figure 1). Confirming their observation, the signed difference in the duration of immediately reciprocated grooming bouts (duration of second episode minus duration of first episode) was correlated to the signed difference in the ranks of the two females (rank of the second groomer minus rank of the first groomer), although the correlation did not quite reach statistical significance (rs =.388, N = 25, p <.06).
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Such correlation, however, depends entirely on the tendency of monkeys to direct their grooming up the hierarchy (see below). Positive rank differences were those in which the highest-ranking female groomed second, and because she also groomed less, the difference in the duration of grooming was also positive. When the highest-ranking female in a dyad happened to groom first, both the rank difference and the grooming duration difference were negative. The result was the positive correlation we observed. A better test of the hypothesis that degree of reciprocation is correlated to rank distance is obtained by using unsigned (absolute) differences. Such correlation is not significant (rs = -.012, N = 25, p = ns) (Figure 2).
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Using the proportion of grooming that was reciprocal (reciprocal/reciprocal + nonreciprocal grooming) as an index of the degree of reciprocation characteristic of each dyad in a matrix correlation analysis confirmed that degree of reciprocation was not significantly associated with rank distance (Mantel test: rs =.051, p = ns).
Rank distance of dyads that (over the whole study period) were observed to engage in immediate grooming reciprocation was smaller than that of dyads that were never observed to reciprocate grooming (Mann-Whitney U test: U = 832, N1 = 26, N2 = 87, p <.05). Such difference, however, was owing to the confounding influence of kinship (kin tend to share similar ranks), so that after excluding kin, there was no significant difference between dyads that did and did not reciprocate grooming (U = 366.5, N1 = 12, N2 = 70, p = ns).
Differences between reciprocal and nonreciprocal grooming
Social rank was significantly correlated to both received reciprocal and received nonreciprocal grooming (reciprocal: rs =.570, N = 22, p <.01; nonreciprocal: rs =.554, N = 22, p <.02) (Figure 3). Reciprocal grooming was directed predominantly up the hierarchy (Wilcoxon matched-pairs test: W = 29, N = 17, p <.05), whereas for nonreciprocal grooming, the difference was in the same direction but did not reach statistical significance (W = 52, N = 19, p <.1) (Figure 4). There were no differences in the grooming directed to adjacently and to distantly ranking females (reciprocal: W = 71, N = 18, p = ns; nonreciprocal: W = 112, N = 21, p = ns) (Figure 5). Overall, the group matrices of reciprocal and nonreciprocal grooming were significantly correlated (Kr test: 
rw = 0.364, p <.0002).
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Reciprocation of total grooming time
When total grooming time was analyzed (both reciprocal and nonreciprocal), there was a significant matrix correlation between grooming and being groomed, that is, between the matrix of grooming and its transposition (
rw = 0.383, p <.0002). Partialing out the effect of kinship did not alter the significance of the correlation (rw = 0.251, p <.0002). |
DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The results of this study show that Japanese macaque females distribute their immediately reciprocated and their nonreciprocated grooming in much the same way. Furthermore, we found no evidence for time matching of immediately reciprocated grooming bouts, and no or equivocal evidence for a relation between rank distance and degree of grooming reciprocation. These results are open to two different interpretations. First, it is possible that biological market models do not adequately describe the grooming behavior of female Japanese macaques. Second, it is possible that the temporal patterning of grooming (immediately reciprocated versus nonreciprocated grooming) does not reliably distinguish between the two different classes of traders (reciprocal versus interchange traders) predicted by the model.
We favor this second possibility for a number of reasons. Each single episode of grooming is likely to have a low cost for the actor, as well as a low benefit for the receiver. Given the good memory of primates and the stability of their grouping, it seems unlikely that selection has favored the evolution of precise and immediate reciprocation of grooming duration, because the cost of being cheated (the cost of a single nonreciprocated grooming episode) is small. Individual monkeys only need to remember past interactions and to balance overall benefits given and received (either in the form of grooming or of tolerance/support). In fact, there is no need to assume (as Barrett et al. [1999] have done) that monkeys in each dyad will act either as reciprocal traders or as interchange traders. Primate interindividual relationships seem more likely to be characterized by a variable mixture of reciprocation and interchange, and disentangling such complex web is unlikely to be a trivial task. In contrast, immediate reciprocation of grooming appears to be the rule in species such as the impala (Aepyceros melampus) characterized by more unstable grouping, little scope for interchange, and possibly worst memory and higher costs associated to grooming (Connor, 1995; Hart and Hart, 1992).
Up to now, support for an application of biological market principles to the study of primate grooming behavior seems to have been based on the implicit equation between temporal reciprocation and functional reciprocation. We have made such previously unrecognized assumption explicit and have shown its weakness.
The Japanese macaques we studied did indeed reciprocate total grooming time, as shown by the significant correlation between grooming and being groomed. Such reciprocation, however, was not necessarily immediate. It is interesting to compare our results with those reported by Leinfelder et al. (2001). Similarly to our findings, they reported that hamadryad (Papio hamadryas) females reciprocated total grooming time, but contrary to our findings, they observed no tendency to direct grooming up the hierarchy. They concluded that hamadryad females could only trade grooming for itself and showed no evidence for interchange. As our Japanese macaques did direct their grooming up the hierarchy, we may speculate that in our group, the possibility of interchange of grooming for support/tolerance existed. Interestingly, the strength of the correlation between grooming and being groomed in our group is weaker than those reported by Leinfelder et al. (2001), implying that a smaller proportion of the variance in grooming time was explained by reciprocation. Apparently, the possibility of interchange trading of grooming decreased the scope for reciprocation. Barrett et al. (1999) reported similar findings when comparing baboon troops experiencing different levels of contest competition and, thus, different scope for interchange of grooming with support/tolerance. More recently, Barrett et al. (2002) observed a covariation of aggression and grooming reciprocity related to ecological changes in the competitive regime experienced by a single troop of wild baboons.
It should also be noted that the overall reciprocation of grooming time is consistent with a role of grooming in parasite removal (Hart, 1990). Its observation in a captive parasite-free environment suggests incorporation of features of the "programmed grooming" hypothesis (see Mooring et al., 2002) into future modeling attempts would be worthwhile.
In conclusion, although the biological market theory is likely to be a promising avenue for the study of animal cooperation (Hammerstein, 2001; Noë, 2001), it appears that its application to a low-cost behavior such as grooming is far from being straightforward. In particular, the attempt to characterize the different classes of traders predicted by the theory on the basis of the temporal patterning of grooming appears unsuccessful. More promising seems to be the characterization of trader classes on the basis of independent criteria. For example, Henzi and Barrett (2002) showed that the amount of grooming directed to baboon mothers in order to gain temporary access to their newborn infants was inversely related to the number of available infants. In other words, when trader classes were unambiguously assigned (mothers versus nonmothers) it was possible to detect a clear effect of varying supply (number of infants) on the "price" (grooming) paid to obtain a resource (access to the infants). Finally, a better understanding of the temporal relationships between grooming and other behavioral candidates for reciprocation/interchange will facilitate the testing of predictions based on theoretical modeling.
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ACKNOWLEDGEMENTS |
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We thank the Bioparco of Rome for allowing us to study their colony of Japanese macaques, and Louise Barrett for her comments on an earlier version of the article.
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