Grooming up the hierarchy: the exchange of grooming and rank-related benefits in a new world primate

Seyfarth's model assumes that female primates derive rank-related benefits from higher-ranking females in exchange for grooming. As a consequence, the model predicts females prefer high-ranking females as grooming partners and compete for the opportunity to groom them. Therefore, allogrooming is expected to be directed up the dominance hierarchy and to occur more often between females with adjacent ranks. Although data from Old World primates generally support the model, studies on the relation between grooming and dominance rank in the New World genus Cebus have found conflicting results, showing considerable variability across groups and species. In this study, we investigated the pattern of grooming in wild tufted capuchin females (Cebus apella nigritus) in Iguazú National Park, Argentina by testing both the assumption (i.e., that females gain rank-related return benefits from grooming) and predictions (i.e., that females direct grooming up the dominance hierarchy and the majority of grooming occurs between females with adjacent ranks) of Seyfarth's model. Study subjects were 9 adult females belonging to a single group. Results showed that grooming was given in return for tolerance during naturally occurring feeding, a benefit that higher-ranking females can more easily grant. Female grooming was directed up the hierarchy and was given more often to partners with similar rank. These findings provide supporting evidence for both the assumption and predictions of Seyfarth's model and represent, more generally, the first evidence of reciprocal behavioural interchanges driven by rank-related benefits in New World female primates.     

Individual contributions to a dyadic interaction: An analysis of baboon grooming

Grooming in dyads of six captive female hamadryas baboons (Papio hamadryas) was analysed. Each dyad was observed in isolation and as part of a group of three to six females. The isolated dyads differed from dyads in groups, as follows. (1) Grooming in isolated dyads mainly depended on the actor's general tendency to groom, whereas actors in groups were more responsive to who the recipient was. (2) In groups, grooming tended to be more frequent among females of high dominance rank and among females who preferred one another in choice tests. The opposites were true for isolated dyads. Females in isolated dyads seemed to use grooming to improve a poor relationship, whereas grooming in groups was used as if to maintain and defend a valuable relationship.     

Grooming reciprocation among female primates: a meta-analysis

The theory of reciprocal altruism offers an explanation for the evolution of altruistic behaviours among unrelated animals. Among primates, grooming is one of the most common altruistic behaviours. Primates have been suggested to exchange grooming both for itself and for rank-related benefits. While previous meta-analyses have shown that they direct their grooming up the hierarchy and exchange it for agonistic support, no comprehensive evaluation of grooming reciprocation has been made. Here we report on a meta-analysis of grooming reciprocation among female primates based on 48 social groups belonging to 22 different species and 12 genera. The results of this meta-analysis showed that female primates groom preferentially those group mates that groom them most. To the extent allowed by the availability of kinship data, this result holds true when controlling for maternal kinship. These results, together with previous findings, suggest that primates are indeed able to exchange grooming both for itself and for different rank-related benefits.     

A dynamic interaction between aggression and grooming reciprocity among female chacma baboons

We used data from a natural experiment on adult female chacma baboons, Papio cynocephalus ursinus, to test the hypothesis that variation in aggression through time influences patterns of grooming reciprocity within a social group. Owing to a change in the baboons' competitive regime, we were able to compare data from periods when aggression was high (period 1) and low (period 2). During period 2, the slope of the relationship between aggression and rank was significantly shallower than during period 1 and less aggression was directed at the lowest-ranking females suggesting there had been a reduction in the dominance gradient. We attributed this to reduced effectiveness of dominance as a means of excluding other females from feeding resources. The reduction in aggression during period 2 was accompanied by an increase in grooming reciprocity between dyads suggesting that high-ranking females no longer attracted grooming by subordinates in exchange for tolerance, and that grooming in period 2 was exchanged for its intrinsic benefits. The loss of rank-related effects on grooming reciprocity in period 2 compared with period 1 further confirmed this. These findings show that female baboons are able to respond flexibly and swiftly to changes in their social circumstances and that a dynamic approach to primate social interactions is worth pursuing. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Affiliation Among Females in Wild Hamadryas Baboons (Papio hamadryas hamadryas)

Previous researchers of hamadryas baboons have described a star-shaped sociogram, whereby the strongest social bonds within hamadryas one-male units are between a leader male and his females and bonds among females are weak by comparison. This type of social organization is also known as cross-bonding to distinguish it from the female-bonding found in most papionin monkeys. Models of female primate socioecology suggest that hamadryas baboons lack female bonding due to their reliance on scarce, widely-dispersed food resources. Here, I report observational data from a wild population of hamadryas baboons in Ethiopia indicating that, while females varied widely in their frequency of social interaction with other females, most females spent about as much social time with other females as they did with the leader male and some females even crossed unit boundaries to interact with one another. The size of a unit was positively correlated with the tendency of its females to interact with other females and was negatively correlated with the tendency of its females to interact with the leader male. Females were equally likely to spend social time with other females whether or not the leader male was available for social interaction at the time. Overall, this study suggests that a star-shaped sociogram does not characterize all hamadryas baboons and that female hamadryas may be, to some extent, female-bonded as well as cross-bonded. The lack of more pronounced female bonding in hamadryas is probably due to the behavior of males rather than to ecological factors.     

Grooming reciprocity in female tibetan macaques macaca thibetana

Grooming among nonhuman primates is widespread and may represent an important service commodity that is exchanged within a biological marketplace. In this study, using focal animal sampling methods, we recorded grooming relationships among 12 adult females in a free-ranging group of Tibetan macaques (Macaca thibetana) at Huangshan, China, to determine the influence of rank and kinship on grooming relationships, and whether females act as reciprocal traders (exchange grooming received for grooming given) or interchange traders (interchange grooming for social tolerance or other commodities). The results showed that: (1) grooming given was positively correlated with grooming received; (2) kinship did not exert a significant influence on grooming reciprocity; and (3) grooming reciprocity occurred principally between individuals of adjacent rank; however, when females of different rank groomed, females tended to groom up the hierarchy (lower ranking individuals groomed higher ranking individuals more than vice versa). Our results support the contention that both grooming reciprocity and the interchange of grooming for tolerance represent important social tactics used by female Tibetan macaques.     

The fourth level of social structure in a multi‐level society: ecological and social functions of clans in hamadryas baboons

Hamadryas baboons are known for their complex, multi‐level social structure consisting of troops, bands, and one‐male units (OMUs) [Kummer, 1968. Social organization of hamadryas baboons. Chicago: The University of Chicago Press. 189p]. Abegglen [1984. On socialization in hamadryas baboons: a field study. Lewisburg, PA: Bucknell University Press. 207p.] observed a fourth level of social structure comprising several OMUs that rested near one another on sleeping cliffs, traveled most closely together during daily foraging, and sometimes traveled as subgroups independently from the rest of the band. Abegglen called these associations “clans” and suggested that they consisted of related males. Here we confirm the existence of clans in a second wild hamadryas population, a band of about 200 baboons at the Filoha site in lowland Ethiopia. During all‐day follows from December 1997 through September 1998 and March 2005 through February 2006, data were collected on activity patterns, social interactions, nearest neighbors, band fissions, and takeovers. Association indices were computed for each dyad of leader males, and results of cluster analyses indicated that in each of the two observation periods this band comprised two large clans ranging in size from 7 to 13 OMUs. All band fissions occurred along clan lines, and most takeovers involved the transfer of females within the same clan. Our results support the notion that clans provide an additional level of flexibility to deal with the sparse distribution of resources in hamadryas habitats. The large clan sizes at Filoha may simply be the largest size that the band can split into and still obtain enough food during periods of food scarcity. Our results also suggest that both male and female relationships play a role in the social cohesion of clans and that males exchange females within clans but not between them. Am. J. Primatol. 71:948–955, 2009. © 2009 Wiley‐Liss, Inc.     

Allogrooming Behavior and Grooming Site Preferences in Captive Bonobos (Pan paniscus): Association with Female Dominance

I tested the utility of Seyfarth's (1977) model of rank-related attractiveness to explain the distribution of allogrooming behavior among captive bonobos (Pan paniscus). Adult female bonobos generally have high social status and may be dominant over males. As predicted by the model, I found that high-ranking adult females received most allogrooming within each of the four investigated groups. Among adult female-adult female dyads, however, allogrooming was not clearly associated with dominance rank. Contradictory to predictions of the model, the highest-ranking females were responsible for most displacements over allogrooming, and grooming competition is positively correlated with dominance rank. In the second part of this study, I investigated the social significance of allogrooming body site preferences. Bonobos direct significantly most allogrooming to the face of conspecifics, and high- and low-ranking individuals, as well as males and females, differ significantly in their preferences for certain allogrooming sites. Subordinates and males tended to avoid facial grooming and preferred the back and anogenital region, while high-ranking individuals and females directed most allogrooming to the face and head of grooming partners. Data from this study support the hypothesis that high-ranking females are the most attractive grooming partners within a female-centered bonobo society. Many other aspects of allogrooming behavior, however, are not consistent with the model of rank-related attractiveness.     

The Absence of Grooming for Rank-Related Benefits in Female Assamese Macaques (Macaca assamensis)

Seyfarth’s model of social grooming proposes that by grooming females higher ranking than themselves, females can gain access to important rank-related benefits, such as agonistic support. This, in turn, produces a distinctive pattern of grooming in which females direct their grooming up the female dominance hierarchy and compete for access to the highest ranking individuals. We aimed to test to what extent the grooming behavior of female Assamese macaques (Macaca assamensis) fits the assumptions and predictions of Seyfarth’s model. During two 1-yr sampling periods (October 2007–September 2008, May 2010–April 2011) we collected >2100 focal hours of data from a single wild group in their natural habitat at Phu Khieo Wildlife Sanctuary, Thailand. Subjects included all adult female group members (N?=?12 in 2007/8; N?=?15 in 2010/11). We collected detailed data on grooming interactions, approaches, and departures as well as all aggressive and submissive behaviors between all subjects. We found no evidence that grooming was exchanged for rank-related benefits. In line with this we found no evidence that the grooming of female Assamese macaques fits the pattern predicted by Seyfarth’s model. These results are surprising given that such deviations from Seyfarth’s model are relatively rare among macaques. We propose that our findings are best explained as a lack of a need for rank-related benefits by females in this group.     

One-male units and clans in a colony of hamadryas baboons (Papio hamadryas hamadryas): effect of male number and clan cohesion on feeding success

In the multilevel societies of hamadryas baboons, adult males can be attached to single one-male units (OMUs) or to clans containing several such OMUs. This paper examines the effect of male number and rivalry between males within a clan on their ability to compete for access to a clumped food resource. The data come from a study of a multilevel colony of hamadryas baboons (Papio hamadryas hamadryas) housed at the Madrid Zoo. The colony consisted of 12 harem-holding males and 40 sexually mature females, and was organized into five single OMUs and two clans (containing three and four OMUs, respectively). The top-ranking male of one of the clans was removed and later reintroduced, so the study involved an analysis of the composition of clans and OMUs and of the males' use of the feeding area across three study periods: preseparation, separation, and reintroduction. The findings reported indicate that both males and females derived clear advantages in the context of contest competition for access to clumped food if they were members of clans, because the males and females from large clans had a feeding advantage over those from smaller clans and single OMUs. Furthermore, rivalry among males within the clan reduced their ability to compete for food against males outside their clan. This paper provides empirical evidence for one of the potential advantages that hamadryas males may enjoy if they are attached to clans, and also provides empirical support for the general hypothesis that a large number of males in a group may provide fitness-related benefits to the group members, provided they are able to cooperate with each other.     

Female dominance and female social relationships among yellow baboons (Papio hamadryas cynocephalus)

Adult females in a female-bonded, cercopithecine species such as baboons are characterized by hierarchically ranked matrilines, i.e., female offspring assume rankings just beneath those of their mothers. In this system of closely ranked matrilines, a female should engage in significantly more affiliative interactions with those individuals who are closely ranked to herself than with those individuals who are more distantly ranked. We examine the hypothesis that females in this troop of feral yellow baboons (Papio hamadryas cynocephalus) who are closely ranked will also show close social affiliation. We collected focal data on 23 feral, adult female subjects (253 possible dyads) over approximately 1 year at the Tana River National Primate Reserve, Kenya. Following Bramblett's [Behav Brain Sci 4: 435, 1981] method of dominance tabulation and utilizing a modified version of Smuts' [Sex and friendship in baboons, Hawthorne: Aldine Publishing Co., 1985] preferred partner index, we describe and compare the dominance matrix and hierarchy, preferred proximity partner and grooming partner sociograms, and the social networks of these 23 focal females. Over 1,400 interactions were utilized in the dominance tabulations, 41 statistically significant proximity partner preferences were documented, and 100 grooming dyads were recorded. We examine both partners' ranks and the presence of an infant as possible factors influencing proximity and grooming partner preferences. We find that in this population there is no direct correspondence between females' ranks and their affiliation partners. Neither proximity nor grooming preferences are consistently predictable from partners' ranks. While proximity preferences were not significantly influenced by the presence of an infant, grooming partner preferences were. Females with infants had more grooming partners and were more often involved in unidirectional grooming relationships as the recipients than were females without infants. We conclude that females' dominance rankings are not good predictors of either proximity partner or grooming partner preferences and that the presence of an infant does have a significant impact on grooming partner preferences in this population.     

Allogrooming, partner choice, and dominance in male anubis baboons

This study was designed to test the hypothesis that among unrelated male baboons (Papio cynocephalus anubis) in single-gender social groups there is no significant association between dominance status and allogrooming performance. The hypothesis was tested using behavioral measures obtained by focal animal sampling techniques. The results indicate that unrelated male baboons established well-defined linear dominance hierarchies, formed allogrooming relationships with one another, and exhibited a nonrandom distribution of allogrooming; however, there were no significant relationships between dominance rank and the frequency of allogrooming. We further tested our results by grouping individuals into three dominance status classes (high, middle, and low) and comparing the classes. Analysis of variance demonstrated no significant differences in rates of allogrooming by dominance class. These results suggest that dominance did not account for the variation in observed allogrooming behavior: Dominance status did not appear to determine the frequency with which animals groomed others, the number of grooming partners, or frequency of grooming that any individual received in comparison to that performed. High-ranking animals did not have significantly more grooming partners than low-ranking animals, and there appeared to be little competition within the groups for subordinates to groom high-ranking animals. When age, kinship, and group tenure are controlled, performance and reception of allogrooming are not strongly associated with dominance in single-gender social groups of male anubis baboons.     

Food Competition and Linear Dominance Hierarchy Among Female Chimpanzees of the Taï National Park

Dominance rank in female chimpanzees correlates positively with reproductive success. Although a high rank obviously has an advantage for females, clear (linear) hierarchies in female chimpanzees have not been detected. Following the predictions of the socio-ecological model, the type of food competition should affect the dominance relationships among females. We investigated food competition and relationships among 11 adult female chimpanzees in the Taï National Park, Côte d'Ivoire (West Africa). We detected a formal linear dominance hierarchy among the females based on greeting behaviour directed from the subordinate to the dominant female. Females faced contest competition over food, and it increased when either the food was monopolizable or the number of competitors increased. Winning contests over food, but not age, was related to the dominance rank. Affiliative relationships among the females did not help to explain the absence of greetings in some dyads. However comparison post hoc among chimpanzee study sites made differences in the dominance relationships apparent. We discuss them based on social relationships among females, contest competition and predation. The cross-site comparison indicates that the differences in female dominance hierarchies among the chimpanzee study sites are affected by food competition, predation risk and observation time.     

Social relationships of mountain baboons: Leadership and affiliation in a non-female-bonded monkey

Instead of close and differentiated relationship among adult females, the accepted norm for savanna baboons, groups of Drakensberg mountain baboons (Papio ursinus) showed strong affiliation of females towards a single male. The same male was usually the decision-making animal in controlling group movements. Lactating or pregnant females focused their grooming on this “leader” male, producing a radially patterned sociogram, as in the desert baboon (P. hamadryas); the leader male supported young animals in the group against aggression and protected them against external threats. Unlike typical savanna baboons, these mountain baboons rarely displayed approach-retreat or triadic interactions, and entirely lacked coalitions among adult females. Both groups studied were reproductively one-male; male-female relationships in one were like those in a unit of hamadryas male at his peak, while the other group resembled the unit of an old hamadryas male, who still led the group, with a male follower starting to build up a new unit and already monoplizing mating. In their mountain environment, where the low population density suggests conditions as harsh for baboons as in deserts, adults in these groups kept unusually large distances apart during ranging; kin tended to range apart, and spacing of adults was greatest at the end of the dry, winter season. These facts support the hypothesis that sparse food is responsible for convergence with hamadryas social organization. It is suggested that all baboons, though matrilocal, are better categorized as “cross-sex-bonded” than “female bonded”.     

Patterns of coalition formation by adult female baboons in Amboseli, Kenya

Coalitionary support in agonistic interactions is generally thought to be costly to the actor and beneficial to the recipient. Explanations for such cooperative interactions usually invoke kin selection, reciprocal altruism or mutualism. We evaluated the role of these factors and individual benefits in shaping the pattern of coalitionary activity among adult female savannah baboons, Papio cynocephalus, in Amboseli, Kenya. There is a broad consensus that, when ecological conditions favour collective defence of resources, selection favours investment in social relationships with those likely to provide coalitionary support. The primary features of social organization in female-bonded groups, including female philopatry, linear dominance hierarchies, acquisition of maternal rank and well-differentiated female relationships, are thought to be functionally linked to the existence of alliances between females. Female savannah baboons display these characteristics, but the frequency and function of their coalitionary aggression is disputed. In our five study groups, 4-6% of all disputes between females led to intervention by third parties. Adult females selectively supported close maternal kin. There was no evidence that females traded grooming for support or reciprocated support with nonkin. High-ranking females participated in coalitionary aggression most frequently, perhaps because they derived more benefits from group membership than other females did or could provide support at lower cost. Females typically supported the higher ranking of two contestants when they intervened in disputes between subordinates, so most coalitions reinforced the existing dominance hierarchy. Results indicate that female baboons participate in coalitionary aggression in a manner strongly influenced by nepotism and individual benefits.     

Effect of resource competition on the long-term allocation of grooming by female baboons: evaluating Seyfarth's model

Seyfarth (1977, Journal of Theoretical Biology, 65, 671-698) proposed an influential model that explained the long-term patterning of grooming relationships between female primates in terms of an interaction between the idealized grooming objectives of females and competition for valuable grooming partners. A critical test of the model requires a demonstration not only that competition for partners exists, but also that females do have an underlying target for the amount of grooming that they would like to receive relative to the amount they need to give. As it is not possible to stipulate a priori what this target is, or to detect it directly, we assessed its applicability by making a set of predictions, within the framework of Seyfarth's model, as to how observed grooming patterns should change with changes in the intensity of resource competition. We tested these predictions with data from a troop of baboons, Papio hamadryas ursinus, for which the within-bout structure of grooming has already been shown to be sensitive to changes in resource competition (Barrett et al. 2002, Animal Behaviour, 63, 1047-1053). We found no evidence of competition for grooming partners and our results do not support the predictions of the modified model with respect to the existence of underlying grooming objectives. The findings that the grooming of female baboons is more diverse and that the mean rank distance separating partners increases when resource competition is greater, together with the absence of rank effects on long-term patterns, are, however, supportive of the recent biological market approach to social interactions. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.      

Distribution and Habitat Associations of Baboons (Papio hamadryas) in Central Eritrea

At least three diurnal primate taxa are still present in Eritrea, NE Africa: hamadryas baboons (Papio hamadryas hamadryas), olive baboons (Papio h. anubis) and grivet monkeys (Chlorocebus aethiops aethiops). However, information on status and distribution of primates and their habitats in Eritrea is outdated and incomplete. We conducted a primate survey, focussing on hamadryas baboons, to obtain data which will be integrated in a national wildlife management and conservation plan in Eritrea. We obtained information about the geographical distribution and abundance of baboons, their altitudinal range, habitat quality of their home-ranges, aggregation sizes at sleeping cliffs and predator presence. We described habitat quality via the Normalized Difference Vegetation Index (NDVI), a vegetation classification of Landsat MSS satellite data. Hamadryas and olive baboons are still present in Eritrea in ample numbers. Their geographical distributions in 1997 and 1998 did not deviate significantly from their historical distributions. An estimated 15,000 Papio hamadryas hamadryas lived in the 25,000-km² area of survey (0.58 baboons/km²). Population densities of hamadryas baboons in many parts of the survey area are higher than at Kummer's (1968) study site in Ethiopia. Hamadryas baboons live at all altitudes in four of five ecogeographical zones of Eritrea. Olive baboons replaced them in the western lowlands. Both baboon taxa tend to select better quality habitats, characterized by a higher normalized difference vegetation index (NDVI) than the average for the respective ecogeographical zones. Hamadryas baboons show a greater ecological plasticity than olive baboons, which are confined to riverbeds with extended gallery forest. By the end of 1999, a hybrid zone could not be confirmed.     

Knowledge acquired and decisions made: triadic interactions during allogrooming in wild bonnet macaques,Macaca radiata.

The pressures of developing and maintaining intricate social relationships may have led to the evolution of enhanced cognitive abilities in many nonhuman primates. Knowledge of the dominance ranks and social relationships of other individuals, in particular, is important in evaluating one''s position in the rank hierarchy and affiliative networks. Triadic interactions offer an excellent opportunity to examine whether decisions are taken by individuals on the basis of such knowledge. Allogrooming supplants among wild female bonnet macaques (macaca radiata) usually involved the subordinate female of a grooming dyad retreating at the approach of a female dominant to both members of the dyad. In a few exceptional cases, however, the dominant member of the dyad retreated; simple non-cognitive hypotheses involving dyadic rank differences and agonistic relationships failed to explain this phenomenon. Instead, retreat by the dominant individual was positively correlated with the social attractiveness of her subordinate companion (as measured by the duration of grooming received by the latter from other females in the troop). This suggests that not only does an individual evaluate relationships among other females, but does so on the basis of the amount of grooming received by them. Similarly, the frequency of approaches received by any female was correlated with her social attractiveness when she was the dominant member of the dyad, but not when she was the subordinate. This indicated that approaching females might be aware of the relative dominance ranks of the two allogrooming individuals. In logistic regression analyses, the probability of any individual retreating was found to be influenced more by her knowledge of her rank difference with both the other interactants, rather than by their absolute ranks. Moreover, information about social attractiveness appeared to be used in terms of correlated dominance ranks. The nature of knowledge acquired by bonnet macaque females may thus be egotistical in that other individuals are evaluated relative to oneself, integrative in that information about all other interactants is used simultaneously, and hierarchical in the ability to preferentially use certain categories of knowledge for the storage of related information from other domains.     

Infants as a commodity in a baboon market

We used data from adult female chacma baboons, Papio cynocephalus ursinus, to provide the first test of hypotheses on interchange trading and the structure of a biological market (Noë & Hammerstein 1994, Behavioral Ecology and Sociobiology,35, 1-11) within a primate group. The interchange commodities selected were grooming and handling of infants less than 3 months of age. Patterns of grooming in relation to infant handling showed strong evidence for interchange. Grooming for infant access was initiated by potential handlers and was significantly likely to be nonreciprocated. More critically, the data show that infant ‘supply’ created a market effect: grooming bout duration (the price ‘paid’ for handling) was inversely related to the number of infants present in the group. In addition, there was an inverse relationship between grooming bout duration and the rank distance between mothers and handlers, suggesting that higher-ranking mothers could demand a higher price for infant handling. Where rank distance was high, females were able to handle infants without grooming. Dominance could thus be used to disrupt the infant market effect. If biological markets models are to be fully applicable to primate groups (and those of other social mammals) then the potentially distorting effect of dominance needs to be incorporated into the framework. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Tool use in captive hamadryas baboons

A subadult male of a captive harem of hamadryas baboons learned, by instrumental trial-and-error learning, to use a tool to supply food for the harem. The behavior did not spread through the harem by imitation. The subadult male's rank in the harem's dominance hierarchy did not change as a result of his tool use.