The Market Effect in the Wood Mouse, Apodemus sylvaticus:Selling Information on Reproductive Status

Grooming in the wood mouse is a means by which males obtain information about the reproductive state of females, as grooming creates a situation which allows the male to smell the groomed female’s anogenital area to ascertain her phase of oestrus. Although grooming is reciprocal in this species, it is asymmetrical in that males groom females more often than vice versa. This grooming asymmetry was studied using Markov chain analysis for grooming sequences in two captive wood mouse colonies, and transition rates were used to represent motivation in both sexes. Grooming sessions were often initiated by a male’s attempt to sniff an immobile female’s anogenital region, while the female would immediately react by avoiding or biting the male. In order to entice the female to remain, the male would begin grooming the female’s head and shoulder area, surreptitiously and consistently grooming downwards towards the female’s anogenital region, until she would again terminate such contact either by avoiding or biting the male. While, therefore, the male’s tendency to sniff the female’s anogenital region was stronger than his tendency to groom her, the female’s tendency to terminate the male’s naso-anal contact was much stronger than her tendency to terminate his grooming bouts. If the male did not initiate grooming after the female terminated naso-anal contact, she avoided further contacts and escaped. In mice, as in most mating systems, the demand for matings by males is far larger than the number of matings females offer. The mating market, therefore, is highly skewed, which gives females the opportunity to demand ‘commodities’ in return for allowing males to mate. This system allows females to ‘bargain’ with males to obtain grooming in return for anogenital contact. Females assess the length of time they receive grooming and will only allow males to attain anogenital contact after a certain threshold value has been passed. If anogenital contact provides the male with information about the female’s reproductive state and/or with sexual stimulation, then this process represents the first quantified example in short-lived mammals of females ‘selling sex’ in terms of the market effect. This paper therefore provides a new view of the regulation of grooming: grooming is not simply reciprocal with both participants concerned that the other does not ‘cheat’ (e.g. tit-for-tat (TFT)-like strategy), rather grooming is a commodity which can be bartered against female reproductive information or matings.     

Social structures in Pan paniscus: testing the female bonding hypothesis

Based on previous research in captivity, bonobos, Pan paniscus, have been called a female-bonded species. However, genetic and behavioural data indicate that wild females migrate. Bonding between these unrelated females would then be in contradiction with socio-ecological models. It has been argued that female bonding has been overemphasized in captive bonobos. We examine patterns of proximity, grooming and support behaviour in six well established captive groups of bonobos. We find that female bonding was not a typical characteristic of all captive bonobo groups. In only two groups there was a trend for females to prefer proximity with other females over association with males. We found no evidence that following or grooming between females was more frequent than between males and unrelated females or between males. Only in coalitions, females supported each other more than male–female or male–male dyads. We also investigated five mother–son pairs. Grooming was more frequent among mothers and sons than in any other dyad, but sons did not groom their mothers more than males groomed unrelated females. Mothers groomed their sons, or provided more support to them than females groomed or supported unrelated males. Thus, while bonds between females were clearly present, intersexual relations between males and either unrelated females or their mothers are of more, or equal importance.     

Grooming and Infant Handling Interchange in <Emphasis Type="Italic">Macaca fascicularis</Emphasis>: The Relationship Between Infant Supply and Grooming Payment

Female long-tailed macaques are attracted to infants and frequently groom mothers bearing them. Such grooming often involves the groomer contacting the infant and may be a trade of grooming for infant handling. To identify if grooming and infant handling are directly traded, I collected samples on times after female-to-mother grooming and on interactions in which a female groomed a mother and contacted her infant. I determined that grooming tended to promote an exchange with infant handling and that the supply of available infants was related to how long a female groomed a mother. Grooming interactions were longer when infants were scarce in the surrounding social environment than when they were abundant, indicating a possible supply-and-demand effect. This supports that grooming may be payment for infant handling. Grooming-infant handling interchanges tended to be unidirectional as mothers usually did not reciprocate grooming. Instead, infant contact occurred. A larger proportion of grooming-infant handling interchanges involved younger infants, but infant age did not seem to influence grooming durations. The length of female-to-mother grooming had no observable effect on handling time. Lower-ranked females groomed higher-ranked mothers and their infants longer than vice versa. Moreover, it was possible to predict up-rank grooming via supply and demand better than down-rank grooming. There was no observable influence of kinship on grooming-infant handling interchange. These results support the conclusion that grooming and infant handling may be traded. Grooming promoted infant handling, while supply and rank predicted the grooming payment a female would offer to access an infant.     

Grooming Between Male Chimpanzees at Ngogo,Kibale National Park. I. Partner Number and Diversity and Grooming Reciprocity

Allogrooming serves many social functions in primates. Grooming can help individuals to service social relationships generally, sometimes reciprocally, and may be particularly important in the development and maintenance of alliances. However, time constraints limit the number of partners with whom one individual can groom enough to maintain cooperative relationships. As a result, the size of its grooming network may reach an asymptote as the size of its group increases, and it may distribute its grooming less equally among potential partners. Chimpanzees live in multimale, fission-fusion communities; males are philopatric, and commonly associate and groom with each other. Males form within-community alliances that influence dominance rank and access to mates, and allies groom with each other regularly; males also cooperate in aggression between communities. The chimpanzee community at Ngogo, in Kibale National Park, Uganda, is unusually large and has more males than any other known community. Field data show that adult Ngogo males groomed far more with other adult males than with females or with adolescent males, in contrast to a previous report (Ghiglieri, 1984). Adolescent males groomed adults much more than the reverse; males groomed and were groomed by females about equally. Individual males groomed mostly with a small number of other males. On average, males at Ngogo had only slightly more male grooming partners overall and had the same number of important partners as those of males in a much smaller community in the Mahale National Park, Tanzania, and they distributed their grooming less equitably. These results fit those expected if limits on available grooming time cause males to have a loyalty problem as the number of potential grooming and alliance partners increases. Despite differences in the extent and equitability of their grooming networks, males at both Ngogo and Mahale showed reciprocity in grooming. Grooming reciprocity has been demonstrated for captive chimpanzee males, but the Ngogo findings are the first demonstrations of reciprocity in wild communities.     

Development of social grooming between mother and offspring in wild chimpanzees

Grooming between female chimpanzees and their offspring was studied in the Mahale Mountains, Tanzania. Infants under 2 years of age rarely groomed their mothers, and mostly groomed accessible parts of their mother's bodies, if they did so. Most older adolescents reciprocated grooming with their mothers almost equally. Daughters appeared to mature socially earlier than sons, judging from the earlier ages at which a female infant began to groom her mother, groom mutually with her, and groom others. Weaning infants groomed their mothers more when they were in oestrus than when they were not. Development of the use of grooming as a means of social manoeuvring is discussed.     

The social grooming of captive female rhesus monkeys: Effects of the births of their infants

We observed the grooming interactions of 13 female rhesus monkeys (Macaca mulatta)before and for 12 weeks after the births of their infants. Mothers groomed for similar amounts of time before and after the birth of their infants, but after the birth, the grooming they directed to their infants may have been at the expense of that directed to other partners. Lactating females did not receive more grooming from other females but were approached more often, suggesting that they were more attractive. Mothers that groomed their infants most groomed others least, as if grooming time was limited for each mother or as if she was trying to compensate for avoiding interactions with other partners. Mothers of male infants groomed others more than mothers with female infants did, which might be due to mothers with daughters receiving more aggression and therefore avoiding interaction. Experienced and high-ranking mothers groomed their newborn infants considerably more than primiparous mothers did in the 24 hr following birth. Grooming was preferentially directed at close kin before the births of the infants. Mothers tended to groom higher-ranked partners more than they were groomed by them, and they tended to receive more grooming from lower-ranked partners than they gave, as suggested in models of rank attractiveness.     

Social grooming in assamese macaques (Macaca assamensis)

Reciprocity and social bonding hypotheses were evaluated as explanations for observed patterns of social grooming in assamese macaques (Macaca assamensis). In accordance with social bonding, females, as the long-term residents of this matrifocal group, groomed each other and juveniles more often than males groomed one another or juveniles. On the other hand, males groomed females more often and for longer durations than females groomed males and, whereas both males and females groomed juveniles more often than juveniles groomed them, juveniles groomed their elders for longer durations. Male grooming of females did not seem directly related to matings as males are single mount ejaculators and use coercive mating tactics. Male grooming of females could not be accounted for in terms of reciprocity; it was not a simple function of dominance. Although both sexes groomed subordinate females more than vice versa, males groomed dominant males more and females groomed subordinate males more than they received grooming from them. Grooming was concluded to function to establish and maintain affiliative social bonds rather than as a specific mechanism to obtain matings or any other specific reciprocation in terms of services or favors.     

Mating patterns,mate choice,and birth season heterosexual relationships in free-ranging rhesus macaques

Birth season adult heterosexual nonkin relationships of 50 free-ranging female rhesus macaques (Macaca mulatta) in two social groups at Cayo Santiago, Puerto Rico were examined using focal follow (289 hr) and ad lib data. Eighty-eight percent of subjects had at least one relationship characterized by particularly high frequencies of spatial proximity, grooming, or both. These were designated “friendships.” Males intervened in aggressive interactions more frequently on behalf of Friends than non-Friends. Female aggressive support of males was extremely rare. Higher-ranking males experienced more friendships than lower-ranking males. High-ranking females had higher-ranking Friends than low-ranking females. Older females had higher-ranking Friends than younger females. Females groomed high-ranking Friends more than they were groomed by them, whereas they groomed low-ranking Friends less than they were groomed by them. In one social group, high-ranking females were more likely than low-ranking females to groom their Friends more than they were groomed by them. Males were more responsible than females for spatial proximity maintenance in 9 of 14 Friend dyads for which sufficient data were available. Neither male nor female dominance rank affected responsibility for proximity maintenance in Friend dyads. Eight of 24 females had friendships with males with whom they had completed copulations during their conception peri-ovulatory period of the preceding mating season. Two of 19 females completed peri-ovulatory copulations with Friends during the following mating season. Friendship was not correlated with either of two demonstrated female mate choice indicators: (1) proximity maintenance during estrus; or (2) cooperation with male “hip-grasp” courtship attempts. Males directed “muzzle-up” courtship signals at lower rates toward Friends than toward non-Friends. These and other investigators' results indicate that (1) protection from aggression is the primary benefit to female rhesus macaques of birth season heterosexual relationships; (2) the most effective protectors are in greatest demand as Friends; and (3) friendship has no effect or an inhibitory effect on mate choice in this species. Benefits to males of friendships were not apparent from this study but may include coalitional support against lower-ranking males.     

Grooming behavior of spider monkeys (Ateles geoffroyi) on barro colorado Island,Panama

Quantitative grooming data are presented for free-ranging black-handed spider monkeys (Ateles geoffroyi) on Barro Colorado Island, Republic of Panama. A total of 126 grooming sessions was recorded, with an average session length of 2.0 min (range, 0.1 to 10.0 min). Grooming was an infrequent behavior; on average, individuals allocated only 2.5% of their daily activity to grooming. Two daily peaks of grooming activity were observed, one near midday and another in the late aftermoon between 1600 and 1700. Adult females groomed most frequently, followed by males and then juveniles. Juveniles were the most frequent recipients of grooming, followed by females and then males. Individual preferences were observed primarily between mother-offspring, male-male, and juvenile-male grooming partners in this male-bonded fission-fusion, species. Grooming interactions reflect many of the social characteristics of spider monkey societies: intraclass grouping preferences, long period of juvenile dependence, male philopatry, and female dispersal.     

Complex patterns of grooming and sexual activity in Barbary macaques (Macaca sylvanus)

Grooming in primates is often considered a “currency” that can be exchanged for other “services” or “commodities” such as reciprocal grooming, coalitionary support, infant handling, tolerance around food sources, active food sharing, or mating opportunities. Previous studies on primate grooming‐for‐sex exchange viewed the males as the demanding class, with the females as suppliers of mating opportunities. In this study, we examine the broader context of grooming‐for‐mating exchange in Barbary macaques in Gibraltar. Our data show that Barbary macaque males groom females with whom they are mating more frequently and for longer periods than other females, and the relationship between grooming and mating remains significant in both sexual and nonsexual contexts. In addition, females groomed males with whom they were mating more frequently and for longer periods than other males. In both sexes, grooming was observed to be far more frequent and to occur for longer durations in sexual compared to nonsexual contexts. We did not find any difference in grooming behavior between presexual and postsexual contexts. Our data suggest that there is no simple model to describe Barbary macaque grooming patterns in sexual contexts. Although our results are partly consistent with male use of grooming as payment for mating, broadly assessed grooming‐mating patterns cannot be solely explained by a male‐driven grooming‐for‐mating exchange.     

Grooming and the Expectation of Reciprocation in Mandrills (<Emphasis Type="Italic">Mandrillus sphinx</Emphasis>)

It is often (implicitly) assumed that the expectation of reciprocation motivates animal altruism, and thus that animals “plan” their social interactions. We tested this hypothesis by studying a captive group of mandrills (Mandrillus sphinx). In our focal group, the alpha male was more likely to provide agonistic support in the minutes after the receipt of grooming than in the absence of previous grooming. This offered other group members the possibility of manipulating the male’s support by grooming him before engaging in an aggression. We used survival analysis to test the hypothesis that the other group members systematically groomed the alpha male just before engaging in aggression, which would suggest that the expectation of reciprocation motivated their grooming. Contrary to the prediction of our hypothesis, we found that other group members did not groom the alpha male just before engaging in aggression, and thus did not benefit from increased support from the most effective ally. These results suggest that mandrills do not plan their social interactions and that the expectation of reciprocation does not motivate them to groom.     

Affiliative relations among male Japanese macaques (Macaca fuscata yakui) within and outside a troop on Yakushima Island

Male Japanese macaques (Macaca fuscata yakui) in a troop on Yakushima Island frequently groom other males. However, previous studies have not compared the social relations of troop males to those of non-troop males. I followed all troop males and non-troop males in and near a troop during a mating season and during the following non-mating season and recorded their neighbors, grooming, and agonistic interactions. Comparisons of the social relations of troop males and non-troop males with other troop members revealed that grooming and agonistic interactions with females during the mating season were similar between troop and non-troop males. However, troop males groomed each other more often and had fewer agonistic interactions among themselves than did non-troop males. Compared to what occurred in the mating season, troop males groomed females less often and exchanged grooming bouts more often with other troop males during the non-mating season. One non-troop male groomed females more frequently than did any troop male in both seasons, and this male groomed troop males more frequently than did any troop male in the non-mating season. This male immigrated into the troop during the following mating season. Regardless of their competition with respect to reproduction, male Japanese macaques on Yakushima Island maintain affiliative relations, probably to cooperatively defend fertile females from non-troop males.     

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.     

Social behaviour and infant carrying in a group of moustached tamarins,Saguinus mystax (primates: Platyrrhini: Callitrichidae), on Padre Isla,Peruvian Amazonia

The social behaviour of a group of eight moustached tamarins,Saguinus mystax, (five males, three females) was studied on Padre Isla in northeastern Peru. About 60% of all allogrooming was done by the two adult males in the group, and about 11% by a young adult female. All other group members groomed very little. The adult breeding female received more grooming than any other group member. After the death of the adult female (preyed upon by an anaconda) the amount of active allogrooming remained constant for all group members except for the young adult female, who increased her contribution to about 30%. Her preferred grooming partner was the subadult female, which generally screamed when being groomed by the young adult female and terminated grooming by going away. This kind of grooming relation is termed “forced grooming” and is interpreted as a possible social control mechanism. The young adult female groomed the adult males more often after the death of the adult female than before. This might have had the function of strengthening the social bond with the adult males and in obtaining the breeding position in the group. After the death of the adult female, the vulva of the young adult female grew to full adult size. Agonistic behaviour was less frequent than allogrooming. Most aggressive interactions (50%) originated from the subadult male of the group. The young adult female was the target of most of these aggressions. Extremely little aggression occurred between the three females. The young adult female was the only individual who tried to emigrate from the group during the study period. Her attempt to join a neighbour group failed due to rejection by all four members of this group. All group members participated in carrying an infant, but the adult males and the young adult female carried most frequently. Contribution to infant carrying varied with the infant's age.     

Grooming Patterns in the Primitively Eusocial Wasp Polistes dominulus

Grooming is a commonly observed behavior in many animals. One function of grooming is to clean the body of debris and parasites. An additional function may be to homogenize chemical cues present on the body. This latter purpose is especially likely in species in which contact‐based chemical communication occurs, such as in eusocial insects. In this study we address the context, sequence, frequency and duration of 683 acts of self‐grooming performed by the paper wasp, Polistes dominulus. In general, individuals groomed heads after cell inspections, and abdomens after sitting, suggesting that grooming serves to remove debris from the body. Although no differences were observed in the total amount of time spent grooming, foundresses groomed significantly more often than did workers. Wasps were equally likely to groom thoraces or abdomens following heads, but were more likely to groom abdomens after thoraces and heads after abdomens. Interestingly, the appendages used to groom individual body parts were highly specific (e.g. the prothoracic legs were used for the head), thus indicating that grooming is not used to homogenize chemical cues across the body surface of the wasp.     

Self‐Grooming Response of Meadow Voles to the Odor of Opposite‐Sex Conspecifics in Relation to the Dietary Protein Content of Both Sexes

Many animals self‐groom when they encounter the scent marks of opposite‐sex conspecifics. Self‐grooming transmits odiferous substances that contain information about the groomer’s condition, which is affected by its nutritional state. We tested the hypothesis that the amount of time that individuals self‐groom to opposite‐sex conspecifics is affected by the amount of protein in their diet and that of the scent donor. We did so by feeding meadow voles (Microtus pennsylvanicus) a diet containing 9%, 13%, or 22% dietary protein for 30 d and observing their self‐grooming behavior when they were exposed to bedding scented by an opposite‐sex conspecific (odor donor) fed one of the three diets, or fresh cotton bedding (control). The hypothesis was partially supported. We found that the protein content of the diet of male and female groomers did not affect the amount of time they self‐groomed. However, the protein content of the diet of male odor donors affected the amount of time that female voles spent self‐grooming. Female voles self‐groomed more in response to male odor donors fed a 22% protein‐content diet than to those produced by male odor donors fed either a 9% or a 13% protein‐content diet. Interestingly, the amount of time males self‐groomed was not affected by the protein content of the diet of the female odor donor. These results may, in part, be explained by the natural history of free‐living meadow voles, sex differences in costs associated with mate attraction and reproduction, and the direct or indirect benefits that females receive from males fed a diet high in protein content.     

'Gatherings' of social grooming among wild chimpanzees: implications for evolution of sociality

Chimpanzees (Pan troglodytes) often groom in gatherings that cannot simply be divided into unilateral dyadic grooming interactions. This feature of grooming is studied at two different levels: grooming cliques and grooming clusters. Grooming cliques are defined as directly connected configurations of grooming interactions at any given moment, and when any member of a clique successively grooms any member of another clique within 5min and within a distance of 3m, all the members of both cliques are defined as being in the same grooming cluster. Twenty-seven types of cliques are observed, with the largest one consisting of seven individuals. Mutual and/or polyadic cliques account for more than 25% of all cliques. The size of grooming clusters varies from two to 23 individuals, and almost 70% of the grooming time is spent in polyadic clusters. Although adult males groom the longest in relatively smaller clusters (size=2-4), adult females groomed the longest in clusters of five or more individuals. A review of the literature implies that mutual and polyadic cliques occur less often in other primate species than in chimpanzees. The importance of overlapping interactions for these kinds of gatherings and its possible significance in the evolution of sociality is discussed in this article.     

The function of allogrooming in domestic cats (Felis silvestris catus); a study in a group of cats living in confinement

Grooming interactions (n=83) occurring in a group of non free-ranging adult neutered male (n=14) and female (n=11) domestic cats (Felis silvestris catus) were analysed. Grooming was not induced by the proximity (distance <=0.5 m) of another animal. Grooming was in general directed at the head-neck area. Higher ranking animals groomed lower ranking animals more often than the other way round. Groomers tended to adopt ‘higher’ (standing, sitting upright) postures than groomees (sitting, lying). Agonistic behaviour occurred in 35% of interactions. Groomers showed offensive behaviour more often than groomees, most often after grooming a partner. Furthermore groomers often groomed themselves after grooming a partner. The degree of relatedness of animals did not affect the frequencies or durations of grooming. These results are consistent with the hypothesis that allogrooming in domestic cats may be a way of redirecting (potential) aggression in situations in which overt aggression is too costly. The data were previously presented at the 29th International Congress of the International Society for Applied Ethology (van den Bos, R. (1995) Allogrooming in domestic cats in confinement, Proceedings of the 29th International Congress of the International Society for Applied Ethology, S.M. Rutter et al. (Eds.), pp. 109–110)     

Decision making in grooming by Japanese macaques (Macaca fuscata)

I analyzed the temporal organization of individual Japanese macaques’ (Macaca fuscata) grooming sequences in 14 mothers and 13 offspring of different age/sex classes and 4 nonkin females. I hypothesized that preceding grooming affects subsequent grooming by the same individual. Grooming bouts were likely to be terminated as the bouts became longer when females groomed nonrelatives. Moreover, the duration of first bouts was longer than that of following bouts. These effects were also seen in grooming of mothers by their offspring > 1 year old and that of adult and adolescent female offspring by their mothers. In contrast, neither the duration of first bouts nor the number of preceding bouts had much effect on the occurrence or duration of subsequent bouts in any subject.     

Dominance,grooming, and clasped-sleeping relationships among bonnet monkeys in India

Social relationships, including dominance, grooming, and clasped-sleeping, were studied in a troop of bonnet monkeys (Macaca radiata) at Dharwar, India, the study period lasting two months and a half. Three measurements, the peanut test, the drinking test, and the spatial distribution test, were used to analyze dominance relationships. The peanut test showed a straight linear ranking order among adult males and females; however, among females drinking and spatial distribution orders are slightly different from that of feeding (peanut test). Grooming was observed more frequently between adult female and adult female and was seldom observed between adult male and juvenile female or between juvenile male and juvenile female. Apparently all monkeys tend to groom with females. On the other hand, monkeys of the same sex tend to sleep with each other. It is clear that monkeys select their partners when they groom and sleep.