Behavioral responses of free-ranging rhesus monkeys to food shortage

During early July 1968, a severe food shortage occurred on Cayo Santiago, an island colony of free-ranging rhesus monkeys (Macaca mulatta). The food shortage produced striking changes in the behavior of the monkeys. Within the one social group intensively studied, the total frequencies of grooming, play and fights decreased significantly; the frequency of matings also dropped; body contact, displacements by other groups, and non-displacement movements decreased, but not in statistically significant amounts. Changes in the percentage of total grooming attributable to related and unrelated monkeys reflected the stability of the rhesus matriline. Comparisons made between Cayo Santiago and other primate groups under analogous situations reveal similar responses to food shortage.     

Quantitative observations of grooming behavior in free-rangingMacaca mulatta

Quantitative methods of observation and analysis were used in a 12-month study of grooming behavior of free-rangingMacaca mulatta on La Cueva Island at La Parguera, Puerto Rico. Observations lasting 30–120 minutes were made from eight positions on the island at a standard time of day when monkeys were either feeding or resting. Two dependent variables were obtained: (1) the number of monkeys present in the observation area were noted by age and sex class at five-minute intervals throughout each observation, and (2) the frequency of grooming encounters was tabulated by the age and sex class(es) of groomer and recipient. These data were computed as grooms/hour/possible interacting combination of monkeys. Grooming frequencies were higher in non-feeding situations than when monkeys were feeding. The largest social group had the lowest mean grooming rates, while the smallest group had the highest grooming frequencies. More grooming occurred during the November-to-February mating season than at other periods of the year. Adult females were involved in over 60% of all grooming behavior, juveniles participated in 25% of the grooming, while adult males groomed females, primarily during the mating season, and rarely groomed other males or juveniles. Genealogical relationships, levels of group aggression and the feeding or resting context all influenced the frequency of grooming. This study provides support for the hypothesis that the basic social unit for rhesus macaques consists of a core of adult females with their juvenile and infant progeny.     

Grooming interactions among adult chimpanzees at Bossou,Guinea, with special reference to social structure

Grooming and proximity interactions among chimpanzees at Bossou, Republic of Guinea, were analyzed as an index of friendly and affinitive relationships among adult males, among adult females, and between the sexes. Data from the first (1976–1977) and the third (1982–1983) study period were used. The expected value of their interactions was calculated from the number of adult males and females in the group and also from the observed frequency of combinations of adult males and females in the parties (temporary foraging groups). In the pooled data from the two periods, there was little difference between grooming and proximity (without grooming). The frequency of male-female grooming and proximity interactions was lower than expected, and that of female-female interactions was higher than expected. The frequencies of male-male grooming and proximity were intermediate but fluctuated. Male-male grooming frequency was lower than that recorded in chimpanzees of East Africa. Characteristics of same-sex affinitive interactions, especially between Bossou chimpanzee females, clearly differ from those of East African chimpanzees and are more like those recorded for female-related groups of Japanese macaques (Macaca fuscata).These differences indicate the variability and flexibility of chimpanzee social structure.     

Book review: Advances in Human Palaeopathology

Severe dental wear and tooth loss is often assumed to impede the processing, breakdown, and energetic conversion of food items, thereby negatively impacting individual health, reproduction, and survival. Ring‐tailed lemurs at the Beza Mahafaly Special Reserve demonstrate exceptionally high frequencies of severe dental wear and antemortem tooth loss, yet often survive multiple years with these impairments. To test the hypothesis that these lemurs mitigate tooth loss through behavioral adjustments, we collected 191 h of observational data from 16 focal subjects, eight without tooth loss and eight with between 3% and 44% loss. These data indicate dentally‐impaired ring‐tailed lemurs show compensatory behaviors consistent with the demands of living in a social group. During early afternoon (12:00–14:30 h) individuals with loss showed trends towards higher frequencies of foraging and grooming, while individuals without loss rested significantly more often. Individuals with >10% loss (n = 7) showed higher frequencies of feeding, foraging, and grooming, and lower frequencies of resting during this period than individuals with <10% loss (n = 9). Individuals with tooth loss maintained relatively higher levels of feeding and foraging throughout the day. These individuals licked tamarind fruit at higher frequencies, likely spending more time softening it before ingestion. These individuals did not demonstrate longer feeding bouts overall, although bouts involving tamarinds were significantly longer. Individuals with marked toothcomb wear engaged in higher rates of certain types of allogrooming, demonstrating that social behaviors are used to compensate for reduced grooming efficiency. These data have implications for interpreting behavioral responses to dental impairment in the fossil record. Am J Phys Anthropol, 2009. © 2009 Wiley‐Liss, Inc.     

Inter-individual relationships in proboscis monkeys: a preliminary comparison with other non-human primates

This is the first report on inter-individual relationships within a one-male group of proboscis monkeys (Nasalis larvatus) based on detailed identification of individuals. From May 2005 to 2006, focal and ad libitum data of agonistic and grooming behaviour were collected in a forest along the Menanggul River, Sabah, Malaysia. During the study period, we collected over 1,968 h of focal data on the adult male and 1,539 h of focal data on the six females. Their social interactions, including agonistic and grooming behaviour, appeared to follow typical patterns reported for other colobines: the incidence of social interaction within groups is low. Of 39 agonistic events, 26 were displacement from sleeping places along the river, 6 were the α male threatening other monkeys to mediate quarrels between females and between females and juveniles, and 7 were displacement from feeding places. Although the agonistic behaviour matrix based on the 33 intra-group agonistic events (excluding events between adults and juveniles and between adults and infants) was indicative of non-significant linearity, there were some specific dominated individuals within the group of proboscis monkeys. Nonetheless, grooming behaviour among adult females within a group were not affected by the dominance hierarchy. This study also conducted initial comparisons of grooming patterns among proboscis monkeys and other primate species. On the basis of comparison of their grooming networks, similar grooming patterns among both-sex-disperse and male-philopatric/female-disperse species were detected. Because adult females in these species migrate to groups repeatedly, it may be difficult to establish the firm grooming exchange relationship for particular individuals within groups, unlike in female-philopatric/male-disperse species. However, grooming distribution patterns within groups among primate species were difficult to explain solely on the basis of their dispersal patterns. Newly immigrated females in some species including proboscis monkeys are eager to have social interactions with senior group members to improve their social position.     

Within-group social bonds in white-faced saki monkeys (Pithecia pithecia) display male-female pair preference

White‐faced saki monkeys (Pithecia pithecia) lack most of the behavioral and physical traits typical of primate monogamy [Fuentes, 1999 ]. In order to determine if social bonds in this species reflect patterns displayed by pair‐bonded groups or larger multimale–multifemale groups, we draw on 17 months of data collected on wild white‐faced sakis at Brownsberg Nature Park, Suriname. We analyzed within‐group social bonds for three habituated groups (one two‐adult and two multiadult groups) by measuring grooming, proximity, and approach/leave patterns between adult and subadult group members. We found that both two‐adult and multiadult groups showed significantly stronger social bonds between a single male–female dyad within each group (deemed “primary dyads”). In all three groups, primary dyads were composed of the oldest adult male and a breeding female. These pairs had significantly higher levels of grooming than other within‐group dyads and were also in close proximity (<1 m) more often than nonprimary dyads. Grooming in primary dyads was nonreciprocal, and consistently biased toward female investment. Grooming patterns in nonprimary dyads varied, but were often more reciprocal. Grooming and proximity of the primary dyad also changed in relation to infant development. Our results suggest that while white‐faced sakis do not show behavioral and physical traits typical of monogamy or pair‐bonding, social bonds are strongest between a single male–female pair. Pitheciine social systems range from small group monogamy in Callicebus to large multimale–multifemale groups in Chiropotes and Cacajao. As the middle taxon in this platyrrhine radiation, behavioral strategies of white‐faced sakis provide a model for how social bonds and affiliation could be influenced by and affect the evolution of larger group size in primates. Am. J. Primatol. 73:1051–1061, 2011. © 2011 Wiley‐Liss, Inc.     

Short-Term Benefits of Play Behavior and Conflict Prevention in Pan paniscus

Most theories on the function of play have focused on ultimate rather than proximate benefits. Play peaks during juvenility but, in some species, it is present in adulthood as well. In primates, social play and grooming often show a matched pattern because they bring individuals into close contact and favor social cohesion. In Pan, researchers have widely documented anticipation of competition at feeding time. Chimpanzees limit aggression over food by grooming (celebration), whereas bonobos use sociosexuality as a reassurance mechanism. We examined the function of play in the context of conflict prevention in the Apenheul bonobo colony. We analyzed the distribution of social play, grooming, and sexual contacts in periods around feeding and in a control condition. Adult-adult and adult-immature play frequencies were significantly higher during prefeeding than in any other condition, thus not supporting the commonly held view that social stress suppresses play. Further, there is a significant positive correlation between adult-adult play and rates of cofeeding. During feeding, adults engaged in their highest levels of sociosexual behaviors, whereas an increase in grooming rates occurred in prefeeding, though not significantly compared to the control rates. In conclusion, bonobos apparently cope with competition and social tension via 2 different mechanisms of conflict management: play to prevent tension, e.g., prefeeding, and sociosexual behaviors as appeasement and reassurance mechanisms once a tense situation emerges.     

Affiliation promotes the transmission of a social custom: handclasp grooming among captive chimpanzees

Handclasp grooming is a unique social custom, known to occur regularly among some, but not all populations of chimpanzees (Pan troglodytes). As with other cultural behaviors, it is assumed that this distinctive grooming posture is learned socially by one individual from another. However, statistical comparisons among factors thought to influence how a behavior spreads within a group have never, to our knowledge, been conducted. In the present study, the origination and spread of handclasp grooming in a group of captive chimpanzees was followed throughout more than 1,500 h of observation over a period of 12 years. We report on the frequency, bout duration, and number and demography of performers throughout the study period, and compare these findings to those reported for wild populations. We predicted that dyads with strong affiliative ties, measured by time spent in proximity to and grooming one another, were likely to develop a handclasp grooming partnership during the study period. A quadratic assignment procedure was used to compare correlations among observed frequencies of grooming and proximity with handclasp grooming in all possible dyads within the group. As predicted, the formation of new handclasp grooming dyads was positively correlated with the rate of overall grooming and proximity within a dyad. In addition, in nearly all dyads formed, at least one individual had been previously observed to handclasp groom. We concluded that affiliation and individual experience determines the transmission of handclasp grooming among captive chimpanzees.     

Why preen others? Predictors of allopreening in parrots and corvids and comparisons to grooming in great apes

Allogrooming in primates serves not only a hygienic function, but also plays a crucial role in maintaining strong affiliative bonds between group members, which in turn, underpin the emergence of cooperative behavior. In contrast, although allopreening occurs in many avian species, we know little about its social functions. Our study addresses this issue by investigating allopreening in a broad comparative data set including six corvid and nine parrot species. We assessed whether rates of allopreening initiations, proportion of time spent allopreening, and the number of grooming partners in captive group-housed birds were comparable to patterns observed in captive chimpanzees and bonobos. While parrots and corvids were found to have similar rates of social grooming to bonobos and chimpanzees, Pan species dedicated significantly more time to social grooming. Animals in larger groups had more grooming partners, but when controlling for the number of potential partners, birds tended to have fewer grooming interaction partners than Pan species. We then investigated whether allopreening in parrots and corvids was predicted by behavioral markers of affiliative social bonds (close physical proximity, active feeding, and low levels of agonistic behavior). Results revealed that providing allopreening to a partner was significantly predicted by often being in close proximity, but not engagement in active feeding or agonistic behavior. We examined the region allopreened in a subset of species and found that preening a partner's head was predicted by both close physical proximity and active feeding, while body allopreening was only predicted by close physical proximity. Head preening may confer more hygienic benefits to recipients, and thus, may be more selectively provided to valued partners. Results support the hypothesis that allopreening in corvids and parrots helps maintain social bonds with an individual's most important social partners, showing some similarities to allogrooming in primates.     

Attributes and validity of dominance hierarchy in the female pigtail macaque

A group of six unrelated female pigtail macaques,Macaca nemestrina, of the same age, was studied in captivity over a period of five years. The animals were observed under six different situations, following changes in the social composition of the group. The following social interactions were recorded: withdrawal, attack, threat, presentation, mount, and grooming. Although behavioural rates varied for each period, their distribution network was remarkably consistent. Each subject could be assigned a rank, which remained stable over the six periods. From an analysis of the number of dyads in which one of the two animal significantly performed both paired behaviours more than the other animal (external validity), behaviours clustered into two main groups: (1) attacks, threats, and withdrawals; and (2) mounts, presentations, and grooming. Quantitative methods were performed to standardize the degree in which linearity, stability, reciprocity, and idiosyncrasy of the interactions under study may account for social variability. When considering these properties, the behaviours clustered in the same two groups (“agonistic” and “affinitive”). A method to describe the dominance style ofMacaca nemestrina was proposed, which can easily be replicated for comparisons with females of other primate species and in different conditions.     

Social Organisation in an Enclosed Group of Red Deer (Cervus elaphus L.) on Rhum

Primate social organisation is often considered to be more complex than that of ‘lower’ mammals. The dominance hierarchy, which is given especial emphasis in most studies of social species, has been criticised on the grounds that rank is poorly related to other aspects of social organisation. These two ideas were investigated in an enclosed group of red deer by looking at the relationships between four aspects of social organisation: the dominance hierarchy; social grooming behaviour; non-copulatory mounting behaviour; spatial organisation. The last three aspects have frequently been studied in primates, but rarely in ungulates.     

Male chimpanzee development focusing on adolescence: Integration of behavioral with physiological changes

Intensive longitudinal behavior observations of male chimpanzees in stable mixed-sex social groups in a semi-natural environment were analyzed by state of development as defined by dental, growth and hormonal signals. Initial increase of sexual behaviors preceded adolescent hormonal changes. Peak prevalence of sexual behaviors coincided with the adolescent period. This period is also characterized by peak activity level and feeding. The major increase in aggression and stabilization of submissive behavior at adult level occurred concomitant with achievement of adult hormone levels and body size, and these were accompanied by increase of grooming affiliative behaviors.     

Social grooming in Tonkean macaques (Macaca tonkeana)

The distribution, form, and contexts of occurrence of social grooming were studied in two captive groups of Tonkean macaques (Macaca tonkeana), using interaction-dependent sampling. The social events surrounding grooming had little influence on its form, the participants' behavior being shaped mainly by physical constraints. Adult females were most often involved in grooming interactions. Grooming between adult females appeared more intimate than that between adult males and females. Kinship and dominance had no effect on the form or distribution of social grooming among adult females. It is concluded that social systems that are characterized by mild dominance relations allow individuals the freedom to interact in the way and with whom they wish.     

The social behavior of a marmoset (Saguinus fuscicollis) group II: Behavior patterns and social interaction

The behavioral patterns and social interaction of a marmoset (Saguinus fuscicollis) group in a semi-naturalistic environment were observed for 14 months. The analysis showed that, of the 32 behavior patterns observed, the 10 most frequent accounted for over 97 per cent of the total behavior. One pattern, sit and look, accounted for 44 per cent of the total behavior. The two most frequent social behavior patterns, grooming and social play, were concentrated in different parts of the group. The focal point of grooming was the adult female; social play was characteristic of younger animals 4–20 months of age. These results were compared with other studies of marmosets and with primate studies on grooming and social play.     

Stimulating effect of sugar dusting on honey bee grooming behaviour

The aim of this research was to investigate whether or not sugar dusting can stimulate the grooming behaviour in Apis mellifera L. (Hymenoptera: Apidae), an important defensive mechanism against Varroa destructor Anderson & Trueman (Acari: Varroidae), and to assess the most effective dose and frequency of treatment. The criterion for evaluation of grooming potential was the percentage of damaged mites (PDM) among the total number collected on the bottom boards of the hives. In each sugar‐treated group PDM was significantly higher in comparison both with the negative control (no treatment) and with the values preceding the treatment. The results point to a stimulating effect of sugar on the grooming behaviour at all doses and frequencies tested. Treatment frequency influenced the stimulating effect of sugar: treatments at 3‐ and 7‐day intervals with 30 and 40 g resulted in significantly higher PDMs than the least frequent treatment (every 14 days); dusting with 20 g influenced PDM only when repeated at 3‐day intervals. Because treatments at 3‐day intervals are time‐consuming, those with 40 or 30 g repeated every 7 days may be recommended. In the positive control (hives treated with amitraz), average PDM was significantly lower than in the negative control and all sugar‐treated groups. Possible causes of the stimulating effect of sugar dusting on bee grooming behaviour are discussed.     

Social grooming and play behavior of a captive group of chimpanzees

Aspects of the social grooming and play behavior of a group of six adolescent and young adult chimpanzees are contrasted and compared. Eleven months’ data indicate that older chimpanzees groomed more and played less than younger individuals. This transition period occurred earlier for females than males. Grooming behavior appeared to vary with reproductive state. A positive correlation was found between the estrous condition of cycling females and the amount of grooming that they received from the males. A mother of a young infant received particularly high levels of grooming from the other group members. Less variation among individuals was found for frequencies of play as compared to grooming. Play dropped following the death of one individual and was entirely inhibited for three weeks following the group’s transfer to a new environment and the reintroduction of a former group member. Comparison to a free-ranging population indicates important differences in both frequencies and general patterns of play and grooming.     

Matrilineal kin relationship and social behavior of wild bonobos (Pan paniscus): Sequencing the D-loop region of mitochondrial DNA

Matrilineal kin-relations among wild bonobos (Pan paniscus) were studied by DNA analysis. Subject individuals were the members of E1 group, living at Wamba, Zaire, which has been studied since 1974. DNA samples were extracted from wadges that bonobos spat out when feeding on sugar cane. The D-loop region of mitochondrial DNA was amplified by the PCR method, and a nucleotide sequence of 350 base pairs was determined for 17 individuals. Nucleotide variations were found at 44 positions of the sequence. Based on these variations, 13 matrilineal units were divided into seven groups, and the mother of an orphan male was determined among several females. These genetic analyses, together with behavioral observation to date, revealed the following facts. High sequence variation in the target region indicated that females transfer between groups of bonobos, which is in agreement with supposition from long-term field studies. For females, there was no relationship between genetic closeness and social closeness that is represented by frequencies of proximity or grooming. After immigration into a new group, females form social associations with senior females without regard to kin relationship.     

Group harmony in gibbons: Comparison between white-handed gibbon (Hylobates lar) and siamang (H. syndactylus)

The siamang (Hylobates syndactylus) is exceptional among gibbons in that its area of distribution almost completely overlaps those of other gibbons, namely the white-handed gibbon (H. lar) and the agile gibbon (H. agilis) of the lar group. The siamang has almost twice the body weight of the gibbons of the lar group (ca. 11 kg vs. 5–6 kg), and it has been suggested that distinct ecological and behavioural differences exist between the siamang and its two sympatric species. The siamang has been claimed to differ from the white-handed gibbon “in the closer integration and greater harmony of group life” (Chivers, 1976, p. 132). However, few quantitative data exist to support this hypothesis. In the present study, intra-group interactions in captive family groups of white-handed gibbons and siamangs (two groups of each species) were recorded by focal-animal sampling. These data failed to show a consistent association between species and most of the behavioural patterns recorded, such as frequency of aggression, percentage of successful food transfer, frequency of social grooming bouts, and duration of social grooming/animal/hr. A significant difference was found for only two of the variables: Individual siamangs in this study showed longer grooming bout durations, and made fewer food transfer attempts than lar individuals. Only the first of these two differences is consistent with the hypothesis mentioned above, whereas the lower frequency of food transfer attempts in siamangs is the opposite of what should be expected under the hypothesis. On the other hand, two of these behavioural patterns showed a significant correlation with the parameters group size and individual age: Both individuals in larger groups and younger individuals tended to show shorter grooming bouts and a smaller proportion of successful food transfers. Our findings indicate that social cohesion within these gibbon groups may be much more flexible according to and depending on social or ecological influences and less rigidly linked to specific gibbon taxa than previously assumed. A considerably larger number of gibbon groups would have to be compared to provide reliable evidence for or against species-specific differences in group cohesion. Another finding of this study—a positive correlation between the frequency of aggression and grooming—is discussed in the light of the functional interpretations commonly attributed to allogrooming behaviour in primates.     

Group size, grooming and fission in primates: a modeling approach based on group structure

In social animals, fission is a common mode of group proliferation and dispersion and may be affected by genetic or other social factors. Sociality implies preserving relationships between group members. An increase in group size and/or in competition for food within the group can result in decrease certain social interactions between members, and the group may split irreversibly as a consequence. One individual may try to maintain bonds with a maximum of group members in order to keep group cohesion, i.e. proximity and stable relationships. However, this strategy needs time and time is often limited. In addition, previous studies have shown that whatever the group size, an individual interacts only with certain grooming partners. There, we develop a computational model to assess how dynamics of group cohesion are related to group size and to the structure of grooming relationships. Groups’ sizes after simulated fission are compared to observed sizes of 40 groups of primates. Results showed that the relationship between grooming time and group size is dependent on how each individual attributes grooming time to its social partners, i.e. grooming a few number of preferred partners or grooming equally or not all partners. The number of partners seemed to be more important for the group cohesion than the grooming time itself. This structural constraint has important consequences on group sociality, as it gives the possibility of competition for grooming partners, attraction for high-ranking individuals as found in primates’ groups. It could, however, also have implications when considering the cognitive capacities of primates.