Greeting behavior during party encounters in captive chimpanzees

Party encounter situations were experimentally produced in a group of captive chimpanzees (Pan troglodytes verus) at the Primate Research Institute of Kyoto University, Japan. During weekends all subjects (two adult males and five adult females) usually stayed together in the rooms (Baseline condition). Under experimental conditions, we shut passages between rooms to divide the subjects into two groups. We examined the effects of temporal separation of group members on affiliative interactions, aggressive interactions, and simple proximity. The frequency of affiliative interactions between male and female chimpanzees and between female chimpanzees increased when they encountered one another after separation, irrespective of male identity or housing history. Therefore we considered affiliative interactions between males and females during party encounters as being the response between separated individuals. The same tendency was not found in the frequency of affiliative interactions between females or between males. Unlike affiliative interactions, neither aggressive interactions nor simple proximity were influenced by separation.     

Male chimpanzee behavior in relation to female ano-genital swelling

This study examined the relationships between male agonistic, affiliative, and sexual behaviors and female estrus condition in captive adolescent and young-adult chimpanzees (Pan troglodytes). Data on agonistic, affiliative, and sexual behaviors of 11 males living in three social groups were collected during daily 45 minute observations over a 5 month period. Female estrus condition was assessed daily using the relative size of the female's ano-genital swelling. It was hypothesized that the presence of maximally tumescent females would generate conflicts between males, so an increase in inter-male agonism was predicted. Males exhibited higher rates of agonism toward other males when at least one female in the group was maximally tumescent. Male affiliative behavior directed toward other males and social play with males were affected by the presence and number of maximally tumescent females. Male sexual behavior increased when maximally tumescent females were present.     

Social behavior in aged rhesus macaques

This study investigated the relationship between chronological age and social behavior in 42 adult male and female rhesus macaques (Macaca mulatta) in three specific areas: social interactions, social roles, and social networks. While both old males and old females share behavioral differences associated with senescence, this study reports that old females and old males are distinct in their social behaviors, both from each other and from other adults. Many of these differences appear progressive across age classes, e.g., declining across age classes in females and increasing across age classes in males. Old females are less social and have smaller social networks than other females, while the opposite was found to be true of old males. An explanation for the sex-based differences in aged social behavior and social networks reported in this study may originate in rhesus matrifocal social structure.     

Development of guidelines for assessing obesity in captive chimpanzees (Pan troglodytes)

Many captive chimpanzees (Pan troglodytes) are subjectively considered to be overweight or obese. However, discussions of obesity in chimpanzees are rare in the literature, despite the acknowledged problem. No study to date has systematically examined obesity in captive chimpanzees. This project develops guidelines for defining obesity in captive chimpanzees through the examination of morphometric and physiologic characteristics in 37 adult female and 22 adult male chimpanzees. During each animal's biannual physical exam, morphometric data was collected including seven skinfolds (mm), body mass index (BMI), waist‐to‐hip ratio (WHR), and total body weight (kg). The morphometric characteristics were correlated with triglycerides and serum glucose concentration, to test the utility of morphometrics in predicting relative obesity in captive chimpanzees. Abdominal skinfold (triglyceride: F=3.83, P=0.05; glucose: F=3.83, P=0.05) and BMI (triglyceride: F=10.42, p=0.003; glucose: F=6.20, P=0.02) were predictive of increased triglycerides and serum glucose in females; however no morphometric characteristics were predictive of relative obesity in males. Results suggest that no males in this population are overweight or obese. For females, there were additional significant differences in morphometric (skinfolds, BMI, WHR, total body weight) and physiologic measurements (systolic and diastolic blood pressure, red blood cells) between individuals classified overweight and those classified non‐overweight. Skinfold measurements, particularly abdominal, seem to be an accurate measure of obesity and thus potential cardiovascular risk in female chimpanzees, but not males. By establishing a baseline for estimated body fat composition in female captive chimpanzees, institutions can track individuals empirically determined to be obese, as well as obesity‐related health problems. Zoo Biol 0:1–12, 2007. © 2007 Wiley‐Liss, Inc.     

Ontogeny of a Social Custom in Wild Chimpanzees: Age Changes in Grooming Hand‐Clasp at Mahale

Among cultural behaviors of chimpanzees, the developmental processes of complex skills involved in tool use are relatively well known. However, few studies have examined the ontogeny of social customs that do not require complex skills. Thus, in this study, we describe the developmental process of the grooming hand‐clasp (GHC), one of the well‐known social customs of chimpanzees at Mahale. We have collected 383 cases of GHC where at least one of the participants was 15 years old or younger during 1994–2007. First performances of GHC with the mother were observed at around 4–6 years old; the earliest observed age was 4 years and 4 months old. The first performances of GHC with nonrelated females were at around age 9 years, and those with adult males at around 11 years. However, some orphans engaged in GHC earlier than nonorphans. By gradually expanding GHC partners from the mother to other females and then to males, chimpanzees increased the number of GHC partners with age. Young males were observed to perform GHC with larger numbers of partners than were young females. GHC by young chimpanzees was shorter in duration than that among adults. Overall, the ontogeny of GHC showed several dissimilarities with that of tool use and was more an extension of the development of typical grooming behavior. For example, infants did not try to perform GHC initially; instead, mothers were more active in the earliest stages. These results suggest that not all socially learned cultural behaviors are acquired in the way of learning tool use. There may be various ways of learning behavioral patterns that are performed continuously in a group and that consequently comprise culture in chimpanzees. Am. J. Primatol. 75:186‐196, 2013. © 2012 Wiley Periodicals, Inc.     

Factors affecting wounding aggression in a colony of captive chimpanzees (Pan troglodytes)

Previous research has suggested that chimpanzees (Pan troglodytes) display higher levels of aggression in captivity than in the wild. One of the challenges of captive management, therefore, is to balance the chimpanzees' need for social interaction with managements' desire to minimize wounding and aggression. Various captive studies have examined the effects of individual and social variables on the frequency of wounding aggression, but none have examined these variables simultaneously. We collected retrospective wounding data for severe wounds from 83 captive chimpanzees (36 males, 47 females) from January 1993 to December 2003. The context of the wounding event, including individual age and sex, group age and sex composition, group duration, and portion of the week (weekday vs. weekend) were collected. Logistic regression analysis was performed to determine which variables had a significant effect on the probability of a severe wounding event. The sex and age composition of the group, group duration, and portion of the week had a statistically significant association with wounding. All‐male groups (Odds Ratio (OR)=6.738) had the highest risk of wounding aggression, with uni‐male groups (OR=3.311) having the next largest. Compared to individuals in all sub‐adult groups, individuals in either all‐adult (OR=4.516) or mixed‐age (OR=3.587) groups had a higher risk of wounding. There was an inverse association between group duration and wounding (OR=0.821). Finally, there was an increased risk of wounding during the work week (OR=1.653). These results suggest that captive management should pay close attention to group composition, as well as levels of human activity, when devising strategies to reduce captive chimpanzee aggression. Zoo Biol 29:351–364, 2010. © 2009 Wiley‐Liss, Inc.     

Hypertension Increases With Aging and Obesity in Chimpanzees (Pan troglodytes)

Cardiovascular disease is a primary cause of morbidity and mortality in captive chimpanzees. Four years of blood pressure (BP) data were analyzed from a captive former laboratory population of 201 healthy adult chimpanzees with assessment of age and obesity on elevated BP. Five different measures of obesity were compared: abdominal girth, basal metabolic rate, body‐mass index (BMI), body weight, and surface area. Systolic BP varied by sex. Obesity did not influence male BP. For females, obesity was a significant determinant of BP. The best measure of female obesity was basal metabolic rate and the worst was BMI. Median systolic BP of healthy weight females (<54.5 kg) was significantly lower (128 mmHg) than overweight or obese females (140 mmHg), but both were lower than all males (147 mmHg). For diastolic BP, neither sex nor any of the five obesity measures was significant. But age was highly significant, with geriatric chimpanzees (>30 years) having higher median diastolic BP (74 mmHg) than young adults of 10–29 years of age (65 mmHg). By these criteria, 80% of this population is normotensive, 7% prehypertensive, and 13% hypertensive. In summary, systolic BP intervals required adjustment for obesity among females but not males. Diastolic BP required adjustment for advanced age (≥30 years). Use of these reference intervals can facilitate timely clinical care of captive chimpanzees. Zoo Biol. 32:79‐87, 2013. © 2012 Wiley Periodicals, Inc.     

Absence of strongly kin-preferential behavior by adult female sooty mangabeys (Cercocebus atys)

The objective of this study was to test the hypothesis that kin-preferential behavior would be present in sooty mangabeys (Cercocebus atys), a species taxonomically close to baboons and macaques. The affiliative behavior of the adult female members of a large captive group of these mangabeys was analyzed to test this prediction. These females groomed, were approached by, were in proximity to, and were in contact with their kin significantly more than expected, but only when all kin were included in the analysis. Removal of only the mother-infant (less than 1 year) dyadic interactions removed all significant kin effects. Kin-preferential behavior was also absent in affiliative interactions among the adult females as a class. Affiliation between mothers and offspring significantly exceeded that for all other kinship categories (such as siblings, etc.), and affiliation with kin other than offspring did not differ from that with nonkin adults. In their interactions with nonkin, the adult females showed some preference (duration of grooming) for those adult females of similar age, an effect predicted by the intensity of interaction among members of the same age cohort during development. These similar-aged females may also be paternally related. In comparing these results with the existing literature on kin-preferential behavior, two conclusions may be reached: (1) age and degree of kinship are primary factors that must be considered in order to avoid the existing overgeneralization of the importance of kinship in primate social organization, and (2) the role and importance of affiliative behavior in kin-selection theory should perhaps be re-examined in light of questions raised by this study.     

Integration of a hand-reared chimpanzee (Pan troglodytes) infant into a social group of conspecifics

Rejections of infants among non-human primates occasionally occur in the wild as well as in captive settings. Controlled adoptions of orphans and introductions of individuals into new groups are therefore sometimes necessary in captivity. Consequently, behavioral research on integration procedures and on the acceptance of infants by adoptive mothers is much needed. In this study, the introduction and subsequent adoption were examined in an 18-month-old hand-reared chimpanzee (Pan troglodytes). The infant was introduced into an age/sex-diversified social group of conspecifics at Furuvik Zoo, Gävle, Sweden, and continuous focal data was collected during the final stage of integration, including infant care exhibited by the group members and the infant’s secure base behavior. The infant was successfully integrated into the group and engaged in positive social interactions with all group members. An adult primiparous female chimpanzee formed a bond resembling a mother–infant relationship with the infant, which continues to be maintained at publication. However, the female initially showed very limited interest in the infant. It was, in fact, two other younger female group members that exhibited most infant care. The infant’s secure base behavior patterns indicate that she adapted well to the new circumstances in the chimpanzee group as the integration progressed. This provides evidence that a final adopter does not necessarily initially show maternal interest and that there can be flexibility in maternal behavior in adult chimpanzee females. Moreover, the methods applied employing gradual familiarization with all the group members and the use of an integration enclosure, may have contributed to a successful result. These findings extend our knowledge of introduction procedures in captivity as well as provide information on foster mother–infant attachment in chimpanzees.     

Development in the Usage and Comprehension of Greeting Calls in a Free‐Ranging Group of Japanese Macaques (Macaca fuscata)

The main objective of this study is to clarify the developmental process involved in both the usage of greeting calls and the response to greeting calls by Japanese macaques. These greeting calls facilitate affiliative interactions by communicating benign intent. Specifically, individuals frequently emit greeting calls when interacting with less‐predictable individuals. Here, we examined whether the targets at which greeting calls are directed, along with associated behavioral responses, differed among the age classes, by conducting a cross‐sectional observation of females aged 0–5 yr and their mothers. We found that infant females showed a weak tendency to emit greeting calls at no specific receivers, unlike that by older females. Adult females emitted greeting calls more frequently when approaching unrelated females than related females. In contrast, young adult or juvenile females exhibited no significant difference in the proportion of the calls with related and unrelated conspecifics. Adult and young adult females were more likely to respond affiliatively to other individuals that approached using greeting calls compared with silent approaches, whereas juveniles did not exhibit different responses to the two types of approaches. This study showed that the target‐specific usage and affiliative response to greeting calls emerge with changes in the developmental stage. Furthermore, the fact that even young adults did not use greeting calls as adults indicates that the usage of greeting calls is modified in conjunction with the expansion of social relationships.     

Group unity of chimpanzees elucidated by comparison of sex differences in short-range interactions in Mahale Mountains National Park,Tanzania

Chimpanzees (Pan troglodytes) form multi-male and multi-female unit groups with fission–fusion grouping patterns. Short-range interaction (SRI) plays an important role in the unity of these groups and in maintaining social bonds among members. This study evaluated three models of chimpanzee social structure that differed according to the emphasis each placed on social bonds between the sexes, i.e., the male-only, the bisexual, and the male-bonded unit-group model. I investigated differences in SRI between the sexes among group members in well-habituated wild chimpanzees in Mahale Mountains National Park, Tanzania. I followed six focal adult males and six females, and quantified their respective SRI with other chimpanzees. Except between subordinate males and adult females, adults in general engaged in SRI with about 60–90% of the individuals with whom they made visual contact each day, whether in large or small parties. Although the number of social grooming (SGR) partners was limited, male–male SGR networks were wider than were either male–female or female–female SGR networks among adults. The number of contact-seeking behavior (CSB) partners was also limited, but dominant males had more CSB partners. Adult females mainly interacted by pant-grunt greeting (PGG) with adult males, but tended to do so mainly with the highest-ranking male(s) within visual contact. These results indicated that the social bonds among adult males were essential to group unity. Because of clear male dominance, adult females established peaceful coexistence with all group members despite less frequent SRI with subordinate males by maintaining affiliative social bonds with dominant males, thereby supporting the male-bonded unit-group model. Adult females had many female SRI partners, but these interactions did not involve performing conspicuous behaviors, suggesting that females maintain social bonds with other females in ways that differ from how such bonds are maintained with and between adult males.     

Stronger social bonds do not always predict greater longevity in a gregarious primate

In group‐living species, individuals often have preferred affiliative social partners, with whom ties or bonds can confer advantages that correspond with greater fitness. For example, in adult female baboons and juvenile horses, individuals with stronger or more social ties experience greater survival. We used detailed behavioral and life history records to explore the relationship between tie quality and survival in a gregarious monkey (Cercopithecus mitis stuhlmanni), while controlling for dominance rank, group size, and life history strategy. We used Cox proportional hazards regressions to model the cumulative (multi‐year) and current (single‐year) relationships of social ties and the hazard of mortality in 83 wild adult females of known age, observed 2–8 years each (437 subject‐years) in eight social groups. The strength of bonds with close partners was associated with increased mortality risk under certain conditions: Females that had strong bonds with close partners that were inconsistent over multiple years had a higher risk of mortality than females adopting any other social strategy. Within a given year, females had a higher risk of death if they were strongly bonded with partners that changed from the previous year versus with partners that remained consistent. Dominance rank, number of adult female groupmates, and age at first reproduction did not predict the risk of death. This study demonstrates that costs and benefits of strong social bonds can be context‐dependent, relating to the consistency of social partners over time.     

Wounding aggression during the formation and maintenance of captive,multimale chimpanzee groups

Although the multimale community is the natural social organization of chimpanzees, both wild and captive adult males have killed other adult males and infants in intercommunity conflicts and intragroup aggression. Despite the potential for serious aggression, the formation of captive, multimale social groups is desirable for the efficient, long-term, humane housing of chimpanzees in socially and physically enriched environments and for the education of zoo visitors. The University of Texas Science Park (UTSP) has maintained multimale groups of chimpanzees for 14 years. In the UTSP outdoor corral housing, multimale/multifemale social groups of unrelated adult and adolescent chimpanzees (42 F, 46 M) were formed by a series of 397 individual introductions. Wounding aggression was minimal during introductions of females to males or other females and upon male-male introductions of formerly single-caged adolescent and young adult males having had long-term prior visual familiarity. Serious wounding occurred during male-male introductions when there were major discrepancies in the age and social experience of the subjects or when adult, socially experienced males were reintroduced to former group mates following lengthy separations. Male wounding in the eight established long-term groups of 5–11 adults (2–7 males) averaged 1.4 episodes per male-year of residence; 14% of male wounding episodes required surgical therapy. Adult wounding was significantly associated with the presence of one or more group females with maximally tumescent genital swellings. No male-perpetrated infanticides occurred. Not all multimale groupings are successful, but the majority of formerly laboratory-housed chimpanzees may live and reproduce safely in multimale groups. Experience with all-male groups at UTSP suggests that bachelor groups are also practical for long-term housing. © 1995 Wiley-Liss, Inc.     

Female Genito-genital Rubbing in a Group of Captive Chimpanzees

Wild and captive female bonobos exhibit a form of noncopulatory sexual behavior—genito-genital (GG) rubbing—in which 2 individuals rub their genital regions together. GG-rubbing in bonobos occurs in several contexts and may serve several functions, including tension reduction and reconciliation. It has not been reported for chimpanzees. In a study of captive, adolescent chimpanzees at the New Iberia Research Center, I observed that females rubbed genital regions at rates equivalent to those of bonobos, though the form of the behavior differed in significant ways from classic bonobo GG-rubbing. I describe the pattern of GG-rubbing in the chimpanzees and provide preliminary tests of 5 hypotheses for why the behavior occurs. All 4 females in the study group participated in GG-rubbing, though the frequency with which they initiated and participated varied. Females that GG-rubbed the most also groomed each other the most, supporting the hypothesis that GG-rubbing reinforces or at least reflects social bonds. The data do not support the hypothesis that females GG-rub to reconcile conflicts, to reduce tension during feeding, to signal social status, or to attract mates.     

Close bonds and social rank similarities favor non-random mating in captive stump-tailed macaques (Macaca arctoides)

Assortative mating is non-random mating by the mutual choice of phenotypes or behavioral types. In polygynandrous species, competition for mating by social rank can lead to assortative mating. However, although not an individual trait, social bonds also influence mating opportunities resembling assortative mating. Stump-tailed macaques form long-term close bonds and organize in a linear dominance–subordination hierarchy. Therefore, we studied whether the strength of the social bond and rank closeness influenced mating decisions and increased mating opportunities, particularly for low- and middle-ranking animals. Firstly, we observed whether females directed proceptive behavior to close-bonded or adjacent rank males. Secondly, we measured whether successful copulations were related to the strength of social bonds and close ranking. Thirdly, to ensure that copulations owed mainly to the aforementioned factors, we also evaluated whether sexual coercion was unrelated to social bonds and rank similarities. Finally, we assessed whether close bonds mediated agonistic support to females. The study subjects were 12 adult female and 11 male captive stump-tailed macaques. We monitored daily females' reproductive status by vaginal cytology. Sexual behavior was recorded by all occurrences sampling and scan sampling to collect the agonistic and affiliative instances required to calculate social ranks, social bond strength, and agonistic support. The results indicated that the probability of females displaying proceptivity increased during the follicular phase toward close-bonded and high-ranking males. Copulation chances increased with male–female social bonds and rank closeness. Forced copulation decreased in close-bonded individuals, while agonistic support increased in close-ranking strong-bonded animals. In conclusion, close social bonds and similar social rank result in non-random mating in stump-tailed macaques.     

Do old female monkeys have a specific social role?

The role of the aged in human society has received much attention from gerontologists, and the notion of a social role for aged monkeys is common in primatology. Four hundred and fifty hours of focal animal data were collected on a sample of 40 adult female Japanese monkeys. The animals are semi-free ranging and of known age. These data were analyzed in an attempt to determine whether old females constitute a behaviorally distinct subgroup. Very little behavioral variation based on age could be documented. Where age related variation occurs, it is better explained as a function of youth, rather than as a function of old age. The expectation that old monkeys will occupy a distinct social role because of their advanced age is discussed in terms of biological versus social aging, human versus non human aging, the evolution of behavioral change in old age, and the application of the social role concept to old female monkeys. It is concluded that there is little evidence that the behavior of the aged females differs significantly from that of the other adult females, and it does not appear that the fact of biological aging creates any radically different social situation which would cue the onset of specific role behavior for aged animals.     

Reproductive development and behavior of captive female chimpanzees

The reproductive histories and behavior of six chimpanzees were analyzed in order to evaluate the female reproductive pattern. This analysis indicated that captive females undergo an earlier menarche and an acceleration of subsequent reproductive phases as compared to wild chimpanzees. Menarche occurred between 7.7–9.3 years of age and first conceptions occurred between 8.2–10.7 years of age. Changes in the females' sex skins across menarche, pregnancy, and the menstrual cycle were also evaluated. The fluctuation in sex skin size was shown to have a marked effect on the occurrence of sexual behavior. In addition, the social context and relative familiarity of the chimpanzees affected the choice of sexual partners.     

Changes in social interactions during adolescence in male mandrills (Mandrillus sphinx)

The adolescent period in male mandrills extends from the time the testicles descend (at the age of 3-4 years) to the time adult characteristics develop (at the age of 10 years), and is thus one of the longest adolescent periods in cercopithecines. In this short cross-sectional study of 11 male mandrills (4.7-9.1 years old), we analyzed social behavioral patterns to investigate partner preference and changes in types of interactions throughout puberty. The mandrills were separated into two clusters on the basis of all of the social interactions scored, as well as the age and sex of the protagonist. During early to mid puberty, immature individuals interacted preferentially with other male adolescents and juveniles. Playing was an important activity, and some affiliative interactions with juveniles were observed. Older adolescents interacted more with adult males and females. These older adolescents were predominantly aggressive toward other adolescents, females, and juveniles, and showed little or no affiliative or playful behaviors. These results indicate a shift in social partners: older males interacted more frequently with adult males, and their behavior involved more aggression and less submission compared to younger adolescents, which showed predominantly submissive and playful behavior. These changes are consistent with preparation for dispersal and future intermale competition.     

Effects of positive reinforcement training techniques on the psychological welfare of zoo‐housed chimpanzees (Pan troglodytes)

Captive environments encompass various factors that can elevate stress levels and jeopardize the wellbeing of the captive animals. The use of positive reinforcement training (PRT) techniques enables researchers and caretakers to reduce tension directly associated with potentially stressful procedures and states. The current study tested the general effect of PRT on the wellbeing of zoo‐housed chimpanzees (Pan troglodytes) by measuring behaviors that reflect poor and good welfare and that were not directly connected to the specific aim of the training session. The behavior of a group of twelve chimpanzees was measured throughout the day from the exhibition yard, at baseline (12 weeks) and during the PRT period (10 weeks). The results show a significant decrease in abnormal and stress‐related behaviors and a significant rise in prosocial affiliative behaviors following implementation of the training program. The training was shown to have a greater positive effect on low‐ranking individuals compared with high‐ranking ones. This research shows for the first time that PRT offers an enrichment effect whose general influence lasts throughout the day, irrespective of any direct link to a specific trained behavior. Consequently, it can be claimed that PRT presents an effective enrichment tool that can be implemented with captive animals. Because of the above‐noted differential effect between high‐ and low‐ranking chimpanzees, however, this should be taken into consideration when combining PRT with the non‐human primates' daily routine. Am. J. Primatol. 71:687–695, 2009. © 2009 Wiley‐Liss, Inc.