Effects of human activity on chimpanzee wounding

Reducing the frequency and/or severity of aggression and wounding is a major concern of people managing socially housed chimpanzees. One factor that has not been investigated intensively for its effect on captive chimpanzee agonism is the presence of humans. Therefore, we examined an archival database of wounding incidents among 88 adult and adolescent members of 8 social groups of chimpanzees (42 females, 46 males) to determine whether variable levels of human activity (higher weekday versus lower weekend-day activity levels) in the colony was associated with changes in chimpanzee wounding patterns. Wounding was tabulated for each group for periods of 38 - 118 months. A series of Chi-square tests indicated that there were a greater than expected number of wounding episodes on weekdays but that day of the week did not affect the age or sex distribution of wounding. Together, these results suggest that the presence of personnel completing routine activities is associated with chimpanzee agonism. Zoo Biol 16:327–333, 1997. © 1997 Wiley-Liss, 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.     

Social Relationships among Males in Multimale Siamang Groups

I quantified social and spatial interactions among adults in 4 multimale siamang (Symphalangus syndactylus) groups to evaluate the importance of aggression and avoidance in mediating male-male relationships. Actual genetic relationships among adults are unknown, but available mitochondrial data suggest that in 3 of 4 groups, neither male was the offspring or maternal sibling of the female, whereas in the fourth group, a matrilineal relationship between the female and 1 adult male was not excluded. Rates of aggression involving male-male dyads were very low. One male-female dyad maintained closer spatial cohesion than those of other adult dyads in 3 of 4 groups. Nonetheless, all adult males spent substantial percentages of their time ≤20 m from other adults in their groups. The percentages of time that male-male dyads spent in social grooming interactions did not differ from those of male-female dyads. In 3 groups, both males copulated with the group female. While previous studies have reported high rates of aggression between adult males and subadult male group members in siamangs, my results suggest that male-male relationships in multimale groups at Way Canguk were relatively harmonious. Acceptance of multimale grouping (and in some cases sexual polyandry) suggests that the benefits outweigh the costs under some circumstances. If there was a genetic relationship between males, then tolerance of delayed dispersal and copulation with the adult female may function as a form of parental investment. Males may also benefit from multimale grouping via enhanced territorial defense or reduced costs of mate defense.     

Wounding patterns in three species of captive macaques

The incidence of wounding in captive groups of rhesus (Macaca mulatta), pigtail (M. nemestrina), and stumptail (M. arctoides) macaques was studied for 21 months. Groups were monitored daily for evidence of wounding. Wounded animals were captured, treated by veterinary staff, and returned following recovery. Records were kept on the age, sex, and species of the recipient, along with the type and location of wound. In each species of macaque, adult males incurred the highest frequency of wounds and multiple wounds of any age-sex class. This contrasted with previously reported behavioral data indicating low frequencies of aggression received by adult males, especially contact aggression and bites. These discrepancies indicate wounding frequencies do not necessarily correspond with behavioral measures of aggression. Inhibition of aggression directed toward infants and the selective avoidance of bites directed to vital body regions were presented as possible mechanisms that modify intragroup aggression. Increased wounding in the birth season under captive conditions suggests that the pattern of increased wounding reported during the breeding season under freeranging conditions may reflect xenophobic responses to immigrating males, rather than direct male-male competition for estrous females.     

The development of affiliative and coercive reproductive tactics in male chimpanzees

Like many animals, adult male chimpanzees often compete for a limited number of mates. They fight other males as they strive for status that confers reproductive benefits and use aggression to coerce females to mate with them. Nevertheless, small-bodied, socially immature adolescent male chimpanzees, who cannot compete with older males for status nor intimidate females, father offspring. We investigated how they do so through a study of adolescent and young adult males at Ngogo in Kibale National Park, Uganda. Adolescent males mated with nulliparous females and reproduced primarily with these first-time mothers, who are not preferred as mating partners by older males. Two other factors, affiliation and aggression, also influenced mating success. Specifically, the strength of affiliative bonds that males formed with females and the amount of aggression males directed toward females predicted male mating success. The effect of male aggression toward females on mating success increased as males aged, especially when they directed it toward females with whom they shared affiliative bonds. These results mirror sexual coercion in humans, which occurs most often between males and females involved in close, affiliative relationships.     

Female genital swellings have no effect on chimpanzee agonism in well-established groups

Reducing the incidence of aggression and wounding is a major concern for those managing socially housed chimpanzees (Pan troglodytes). Competition among adult males for access to sexually receptive females is believed to be one factor contributing to undesirably high levels of agonism. An observational analysis of two chimpanzee groups (n = 9, n = 8) was initiated to study this phenomenon. All-events sampling was used to record agonistic and sexual behavior on days when one female in the group showed a maximal genital swelling and on other days when no female in the group had a tumescent swelling. The result of the multivariate analysis of variance indicated that the presence of a female with a tumescent swelling had no effect on bluff displays or aggressive, submissive, or reconciliatory behavior but that sexual behavior was significantly increased. These results may be explained by the fact that long-term stability in group membership may reduce male–male competition for sexual access to females and the sometimes associated aggression and wounding. Colony managers dealing with well-established groups of chimpanzees should invest more of their effort in controlling aggression elicited by factors other than the cycling of a single female group member.     

Male-male Interactions in Heterosexual and All-male Wild Mountain Gorilla Groups

Variation in male dispersal and behavior patterns are components of intraspecific differences in social systems. A comparison of male behavior in different social settings can be useful for determining which behavioral mechanisms contribute to variability in social systems. Two heterosexual multimale groups and one all-male group of mountain gorillas (Gorilla gorilla beringei) were observed for over 1100 h at the Karisoke Research Centre, Rwanda. Data on proximity patterns, dominance relationships, aggression, agonistic interventions, affiliation, and homosexual behavior were compared among the males in these groups to examine the influence of female presence, sex ratio, group size, and kinship on male—male interactions. Males in the all-male group stayed closer together, affiliated more, exhibited more homosexual behavior, and were more aggressive toward each other than males in heterosexual groups. However, the males in heterosexual groups showed more wounding and more consistent dominance relationships. Kinship did not influence male-male relationships in the all-male group. The males in the heterosexual groups rarely interacted with one another; they may actively avoid close proximity to reduce aggression. Results suggest that the variable social system of mountain gorillas may be more strongly influenced by demographic factors, male-female social relationships, and male-male competition for mates than by any benefits of male-male relationships.     

Male Social Behavior and Dominance Hierarchy in the Sulawesi Crested Black Macaque (Macaca nigra)

In a 6-week study of the social behavior of wild Sulawesi crested black macaques (Macaca nigra), we found a linear and transitive dominance hierarchy among the six adult males in one social group. Dominance rank, as determined by the direction of supplantations, correlated strongly with percentage of time near more than four neighbors, frequency of grooming received from adult females, and percentage of time with an adult female as nearest neighbor. These results suggest that high-ranking males are socially attractive. Adult females sexually solicited high-ranking males more often than low-ranking males, but frequency of copulation was not correlated with dominance rank. Frequency and intensity of aggression between males are strongly correlated with rank distance, but aggression toward females was greatest for mid-ranking males. Males of all rank displayed significantly more aggression toward sexually receptive females than toward females in other estrous states. These data indicate that male Sulawesi crested black macaques display a social organization similar to that reported for multimale groups in other macaque species rather than the egalitarian social organization described for female Sulawesi macaques.     

Advanced age influences chimpanzee behavior in small social groups

Management strategies for captive chimpanzees (Pan troglodytes) must begin to take into account the increasing age of the captive chimpanzee population. This study represents a baseline assessment of the relationship between advancing age and behavior among male and female chimpanzees living in pairs and trios in indoor/outdoor runs. Data collected on 14 old individuals (30–44 years old) and 20 younger adult individuals (11–22 years old) totaled 240 hours. Levels of agonistic and affiliative social behavior, non‐social activity, abnormal behaviors, and behavioral indicators of anxiety were evaluated. In the same captive setting, the behavior of old chimpanzees was significantly different from younger chimpanzees. Old chimpanzees showed less aggression and moved about their enclosures less. Old females behaved submissively more often than younger adult females; the reverse was found among males. However, affiliative social behavior occurred at similar levels in old and younger adult chimpanzees, implying continued need for social housing with advancing age. The effect of enrichment devices may differ for aged female chimpanzees, given their submissiveness and the lower levels of object manipulation found in aged subjects. These results suggest that aging in chimpanzees may be accompanied by altered patterns of social interaction, requiring careful attention to the compatibility of social partners. Zoo Biol 19:111–119, 2000. © 2000 Wiley‐Liss, Inc.     

Injury risks among chimpanzees in three housing conditions

Meeting the psychological needs of chimpanzees (Pan troglodytes) can be a challenge given their aggressiveness on the one hand and the complexity of their social lives on the other. It is unclear how to balance the need to provide opportunities for species-appropriate behavior against potential risks of injury chimpanzees may inflict on each other. This study evaluates the suggestion that simpler social environments protect chimpanzees from wounding. Over a two-year period all visible injuries to 46 adult males, 64 adult females, and 25 immature chimpanzees were recorded at the Yerkes Regional Primate Research Center. Approximately half of the subjects were mother-reared, and the rest were nursery-reared. Housing included compounds containing about 20 chimpanzees, interconnected indoor-outdoor runs for groups of up to 12 individuals, and smaller indoor-outdoor runs for pairs and trios. Annual wounding rates were calculated for serious wounds (extensive injuries and all those requiring veterinary intervention) as well as for minor wounds. Compound-housed chimpanzees incurred the highest level of minor wounding, but serious wounding levels were not affected by housing condition. Even with a period of dominance instability and elevated levels of wounding in one compound, compound chimpanzees were not injured more than those in smaller social groups over the long term. Nursery-reared females in moderate-sized groups were wounded more than mother-reared females. Also, nursery-reared males and females were wounded less often when paired with mother-reared companions. Overall, this study indicates that maintaining chimpanzees in pairs and trios would not be an effective means for reducing injuries. The management of wounding in chimpanzee colonies is influenced more by the sex and rearing composition of a colony.     

Male-male relationships among wild bonobos (Pan paniscus) at Wamba,Republic of Zaire

Male-male relationships among wild bonobos (Pan paniscus) in two adjacent unitgroups (E1 and E2 groups), which were formed by division of the E group, were studied at Wamba, in the Central Zaire Basin, by analyzing the proximity and social interactions among males. Dominant-subordinate relationships between a male-male dyad were easily recognized from the directions of individual agonistic interactions. Male bonobos rarely joined forces in aggression. Clear differences in social status existed between adult and adolescent male bonobos in both groups, as reported in the case of chimpanzees (Pan troglodytes). The presence of mothers in the unit-group greatly influenced the dominant-subordinate relationships among males through strong mother-son bonds in both groups. However, the extent of the mother-son bonds differed between the groups. Males in the E2 group participated more frequently in agonistic or affinitive interactions than did males in the E1 group. Males in the E1 group were divided spatially into several clusters, while there were cohesive relationships among the adult males in the E2 group. The difference in intensities of mother-son bonds between the groups may be explained by the distribution of males at the time of the division of the E group. Differences in male-male relationships between bonobos and chimpanzees seem to be related to differences in intra- and inter-unit-group competition among males between the two species. Male chimpanzees may achieve coexistence by manipulating ambivalent relationships that are caused by intra- and inter-unit-group competition among them, while male bonobos may achieve coexistence by decreasing intra- and inter-unit-group competition among them.     

Aggression with mixed age-sex groups of bolivian squirrel monkeys following single animal introductions and new group formations

The social organization of the Bolivian squirrel monkey (Saimiri boliviensis boliviensis) is thought to be sexually segregated, with males and females forming separate social groups during the nonbreeding season. To investigate the influence of this social order on patterns of aggression, controlled single animal introductions within established groups and establishment of new groups were studied in a systematic manner. Behavioral observations were made using an all-occurrences technique to sample all agonistic interactions. In study I, 4 animals of each age-sex class (adult males and females, juvenile males and females) were introduced one at a time into 4 different social groups composed of 1 adult male and 8 to 10 adult females. Behavioral observations were made prior to and after the introductions. Newly introduced adult males received significantly more contact aggression than other age classes. Only the adult females increased aggression after the introduction of new animals. In study II, new social groups were formed and behavioral observations were made following formation. One group was formed from 7 pairs of familiar females and an unfamiliar adult male. This group had a high frequency of aggression during the first half hour, with contact aggression rising to peaks at 3 and 5 h. The second group consisted of 10 familiar females, 2 pairs of familiar females and an unfamiliar male. There was a significant peak in contact aggression 3 h into the observation.     

Introduction and integration of strangers into captive groups of tufted capuchins (Cebus apella)

We introduced two to four unfamiliar animals into three established groups (N = 6–9 per group) of tufted capuchins (Cebus apella).We present findings on the behavioral consequences of introductions as a function of age, sex, and residency status and long-term consequences for health and reproduction. No morbidity from aggression occurred at the time of introductions or during several months following, and reproduction was not compromised. Activity budgets and patterns of social spacing and interaction were little changed following the introductions except for increases in vigilance behavior, especially by newly introduced adult females. Adult females exhibited the strongest and longest-lasting response to changes in group composition. The results indicate that in this species (1) introductions of adult females can be carried out with acceptable risk to the newcomers provided that careful monitoring occurs, so that the onset of severe aggression instigated by resident females toward new females can be avoided, (2) juveniles can be introduced with minimal risk, and (3) adult males can be introduced into groups lacking resident adult males with minimal risk. Capuchins differ in important ways from the better-studied Old World monkeys in their response to introductions of strangers. The differences are instructive with regard to processes supporting species-typical social structure, which is less overtly hierarchical in capuchins than in macaques.     

Sociodemographic Correlates of Fecal Androgen Levels in Wild Male White-Handed Gibbons (Hylobates lar)

Despite the central role of testosterone in influencing many aspects of the male life cycle, information on the influence of social and behavioral factors associated with androgen output is available for only a few primate species, mainly those living in multimale–multifemale societies. We collected 322 fecal samples and measured fecal testosterone metabolite levels in 19 adult male white-handed gibbons (Hylobates lar) from 13 groups living in the Khao Yai National Park, Thailand, to examine the extent to which androgen output is related to sociodemographic variables (social organization, social status, presence of infants, age) in a socially flexible species, i.e., pair-living/multimale groups. We predicted that androgen levels would be higher in males 1) that live in potentially more unstable single-male/single-female units; 2) that are primary (dominant) vs. secondary; 3) that live in groups with dependent infants; and 4) that are of prime vs. senior age. We found marked differences in androgen levels among males and a significant effect of time of the year. Males living in pairs exhibited significantly higher androgen concentrations vs. males living in multimale groups, and males residing in groups with infants showed a significant increase in androgen levels throughout the sampling year. However, we found no relationship with male age or social status. The increased androgen output found in both pair-living males and those residing with infants might be a physiological mechanism that facilitates male aggression to cope with potential threats posed by social challenges and the demand for infant/group defense, respectively. More generally, our data indicate that in socially flexible species male androgen output is less strongly linked to key life-history variables than in species that live permanently in multimale–multifemale groups.     

Mahale chimpanzees: grouping patterns and cycling females

The social system of chimpanzees (Pan troglodytes schweinfurthii) is characterized by the fission-fusion of social groups. Several studies have reported that females are less gregarious than males. In the current study, adult female gregariousness depended on their reproductive state. Noncycling adult females (pregnant, lactating, or post reproductive) were observed in large bisexual parties less often than cycling adult females. On the other hand, cycling adult females were observed in large bisexual parties as often as males, regardless of their estrous state. More males were in parties that included cycling adult females with maximal genital swelling (estrous females) than in parties without them. Moreover, a bisexual party including more estrous females contained more males. These results suggest that large bisexual parties of chimpanzees are constructed by a dual mechanism. First, cycling adult females are attracted to parties that consist of the top ranking male and large numbers of adult and adolescent males. Second, adult and adolescent males that did not belong to parties originally are attracted by estrous females and join them. Thus, in Mahale Mountains National Park, Tanzania, bisexual parties of chimpanzees can be characterized as "parties for reproduction."     

Male spotted hyenas (Crocuta crocuta) queue for status in social groups dominated by females

A long-term study of immigrant male spotted hyenas (Crocuta crocuta) living in large multimale/multifemale groups (clans) demonstrated that males acquire social status by queuing. Maximumlikelihood estimates of parameters of a stochastic queuingmodel that assessed queuing discipline confirmed that immigrantmales respected the convention that their positions in a queueof typically 15 or more individuals was determined by theirsequence of arrival. Levels of aggression among males were low;males did not attempt to improve their social status throughphysical contests. Size and body mass did not influence malesocial status. The stability of queues was insured by an increasein the rate at which males formed coalitions against othermales as they rose in social status and by coalitions between high-ranked males and dominant females. High-ranked, long-tenuredmales chiefly consorted with ("shadowed") and focused theiraffiliative behavior on females of high reproductive valueand disrupted attempts by subordinate males to associate withthese females. High-ranked males also supported females againstlower-ranked males that harassed them. In contrast, lower-ranked,short-tenured males focused their affiliative behavior on young adult females and rarely shadowed or defended females. Malesthat did not disperse from their natal clan (nondispersers)quickly acquired top rank in the male social hierarchy. Irrespectiveof the social status acquired from their mother when young,nondisperser adult males submitted to all adult females.     

Spacing system of the Mysore slender loris (Loris lydekkerianus lydekkerianus)

Loris lydekkerianus lydekkerianus has been shown to have a promiscuous copulatory pattern, to maintain social networks via frequent loud calls, to interact socially throughout the night with all age classes, and to sleep socially. Though these behaviors point towards a multimale social system, no study of their spacing system has yet been provided to support this view. From October 1997-August 1998, I conducted a study of the Mysore slender loris in Ayyalur, India. During 1,400 field hours, data were collected on range use of 3 adult females, 3 adult males, 1 subadult female, and 1 subadult male. Lorises slept in groups averaging 4 individuals, composed of an adult female, her offspring, and 1-2 adult and subadult males. Sleeping sites for three groups were located within 1.9 ha in the center of the study area. The minimum convex polygon in hectares encompassing each animal's range was determined, as well as overlap among home ranges of individual lorises. Average home range sizes were: adult males, 3.6 ha +/- 0.09; subadult/smaller males, 1.17 ha +/- 0.26; and adult and subadult females, 1.59 ha +/- 0.24. Male ranges overlapped with at least 2-3 other adult males (0.72 ha +/- 0.23). Female ranges overlapped slightly with at least 2 other female ranges (0.22 ha +/- 0.25). Male ranges overlapped those of at least 3 females (0.82 ha +/- 0.51). Patterns of home range and sleeping site support previous suggestions of a multimale social system, similar to aye ayes and some galagos.     

Behavioral solutions to breeding cheetahs in captivity: Insights from the wild

Knowledge of cheetahs' behavior is increasingly seen as the key to solving the mystery of cheetahs' poor breeding performance in captivity. In the absence of zoos' maintaining systematic records of individuals' behavior during introductions, behavior of free-living animals can be informative. In the wild, most female cheetahs probably mate with males living in small groups or coalitions; thus, zoos may benefit from replicating these social conditions, provided injuries can be minimized. Relations between free-living coalition members are amicable, and escalated aggression was never witnessed during 4 years of observation. Some antagonism was seen in newly formed trios, although this had disappeared in longer established coalitions. Minor aggression occurred over carcasses, being greater at small and intermediate sized kills than at large ones. In the presence of females, mild intramale aggression was only seen within 1 of 7 coalitions. Free-living females showed similar rates of behavior in the presence of different numbers of males, aside from more frequent growling at large groups. These findings suggest that captive institutions should be less nervous about housing male cheetahs together and introducing females to groups of males for purposes of breeding. © 1993 Wiley-Liss, Inc.     

Female social relationships in a captive group of Campbell's monkeys (Cercopithecus campbelli campbelli)

A study group of Campbell's monkeys (Cercopithecus c. campbelli) provided data on affiliative and agonistic relationships between females. Over a period of two years (involving 111 hr), we conducted observations of a captive group which had a composition similar to wild groups. We were able to identify a monitor-adjust social system with frequent affiliative interactions, directed gazing and avoidances rather than aggressive acts. We described long-term differentiated affiliative bonds: adult females interacting more often with some group mates than others, especially if they were relatives. Interactions between matrilines concerned essentially play and young adult females. We found a significant linear hierarchy of dominance with rare reversals and a stable intermatriline dominance. In contrast to other single-male groups, our adult male was socially integrated into the group although this may have been because of the housing conditions. Comparisons with the social organization of other captive and wild guenon groups are discussed.