Factors affecting aggression among females in captive groups of rhesus macaques (Macaca mulatta)

Captive groups of primates often exhibit higher rates of aggression than wild, free-ranging groups. It is important to determine which factors influence aggression in captivity because aggression, particularly intense aggression, can be harmful to animal health and well-being. In this study, we investigated the effect of ground substrate as well as season, rank, age, and group size on rates of agonistic interactions per female in seven captive groups of rhesus macaques (n = 70 females, 1,723 focal samples) at the California National Primate Research Center. Agonistic interactions were divided into three categories: displacements, mild aggression, and intense aggression. Females living in enclosures with gravel substrate were 1.7 times more likely to be involved in intense aggression (e.g. chases and physical contact) than females living in enclosures with grass (Poisson regression model: P < 0.001). High-ranking females were at least 1.3 times more likely to be involved in mild (e.g. threats and lunges) aggression than lower-ranking females (low rank: P = 0.03; mid rank: P = 0.001). Females of all ranks were 1.5-1.9 times more likely to be involved in both intense and mild aggression during the breeding season than other seasons. Age and group size did not affect rates of mild or intense aggression. These findings indicate that although some aggression appears to be natural and unavoidable, i.e. aggression during the breeding season, the well-being of captive macaques can be improved by developing grass substrate in outdoor enclosures.     

Special relationships instead of female dominance for redfronted lemurs,Eulemur fulvus rufus

Most lemurs yet studied in detail exhibit some mode of adult female social dominance over males. The known exception, a brown lemur subspecies known as rufous or redfronted lemurs (Eulemur fulvus rufus), forms multimale–multifemale social groups within which unambiguous dominance relations are not observed among adults. Resting groups of redfronted lemurs consistently include huddling adult male–female pairs whose males selectively scentmark and rub their heads in the scentmarks of their female huddling partners. Quantitative observations confirmed that some of these male–female pairs maintain special relationships satisfying all criteria originally developed in research on cercopithecine monkeys. Observations before, during, and after mating season, intergroup encounters, male transfers, and changes in male–female affiliations illuminated developmental and functional aspects of male–female partnerships. Each adult female in two semi-free-ranging study groups shared high rates of association, grooming, and agonistic support and low rates of agonistic interaction with one unrelated or distantly related adult male partner. Such affinity characterized small proportions of adult male–female relationships. Several males directed not only support but also aggression toward adult females with whom they sought to affiliate. All bonded males sought to copulate with their partners, and some appeared to ignore estrus in nonpartners. All females accepted copulation attempts from partners and some seemed to prefer their partners as mates. Partial synchronization of brief estrus periods together with concealed ovulation appeared to minimize chances for polygynous mating. Results support the view that the male–female pair is the fundamental social unit of E. fulvus and suggest that female partnership with individual males obviates dominance behavior, including female dominance, in this lemurid primate. Am. J. Primatol. 43:239–258, 1997. © 1997 Wiley-Liss, Inc.     

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.     

Do wild brown lemurs reconcile? Not always

Post-conflict behaviour has been widely investigated in anthropoid primates but not extensively in prosimians. Here, we report the reconciliation pattern of a 14-individual group of wild brown lemurs (Eulemur fulvus) in the Berenty gallery forest (South Madagascar). We found that reconciliation occurs only in the non-feeding context and that it works in reducing the risk of renewed aggression. Thus, reconciliation would provide an immediate positive feedback that is probably independent of the quality of the relationship between opponents. Reconciliation may also be a hic-et-nunc mechanism, needed to avoid conflict spreading across group members, possibly leading to social disruption.     

The role of scent marking in Lemur catta agonistic behavior

Certain forms of marking behavior in Lemur catta have been considered to be aggressive in nature but had not been analyzed specifically in this respect. This study examines the relationship between the occurrence of all forms of marking behavior displayed by a captive group of lemurs and their physical and nonphysical aggressive interactions. All forms of marking behavior, especially males' tail mark and tail wave displays, were found to correlate with aggressive behavior including female-instigated agonism. In comparison, allogrooming, a behavior thought not to have an agonistic component, was not significantly correlated with any marking nor agonistic category. The data suggest that in intersexual interactions male marking behavior is an aggressive but nonphysical substitute for physical aggression toward females who have generally been regarded as dominant to males in this species.     

Food Intake and Dietary Overlap in Native Lemur catta and Propithecus verreauxi and Introduced Eulemur fulvus at Berenty,Southern Madagascar

The introduction of Eulemur fulvus in 1975 into the Berenty Reserve and their recent attainment of population densities comparable to those of Lemur catta led us to analyze food partitioning among the 3 large prosimian species in the gallery forest. We assessed the diets of ring-tailed lemurs (Lemur catta), brown lemurs (Eulemur fulvus) and sifakas (Propithecus verreauxi) from food intake measurements during 3 successive short-term studies. All species exhibited marked seasonal changes in their major food categories. Dietary overlap was very high between ring-tailed lemurs and brown lemurs during 2 of 3 seasons, including the middle of the dry season. During the latter period, Eulemur appeared to compensate for a low quality diet by increasing the amount of food eaten. In contrast, Lemur fed on lower amounts of food and seemed more efficient at coping with fibrous plant materials. There is low dietary overlap of Lemur catta and Eulemur fulvus versus Propithecus, which exhibit by far the highest dietary diversity of the 3 species. We discuss sustainable coexistence among them, based on respective dietary adaptations and potential for dietary flexibility.     

Body weights of wild and captive lemurs

The mean body weight of a species is often used as a summary measure of size in evolutionary and functional studies. Additionally, body weight is often used to assess the health of captive animals. Contrasts of the captive and wild body weights of a species can be used to examine the effects of captivity on the species. We provide an analysis of adult body weight in nine taxa of Malagasy lemurs. We compare weights of wild and captive lemurs and provide analyses of relationships between captive weight variation and management actions. Body weights are derived from a number of sources, the majority from the Duke University Primate Center (DUPC) capture and husbandry records. Captive animals are, on average, heavier than wild conspecifics. However, the difference is significant in only three taxa (Hapalemur griseus griseus, Eulemur coronatus, E. macaco flavifrons). Based on a retrospective analysis of DUPC records, we assess patterns of adult weight relative to caging conditions and evaluate changes in mean weight over a period of approximately 20 years. Cage type appears to have no effect on body weight. Mean weight has decreased for some taxa housed at the DUPC over time. We calculate a weight-based criterion for identifying obese animals and demonstrate that obesity is not currently a prevalent condition in DUPC lemurs. Examinations of the physiological correlates of excessive weight, and especially relationships between weight and reproductive success, await further analysis. These analyses need to be based, in part, on reliable measures of body weight. We suggest that systematic weighing of wild and captive animals is important for further examinations of the overall health of captive animals as well as for studies ranging in scope from evolutionary to clinical. Zoo Biol 16:17–30, 1997. © 1997 Wiley-Liss, Inc.     

Sequences of primate signs. Review of teaching sign language to chimpanzees,edited by R. Allen Gardner,Beatrix T. Gardner,and Thomas E. Van Cantfort. Albany,State University of New York Press, 1989, 324 pp, 20 fig, 45 tab, $59.59 (cloth), $19.95 (paper)

Female social dominance over males is thought to characterize most of the prosimian primates of Madagascar. It has been reported in Propithecus verreauxi coquereli in the wild but intersexual relations were not fully characterized. In this paper we examine female-male spatial and agonistic relations in semi-free-ranging P. v. coquereli in order to evaluate intersexual social dominance and related behavioral asymmetries. Two hundred hours of focal sampling were conducted on two pairs of P. v. coquereli at the Duke University Primate Center, Durham, NC. Behavioral categories including approach, departure, follow, pass, replace, and aggression were scored and recorded. Our results show strong asymmetry of aggressive encounters, suggesting female dominance over males. No submissive signals were observed. The analysis of spatial relations showed that males were more active than females in maintaining proximity and, on average, male spatial movements could be predicted by female location and activities more often than vice versa. These results indicate a spatially central role for the female of each pair. © 1992 Wiley-Liss, Inc.     

Social organization of free-ranging ruffed lemurs,Varecia variegata variegata: mother-adult daughter relationship

The relationship between a mother and an adult daughter is examined in a group of free-ranging ruffed lemurs (Varecia variegata) at the Duke University Primate Center (DUPC). Although the two females were affiliative during the birth season, interactions during the mating season were predominantly agonistic. The maturing daughter was dominant to the mother, as has been observed in many caged social groups at the DUPC. Although both mother and daughter produced offspring in the same group, the daughter subsequently aggressively evicted the mother from the enclosure. It was not possible to maintain more than one long-term resident breeding female in the same social group. This pattern contrasts with observations of affiliation among breeding females in the wild. © 1992 Wiley-Liss, Inc.     

Behavior of the mayotte lemur,Lemur fulvus mayottensis,in captivity

A group of one male and two female Mayotte lemurs was observed at Chester Zoo, and their behaviors compared with published observations of wild populations of this and related forms of the brown lemur. It was found that the captive animals were active by both day and night, but that the pattern of activity was different from wild lemurs. The captive lemurs were less active than their wild counterparts and showed different timing of activity because of the feeding regimen at the zoo. The animals did not ignore the public at the zoo, but, on the contrary, directed some behaviors at the zoo visitors, particularly if the zoo visitors attempted to interact with the lemurs; under these conditions there was also an increase in the movements of the lemurs in the cage. Levels of aggression in the zoo lemurs were higher than those reported for wild populations, and aggression appeared to occur predominantly in the birth season. Levels of affiliative behaviors, particularly allogrooming, were comparable with those in the wild. Olfactory behaviors such as scent marking and anogenital sniffing also showed seasonal peaks and again appeared to occur at higher rates than in the wild.     

Habitat use and social structure of a brown lemur hybrid population in the Berenty Reserve, Madagascar

The population of brown lemurs has rapidly grown since their founders were introduced to the Berenty Reserve. The founders consist of two species (Eulemur fulvus rufus and E. collaris). To characterize the behavior of the population and to examine whether these characteristics affect population growth, I investigated the habitat use and social structure of the population of brown lemurs at Berenty (Berenty Eulemur). Behavior data were collected focusing on horizontal and vertical habitat use, activity rhythms, and intergroup relationships. These data were compared with the data of E. fulvus in other areas, with the previous studies done at Berenty, and with data on Berenty Lemur catta. Berenty Eulemur maintained a home range size comparable to E. f. rufus in the western deciduous dry forest, but was found at a lower level of the forest and had larger overlapping home ranges. Berenty Eulemur use food resources earlier in the morning than L. catta, intergroup conflict was avoided by vocal communication, and Berenty Eulemur made suitable use of their limited habitat. I suggest that a number of behavioral characteristics of Berenty Eulemur may contribute to their population growth.     

Agonistic and grooming behavior of captive crowned lemurs (Lemur coronatus) during the breeding season

Captive breeding of rare and endangered prosimians may be enhanced by an increased understanding of all aspects of their seasonal mating behavior. In this study, the agonistic and grooming behaior of captiveL. coronatus were studied during their annual breeding season. Between October and March, selected aspects of agonistic and grooming behavior of four male-female groups were recorded. Males initiated significantly more allogrooming than females. The frequency of this behavior pattern increased significantly in the weeks of estrus. Females performed significantly more agonistic behavior patterns than males. The mean frequency of agonistic interactions decreased significantly during the breeding season. In successfully reproducing groups males showed much less agonism towards females, than they did in unsuccessful groups. Inter-specific comparisons demonstrated that the patterns of agonistic interactions during the breeding season are very different among closely related species of lemurids. The conclusions drawn from this study are that captive breeding of crowned lemurs may be enhanced by keeping permanent multi-male, multi-female groups.     

Innovative social behavior in chimpanzees (Pan troglodytes)

We present evidence of agonistic buffering in captive chimpanzees, recorded from 1993 until 2005, mainly from ad libitum sampling in over 2000 hr of observation. A total of 33 agonistic buffering episodes were analyzed for context and effects of this complex social behavior. Agonistic buffering was directed at the whole chimpanzee colony as they supported an individual who initially received aggression from the alpha male, independently of the victim's age, sex or social rank. Chimpanzee agonistic buffering behavior is compared with that in other nonhuman primate species, and we describe some particularities of chimpanzee agonistic buffering: the status of the buffers used-socially important offspring such as those from the alpha female-and the social rank of the adult male responsible for the buffering episode-alpha male. Possible functions for this behavior in chimpanzees are suggested as appeasement of group members in a particularly crowded captive setting, and/or as a "forced reconciliation" mechanism. Chimpanzees exhibit behavioral flexibility by adapting themselves to new social and physical situations and use novel behavior to achieve social benefits.     

Evidence for social enhancement of reproduction in two Eulemur species

Across the past 20 years, captive reproduction has declined steeply in mongoose lemurs (Eulemur mongoz) and has been only moderately successful in black lemurs (E. macaco). At the same time, reproduction has been so successful in brown lemurs (E. fulvus) that contraception has been used since 1987 to limit captive numbers. No obvious cause for the differential reproductive success has been identified. Our experience with a pair of unrelated mongoose lemurs at the Philadelphia Zoological Garden suggested that they reproduced in only those years when they were caged in close proximity to another nonreproductive, full-sibling pair of mongoose lemurs. Examination of the worldwide pattern of captive reproduction by Eulemur species during the past two decades revealed that female black and mongoose lemurs housed in institutions with either additional conspecific males or additional conspecific pairs had a higher rate of reproduction than those maintained as an isolated pair. Black lemurs also had higher rates of reproduction when additional conspecific females were present. No similar pattern was found for brown lemurs or for two comparable mammals, the pudu (Pudu pudu) and the okapi (Okapia johnstoni). The evidence presented for the black and mongoose lemurs supports the existence of the Allee effect in these two species, namely, that reproduction is enhanced by the presence of conspecifics. © 1996 Wiley-Liss, Inc.     

Agonistic behavior and dominance relationships in female Phayre's leaf monkeys -- preliminary results

Socioecological theory suggests a link between the strength of competition for food/safety, rates of agonism, structure of dominance hierarchies, and dispersal among group-living females. This study presents preliminary data on agonistic behavior and dominance relationships for female Phayre's leaf monkeys (Trachypithecus phayrei), a species in which females routinely disperse. Behavioral observations were conducted on two groups (four adult females, and five adult females plus two juvenile females, respectively) at Phu Khieo Wildlife Sanctuary, northeast Thailand. Rates of agonistic behavior were analyzed from focal continuous recordings, while dominance hierarchies were constructed from all agonistic behaviors (focal and ad libitum sampling). Overall, female-female agonistic behaviors (aggression, submission, and displacements) occurred at a rate of < 0.25 interactions per hour. Agonistic interactions involving food occurred more frequently than expected based on feeding time. Females in both groups exhibited linear dominance hierarchies with some reversals, and possibly an age-inversed hierarchical structure in the larger group. The results fit well with previous results for colobine monkeys regarding frequency of interactions, displacements predominating agonistic behavior, and the possibility of an age-inversed hierarchy. The results contradict the suggested link between linearity of hierarchies and female philopatry. Future studies should consider the notion that female dispersal may coexist with linear dominance hierarchies.     

Triadic interactions in captive Barbary macaques (Macaca sylvanus,Linnaeus, 1758): “Agonistic buffering”?

This study presents data on the expression of male-immature triadic interactions, previously termed agonistic buffering, in a captive Macaca sylvanus group. Agonistic buffering has been hypothesized as inhibiting or modifying the expression of aggression. This was tested by examining (1) the dominance ranks of the animals involved in the triadic interactions, (2) the events preceding and following the triadic interactions, and (3) the presence of an infant in nonagonistic encounters between juvenile, subadult, and adult males. The results obtained do not support the hypothesis of agonistic buffering as the single explanation for triadic interactions, but emphasize the contextual variability in the expression of these triadic interactions.     

Aggression Levels Affect Social Interaction in the Non‐Breeding Territorial Aggression of the Weakly Electric Fish,Gymnotus omarorum

Animals typically decide whether to fight or retreat from conspecifics based on their individual estimates of the costs and benefits of fighting. Theoretical models predict how contenders solve a conflict, but the evaluation processes involved in these decisions depend on multiple factors that are difficult to explore experimentally. We addressed these questions using the non‐breeding territorial aggression of Gymnotus omarorum, in which subordinates make three distinctive decisions to signal their submission during a fight: (1) interruption of their electric discharges to hide from the dominant, (2) stop attacking and retreat, and (3) emission of ‘chirps’, transient submissive electric signals. We confirmed that subordinates take into account the aggressive performance of dominants to shape their own agonistic decisions and performance. The intensity of aggression is highly correlated with an agonistic dyad, and the decision of subordinates to retreat is influenced by the attack rates of dominants. When we lowered the aggression of expected dominants with a 5‐HT_1A receptor agonist, the correlation between the two contenders' aggression levels was lost and subordinates completely stopped emitting electric chirp signals. The aforementioned results contribute to the understanding of the decision‐making strategies driven by social challenge inherent to agonistic encounters.     

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.     

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.