Like Threaten Like in Mangabeys and People?

Abstract

Adult golden-bellied mangabeys (Cercocebus galeritus chrysogaster) housed in three structures directed more frequent aggressive facial displays toward human visitors of their same sex than toward humans of other sex. The human male visitors showed the same patterns as did the mangabeys, with men harassing males. Human females were the only ones that did not display this pattern. Infants and small juveniles did not threaten each other across species. All targets of aggression do not produce the same sex differences in mangabey facial threats.     

Evidence for sexually selected infanticide in captiveCercopithecus mitis,Cercocebus torquatus,andMandrillus leucophaeus

Adult resident males of one-male-multi-female primate groups housed at the Hannover Zoo exhibited aggression, when confronted with nonadult individuals, which were fathered by other males: (1) a new adult resident male in a group of blue monkeys killed a 5.8-month-old female infant: (2) a new adult resident male in a group of white collared mangabeys injured a 24.0-month-old female and an 18.9-month-old male severely; they would have died without veterinary care; and (3) the resident male of a group of drills threatened an 1.8-month-old foreign female infant seriously; efforts to introduce the infant were discontinued. Pathological explanations are unlikely because the adult males showed no aggression towards own nonadult offspring under the same captive conditions. By and large, the events support the theory that infanticide is the result of sexual selection among males.     

Primates and the Ecology of their Infectious Diseases: How will Anthropogenic Change Affect Host‐Parasite Interactions?

The sudden appearance of diseases like SARS (severe acute respiratory syndrome 1 ), the devastating impacts of diseases like Ebola on both human and wildlife communities, 2 , 3 and the immense social and economic costs created by viruses like HIV 4 underscore our need to understand the ecology of infectious diseases. Given that monkeys and apes often share parasites with humans, understanding the ecology of infectious diseases in nonhuman primates is of paramount importance. This is well illustrated by the HIV viruses, the causative agents of human AIDS, which evolved recently from related viruses of chimpanzees (Pan troglodytes) and sooty mangabeys (Cercocebus atys 5 ), as well as by the outbreaks of Ebola virus, which trace their origins to zoonotic transmissions from local apes. 6 A consideration of how environmental change may promote contact between humans and nonhuman primates and thus increase the possibility of sharing infectious diseases detrimental to humans or nonhuman primates is now paramount in conservation and human health planning.     

Correlates of Self-directed Behaviors in Captive <Emphasis Type="Italic">Cercopithecus aethiops</Emphasis>

Researchers have widely used self-directed behaviors (SDB) as a behavioral indicator of anxiety in nonhuman primates. We examined if SDB rates in captive vervets (Cercopithecus aethiops) were associated with 1) proximity to conspecifics in general, 2) relative dominance rank of proximity partners, and 3) postconflict situations. Subjects were members of a captive group of vervets at the Lisbon Zoo, Portugal. The group comprised 3 males and 7 females, which were focal sampled for 10.5 h each. Vervets did not engage in more SBD while in proximity of conspecifics than while alone, and individual SDB rates were not generally influenced by dominance ranks of neighbors. Yet, victims of conflicts significantly increased their SDB rates after agonistic episodes, which is consistent with the view that SDB rates are an index of anxiety in Cercopithecus aethiops.     

Rank,relationships, and responses to intruders among adult male vervet monkeys

We examined the influences of dyadic relationships among captive adult male vervet monkeys (Cercopithecus aethiops sabaeus) on behavior directed toward caged “intruder” males placed inside subjects' enclosures. Subjects were all 9 adult male residents from three stable social groups, each of which contained 3 adult males, at least 3 adult females, and their immature offspring. Every male was observed in two 3-hour sessions, each time with one of the 2 other adult males from his group. Observation sessions consisted of six consecutive 30-min stages in which group composition and the presence of the intruder were manipulated. All groups exhibited a stable, linear male dominance hierarchy prior to and throughout the study. In each group, there was one pair of males, when together, in which each member exhibited higher rates of intruder-directed approach and aggressive behaviors than when either animal was paired with the third male of his social group. Such pairs were also distinguished by high levels of within-pair agonistic interactions. The higher-ranking member of each dyad was the most aggressive male toward the intruder in his social group, although only one of these animals was the dominant male of his group. Mutual facilitation of aggression against intruding males is interpreted as cooperative behavior benefitting both males by increasing the likelihood of repelling a potential competitor for resident females. Such cooperation provides further evidence in nonhuman primates for cohesive male-male dyads between animals whose social interactions are characterized by agonism. © 1993 Wiley-Liss, Inc.     

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.     

Dominance,Coloration, and Social and Sexual Behavior in Male Drills <Emphasis Type="Italic">Mandrillus leucophaeus</Emphasis>

Sexual selection has driven the evolution and elaboration of a wide variety of displays and ornaments in male nonhuman primates, including capes, cheek flanges, and sexual coloration. Among the most sexually dimorphic of all primates is the drill (Mandrillus leucophaeus), the males of which can be 3 times the mass of females, possess large canines, and exhibit extremely bright sexual skin coloration. However, the function of male coloration in this species has never been examined. Here, we present data on male color (measured objectively using digital photography), dominance rank, measures of male-female association, and key sexual behaviors, of adult male drills (n = 17) living in four semi free-ranging enclosures at the Drill Rehabilitation and Breeding Center in Nigeria. We test the hypothesis that male coloration is a badge of status, indicating dominance rank, and the hypothesis that male coloration attracts females. We found that male coloration did indicate rank, and that high ranking, strongly colored males were more likely to associate with adult females, and more specifically with fully tumescent females. These males also engaged in more sexual activity. However, measures of male-female association and sexual behaviors were not related to male color once rank had been taken into consideration; i.e., for males of a given rank, females did not prefer those that were more colorful. We discuss the results in light of what is known about the wild drill social system, in which unfamiliar individuals may come together in “supergroups,” and in which quality indicators of competitive ability may be particularly important.     

Population Sizes and Distribution of Primates in the Lower Tana River Forests,Kenya

We studied the population size and distribution of diurnal primates in the lower Tana River forests, Kenya. They are the only remaining habitats for 2 threatened primates: the Tana River red colobus (Procolobus rufomitratus) and the Tana River crested mangabey (Cercocebus galeritus galeritus). We conducted censuses in 73 forest patches from January through March 2001. We estimate population size of the red colobus to be 788 individuals in 82 groups and that of the crested mangabeys to be 2,070 individuals in 59 groups. The data suggest that over a 7-year period (1994-2001), there was an 18% increase in the crested mangabey population and a 5% decline in red colobus numbers. Further, the red colobus range has expanded both north and south, whereas that of crested mangabeys has only expanded south. Fifty-six percent of crested mangabeys and 46% of red colobus groups were inside the Tana River Primate National Reserve (TRPNR). Other primates encountered included 170 groups of Sykes' monkeys (Cercopithecus mitis), 70 groups of yellow baboons (Papio cynocephalus) and 4 groups of grivets [Chlorocebus (Cercopithecus) aethiops]. Mean group densities of the 2 endangered primates and of baboons were higher inside than outside the TRPNR, reinforcing the importance of TRPNR for their conservation. An intervention program is required to stem further decline in the red colobus population and to protect small isolated groups in forest patches outside TRPNR.     

Do Dispersing Monkeys Follow Kin? Evidence from Gray-cheeked Mangabeys (<Emphasis Type="Italic">Lophocebus albigena</Emphasis>)

Among social vertebrates, immigrants may incur a substantial fitness cost when they attempt to join a new group. Dispersers could reduce that cost, or increase their probability of mating via coalition formation, by immigrating into groups containing first- or second-degree relatives. We here examine whether dispersing males tend to move into groups containing fathers or brothers in gray-cheeked mangabeys (Lophocebus albigena) in Kibale National Park, Uganda. We sampled blood from 21 subadult and adult male mangabeys in 7 social groups and genotyped them at 17 microsatellite loci. Twelve genotyped males dispersed to groups containing other genotyped adult males during the study; in only 1 case did the group contain a probable male relative. Contrary to the prediction that dispersing males would follow kin, relatively few adult male dyads were likely first- or second-degree relatives; opportunities for kin-biased dispersal by mangabeys appear to be rare. During 4 yr of observation, adult brothers shared a group only once, and for only 6 wk. Mean relatedness among adult males sharing a group was lower than that among males in different groups. Randomization tests indicate that closely related males share groups no more often than expected by chance, although these tests had limited power. We suggest that the demographic conditions that allow kin-biased dispersal to evolve do not occur in mangabeys, may be unusual among primates, and are worth further attention.     

Advantages and limitations of nonhuman primates as animal models in genetic research on complex diseases

Abstract: The genetic similarity between humans and nonhuman primates makes nonhuman primates uniquely suited as models for genetic research on complex physiological and behavioral phenotypes. By comparison with human subjects, nonhuman primates, like other animal models, have several advantages for these types of studies: 1) constant environmental conditions can be maintained over long periods of time, greatly increasing the power to detect genetic effects; 2) different environmental conditions can be imposed sequentially on individuals to characterize genotype-environment interactions; 3) complex pedigrees that are much more powerful for genetic analysis than typically available human pedigrees can be generated; 4) genetic hypotheses can be tested prospectively by selective matings; and 5) essential invasive and terminal experiments can be conducted. Limitations of genetic research with nonhuman primates include cost and availability. However, the ability to manipulate both genetic and environmental factors in captive primate populations indicates the promise of genetic research with these important animal models for illuminating complex disease processes. The utility of nonhuman primates for biomedical research on human health problems is illustrated by examples concerning the use of baboons in studies of osteoporosis, alcohol metabolism, and lipoproteins.     

Dispersal Patterns Among Olive Colobus in Taï National Park

In Primates, females are more likely to be philopatric than males. However, in some species like Procolobus verus, females or individuals of both sexes disperse. In Taï National Park, Ivory Coast, olive colobus groups are small, with one or two adult males and 6 females. Dispersal is common for juveniles and adults of both sexes. Adult male dispersal is less common than adult female dispersal. Adult females immigrated especially into small, one-male groups indicating that food competition played a role. Furthermore, unknown sexually receptive females visited resident groups and mated with the resident males for a few days before disappearing again. Adult males dispersed when this improved their mating opportunities. All juveniles left their natal groups. The dispersal of juveniles may be a strategy to prevent inbreeding with their parents. Dispersal by juvenile males furthermore seemed to be the result of mate competition. The high dispersal rates, visits by receptive females, and dispersal of all individuals in the population suggest that moving between groups is a strategy that can be used ad hoc in several situations more easily in the olive colobus than in most other primates. The predation risks related to moving between groups were reduced by dispersing in conspecific or allospecific groups and by dispersing to neighboring groups.     

Intestinal Parasites in Gorillas,Chimpanzees, and Humans at Mondika Research Site,Dzanga-Ndoki National Park,Central African Republic

We report prevalences and eggs/protozoa per g (EPG; PPG) of helminths and protozoa in gorillas, chimpanzees, agile mangabeys, indigenous Ba'Aka and Bantu, and western researchers at a remote field site in the Central African Republic. We examined fecal samples for eggs, larvae, proglottids, cysts, amoeba, trophozoites, and flagellates. For helminths, strongylates were most prevalent, infecting 82–94% of nonhuman primates (NH) and 30–93% of human (H) groups, followed by ascaroids (14–88% NH; 0–15% H), and threadworms (0–22% NH; 0–29% H). For protozoa, Entamoeba histolytica (2–100% NH; 33–52% H) and trichomonads (11–88% NH; 0–54% H) were most prevalent. Among gorilla samples (n = 156) there were significant age/sex differences in EPG/PPG for strongylates, threadworms, Entamoeba histolytica, and trichomonads, with infants exhibiting the highest mean EPG/PPG for all parasites except trichomonads. Between group analyses revealed that the Ba'Aka had significantly higher mean EPG of strongylates, ascaroids and threadworms than all other primate groups, except the mangabeys. For Entamoeba histolytica, E. coli, Balantidium coli, and Iodamoeba butschlii, the agile mangabeys had significantly higher mean PPG than other groups; for trichomonads, the chimpanzees, and mangabeys had the highest mean PPG. Relative to other African ape sites, the gorillas and chimpanzees at Mondika appear to have high prevalences of intestinal parasites. This may be the result of the high proportion of swamp and seasonally flooded areas, which provide optimal viability for parasite eggs and ova. At Mondika, the significantly higher parasite levels of Ba'Aka probably result from more traditional methods of hygiene and lack of available medical treatment. All workers at research sites should be monitored and treated to minimize cross-transmission between humans and local fauna.     

Inbreeding depression in ring-tailed lemurs (<Emphasis Type="Italic">Lemur catta</Emphasis>): genetic diversity predicts parasitism,immunocompetence, and survivorship

The consequences of inbreeding have been well studied in a variety of taxa, revealing that inbreeding has major negative impacts in numerous species, both in captivity and in the wild; however, as trans-generational health data are difficult to obtain for long-lived, free-ranging species, similar analyses are generally lacking for nonhuman primates. Here, we examined the long-term effects of inbreeding on numerous health estimates in a captive colony of ring-tailed lemurs (Lemur catta), housed under semi-natural conditions. This vulnerable strepsirrhine primate is endemic to Madagascar, a threatened hotspot of biodiversity; consequently, this captive population represents an important surrogate. Despite significant attention to maintaining the genetic diversity of captive animals, breeding colonies invariably suffer from various degrees of inbreeding. We used neutral heterozygosity as an estimate of inbreeding and showed that our results reflect genome-wide inbreeding, rather than local genetic effects. In particular, we found that genetic diversity affects several fitness correlates, including the prevalence and burden of Cuterebra parasites and a third (N = 6) of the blood parameters analyzed, some of which reflect immunocompetence. As a final validation of inbreeding depression in this captive colony, we showed that, compared to outbred individuals, inbred lemurs were more likely to die earlier from diseases. Through these analyses, we highlight the importance of monitoring genetic variation in captive animals—a key objective for conservation geneticists—and provide insight into the potential negative consequences faced by small or isolated populations in the wild. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Effect of Dominance,Reproductive State,and Group Size on Body Mass in Macaca radiata

Body mass can impact reproductive performance in males and females. In nonhuman primates the relationship is often mediated by dominance. We measured body mass monthly in a provisioned group of bonnet macaques (Macaca radiata) living at a Hindu temple. We also measured body mass on 3 occasions in a wild population of bonnet macaques. In the temple group, females that reproduced lost body mass, while females that did not reproduce gained body mass. Mass loss among females occurred primarily while they were nursing. Adult males from the temple group lost mass during the mating season and gained it during the non-mating season. Subadult males experienced less seasonal variation in body mass. Body mass and changes in mass were not related to dominance rank in either the temple or the forest group. Furthermore, maternal dominance rank did not affect infant mass. Females from the smallest forest group weighed significantly less than females from the two larger forest groups, which suggests intergroup competition in the population. Body mass was not related to dominance rank in a straightforward manner but may indirectly affect reproductive performance. The pattern of body mass change suggests that the period of lactation is critical for females and endurance rivalry is an important form of competition among males.     

Pregnancy,gestation and parturition in free-ranging tana river crested mangabeys (Cercocebus galeritus galeritus)

Mean gestation for seven free-ranging Tana River crested mangabeys (Cercocebus galeritus galeritus) is 180 days (SE = 4.49). All females showed postconception sexual swellings after the first 2 months of pregnancy, and two of the seven copulated with males at this time. One birth was observed; observations of a second infant began less than 1 hr after birth. Details of parturition are given, with responses of group members to the events. Adult and juvenile females showed more sustained interest in the new infants than adult or juvenile males.     

Maternal age, parity, and reproductive outcome in captive chimpanzees (Pan troglodytes)

As early as the 1970s, it was suggested that nonhuman primates may serve as models of human reproductive senescence. In the present study, the reproductive outcomes of 1,255 pregnancies in captive chimpanzees (Pan troglodytes) were examined in relation to parity and its covariate, maternal age. The results show that the percentage of positive pregnancy outcomes was negatively correlated with increasing parity. In addition, spontaneous abortions, stillbirths, and caesarian sections (C-sections) were positively correlated with increasing parity. Maternal age, rather than parity, was found to be the most important predictor of negative birth outcome. This study supports research demonstrating reproductive decline and termination in nonhuman primates, and is the first to quantitatively account for this phenomenon in captive female chimpanzees.     

Relationship between sunlight exposure, housing condition, and serum vitamin D and related physiologic biomarker levels in captive chimpanzees (Pan troglodytes)

In primates, the primary source of vitamin D is synthesis in the skin through sun exposure. Decreased sun exposure may lead to vitamin D deficiency and consequently other health issues. In laboratory, sanctuary, and zoo settings, chimpanzees (Pan troglodytes) may be housed indoors for prolonged periods of time without regular exposure to unfiltered sunlight. However, little research has examined the relationship between housing conditions and vitamin D serum levels in captive chimpanzees. In this study, we retrospectively compared serum levels of total vitamin D, calcium, ionic calcium, phosphorous, albumin, and alkaline phosphatase in 18 female and 12 male chimpanzees as they cycled between indoor-only and indoor-outdoor enclosures. Total vitamin D was significantly lower and alkaline phosphatase significantly higher when subjects were in the indoor-only enclosures compared with when they had regular access to outdoor enclosures. A vitamin D effect occurred only in young and prime-adult animals. Changes were significant in female but not in male chimpanzees. Calcium, ionic calcium, phosphorus, and albumin did not differ between indoor-only and indoor-outdoor enclosures. However, female chimpanzees exhibited significantly lower calcium and phosphorous levels while in the indoor-only enclosures. These results suggest that adult captive chimpanzees experience vitamin D deficiency when housed without regular access to unfiltered sunlight and that these effects may be more acute for adult female animals.     

Sexual behavior and reproduction ofCercocebus albigena johnstonii in Kibale forest,Western Uganda

Gray-cheeked mangabeys live in multimale social groups. Two groups of these monkeys were studied extensively over a period of 22 months, and a further eight groups were observed opportunistically. Data on the occurrence of sexual swelling infernales were collected and the different phases of swelling and deflation are described in detail together with data on their duration. The data were found to agree broadly with those presented by other workers on captive animals. Pre and postpartum swellings are described. The majority of copulations was observed to occur at peak swelling and a specific gesture, the head flag, was noted as a solicitation. The data on initiation of copulations show that the males initiated more copulations than the females. However, female-initiated copulations ended in ejaculation more often than male-initiated copulations. The behaviors of the mangabeys during precopulation and copulation were found to be broadly similar to those of the macaque. Copulations were observed most often on the day of peak swelling;however, adult males were the only animals to copulate prior to peak swelling. Subadult male copulations were most often after peak swelling. Masturbation was observed to ejaculation on two occasions. The data show gestation periods of between 184 and 189 days. A mean interbirth interval was calculated to be 33.33 ± 15.87 months.     

Descriptive accounts of the behavior of breeding and nonbreeding pairs of golden-bellied mangabeys (Cercocebus galeritus chrysogaster)

Four adult heterosexual pairs of golden-bellied mangabeys (Cercocebus galeritus chrysogaster) were observed at the Sacramento Zoo. The behaviors of the pairs differed with the histories of the individuals involved, degrees of swelling of the females, presence of offspring in their cages, and the nature of distractions near their enclosures. Young wild-born adults without a nursing-aged infant displayed sexual behavior and observer-directed threats. Experienced wild-born breeders with nursing-aged infants and older juveniles showed intense interest in the sexual behavior of the young pair. These breeders displayed mild aggression, both protective and punitive, toward the juveniles and the infant living with them. Captive and abnormally behaving adults displayed self-biting, bizarre postures, and other stress-related behaviors as well as large amounts of visitor-directed aggression. An experienced breeder male paired with the captive female was unable to achieve copulation. To reduce stress in these and other relatively aggressive primate species, careful attention should be paid to housing location, social history, stage of estrus, and presence of offspring.     

Social compatibility in a newly formed all‐male group of white crowned mangabeys (Cercocebus atys lunulatus)

Surplus males in primate captive populations are a common problem for zoos. Some captive breeding programs promote all‐male groups as an adequate option to house surplus males, but there have been few attempts to assess the feasibility of this management technique across primate species. The present study provides preliminary data regarding social compatibility within a newly formed all‐male group of four white crowned mangabeys (Cercocebus atys lunulatus). The study was conducted at the Valencia Zoo (Spain), where data on social behavior were collected over 6 months using continuous focal animal sampling for a total of 87 hr of observation. Results show that low intensity aggressive behaviors (facial threats) were expressed at high rates, whereas physical aggression (fights) rarely occurred. Aggression was more frequent among individuals belonging to the same age–gender class. Regarding affiliative behaviors, every individual actively sought proximity to all other group members through positive approaches, and although not all males carried out social grooming, every male was groomed by at least one group member. Our results suggest that the group was compatible socially because social relationships among the individuals were not neutral, and physical aggression occurred at low rates. The present study provides preliminary data supporting the feasibility of all‐male groups as a management option for surplus males in captive populations of white crowned mangabeys. Nevertheless, further studies are needed to be able to generalize both within and across species. Zoo Biol 0:1–7, 2007. © 2006 Wiley‐Liss, Inc.