Research involving nonhuman primates (NHPs) has played a vital role in many of the medical and scientific advances of the past century. NHPs are used because of their similarity to humans in physiology, neuroanatomy, reproduction, development, cognition, and social complexity-yet it is these very similarities that make the use of NHPs in biomedical research a considered decision. As primate researchers, we feel an obligation and responsibility to present the facts concerning why primates are used in various areas of biomedical research. Recent decisions in the United States, including the phasing out of chimpanzees in research by the National Institutes of Health and the pending closure of the New England Primate Research Center, illustrate to us the critical importance of conveying why continued research with primates is needed. Here, we review key areas in biomedicine where primate models have been, and continue to be, essential for advancing fundamental knowledge in biomedical and biological research.
Scientific reports of personality in nonhuman primates are now appearing with increasing frequency across a wide range of disciplines, including psychology, anthropology, endocrinology, and zoo management. To identify general patterns of research and summarize the major findings to date, we present a comprehensive review of the literature, allowing us to pinpoint the major gaps in knowledge and determine what research challenges lay ahead. An exhaustive search of five scientific databases identified 210 relevant research reports. These articles began to appear in the 1930s, but it was not until the 1980s that research on primate personality began to gather pace, with more than 100 articles published in the last decade. Our analyses of the literature indicate that some domains (e.g., sex, age, rearing conditions) are more evenly represented in the literature than are others (e.g., species, research location). Studies examining personality structure (e.g., with factor analysis) have identified personality dimensions that can be divided into 14 broad categories, with Sociability, Confidence/Aggression, and Fearfulness receiving the most research attention. Analyses of the findings pertaining to inter-rater agreement, internal consistency, test retest reliability, generally support not only the reliability of primate personality ratings scales but also point to the need for more psychometric studies and greater consistency in how the analyses are reported. When measured at the level of broad dimensions, Extraversion and Dominance generally demonstrated the highest levels of inter-rater reliability, with weaker findings for the dimensions of Agreeableness, Emotionality, and Conscientiousness. Few studies provided data with regard to convergent and discriminant validity; Excitability and Dominance demonstrated the strongest validity coefficients when validated against relevant behavioral criterion measures. Overall, the validity data present a somewhat mixed picture, suggesting that high levels of validity are attainable, but by no means guaranteed. Discussion focuses on delineating major theoretical and empirical questions facing research and practice in primate personality. Am. J. Primatol. 72:653-671, 2010. (c) 2010 Wiley-Liss, Inc.
Tamarins are reported to live in small multimale-multifemale groups characterized by a single breeding female. Here we present information on the composition and genetic relatedness of individuals in 12 wild-trapped groups of Weddell's saddleback tamarins (Saguinus weddelli) from northern Bolivia to determine if groups are best described as nuclear or extended families suggesting social monogamy or whether groups contain several unrelated same sex adults indicative of social polyandry/polygyny. Mean group size was 6.25 including an average of 2.16 adult males (range 1-4) and 2.08 adult females (1-3). No group contained only one adult male and one adult female and 25% of groups contained two parous females. We estimated the genetic relatedness among individuals using 13 polymorphic microsatellite markers. Across the population, mean relatedness was low and not significantly different among adult males versus among adult females, suggesting that both sexes disperse from their natal groups. Adults of both sexes also tended to have close same-sex adult relatives within their groups; relatedness among adult females of the same group averaged 0.31 and among adult males was 0.26. This suggests that tamarins of one or both sexes sometimes delay dispersal and remain as adults in their natal group or that emigration of same-sexed relatives into the same group may be common. Finally, parentage analyses indicated that, whereas the parents of juveniles generally were present in the group, this was not always the case. Based on these data, published reports of the presence of multiple breeding males and occasionally multiple breeding females in the same group, and the fact that less than 10% of groups in the wild contain a single adult male-adult female pair, we argue that social polyandry best characterizes the composition of tamarin groups and that monogamy is not a common mating pattern in Saguinus weddelli or other tamarin species. Am. J. Primatol. 78:298-314, 2016. (c) 2015 Wiley Periodicals, Inc.
A large body of theoretical and empirical research suggests that kinship influences the development and maintenance of social bonds among group-living female mammals, and that human females may be unusual in the extent to which individuals form differentiated social relationships with nonrelatives. Here we combine behavioral observations of party association, spatial proximity, grooming, and space use with extensive molecular genetic analyses to determine whether female chimpanzees form strong social bonds with unrelated individuals of the same sex. We compare our results with those obtained from male chimpanzees who live in the same community and have been shown to form strong social bonds with each other. We demonstrate that party association is as good a predictor of spatial proximity and grooming in females as it is in males, that the highest party association indices are consistently found between female dyads, that the sexes do not differ in the long-term stability of their party association patterns, and that these results cannot be explained as a by-product of the tendency of females to selectively range in particular areas of the territory. We also show that close kin (i.e. mother-daughter and sibling dyads) are very rare, indicating that the vast majority of female dyads that form strong social bonds are not closely related. Additional analyses reveal that "subgroups" of females, consisting of individuals who frequently associate with one another in similar areas of the territory, do not consist of relatives. This suggests that a passive form of kin-biased dispersal, involving the differential migration of females from neighboring communities into subgroups, was also unlikely to be occurring. These results show that, as in males, kinship plays a limited role in structuring the intrasexual social relationships of female chimpanzees. Am. J. Primatol. 71:840-851, 2009. (C) 2009 Wiley-Liss, Inc.
Captive rhesus macaques sometimes exhibit undesirable abnormal behaviors, such as motor stereotypic behavior (MSB) and self-abuse. Many risk factors for these behaviors have been identified but the list is far from comprehensive, and large individual differences in rate of behavior expression remain. The goal of the current study was to determine which experiences predict expression of MSB and self-biting, and if individual differences in personality can account for additional variation in MSB expression. A risk factor analysis was performed utilizing data from over 4,000 rhesus monkeys at the California National Primate Research Center. Data were analyzed using model selection, with the best fitting models evaluated using Akaike Information Criterion. Results confirmed previous research that males exhibit more MSB and self-biting than females, MSB decreases with age, and indoor reared animals exhibit more MSB and self-biting than outdoor reared animals. Additionally, results indicated that animals exhibited less MSB and self-biting for each year spent outdoors; frequency of room moves and number of projects positively predicted MSB; pair separations positively predicted MSB and self-biting; pair housed animals expressed less MSB than single housed and grate paired animals; and that animals expressed more MSB and self-biting when in bottom rack cages, or cages near the room entrance. Based on these results we recommend limiting exposure to these risk factors when possible. Our results also demonstrated a relationship between personality and MSB expression, with animals low on gentle temperament, active in response to a human intruder, and high on novel object contact expressing more MSB. From these results we propose that an animal's MSB is related to its predisposition for an active personality, with active animals expressing higher rates of MSB. Am. J. Primatol. 75:995-1008, 2013. (c) 2013 Wiley Periodicals, Inc.
Based on morphological and genetic characteristics, we describe a new species of hoolock gibbon ( Hoolock tianxing ) that is distributed between the Irrawaddy‐Nmai Hka Rivers and the Salween River, which is previously assigned to H. leuconedys .
The notion of animal culture has been well established mainly through research aiming at uncovering differences between populations. In chimpanzees (Pan troglodytes verus), cultural diversity has even been found in neighboring communities, where differences were observed despite frequent immigration of individuals. Female chimpanzees transfer at the onset of sexual maturity at an age, when the behavioral repertoire is fully formed. With immigrating females, behavioral variety enters the group. Little is known about the diversity and the longevity of cultural traits within a community. This study is building on previous findings of differences in hammer selection when nut cracking between neighboring communities despite similar ecological conditions. We now further investigated the diversity and maintenance of cultural traits within one chimpanzee community and were able to show high levels of uniformity in group-specific behavior. Fidelity to the behavior pattern did not vary between dispersing females and philopatric males. Furthermore, group-specific tool selection remained similar over a period of 25 years. Additionally, we present a study case on how one newly immigrant female progressively behaved more similar to her new group, suggesting that the high level of similarity in behavior is actively adopted by group members possibly even when originally expressing the behavior in another form. Taken together, our data support a cultural transmission process in adult chimpanzees, which leads to persisting cultural behavior of one community over time. Am. J. Primatol. 76:649-657, 2014. (c) 2014 Wiley Periodicals, Inc.
Indonesia has amongst the highest primate species richness, and many species are included on the country's protected species list, partially to prevent over-exploitation. Nevertheless traders continue to sell primates in open wildlife markets especially on the islands of Java and Bali. We surveyed 13 wildlife markets in 2012-2014 and combined our results with previous surveys from 1990-2009 into a 122-survey dataset with 2,424 records of 17 species. These data showed that the diversity of species in trade decreased over time, shifting from rare rainforest-dwelling primates traded alongside more widespread species that are not confined to forest to the latter type only. In the 1990s and early 2000s orangutans, gibbons and langurs were commonly traded alongside macaques and slow lorises but in the last decade macaques and slow lorises comprised the bulk of the trade. In 2012-2014 we monitored six wildlife markets in Jakarta, Bandung and Garut (all on Java), and Denpasar (Bali). During 51 surveys we recorded 1,272 primates of eight species. Traders offered long-tailed macaque (total 1,007 individuals) and three species of slow loris (228 individuals) in five of the six markets, whereas they traded ebony langurs (18 individuals), and pig-tailed macaques (14 individuals) mostly in Jakarta. Pramuka and Jatinegara markets, both in Jakarta, stood out as important hubs for the primate trade, with a clear shift in importance over time from the former to the latter. Slow lorises, orangutans, gibbons and some langurs are protected under Indonesian law, which prohibits all trade in them; of these protected species, only the slow lorises remained common in trade throughout the 25-year period. Trade in non-protected macaques and langurs is subject to strict regulationswhich market traders did not followmaking all the market trade in primates that we observed illegal. Trade poses a substantial threat to Indonesian primates, and without enforcement, the sheer volume of trade may mean that species of Least Concern or Near Threatened may rapidly decline. Am. J. Primatol. 79:e22517, 2017. (c) 2015 Wiley Periodicals, Inc.
Research on oxytocin thus far has involved multiple distinct theories for its effects on social behavior. We provide a multistage framework to integrate these hypotheses and conceptualize the seemingly divergent results across both behavioral and neural studies of oxytocin.
There has been an enduring interest in primate tool-use and manipulative abilities, most often with the goal of providing insight into the evolution of human manual dexterity, right-hand preference, and what behaviours make humans unique. Chimpanzees (Pan troglodytes) are arguably the most well-studied tool-users amongst non-human primates, and are particularly well-known for their complex nut-cracking behaviour, which has been documented in several West African populations. However, their sister-taxon, the bonobos (Pan paniscus), rarely engage in even simple tool-use and are not known to nut-crack in the wild. Only a few studies have reported tool-use in captive bonobos, including their ability to crack nuts, but details of this complex tool-use behaviour have not been documented before. Here, we fill this gap with the first comprehensive analysis of bonobo nut-cracking in a natural environment at the Lola ya Bonobo sanctuary, Democratic Republic of the Congo. Eighteen bonobos were studied as they cracked oil palm nuts using stone hammers. Individual bonobos showed exclusive laterality for using the hammerstone and there was a significant group-level right-hand bias. The study revealed 15 hand grips for holding differently sized and weighted hammerstones, 10 of which had not been previously described in the literature. Our findings also demonstrated that bonobos select the most effective hammerstones when nut-cracking. Bonobos are efficient nut-crackers and not that different from the renowned nut-cracking chimpanzees of Bossou, Guinea, which also crack oil palm nuts using stones.
The growing recognition that social needs of primates in captivity must be addressed can present challenges to staff at primate facilities charged with implementing pair-housing solutions for animals. Unfortunately, there are few published papers that identify individual characteristics that might facilitate the social pairing process, and those that have looked at pre-pairing measures of behavior have produced mixed results. Using a database of n=340 isosexual pairing attempts, we report that measures associated with responses to a standardized infant assessment protocol (the BioBehavioral Assessment program) predict success in pairing attempts that occurred years later. Behavioral responses to a brief separation and relocation, to a human intruder challenge, as well as ratings of temperament, were obtained from rhesus monkeys at 3–4 months of age. Logistic regression was used to identify potential predictors of success when animals were paired up to 10 years after the behavioral assessments. Among females, success was higher when members of a pair were more similar (i.e., a smaller difference scores) in patterns of emotional responding (emotionality, nervous temperament) during the infant assessments. In contrast, among males, success was higher when the pair had lower mean values for Gentle and Nervous temperament scores; when the members were younger; when pairs had a greater weight difference; and when they came from the same rearing background. Together, our results suggest that broad measures reflecting patterns of emotionality in response to challenge, which can be assessed in infancy (but which remain relatively stable throughout life) can be usefully employed to increase the likelihood of success in pairing attempts.
Old World monkeys provide naturally occurring and experimentally induced phenotypes closely resembling the highly prevalent polycystic ovary syndrome (PCOS) in women. In particular, experimentally induced fetal androgen excess in female rhesus monkeys produces a comprehensive adult PCOS-like phenotype that includes both reproductive and metabolic dysfunction found in PCOS women. Such a reliable experimental approach enables the use of the prenatally androgenized (PA) female rhesus monkey model to (1) examine fetal, infant and adolescent antecedents of adult pathophysiology, gaining valuable insight into early phenotypic expression of PCOS, and (2) to understand adult pathophysiology from a mechanistic perspective. Elevated circulating luteinizing hormone (LH) levels are the earliest indication of reproductive dysfunction in late gestation nonhuman primate fetuses and infants exposed to androgen excess during early (late first to second trimester) gestation. Such early gestation-exposed PA infants also are hyperandrogenic, with both LH hypersecretion and hyperandrogenism persisting in early gestation-exposed PA adults. Similarly, subtle metabolic abnormalities appearing in young nonhuman primate infants and adolescents precede the abdominal adiposity, hyperliplidemia and increased incidence of type 2 diabetes that characterize early gestation-exposed PA adults. These new insights into the developmental origins of PCOS, and progression of the pathophysiology from infancy to adulthood, provide opportunities for clinical intervention to ameliorate the PCOS phenotype thus providing a preventive health-care approach to PCOS-related abnormalities. For example, PCOS-like traits in PA monkeys, as in PCOS women, can improve with better insulin-glucose homeostasis, suggesting that lifestyle interventions preventing increased adiposity in adolescent daughters of PCOS mothers also may reduce their risk of acquiring many PCOS-related metabolic abnormalities in adulthood. Am. J. Primatol. 71:776-784, 2009. (C) 2009 Wiley-Liss, Inc.
Substantial progress has been made in microbiome research, although less attention has been given to host‐associated microbiomes in nonhuman primates (NHPs). This review explores what is currently understood about the microbiome across the complex world of NHPs, and what the future holds.
The gut microbiota contributes to host health by maintaining homeostasis, increasing digestive efficiency, and facilitating the development of the immune system. The composition of the gut microbiota can change dramatically within and between individuals of a species as a result of diet, age, or habitat. Therefore, understanding the factors determining gut microbiota diversity and composition can contribute to our knowledge of host ecology as well as to conservation efforts. Here we use high-throughput sequencing to describe variation in the gut microbiota of the endangered ring-tailed lemur (Lemur catta) at the Beza Mahafaly Special Reserve (BMSR) in southwestern Madagascar. Specifically, we measured the diversity and composition of the gut microbiota in relation to social group, age, sex, tooth wear and loss, and habitat disturbance. While we found no significant variation in the diversity of the ring-tailed lemur gut microbiota in response to any variable tested, the taxonomic composition of the gut microbiota was influenced by social group, age, and habitat disturbance. However, effect sizes were small and appear to be driven by the presence or absence of relatively low abundance taxa. These results suggest that habitat disturbance may not impact the lemur gut microbiota as strongly as it impacts the gut microbiota of other primate species, highlighting the importance of distinct host ecological and physiological factors on host-gut microbe relationships. Am. J. Primatol. 78:883-892, 2016. (c) 2016 Wiley Periodicals, Inc.
We describe a newly discovered Macaca species from the Medog, in southeastern Tibet, China, Macaca leucogenys sp. nov or the white-cheeked macaque. Based on 738 photos taken during direct observations and captured by camera traps this new species appears to be distinct from the Macaca sinica species group. Moreover, the species is distinguished from all potential sympatric macaque species (M. mulatta, M. thibetana, M. assamensis, and M. munzala) in exhibiting a suite of pelage characteristics including relatively uniform dorsal hair pattern, hairy ventral pelage, relative hairless short tail, prominent pale to white side- and chin-whiskers creating a white cheek and round facial appearance, dark facial skin on the muzzle, long and thick hairs on its neck, and a round rather than arrow-shaped male genitalia. This new macaque species was found to exploit a diverse set of habitat types from tropical forest at 1395m, to primary and secondary evergreen broad-leaved forest at 2000m, as well as mixed broadleaf-conifer forest at 2700m. Its range may extend to neighboring counties in Tibet and the part of southeastern Tibet controlled by India. The white-cheeked macaque is threatened by illegal hunting and the construction of hydropower stations. Discovery of this new primate species further highlights the high value for biodiversity conservation of southeastern Tibet and calls for more intensive surveys, studies, and environmental protection in this area. Am. J. Primatol. 77:753-766, 2015. (c) 2015 Wiley Periodicals, Inc.
First report of group fission in vervets reveals high tradition resilience. Initial group was trained to prefer one of two foods but low‐rankers sampled non‐preferred option. After fission these monkeys ate only the parent group's preferred option.