Development of Y-chromosomal microsatellite markers for nonhuman primates

We have analysed 136 newly identified human Y-chromosomal microsatellites in five (sub)species of nonhuman primates. We identified 83 male-specific loci for central chimpanzees, 82 for western chimpanzees, 67 for gorillas, 45 for orangutans and 19 loci for mandrills. Polymorphism was detected at 56 loci in central chimpanzees, 29 in western chimpanzees, 24 in western gorillas, 17 in orangutans and at three in mandrills. Success in male-specific amplification of human Y-chromosomal microsatellites in nonhuman primates was significantly negatively correlated with divergence time from the human lineage. We observed significantly more Y-chromosomal microsatellite diversity in central chimpanzees than in western chimpanzees. There were significantly more male-specific loci with longer alleles in humans than with longer alleles in the nonhuman primates; however, this significant difference disappeared when only the loci which are polymorphic in nonhuman primates were analysed, suggesting that ascertainment bias is responsible. This study provides primatologists with a large number of polymorphic, male-specific microsatellite markers that will be valuable for investigating relevant questions in behavioural ecology such as male reproductive strategies, kin-based cooperation among males and male-specific dispersal patterns in wild groups of nonhuman primates.     

Brief communication: Locomotor limb preferences in captive chimpanzees (Pan troglodytes): implications for morphological asymmetries in limb bones

Understanding the evolutionary origins of hemispheric specialization remains a topic of considerable interest in a variety of scientific disciplines. Whether nonhuman primates exhibit population-level limb preferences continues to be a controversial topic. In this study, limb preferences for ascending and descending locomotion were assessed as a means of examining the hypothesis that asymmetries in forelimb bones might be attributed to asymmetries in posture. The results indicated that captive chimpanzees showed a population-level leftward asymmetry in descending locomotion but no group bias for ascending locomotion. The results are consistent with previous behavioral studies in captive chimpanzees as well as studies on skeletal asymmetries of the forelimbs of chimpanzees.     

Potential applications of urinary C-peptide of insulin for comparative energetics research

The study of comparative energetics offers a valuable way to identify broad ecological principles and assess the functional significance of energetic adaptations during the course of evolution. Yet, the quantification of energetic status for nonhuman primates under natural conditions remains one of the most challenging aspects of comparative energetics research. Here, we report on the development of a noninvasive field method for measuring energetic status in great apes, humans, and possibly other nonhuman primates. Specifically, we have explored measurement of a urinary metabolite of insulin (C-peptide) as a physiological marker of energetic condition in chimpanzees and orangutans. We performed three validation studies and successfully measured C-peptide in urine samples from captive chimpanzees, wild chimpanzees, and wild orangutans. Urinary C-peptide measures gave indications of being a reliable signal of energetic status in both species. For chimpanzees and orangutans in the wild, baseline urinary C-peptide levels were higher during periods of fruit abundance than periods of low fruit availability. Urinary C-peptide levels were also higher for well-fed captive chimpanzees compared with wild chimpanzees. Although sample size was small, top-ranking male chimpanzees showed higher C-peptide levels in the wild than low-ranking males only during the period of fruit abundance. These preliminary results indicate that further development of the urinary C-peptide method could expand opportunities to quantify energetic condition for great apes in the wild and generate new data for comparative research. We highlight specific applications for studying great ape reproduction as well as the nutritional ecology of human foragers.     

Termination of reproduction in nonhuman and human female primates

We examined demographic records from 13 captive primate species and a human population to determine age-related changes in female reproduction. In most species age-specific fertility declined and interbirth intervals increased with age. Using an operational definition of termination of reproduction based on individual variance in interbirth intervals, a proportion of females in most nonhuman species had terminated reproduction before death. Compared to other primates, a greater proportion of chimpanzees and human females ceased reproduction, and humans, in particular, were reproductively inactive for relatively longer than would be expected from their body weight. These empirical data quantify the extent of reproductive termination and thereby extend hitherto anecdotal accounts of this phenomenon in primates.     

Reproductive aging in captive and wild common chimpanzees: factors influencing the rate of follicular depletion

We examine and discuss evidence of contrasting differences in fertility patterns between captive and wild female chimpanzees, Pan troglodytes, as they age; in the wild females reproduce in their 40s, but captive studies suggest that menopause occurs around that time. Thus, despite the increased longevity generally observed in captive populations reproductive life span is shortened. We outline a hypothesis to explain the apparent differential pace of reproductive decline observed between wild and captive populations. The breeding schedules of captive primates may contribute to accelerated reproductive senescence because continuous cycling in captive animals results in early depletion of the ovarian stock and premature senescence. Available evidence supports the hypothesis that women with patterns of high oocyte loss experience earlier menopause. Chimpanzees in captivity live longer, and thus, similar to humans, they may experience follicular depletion that precedes death by many years. In captivity, chimpanzees typically have an early age at menarche and first birth, shorter interbirth intervals associated with short lactational periods as young mature faster, and nursery rearing, which allows mothers to begin cycling earlier. Variables typical of wild chimpanzee populations, including late age at menarche and first birth, long interbirth intervals associated with prolonged lactational periods, and a long period of female infertility after immigration, spare ovulations and may be responsible for the later age at reproductive termination. Finally, we describe and discuss the timing of specific reproductive landmarks that occur as female chimpanzees age, distinguishing between functional menopause (age at last birth) and operational menopause (end of cycling). Am. J. Primatol. 71:271–282, 2009. © 2008 Wiley‐Liss, Inc.     

Termination of reproduction in nonhuman and human female primates

We examined demographic records from 13 captive primate species and a human population to determine age-related changes in female reproduction. In most species age-specific fertility declined and interbirth intervals increased with age. Using an operational definition of termination of reproduction based on individual variance in interbirth intervals, a proportion of females in most nonhuman species had terminated reproduction before death. Compared to other primates, a greater proportion of chimpanzees and human females ceased reproduction, and humans, in particular, were reproductively inactive for relatively longer than would be expected from their body weight. These empirical data quantify the extent of reproductive termination and thereby extend hitherto anecdotal accounts of this phenomenon in primates.     

A stereo music system as environmental enrichment for captive chimpanzees

Music has been shown to have beneficial effects on humans but little is known about the effects of music on nonhuman primates in biomedical research settings. The authors monitored the effects of music on the behavior of captive chimpanzees and found that music had significant positive effects, including a reduction in agitated and aggressive behaviors.     

Positive reinforcement training as a technique to alter nonhuman primate behavior: quantitative assessments of effectiveness

Many suggest that operant conditioning techniques can be applied successfully to improve the behavioral management of nonhuman primates in research settings. However, relatively little empirical data exist to support this claim. This article is a review of several studies that discussed applied positive reinforcement training techniques (PRT) on breeding/research colonies of rhesus macaques (Macaca mulatta) and chimpanzees (Pan troglodytes) at The University of Texas M. D. Anderson Cancer Center and measured their effectiveness. Empirical analyses quantified the amount of time required to train rhesus monkeys to come up, station, target, and stay. Additionally, a study found that time spent affiliating by female rhesus was changed as a function of training low affiliators to affiliate more and high affiliators to affiliate less. Another study successfully trained chimpanzees to feed without fighting and to come inside on command. PRT is an important behavioral management tool that can improve the care and welfare of primates in captivity. Published empirical findings are essential for managers to assess objectively the utility of positive reinforcement training techniques in enhancing captive management and research procedures.     

The question of animal culture

In this paper I consider whether traditional behaviors of animals, like traditions of humans, are transmitted by imitation learning. Review of the literature on problem solving by captive primates, and detailed consideration of two widely cited instances of purported learning by imitation and of culture in free-living primates (sweet-potato washing by Japanese macaques and termite fishing by chimpanzees), suggests that nonhuman primates do not learn to solve problems by imitation. It may, therefore, be misleading to treat animal traditions and human culture as homologous (rather than analogous) and to refer to animal traditions as cultural.     

Examining the terminal investment hypothesis in humans and chimpanzees: associations among maternal age, parity, and birth weight

The terminal investment hypothesis (Williams [1966] Adaptation and Natural Selection; Princeton, NJ: Princeton University Press) holds that reproductive effort should increase over time in iteroparous species in which reproductive value declines with age. Attempts to model this hypothesis and test it in various species have produced mixed results. Clutton-Brock ([ 1984] Am. Nat. 123:212-229) argued that simply testing for changes in propagule size with age fails to recognize that the costs of producing offspring of a given size may increase over the lifespan, hence absence of a positive correlation does not defeat the hypothesis. However, this interpretation is weakened by evidence of sequential increases in propagule size independent of age, as such changes reveal a capacity to increase absolute investment over time. Humans and chimpanzees meet the preconditions of the terminal investment hypothesis. Surveying the obstetrics literature, we show that the majority of published studies indicate that parity has a positive effect on birth weight, but age has no effect. Analyzing 436 captive chimpanzee births, we document a positive influence of parity and a negative influence of age. We therefore conclude that, though it is yet to be replaced by a more compelling alternative, the terminal investment hypothesis is not supported in these two species, as absence of a positive effect of age on birth weight cannot be interpreted in a manner congruent with the hypothesis.     

Menopause in nonhuman primates?

A gradual alteration in the mechanisms underlying reproduction and fertility characterizes the aging process in human females. These changes culminate in menopause, conventionally defined as a cessation of menstrual cycles that marks the end of reproductive capacity. In fact, a central and defining event in menopause is the discontinuation of ovulation, which is correlated with a number of structural and functional changes in the reproductive axis. Despite several decades of research, a degree of uncertainty remains as to whether nonhuman primates undergo menopause, and whether they are suitable models of human reproductive senescence. We review some of the controversies that have clouded our understanding of reproductive aging in nonhuman primates, including issues of definition, timing, comparability of data from wild versus captive populations, and cross-species comparisons. The existing data support the view that menopause occurs in a number of primate species and is not unique to humans.     

Specific pathogen-free macaques: definition, history, and current production

Specific pathogen-free (SPF) macaque colonies are now requested frequently as a resource for research. Such colonies were originally conceived as a means to cull diseased animals from research-dedicated colonies, with the goal of eliminating debilitating or fatal infectious agents from the colony to improve the reproductive capacity of captive research animals. The initial pathogen of concern was Mycobacterium tuberculosis (M.tb.), recognized for many years as a pathogen of nonhuman primates as well as a human health target. More recently attention has focused on four viral pathogens as the basis for an SPF colony: simian type D retrovirus (SRV), simian immunodeficiency virus (SIV), simian T cell lymphotropic/leukemia virus (STLV), and Cercopithecine herpesvirus 1 (CHV-1). New technologies, breeding, and maintenance schemes have emerged to develop and provide SPF primates for research. In this review we focus on the nonhuman primates (NHPs) most common to North American NHP research facilities, Asian macaques, and the most common current research application of these animals, modeling of human AIDS.     

High prevalence of antibodies against hepatitis A virus among captive nonhuman primates

Hepatitis A virus (HAV) can infect not only humans but also several other nonhuman primates. This study has been conducted to evaluate the comprehensive anti-HAV seroprevalence in captive nonhuman primate populations in Thailand. The prevalence of antibodies against HAV in 96 captive nonhuman primates of 11 species was evaluated by competitive enzyme immunoassay (EIA). HAV antibodies were found in 64.7% (11/17) of macaques, 85.7% (6/7) of langurs, 28.4% (10/35) of gibbons, and 94.6% (35/37) of orangutans. However, anti-HAV IgM was not found in any sera. These results indicate that the majority of captive nonhuman primates in Thailand were exposed to HAV. It is possible that some of the animals were infected prior to capture.     

The implementation and initial evaluation of a physical therapy program for captive chimpanzees (Pan troglodytes)

Due to advances in captive nonhuman primate (NHP) medical care, the number of geriatric chimpanzees (≥35-years old) is growing. With old age comes a variety of physical conditions, including arthritis, stroke, and mobility impairments. Programs aimed at enhancing the welfare of geriatric chimpanzees are now quite common, but there are few published empirical evaluations of the efficacy of such programs. The current study aimed to create, implement, and evaluate the effects of participation in a physical therapy (PT) program on physical health, mobility, welfare, and behavior. Nine chimpanzees with mobility impairments participated in personalized PT routines (using positive reinforcement training) twice per week for 5 months. Additionally, nine control chimpanzees (non-mobility-impaired, matched with PT chimpanzees on age and gender) participated in body exam behavior sessions (also using positive reinforcement training) twice per week. All chimpanzees were rated on 14 health, well-being, and behavior items, as well as level of mobility throughout the PT program. Chimpanzees that participated in the PT program showed significant increases in ratings of physical health, well-being, and activity levels across phases of the program. Furthermore, compared to control chimpanzees, PT chimpanzees showed significant increases in ratings of ease of movement. Because raters were not blind to physical therapy treatment, our results represent an initial evaluation of the program that may suggest that participation in the PT program has physical, behavioral, and welfare benefits. Assessments of novel geriatric-focused care strategies and programs are essential to further enhance the welfare of the captive chimpanzee population, which is currently comprised of many geriatric animals, whose proportion of the captive population will only increase.     

Validation and utility of a body condition scoring system for chimpanzees (Pan troglodytes)

Obesity is a problem in captive chimpanzee colonies that can lead to increased risk for disease; therefore, implementation of effective weight management strategies is imperative. To properly implement a weight management program, captive managers should be able to noninvasively identify and assess overweight or obese individuals. Traditional means of categorizing obese individuals involve sedating the animals to obtain body weights or skin fold measurements. The current study aimed to validate a noninvasive, subjective body condition score (BCS) system for captive chimpanzees. The system utilizes a 10-point scale, with one rated as “emaciated,” five as “normal,” and 10 as “extremely obese.” Between 2013 and 2014, 158 chimpanzees were weighed and scored using this system (a) while sedated and (b) while awake in their social group within 1–3 days of sedation (“In-group” ratings). We found high inter-rater reliability between In-group raters, as well as between sedated and In-group scores. BCSs, which require observation only, were significantly positively correlated with weight (an objective measure of obesity often requiring anesthetization), supporting the scale's validity. The BCS system identified 36 individuals as “overweight,” while the use of weights alone identified only 26 individuals as “overweight.” Furthermore, the BCS system was able to classify individuals of the same sex and weight as having different BCSs, ranging from normal to overweight. Lastly, using focal animal behavioral observations from 2016 to 2018 (N = 120), we found that In-group BCS predicted individual levels of inactive behavior more than 2 years later, demonstrating the predictive validity of the scale. These results illustrate the utility of the BCS system as a noninvasive, reliable, and valid technique that may be more sensitive than traditional methods in identifying and quantifying obesity in chimpanzees. This system can be a useful tool for captive managers to monitor and manage the weight of chimpanzees and other nonhuman primates.     

Welfare based primate rehabilitation as a potential conservation strategy: does it measure up?

Many primate species are threatened with extinction and are the focus of extensive conservation efforts including re-introduction, captive breeding and habitat conservation. Welfare-based rehabilitation (hereafter also ‘rehabilitation’) is a management strategy commonly used for primates, particularly those species targeted by the pet and bush meat trades. Rehabilitation of rescued primates typically has the dual motivation of welfare and conservation, but has not been assessed as a conservation strategy. As the species involved in rehabilitation are often endangered (e.g. chimpanzees, gorillas, orang-utans), it is important for rehabilitation projects to follow a ‘best practice’ model in order to increase positive outcomes. In this study, we compared the approaches of 28 welfare-based primate rehabilitation projects to the ‘IUCN guidelines for nonhuman primate re-introductions’, in addition to components of the ‘Best practice guidelines for the re-introduction of great apes’ in order to assess where additional work might be needed for released animals to contribute to conservation outcomes. Few projects examined complied with the guidelines for re-introduction, failing to incorporate important factors such as quarantine, long term post-release monitoring and training for predator awareness. Further development of species-specific rehabilitation guidelines may improve the outcomes of future rehabilitation projects. To support this, we recommend that detailed methods and results be published for all rehabilitation efforts, regardless of the outcome.     

An apparatus and procedure for studying the choice component of foraging in a captive group of chimpanzees (Pan troglodytes)

An apparatus is described which was used to investigate the choice component of foraging in a captive group of chimpanzees maintained in a large, outdoor compound at the Yerkes Regional Primate Research Center Field Station. The utilization of more than one apparatus would allow the investigation of other ecological and psychological concepts in nonhuman primates housed under semi-natural conditions.     

Development of the visual preference of chimpanzees (<Emphasis Type="Italic">Pan troglodytes</Emphasis>) for photographs of primates: effect of social experience

In a study by Tanaka (2003) five captive chimpanzees preferred photographs of humans to those of chimpanzees. All the subjects were raised by humans and lived in captivity for many years. This suggests their preference might have developed through social experience. In this study examined this hypothesis by using three young chimpanzees raised by their mothers in a captive chimpanzee community. The young chimpanzees were tested four times before six years of age. I also tested eight adult chimpanzees that had been in captivity for more than 20 years. Each subject was presented with digitized color photographs of different species of primates on a touch-sensitive screen. The subjects received a food reward when they touched a photograph, irrespective of which photograph they touched. All the adult chimpanzees touched photographs of humans more frequently than those of any other species of primate. Two of the young chimpanzees showed no species preference before reaching 5 years of age, when they started to show preference for humans. The remaining young chimpanzee consistently preferred chimpanzees. These results suggest that development of visual preference of chimpanzees is affected by social experience during infancy.     

Reproductive Coordination in a Nonseasonally Breeding Primate Species,Macaca silenus

Varying types of reproductive coordination among females have been described for several mammals. Among nonhuman primates, female reproductive coordination has usually been described as breeding seasonality, or in few cases, closer synchrony within the breeding or birth season. We examined birth records from a large captive colony of lion-tailed macaques, Macaca silenus, a nonseasonally breeding species, in order to determine the degree of female reproductive synchrony in this population. Births were nonrandomly distributed over the 10-year study period. Of the total of 28 births, the majority (21 or 75 %) of births occurred in cohorts, in spite of wide variations in interbirth intervals among cohort birth mothers. Cohorts consisted of two to five infants born within a 90-d period or less. Of the remaining 7 “isolated” births, four were in the three years in which only one or two births occurred. The pattern of cohort births was nonrandomly distributed according to mother's parity: three of the isolated births were to primiparous mothers, whereas only one of the 21 cohort births was to a primiparous mother. Estrous synchrony results showed that females in the longer-established of two groups exhibited greater synchrony, suggesting social facilitation of reproductive coordination. It is thus suggested that synchrony in this sample was the result of social rather than ecological mechanisms, as has been hypothesized for some other mammalian species.