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In apes and humans, neutrophil to lymphocyte ratio (NLR) can be used as a predictive indicator of a variety of clinical conditions, longevity, and physiological stress. In chimpanzees specifically, NLR systematically varies with age, rearing, sex, and premature death, indicating that NLR may be a useful diagnostic tool in assessing primate health. To date, just one very recent study has investigated NLR in old world monkeys and found lower NLR in males and nursery-reared individuals, as well as a negative relationship between NLR and disease outcomes. Given that baboons are increasingly used as research models, we aimed to characterize NLR in baboons by providing descriptive data and examinations of baboon NLR heritability, and of the relationships between NLR, age, rearing, and sex in 387 olive baboons (Papio anubis) between 6 months and 19 years of age. We found that (1) mother-reared baboons had higher NLRs than nursery-reared baboons; (2) females had higher NLRs than males; and (3) there was a quadratic relationship between NLR and age, such that middle-aged individuals had the highest NLR values. We also examined NLR as a function of transport to a new facility using a subset of the data. Baboons exhibited significantly higher transport NLRs compared to routine exam NLRs. More specifically, adult baboons had higher transport NLRs than routine NLRs, whereas juveniles showed no such difference, suggesting that younger animals may experience transport stress differently than older animals. We also found that transport NLR was heritable, whereas routine NLR was not, possibly suggesting that stress responses (as indicated in NLR) have a strong genetic component. Consistent with research in humans and chimpanzees, these findings suggest that NLR varies with important biological and life history variables and that NLR may be a useful health biomarker in baboons., (© 2024 Wiley Periodicals LLC.)

Several primate species have been shown to exhibit age-related changes in cognition, brain, and behavior. However, severe neurodegenerative illnesses, such as Alzheimer's disease (AD), were once thought to be uniquely human. Recently, some chimpanzees naturally were documented to develop both neurofibrillary tangles and amyloid plaques, the main characteristics of AD pathology. In addition, like humans and other primates, chimpanzees show similar declines in cognition and motor function with age. Here, we used voxel-based morphometry to examine the relationships among gray matter volume, age, and cognition using magnetic resonance imaging scans previously acquired from chimpanzees (N = 216). We first determined the relationship between age and gray matter volume, identifying the regions that declined with age. With a subset of our sample (N = 103), we also determined differences in gray matter volume between older chimpanzees with higher cognition scores than expected for their age, and older chimpanzees with lower than expected scores. Finally, we ran a conjunction analysis to determine any overlap in brain regions between these two analyses. We found that as chimpanzees age, they lose gray matter in regions associated with cognition. In addition, cognitively healthy older chimpanzees (those performing better for their age) have greater gray matter volume in many brain regions compared with chimpanzees who underperform for their age. Finally, the conjunction analysis revealed that regions of age-related decline overlap with the regions that differ between cognitively healthy chimpanzees and those who underperform. This study provides further evidence that chimpanzees are an important model for research on the neurobiology of aging. Future studies should investigate the effects of cognitive stimulation on both cognitive performance and brain structure in aging nonhuman primates., (© 2021 Wiley Periodicals LLC.)

Previous studies of aging cynomolgus monkeys from our group identified spontaneous age-associated cognitive declines associated with biomarkers and brain lesions reminiscent of Alzheimer's Disease (AD), in a proportion of aged monkeys. However, the molecular mechanisms that underlie the spontaneous amyloid disorders and cognitive declines observed in these affected monkeys have yet to be investigated in detail. Using reverse transcriptase quantitative real time PCR techniques, normalized to the ACTB housekeeping gene, we analyzed the expression patterns of a number of genes which have been implicated in amyloid and tau abnormalities, in well-characterized aged cynomolgus monkeys with cognitive decline. A significantly increased expression of the genes coding for glyceraldehyde 3-phosphate dehydrogenase (GAPDH), was found in aged-cognitive decline monkeys compared to age-matched healthy controls. GAPDH has been implicated in several neurodegenerative diseases and interacts with beta amyloid precursor proteins. These findings provide support for the utilization of cynomolgus macaques in translational preclinical research as valid spontaneous models in experimental investigations of the relationships among aging, cognitive decline, and the neuropathy of AD., (© 2021 Wiley Periodicals LLC.)

Chimpanzees are the species most closely related to humans, yet age-related changes in brain and cognition remain poorly understood. The lack of studies on age-related changes in cognition in chimpanzees is particularly unfortunate in light of the recent evidence demonstrating that this species naturally develops Alzheimer's disease (AD) neuropathology. Here, we tested 213 young, middle-aged, and elderly captive chimpanzees on the primate cognitive test battery (PCTB), a set of 13 tasks that assess physical and social cognition in nonhuman primates. A subset of these chimpanzees (n = 146) was tested a second time on a portion of the PCTB tasks as a means of evaluating longitudinal changes in cognition. Cross-sectional analyses revealed a significant quadratic association between age and cognition with younger and older chimpanzees performing more poorly than middle-aged individuals. Longitudinal analyses showed that the oldest chimpanzees at the time of the first test showed the greatest decline in cognition, although the effect was mild. The collective data show that chimpanzees, like other nonhuman primates, show age-related decline in cognition. Further investigations into whether the observed cognitive decline is associated with AD pathologies in chimpanzees would be invaluable in understanding the comparative biology of aging and neuropathology in primates., (© 2020 Wiley Periodicals LLC.)

The marginal value theorem is an optimal foraging model that predicts how efficient foragers should respond to both their ecological and social environments when foraging in food patches, and it has strongly influenced hypotheses for primate behavior. Nevertheless, experimental tests of the marginal value theorem have been rare in primates and observational studies have provided conflicting support. As a step towards filling this gap, we test whether the foraging decisions of captive chimpanzees (Pan troglodytes) adhere to the assumptions and qualitative predictions of the marginal value theorem. We presented 12 adult chimpanzees with a two-patch foraging environment consisting of both low-quality (i.e., low-food density) and high-quality (i.e., high-food density) patches and examined the effect of patch quality on their search behavior, foraging duration, marginal capture rate, and its proxy measures: giving-up density and giving-up time. Chimpanzees foraged longer in high-quality patches, as predicted. In contrast to predictions, they did not depress high-quality patches as thoroughly as low-quality patches. Furthermore, since chimpanzees searched in a manner that fell between systematic and random, their intake rates did not decline at a steady rate over time, especially in high-quality patches, violating an assumption of the marginal value theorem. Our study provides evidence that chimpanzees are sensitive to their rate of energy intake and that their foraging durations correlate with patch quality, supporting many assumptions underlying primate foraging and social behavior. However, our results question whether the marginal value theorem is a constructive model of chimpanzee foraging behavior, and we suggest a Bayesian foraging framework (i.e., combining past foraging experiences with current patch sampling information) as a potential alternative. More work is needed to build an understanding of the proximate mechanisms underlying primate foraging decisions, especially in more complex socioecological environments., (© 2020 Wiley Periodicals LLC.)

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., (© 2020 Wiley Periodicals LLC.)

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., (© 2020 Wiley Periodicals, Inc.)

The National Institutes of Health and the Association of Zoos and Aquariums recommend that captive chimpanzees be housed in multi-male, multi-female, age-diverse groups of no less than seven individuals. These recommendations are rooted in the idea that captive chimpanzee groups should be modeled after free-ranging, wild, fission-fusion chimpanzee societies. However, captive chimpanzees do not face the environmental pressures faced by wild chimpanzees, including food scarcity, inter-group competition, and predation. As such, it has been posited that wild, natural conditions may not be the most relevant metric for defining optimal captive chimpanzee group sizes and compositions. Additionally, captive housing poses a set of restrictions on group sizes and compositions, including the need to balance large, multi-male groups with space per animal limitations and intra-group aggression. In the present study, we examined the behavioral effects of group size, within-group age range, and percentage of males in the group. We collected 713 hr of focal animal samples across 120 captive chimpanzees housed in social groups of 4-10 individuals using a 58-behavior ethogram. Chimpanzees housed in groups with a large age range exhibited less inactivity and more locomotion than chimpanzees housed in groups with smaller age ranges. Additionally, chimpanzees in groups of ≥7 with less than half males showed the highest levels of locomotion. Lastly, chimpanzees in groups of ≥7 with at least half males showed the highest levels of affiliation. There were no other significant differences in behavior as a function of these variables or their interactions. These findings lend some support to the existing group size and composition recommendations, providing empirical evidence that there may be certain advantages to housing captive chimpanzees in larger groups with a more diverse age range and/or more males. These results also have practical implications for behavioral management programs across captive settings., (© 2019 Wiley Periodicals, Inc.)

Space per animal, or animal density, and enclosure type are important elements of functionally appropriate captive environments (FACEs) for chimpanzees. The National Institutes of Health (NIH) recommends that captive chimpanzees be maintained in areas of >250 ft 2 /animal. Several studies have investigated chimpanzee behavior in relation to space per animal, but only two studies have examined these variables while attempting to hold environmental complexity constant. Both have found few, if any, significant differences in behavior associated with increased space per animal. The NIH does not provide recommendations pertaining to enclosure type. Although Primadomes™ and corrals are considered acceptable FACE housing, no studies have investigated chimpanzee behavior in relation to these two common types of enclosures. We examined the NIH space per animal recommendation, and the effects of enclosure type, while maintaining similar levels of environmental complexity. We used focal animal observations to record the behavior of 22 chimpanzees in three social groups following within-facility housing transfers. Chimpanzees that were moved from an area with space below the NIH recommendation to the same type of enclosure with space above the recommendation (dome to double dome) exhibited significantly more locomotion and behavioral diversity post-transfer. Chimpanzees that were moved from an area with space below the recommendation to a different type of enclosure with space above the recommendation (dome to corral) exhibited significant increases in foraging and behavioral diversity, and a decrease in rough scratching. Lastly, chimpanzees that were moved from an area above the recommendation to a different enclosure type with space equal to the recommendation (corral to double dome) exhibited an increase in behavioral diversity. These results add to the body of literature that addresses the concept of specific minimum space requirements per chimpanzee, and highlight the need for more empirical investigation of the relationship between space per chimpanzee, behavior, and welfare., (© 2018 Wiley Periodicals, Inc.)

Chimpanzees (Pan troglodytes) demonstrate much cultural diversity in the wild, yet a majority of novel behaviors do not become group-wide traditions. Since many such novel behaviors are introduced by low-ranking individuals, a bias toward copying dominant individuals ("rank-bias") has been proposed as an explanation for their limited diffusion. Previous experimental work showed that chimpanzees (Pan troglodytes) preferentially copy dominant over low-rank models. We investigated whether low ranking individuals may nevertheless successfully seed a beneficial behavior as a tradition if there are no "competing" models. In each of four captive groups, either a single high-rank (HR, n = 2) or a low-rank (LR, n = 2) chimpanzee model was trained on one method of opening a two-action puzzle-box, before demonstrating the trained method in a group context. This was followed by 8 hr of group-wide, open-access to the puzzle-box. Successful manipulations and observers of each manipulation were recorded. Barnard's exact tests showed that individuals in the LR groups used the seeded method as their first-choice option at significantly above chance levels, whereas those in the HR groups did not. Furthermore, individuals in the LR condition used the seeded method on their first attempt significantly more often than those in the HR condition. A network-based diffusion analysis (NBDA) revealed that the best supported statistical models were those in which social transmission occurred only in groups with subordinate models. Finally, we report an innovation by a subordinate individual that built cumulatively on existing methods of opening the puzzle-box and was subsequently copied by a dominant observer. These findings illustrate that chimpanzees are motivated to copy rewarding novel behaviors that are demonstrated by subordinate individuals and that, in some cases, social transmission may be constrained by high-rank demonstrators., (© 2017 Wiley Periodicals, Inc.)

A fundamental characteristic of human language is multimodality. In other words, humans use multiple signaling channels concurrently when communicating with one another. For example, people frequently produce manual gestures while speaking, and the words a person perceives are impacted by visual information. For this study, we hypothesized that similar to the way that humans regularly couple their spoken utterances with gestures and facial expressions, chimpanzees regularly produce vocalizations in conjunction with other communicative signals. To test this hypothesis, data were collected from 101 captive chimpanzees living in mixed-sex social groupings of seven to twelve individuals. A total of 2,869 vocal events were collected. The data indicate that approximately 50% of the vocal events were produced in conjunction with another communicative modality. In addition, approximately 68% were directed to a specific individual, and these directed vocalizations were more likely to include a signal from another communicative modality than were vocalizations that were not directed to a specific individual. These results suggest that, like humans, chimpanzees often pair their vocalizations with signals from other communicative modalities. In addition, chimpanzees appear to use their communicative signals strategically to meet specific socio-communicative ends, providing support for the growing literature that indicates that at least some chimpanzee vocal signaling is intentional., (© 2015 Wiley Periodicals, Inc.)

One effective method for measuring personality in primates is to use personality trait ratings to distill the experience of people familiar with the individual animals. Previous rating instruments were created using either top-down or bottom-up approaches. Top-down approaches, which essentially adapt instruments originally designed for use with another species, can unfortunately lead to the inclusion of traits irrelevant to chimpanzees or fail to include all relevant aspects of chimpanzee personality. Conversely, because bottom-up approaches derive traits specifically for chimpanzees, their unique items may impede comparisons with findings in other studies and other species. To address the limitations of each approach, we developed a new personality rating scale using a combined top-down/bottom-up design. Seventeen raters rated 99 chimpanzees on the new 41-item scale, with all but one item being rated reliably. Principal components analysis, using both varimax and direct oblimin rotations, identified six broad factors. Strong evidence was found for five of the factors (Reactivity/Undependability, Dominance, Openness, Extraversion, and Agreeableness). A sixth factor (Methodical) was offered provisionally until more data are collected. We validated the factors against behavioral data collected independently on the chimpanzees. The five factors demonstrated good evidence for convergent and predictive validity, thereby underscoring the robustness of the factors. Our combined top-down/bottom-up approach provides the most extensive data to date to support the universal existence of these five personality factors in chimpanzees. This framework, which facilitates cross-species comparisons, can also play a vital role in understanding the evolution of personality and can assist with husbandry and welfare efforts., (© 2013 Wiley Periodicals, Inc.)

In captive research environments for nonhuman primates (NHP), social housing strategies are often in conflict with protocols designed to minimize disease transmission. This is particularly true in breeding colonies, and is especially relevant when attempting to eliminate specific pathogens from a population of primates. Numerous strategies have been used to establish such specific pathogen free (SPF) breeding colonies (primarily of macaques), ranging from nursery rearing of neonates to single housing of socially reared yearlings to the rearing of infants in large social groups. All these strategies attempt to balance the effects of the chosen socialization strategy on parameters related to disease transmission, including the ultimate elimination of the target pathogens. Such strategies may affect the overall disease states of NHP breeding colonies through selective breeding processes. This can occur either by creating subpopulations of animals that do not have target diseases (SPF colonies), but may have other issues; or by creating situations in which the "best" animals are sold and the breeding colony is stocked with animals that may be more disease susceptible than those that were sold. The disease states of NHP research colonies also may be affected by selective utilization programs, in which animals removed from the breeding colony for health/behavior reasons, are preferentially chosen for use in scientific investigations. Such utilization criteria raise the question of whether ideal subjects are being chosen for use in research. Finally, captive primate colonies, where both socialization and disease states are intensely managed, may provide opportunities for those testing predictions from models of the interactions of socialization and disease transmission in the evolution of wild populations of NHP. This would be especially true for some extreme conditions of these disease ecology models, given the exceedingly high social densities and levels of pathogen control that exist in many captive nonhuman primate colonies., (© 2011 Wiley Periodicals, Inc.)

Video displays for behavioral research lend themselves particularly well to studies with chimpanzees (Pan troglodytes), as their vision is comparable to humans', yet there has been no formal test of the efficacy of video displays as a form of social information for chimpanzees. To address this, we compared the learning success of chimpanzees shown video footage of a conspecific compared to chimpanzees shown a live conspecific performing the same novel task. Footage of an unfamiliar chimpanzee operating a bidirectional apparatus was presented to 24 chimpanzees (12 males, 12 females), and their responses were compared to those of a further 12 chimpanzees given the same task but with no form of information. Secondly, we also compared the responses of the chimpanzees in the video display condition to responses of eight chimpanzees from a previously published study of ours, in which chimpanzees observed live models. Chimpanzees shown a video display were more successful than those in the control condition and showed comparable success to those that saw a live model. Regarding fine-grained copying (i.e. the direction that the door was pushed), only chimpanzees that observed a live model showed significant matching to the model's methods with their first response. Yet, when all the responses made by the chimpanzees were considered, comparable levels of matching were shown by chimpanzees in both the live and video conditions., (© 2012 Wiley Periodicals, Inc.)

Copulation preferences in our closest living relative, the chimpanzee, suggest that males prefer older females who have had previous offspring. However, this finding is counter to some behavioral models, which predict that chimpanzee males, as promiscuous breeders with minimal costs to mating, should show little or no preference when choosing mating partners (e.g. should mate indiscriminately). To determine if the preferences indicated by copulations appear in other contexts as well as how they interact, we examined how male chimpanzees' grooming patterns varied amongst females. We found that males' preferences were based on interactions among females' fertility status, age, and parity. First, grooming increased with increasing female parity. We further found an effect of the estrous cycle on grooming; when females were at the lowest point of their cycle, males preferentially groomed parous females at peak reproductive age, but during maximal tumescence, males preferred the oldest multiparous females. Nulliparous females received relatively little grooming regardless of age or fertility. Thus, male chimpanzees apparently chose grooming partners based on both female's experience and fertility, possibly indicating a two-pronged social investment strategy. Male selectivity seems to have evolved to effectively distribute costly social resources in a pattern which may increase their overall reproductive success., (© 2011 Wiley-Liss, Inc.)

Understanding the relationship between physical environments and nonhuman primate behavior is a key element for effective care and management in a range of settings. The physical features of the captive environment, including not only gross useable space but also environmental complexity, can have a significant influence on primate behavior and ultimately, animal welfare. But despite this connection, there remains relatively little conclusive data on how captive primates, especially great apes, use the spaces provided to them, especially in modern, indoor-outdoor enclosures that have become more prevalent in recent years. In this study, we used four years of detailed data on where 23 great apes (chimpanzees and gorillas) positioned themselves within a modern, indoor-outdoor zoo enclosure to determine not only how the apes utilized their space but also how access to outdoor areas affected their spatial selectivity. We found that both species used relatively little of their available space: chimpanzees and gorillas spent half their time in only 3.2 and 1.5% of their useable three-dimensional space, respectively. Chimpanzees utilized the outdoor space more than gorillas, but access to the outdoors did not affect space selectivity in the indoor area for either species. Although both species of ape were highly selective in their space use, consideration should be given to the importance of providing the choice to locate in a variety of spaces, including outdoor areas. These data represent an extremely detailed account of space selectivity by great apes in an indoor-outdoor environment and have substantial implications for future facility design and captive primate management., (© 2010 Wiley-Liss, Inc.)

In many facilities, primates are voluntarily transferred between different enclosures on a daily basis to facilitate animal husbandry and exhibit maintenance. This procedure is particularly relevant in the management of great apes living in zoos, where the requirements of functional management must be balanced with the desire to maintain enriching and naturalistic exhibit enclosures that benefit ape residents and attract the visiting public. In these settings, examinations of ape behavior and welfare typically focus exclusively on activity in the primary exhibit area. However, physical, social and sensory experiences unique to each area may shape different patterns of behavior. In the current study, zoo-living chimpanzees and gorillas were moved each day from exhibit areas to off-exhibit holding areas for a short duration as a part of regular management procedures. Behavioral data indicated species-specific reactions to the holding area, including increased aggression and self-directed behavior by chimpanzees and increased activity and prosocial behavior among gorilla subjects. Both species showed more feeding-foraging behavior while in the exhibit enclosure. Results suggest that holding areas may not meet all behavior needs of captive great apes and demonstrate the importance of including all components of the captive enclosure in comprehensive analyses of great ape behavior and welfare., (© 2010 Wiley-Liss, Inc.)

Positive reinforcement training (PRT) techniques have received considerable attention for their stress reduction potential in the behavioral management of captive nonhuman primates. However, few published empirical studies have provided physiological data to support this position. To address this issue, PRT techniques were used to train chimpanzees (Pan troglodytes) to voluntarily present a leg for an intramuscular (IM) injection of anesthetic. Hematology and serum chemistry profiles were collected from healthy chimpanzees (n=128) of both sexes and various ages during their routine annual physical examinations over a 7-year period. Specific variables potentially indicative of acute stress (i.e., total white blood cell (WBC) counts, absolute segmented neutrophils (SEG), glucose (GLU) levels, and hematocrit (HCT) levels) were analyzed to determine whether the method used to administer the anesthetic (voluntary present for injection vs. involuntary injection) affected the physiological parameters. Subjects that voluntarily presented for an anesthetic injection had significantly lower mean total WBC counts, SEG, and GLU levels than subjects that were involuntarily anesthetized by more traditional means. Within-subjects analyses revealed the same pattern of results. This is one of the first data sets to objectively demonstrate that PRT for voluntary presentation of IM injections of anesthetic can significantly affect some of the physiological measures correlated with stress responses to chemical restraint in captive chimpanzees.

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., (Copyright 2005 Wiley-Liss, Inc.)

We assessed the use of nonhuman primates and nonhuman primate biological material in research by reviewing studies published in 2001 in peer-reviewed journals. The number and species of primates used, the origin of the animals, the type of study, the area of research of the investigation, and the location at which the research was performed were tabulated. Additionally, factors related to the animals that may have affected the outcome of the experiments were recorded. A total of 2,937 articles involving 4,411 studies that employed nonhuman primates or nonhuman primate biological material were identified and analyzed. More than 41,000 animals were represented in the studies published in 2001. In the 14% of studies for which re-use could be determined, 69% involved animals that had been used in previous experiments. Published studies most commonly used nonhuman primates or nonhuman primate biological material from the species Chlorocebus aethiops (19%), Macaca mulatta (18%), M. fascicularis (9%), and Papio spp. (6%). Of these studies, 54% were classified as in vitro studies, 14% as noninvasive, 30% as chronic, and 1% were considered acute. Nonhuman primates were primarily used in research areas in which they appear to be the most appropriate models for humans. The most common areas of research were microbiology (including HIV/AIDS (26%)), neuroscience (19%), and biochemistry/chemistry (12%). Most (84%) of the primate research published in 2001 was conducted in North America, Europe, and Japan. The animals and conditions under which they were housed and used were rarely described. Although it is estimated that nonhuman primates account for an extremely small fraction of all animals used in research, their special status makes it important to report the many husbandry and environmental factors that influence the research results generated. This analysis has identified that editors rarely require authors to provide comprehensive information concerning the subjects (e.g., their origin), treatment conditions, and experimental procedures utilized in the studies they publish. The present analysis addresses the use of primates for research, including the effects of a shortage of suitable nonhuman primate subjects in many research areas., (Copyright 2004 Wiley-Liss, Inc.)

Social housing, whether continuous, intermittent, or partial contact, typically provides many captive primates with opportunities to express affiliative behaviors, important components of the species-typical behavioral repertoire. Positive reinforcement training techniques have been successfully employed to shape many behaviors important for achieving primate husbandry goals. The present study was conducted to determine whether positive reinforcement training techniques could also be employed to alter levels of affiliative interactions among group-housed rhesus macaques. Twenty-eight female rhesus were divided into high (n = 14) and low (n = 14) affiliators based on a median split of the amount of time they spent affiliating during the baseline phase of the study. During the subsequent training phase, half of the low affiliators (n = 7) were trained to increase their time spent affiliating, and half of the high affiliators (n = 7) were trained to decrease their time spent affiliating. Trained subjects were observed both during and outside of training sessions. Low affiliators significantly increased the amount of time they spent affiliating, but only during nontraining sessions. High affiliators on the other hand, significantly decreased the amount of time they spent affiliating, but only during training sessions. These data suggest that positive reinforcement techniques can be used to alter the affiliative behavior patterns of group-housed, female rhesus monkeys, although the two subgroups of subjects responded differently to the training process. Low affiliators changed their overall behavioral repertoire, while high affiliators responded to the reinforcement contingencies of training, altering their proximity patterns but not their overall behavior patterns. Thus, positive reinforcement training can be used not only as a means to promote species-typical or beneficial behavior patterns, but also as an important experimental manipulation to facilitate systematic analyses of the effects of psychosocial factors on behavior and potentially even immunology., (Copyright 2001 Wiley-Liss, Inc.)

Certain types of inanimate environmental enrichment have been shown to positively affect the behavior of laboratory primates, as has housing them in appropriate social conditions. While social housing is generally advocated as an important environmental enhancement, few studies have attempted to measure the influence of social conditions on the effects of inanimate enrichment or to compare the relative merits of social and inanimate enhancements. In the present study, inanimate enrichment (predominately physical and feeding enhancements) resulted in increased species-typical behavior for socially restricted subjects. However, social enrichment (living in groups) appeared to be more beneficial for young rhesus monkeys, leading to increased species-typical activities and decreased abnormal activities. The behavior of one cohort of yearling rhesus monkeys (Macaca mulatta) housed in small peer groups was compared with the behavior of four yearling cohorts housed in single cages. Half the animals in each cohort received a three-phase enrichment program and the rest served as controls. Group-housed yearlings spent significantly more time feeding and exploring and significantly less time behaving abnormally, self-grooming, and drinking than did singly housed yearlings. Enriched subjects spent significantly more time playing by themselves, and significantly less time self-grooming and exploring than did controls. Among group-housed subjects only, there were no differences between enriched and control monkeys. Captive primates should be housed socially, whenever appropriate, as the first and most important step in an enrichment program, with the provision of inanimate enhancements being considerably less important. Limited resources for inanimate enrichment programs instead should be focused on those individuals who can not be housed socially. © 1996 Wiley-Liss, Inc., (Copyright © 1996 Wiley‐Liss, Inc.)

Three cohorts of yearling rhesus monkeys (Macaca mulatta) were maintained in single cages for one year as part of a derivation program to produce a breeding colony of specific pathogen-free (SPF) monkeys. During this year of social restriction, subjects were provided with three different types of environmental enrichment (physical, feeding, and sensory) to counteract the known effects of social restriction and to quantify the effects of these different conditions of enhancement on their behavior. Focal animal observations were conducted on enriched and control subjects for all cohorts. Enrichment conditions were presented in a different order to each cohort. Monkeys provided with enrichment spent significantly more time playing and less time self-grooming than did control monkeys in unenriched cages, suggesting that the overall enrichment program was of some benefit to the monkeys, because these changes in behavior were in species-typical directions. Among enriched subjects only, there were significant differences in the amount of time spent drinking, grooming, feeding, playing, exploring, and using enrichment across the three enrichment conditions. Both the physical and feeding enrichment conditions led to species-appropriate changes in behavior, therefore enhancing psychological well-being as some define it. Sensory enrichment was of little benefit. The first cohort was housed indoors, received less stimulation from the environment outside of the single cage, and used enrichment more than did the other two cohorts housed outdoors. This suggests that the external environment influences behavior in the single cage and that enrichment may be most effective for animals housed indoors. © 1995 Wiley-Liss, Inc., (Copyright © 1995 Wiley‐Liss, Inc., A Wiley Company.)

Among captive primates, inanimate environmental enrichment can lead to measurable changes in behavior indicative of an improvement in psychological well-being. Although this has been demonstrated repeatedly for singly caged primates, the relationship is not as well studied for pairhoused animals. Study of the pair-housed setting has become increasingly relevant because of the social housing mandate of the Animal Welfare Act regulations. We therefore observed 68 juvenile rhesus monkeys born in 1988 and 1989 and living in mixed-sex pairs from the ages of 2 to 3 years. All pairs were compatible. Half of the pairs received two types of enrichment, while the remaining pairs served as controls. Enriched and control juvenile subjects differed in the amount of time that they spent being inactive, playing, and drinking, but did not differ in the amount of time they spent interacting with their partner. Grooming and play were the two most common socially directed activities in both groups, a species-appropriate pattern. Males played more and vocalized less than did females. Overall, enriched and control subjects spent equivalent amounts of time located within a social distance of one another, but there was some difference between groups in allocation of behaviors while near the pairmate. Environmental enhancers were frequently utilized, and led to relatively small changes in behavior between control and enriched subjects, suggesting that the presence of a partner for juvenile rhesus monkeys acts as a form of enrichment that may dilute the effects of inanimate environmental enhancements. © 1994 Wiley-Liss, Inc., (Copyright © 1994 Wiley‐Liss, Inc., A Wiley Company.)