Nonhuman primate abnormal behavior: Etiology, assessment, and treatment.

Across captive settings, nonhuman primates may develop an array of abnormal behaviors including stereotypic and self-injurious behavior. Abnormal behavior can indicate a state of poor welfare, since it is often associated with a suboptimal environment. However, this may not always be the case as some behaviors can develop independently of any psychological distress, be triggered in environments known to promote welfare, and be part of an animal's coping mechanism. Furthermore, not all animals develop abnormal behavior, which has led researchers to assess risk factors that differentiate individuals in the display of these behaviors. Intrinsic risk factors that have been identified include the animal's species and genetics, age, sex, temperament, and clinical condition, while environmental risk factors include variables such as the animal's rearing, housing condition, husbandry procedures, and research experiences. To identify specific triggers and at-risk animals, the expression of abnormal behavior in captive nonhuman primates should be routinely addressed in a consistent manner by appropriately trained staff. Which behaviors to assess, what assessment methods to use, which primates to monitor, and the aims of data collection should all be identified before proceeding to an intervention and/or treatment. This article provides guidance for this process, by presenting an overview of known triggers and risk factors that should be considered, steps to design a comprehensive evaluation plan, and strategies that might be used for prevention or treatment. It also outlines the tools and processes for assessing and evaluating behavior in an appendix. This process will lead to a better understanding of abnormal behavior in captive primate colonies and ultimately to improved welfare.

Hair cortisol in captive corral-housed baboons.

Hair cortisol concentrations (HCCs) are measures of long-term hypothalamic-pituitary-adrenocortical (HPA) activity and can be used as indicators of chronic stress. However, intrinsic factors such as an animal's age and sex can also have an impact on resulting HCCs. Although baboons are commonly studied in captivity, little is known about baseline HCC in this population. Here we measured HCC in two same-sex groups of captive olive (Papio hamadryas anubis) baboons and olive/yellow baboon (Papio hamadryas cynocephalus) crosses housed in large outdoor corrals, and we assessed the impact of age and sex on HCC as major variables of interest. Hair was gently shaved from the back of the neck when the animals were sedated for routine physicals. Subjects were divided into three age categories: juvenile (2-4 years), adult (9-12 years), and senior (13-19 years). The "senior" category contained only males. Results confirm an effect of sex and age on HCCs. Females had higher levels of hair cortisol than males, and juveniles had higher levels than adults. There was also a significant sex × age interaction. There were no sex differences in HCCs in juveniles, but there was a greater decline in HCCs in adult males than in adult females. Within males, there was a significant difference in levels of hair cortisol across the three age categories. Juveniles had higher levels than did adults and seniors, but adults and seniors were not significantly different from one another. These results provide baseline measures of hair cortisol in captive baboons and demonstrate effects of sex and age on HCCs.

Alopecia in rhesus macaques (Macaca mulatta): Association with pregnancy and chronic stress.

BACKGROUND: Alopecia in captive non-human primates is often presented as a welfare issue. However, it is a complex condition with a number of possible causes. The purpose of this study was to assess the impact of pregnancy and hair cortisol concentrations on alopecia in rhesus macaques. METHODS: Subjects were 113 socially housed adult female rhesus macaques (27 pregnant, 35 nursing infants, 51 controls). During routine physicals, photographs were taken for alopecia assessment and hair samples were collected for cortisol assay. RESULTS: Alopecia was more prevalent in pregnant than in control females, but there was no association between alopecia and hair cortisol. However, there was a significant effect of pregnancy on hair cortisol. Nursing females had higher hair cortisol levels than pregnant females, which had higher levels than control females. CONCLUSIONS: Although alopecia does not appear to be associated with hair cortisol, both alopecia and hair cortisol were associated with pregnancy.

A cross-species comparison of abnormal behavior in three species of singly-housed old world monkeys.

Abnormal behavior occurs in a number of captive nonhuman primate species and is often used as an indicator of welfare. However, reported levels of abnormal behavior often vary across species, making general welfare judgments difficult. The purpose of this study was to assess differences in levels of abnormal behavior and associated risk factors across three species of Old World monkeys in order to identify similarities and differences across species. The subjects were 415 (109 females) cynomolgus macaques (Macaca fascicularis), 365 (181 females) rhesus macaques (Macaca mulatta), and 331 (187 females) baboons (Papio hamadryas) that had been singly-housed for 30-120 days. A 5-min observation using one-zero sampling recorded the presence or absence of abnormal behavior for each animal. Macaques exhibited higher levels of abnormal behavior than baboons (29% vs. 14%; χ2(1) = 24.849, p < 0.001), but there was no difference between macaque species (30% vs. 28%; χ2(1) = 0.263, p = 0.608). Risk factors also varied. Overall, males exhibited greater levels of motor stereotypies (b = 0.425, p < 0.05), females greater levels of abnormal appetitive behavior (b = 1.703, p < 0.05), and older animals greater levels of self-directed behavior (b = 0.065, p < 0.05). However, macaques exhibited greater levels of motor stereotypy (b = 2.527, p < 0.001) and self-directed behavior (b = 2.968, p < 0.005) than did baboons. There was also a genus × sex interaction for abnormal appetitive behavior (b = -2.379, p < 0.01) and a genus × age interaction for motor stereotypy (b = -0.167, p < 0.05). These results demonstrate that differences in abnormal behavior exist across closely-related primate species. Therefore, a single species cannot be used generally as a model for abnormal behavior or animal welfare.

Assessing significant (>30%) alopecia as a possible biomarker for stress in captive rhesus monkeys (Macaca mulatta).

Hair loss is common in macaque colonies. Very little is known about the relationship between psychological stress and hair loss. We initially examined alopecia and hair cortisol concentrations in 198 (89 male) rhesus macaques from three primate centers and demonstrated replicability of our previous finding that extensive alopecia (>30% hair loss) is associated with increased chronic cortisol concentrations and significantly affected by facility. A subset of these monkeys (142 of which 67 were males) were sampled twice approximately 8 months apart allowing us to examine the hypotheses that gaining hair should be associated with decreases in cortisol concentrations and vice versa. Hair loss was digitally scored using ImageJ software for the first sample. Then visual assessment was used to examine the second sample, resulting in three categories of coat condition: (i) monkeys that remained fully haired; (ii) monkeys that remained alopecic (with more than 30% hair loss); or (iii) monkeys that showed more than a 15% increase in hair. The sample size for the group that lost hair was too small to be analyzed. Consistent with our hypothesis, monkeys that gained hair showed a significant reduction in hair cortisol concentrations but this effect only held for females. Coat condition changed little across sampling periods with only 25 (11 male) monkeys showing a greater than 15% gain of hair. Twenty (7 male) monkeys remained alopecic, whereas 97 (49 males) remained fully haired. Hair cortisol was highly correlated across samples for the monkeys that retained their status (remained alopecic or retained their hair). Am. J. Primatol. 79:e22547, 2017. © 2016 Wiley Periodicals, Inc.

The correlation between alopecia and temperament in rhesus macaques (Macaca mulatta) at four primate facilities.

Alopecia is a ubiquitous, multifaceted problem at facilities caring for captive rhesus macaques. There is a wide range of potential etiologies for the hair loss, including compromised immune function, dermatological pathologies, and environmental factors. However, few studies have examined whether various temperamental traits affect vulnerability to develop alopecia. We examined the correlation between alopecia and temperament in 101 (51M) indoor-housed rhesus macaques at four national primate centers. We utilized a cage side version of the Human Intruder test (HIT) to assess response to four conditions: no human present (Alone), human intruder standing next to the cage without making eye contact (Profile), intruder making direct eye contact (Stare) and intruder with back turned (Back). Behavior from all videos was quantified at one facility. We used generalized linear modeling to examine the relationship between behavior on the HIT and alopecia, controlling for facility, age, and sex. There was a significant negative correlation between alopecia and various behaviors associated with an inhibited or anxious temperament, including self-directed behavior (ß = -0.15, P < 0.001) and freeze in the Profile period (ß = -0.0092, P < 0.001), and defensive behaviors (ß = -0.0094, P < 0.001) and time spent in the back of the cage in the Stare period (ß = -0.0023, P = 0.015). Individuals with an inhibited or anxious temperament had less alopecia than others. Further, there were facility differences with respect to several variables on the HIT, including defensive behavior in Stare and freeze in Profile. These results suggest that temperament can influence the development of alopecia in rhesus macaques. Our results also highlight the degree to which facility differences can affect outcomes on standardized behavioral tests. Am. J. Primatol. 79:e22504, 2017. © 2015 Wiley Periodicals, Inc.

Responses to the Human Intruder Test are related to hair cortisol phenotype and sex in rhesus macaques (Macaca mulatta).

Measurement of cortisol in hair provides a chronic index of hypothalamic-pituitary-adrenal (HPA) axis activity and has been applied to assessments of temperament (stable behavioral differences between individuals). However, the extent to which chronically high HPA axis activity relates to a correspondingly high degree of behavioral reactivity is as yet unknown. Therefore, the goal of the present experiment was to assess the relationship between hair cortisol and a reactive temperament. We administered the Human Intruder Test (HIT) twice to 145 (80 male) rhesus macaques (Macaca mulatta) in order to assess behavioral reactivity. The HIT presents monkeys with an unfamiliar experimenter and is composed of a Baseline phase (no intruder) followed by three experimental phases in which the orientation of the intruder changes (Profile, Stare, Back). Behavioral responses to the test were videotaped and behaviors thought to reflect a reactive response to the intruder were scored for duration. Hair samples collected within ±1 month of the first HIT session were analyzed for cortisol by enzyme immunoassay. Subjects were assigned to three groups based on hair cortisol concentration: high, intermediate, and low cortisol phenotypes. Monkeys with the high cortisol phenotype were more reactive to the presence of the intruder than those with the low cortisol phenotype: they were more aggressive, scratched more, and spent more time in the back half of the cage. Males yawned significantly more while females spent more time immobile and in the back of the cage. Overall, monkeys with higher hair cortisol demonstrated an exaggerated response to the presence of the human intruder, supporting a relationship between high levels of chronic HPA axis activity and a reactive temperament. These results indicate that high levels of HPA axis activity, which may result from either genetic variation or environmental stress, correspond with heightened behavioral responses to a stressful experience. Am. J. Primatol. 79:e22526, 2017. © 2016 Wiley Periodicals, Inc.

Factors influencing alopecia and hair cortisol in rhesus macaques (Macaca mulatta).

BACKGROUND: Alopecia can occur in captive non-human primates, but its etiology is poorly understood. The purpose of this study was to assess alopecia and hair cortisol in rhesus monkeys and to identify the potential risk factors. METHODS: Subjects were 117 rhesus monkeys at two National Primate Research Centers. Photographs and hair samples were obtained during routine physicals. Photographs were analyzed using Image J software to calculate hair loss, and hair samples were assayed for cortisol. RESULTS: Age, days singly housed, and their interactions contributed to the alopecia model for both facilities. Sex and location changes contributed to the hair cortisol model for Facility 1; sedations contributed for Facility 2. Alopecia and hair cortisol were associated at Facility 1. CONCLUSIONS: Captive management practices can affect alopecia and hair cortisol. However, there are facility differences in the relationship between alopecia and hair cortisol and in the effect of intrinsic variables and management procedures.

Abnormal behavior and associated risk factors in captive baboons (Papio hamadryas spp.).

Abnormal behavior, ranging from motor stereotypies to self-injurious behavior, has been documented in captive nonhuman primates, with risk factors including nursery rearing, single housing, and veterinary procedures. Much of this research has focused on macaque monkeys; less is known about the extent of and risk factors for abnormal behavior in baboons. Because abnormal behavior can be indicative of poor welfare, either past or present, the purpose of this study was to survey the presence of abnormal behavior in captive baboons and to identify potential risk factors for these behaviors with an aim of prevention. Subjects were 144 baboons (119 females, 25 males) aged 3-29 (median = 9.18) years temporarily singly housed for research or clinical reasons. A 15-min focal observation was conducted on each subject using the Noldus Observer® program. Abnormal behavior was observed in 26% of the subjects, with motor stereotypy (e.g., pace, rock, swing) being the most common. Motor stereotypy was negatively associated with age when first singly housed (P < 0.005) while self-directed behavior (e.g., hair pull, self-bite) was positively associated with the lifetime number of days singly housed (P < 0.05) and the average number of blood draws per year (P < 0.05). In addition, abnormal appetitive behavior was associated with being male (P < 0.05). Although the baboons in this study exhibited relatively low levels of abnormal behavior, the risk factors for these behaviors (e.g., social restriction, routine veterinary procedures, and sex) appear to remain consistent across primate species.

Effect of Pregnancy and Age on Alopecia in Adult Female Baboons (Papio hamadryas spp).

Alopecia occurs frequently in captive populations of nonhuman primates. Because multiple factors can play a role in alopecia, a better understanding of its etiology will help identify potential welfare concerns. The purpose of this study was to investigate risk factors for alopecia in a breeding colony of baboons with a focus on pregnancy and age. Alopecia was scored on a scale of 0 (no alopecia) to 5 (severe alopecia) in 253 female baboons during routine physicals. The subjects ranged in age from 4 to 23 y (Mean = 9.6) and were categorized as pregnant (n = 83), nursing (n = 60) or control (n = 110). Resulting alopecia scores were combined into 2 categories (mild = 0 or 1; moderate = 2 or 3); no animals scored a 4 or 5. Significantly more pregnant females had moderate alopecia than did control females. There was no effect of age on alopecia. An unexpected outcome was that among nursing females, more of those with female infants had moderate alopecia than did those with male infants. The impact of the infant's sex on alopecia may be due to sex differences in maternal contact or maternal investment. This information adds to our understanding of alopecia risk factors in captive nonhuman primates.

The Influence of Observer Presence on Baboon (Papio spp.) and Rhesus Macaque (Macaca mulatta) Behavior.

A common method for collecting behavioral data is through direct observations. However, there is very little information available on how a human observer affects the behavior of the animals being observed. This study assesses the effects of a human observer on the behavior of captive nonhuman primates. The subjects were 19 singly housed baboons (nine male, 10 female) and 20 singly housed rhesus macaques (10 male, 10 female) that were not habituated to the presence of an observer. Four 30-min observations were conducted on each animal. Two observations were conducted with an observer present ("present" condition), while the remaining two observations had no observer present ("absent" condition). All observations were recorded with a video camera and were balanced for time of day, with one of each type of observation taking place in the morning and afternoon. In the presence of an observer, appetitive behavior was significantly reduced in both species [F(1,35) = 8.22, P < 0.01]. When an observer was present, females of both species also rested more and performed fewer manipulative behaviors than males [rest: F(1,35) = 7.10, P < 0.05; manipulative: F(1,35) = 6.66, P < 0.05]. Likewise, macaques rested significantly more [F(1,35) = 11.62, P < 0.005] and exhibited fewer manipulative behaviors in the presence of an observer [F(1,35) = 11.06, P < 0.005], while baboons showed no change. Female macaques showed the greatest decrease in activity while an observer was present [F(1,35) = 4.22, P <0.05]. Based on these results, the presence of a human observer does appear to affect the behavior of unhabituated, singly housed baboons and macaques, but the effect differs by both sex and species.

Survey of Behavioral Indices of Welfare in Research Chimpanzees (Pan troglodytes) in the United States.

Chimpanzees demand specialized housing and care and the highest degree of attention to animal welfare. The current project used a survey method to collate information on chimpanzee housing and behavioral indices of welfare across all 6 of the chimpanzee research facilities in the United States. Data were compiled on 701 chimpanzees ranging from 2 to 62 y old (mean age, 26.0 y). All chimpanzees except for one were socially housed; the median group size was 7 animals, and group sizes ranged from 1 to 14. All of the subjects had access to outdoor spaces each day. Daily access to a natural substrate in the chimpanzee's enclosure was available for 63.8% of the subjects. Overall, 94.1% of the chimpanzees used tools to acquire food, 48.1% built nests, 75.8% copulated, and 83.3% initiated grooming bouts. The following atypical behaviors were reported most often: rocking (13.0%), coprophagy (10.0%), and stereotyped behaviors other than rocking (9.4%). There was widespread evi- dence of positive animal training techniques, with nearly all (97.7%) subjects reported to generally voluntarily cooperate with shifting in their enclosure, and 72.2% were reported to present for an injection of anesthetic. We include some comparison between these findings and data describing zoo-housed chimpanzees. In addition, we discuss survey findings in reference to recommendations made by the NIH Working Group on the Use of Chimpanzees in NIH-supported Research. The current survey assessed a larger sample of chimpanzees living under human care than has been published previously. This broad analysis can help to guide future improvements in behavioral management to address behavioral problems or deficits.

Porches as Enrichment for Singly Housed Cynomolgus Macaques (Macaca fascicularis).

Effective environmental enrichment is used by animals, promotes species-typical behavior, and decreases abnormal behavior. Porches attached to the front of an animal's cage provide additional space, perching opportunities, and a better view of the surroundings. Here we assessed the effectiveness of porches as a form of enrichment and identified characteristics of the animals most likely to use the porches. We videorecorded and scored the behavior of 18 (9 male, 9 female) singly housed cynomolgus macaques (Macaca fascicularis) during 3 observation intervals (15 min each) the week before, during, and after exposure to the porches. Changes in abnormal and tension-related behaviors (pacing, yawning, scratching) and speciestypical behaviors were compared across the 3 wk of observation. Novel object temperament tests were performed before and after the study. During observation periods, subjects spent an average of 75% of time in the porch. No changes in pacing or tension-related behaviors occurred, but activity decreased during and after porch exposure, rest increased during the porch exposure, and consumption decreased afterward. Eight subjects were categorized as having a bold temperament, and the remaining 10 subjects had an intermediate temperament. Sex and a temperament×cage location interaction were predictors of porch usage. Males used the porches more than did females, and those with an intermediate temperament were less likely to use the porches when they were located in the lower cages. Porches are beneficial in that they are used for extensive periods of time, but the benefits can vary according to the individual animal.

The physiology and neurochemistry of self-injurious behavior: a nonhuman primate model.

Self-injurious behavior (SIB) is a serious behavioral condition that afflicts millions of individuals in the United States alone. The underlying factors contributing to the development of self-injury in people are poorly understood, and existing treatment strategies for this condition are limited. A low but persistent percentage of socially reared individually housed rhesus monkeys also spontaneously develop SIB. Data obtained from colony records suggest that the risk of developing SIB in socially reared rhesus monkeys is heightened by adverse early experience and subsequent stress exposure. The present review summarizes the physiological and neurochemical findings obtained in this nonhuman primate model of SIB, focusing on monoamine neurotransmitters, neuropeptides, and neuroendocrine systems. The results indicate that monkeys with SIB exhibit long-lasting disturbances in central and peripheral opioid and stress response systems, which lead to increased levels of anxiety. Based on these findings, we propose an integrated developmental-neurochemical hypothesis in which SIB arises from adverse life events in a subset of vulnerable monkeys, is maintained by a persisting dysregulation of several neurochemical and physiological systems, and functions to periodically reduce anxiety when the levels of anxiety become excessive. Implications of this hypothesis for understanding self-injury in patients with borderline personality disorder and members of the general population are discussed.

Environmental enrichment for nonhuman primates: theory and application.

Investigators have an obligation to promote the psychological well-being of nonhuman primates used in research. Considerable emphasis has been placed on providing nonhuman primates with enriched environments as a means to achieve this objective. A framework is provided that consists of a set of hypotheses about well-being, and the extent to which exposure to various enrichment devices and procedures actually promotes well-being is evaluated. Two hypotheses are concerned with fostering species-typical behavior: use (versus nonuse) of the enrichment, and whether use of enrichment helps normalize other aspects of the behavioral repertoire. Two additional hypotheses are concerned with abnormal behavior: whether currently existing enrichment lowers levels of abnormal behavior, and whether it prevents the behavior. This framework is applied to various enrichment strategies ranging from toys and foraging devices to social interaction. Most devices are used by nonhuman primates and thus constitute an important way to enrich the captive environment. However, enrichment devices vary as to their effectiveness in normalizing the behavioral repertoire and eliminating abnormal behavior. Only social contact satisfies the goal of promoting a wide variety of species-typical activities while at the same time reducing or preventing the development of abnormal behavior.

Alopecia in Outdoor Group- and Corral-Housed Baboons (Papio hamadryas spp.).

Alopecia has been reported to occur in several species of captive NHP. Much of this research has focused on macaque monkeys; whether other primate species such as baboons are affected similarly is unknown. Because alopecia can be a focus of inspectors and a possible marker of wellbeing, the purpose of the current study was to survey the occurrence of alopecia in 2 baboon populations and to identify potential risk factors. Subjects were 262 group-housed and 279 corral-housed baboons. Alopecia was assessed cage-side (group-housed) and on sedated animals (corral-housed). Although alopecia was mild in both populations, there were significant effects of season and sex. Alopecia was greater in the winter (group-housed) and the fall (corral-housed) and in female baboons. In addition, the group-housed baboons showed a significant negative effect of age and a lesser effect of group size on alopecia. These results demonstrate that variables other than those associated with animal management practices can affect hair loss in baboons.

The Effect of a Feeding Schedule Change and the Provision of Forage Material on Hair Eating in a Group of Captive Baboons (Papio hamadryas sp.).

Hair eating in nonhuman primates is thought to result from a frustrated appetitive drive produced by an inappropriate diet. To investigate whether hair eating could be reduced through changes in diet, a 2-part study was conducted with a group of baboons (Papio hamadryas sp.). The 1st part involved changing to a twice-daily feeding routine, thus providing prolonged access to an appropriate food source. The 2nd part involved scattering a grain mix to encourage more foraging while maintaining a once-daily feeding routine. Changing the feeding routine unexpectedly resulted in a significant increase in hair manipulation and ingestion. Providing additional grain did not significantly decrease hair manipulation and ingestion, but several individuals did show a reduction in these behaviors. Prolonged access to biscuits and the provision of a grain mix may have failed to satisfy the urge to forage because little effort was needed for their collection prior to consumption. Although the current study failed to significantly decrease hair eating, it provides valuable insight into further avenues of research on the behavior.

Self-injurious behavior in male rhesus macaques does not reflect externally directed aggression.

Self-injurious behaviors (SIB), such as self-biting and self-wounding, have been observed in a small percentage of captive nonhuman primates. Because rhesus monkeys that exhibit SIB also tend to be more aggressive, it was hypothesized that SIB is related to externally directed aggression and is associated with contexts in which physical contact between participants is prevented. The purpose of this study was to test the hypothesized relationship between SIB and outward aggression. Subjects were first presented with videotapes of conspecifics, scenery and a blank screen, and their behavior was recorded. Levels of salivary cortisol, an indicator of stress, were also measured before and after presentation of the videos. Although aggression increased when subjects viewed tapes containing conspecifics, neither cortisol levels nor self-biting behavior varied as a function of tape content. The subjects were then placed in two additional test situations: an empty room and the same room containing an unfamiliar conspecific. Aggression was significantly higher in the stranger condition compared to the empty room condition. The two situations yielded parallel increases in cortisol, suggesting that being alone was just as stressful as being paired with an unfamiliar conspecific. Self-biting rates were also similar in these two conditions. Thus, contrary to our prediction, increases in aggression did not correlate with increases in SIB. These results suggest that under similarly stressful conditions, SIB and externally directed aggression are unrelated.

Stereotypic behavior in nonhuman primates as a model for the human condition.

Stereotypies that develop spontaneously in nonhuman primates can provide an effective model for repetitive stereotyped behavior in people with neurodevelopmental or obsessive-compulsive disorders. The behaviors are similar in form, are similarly affected by environmental conditions, and are improved with similar treatment methods such as enrichment, training, and drug therapy. However, because of a greater number of commonalities in these factors, nonhuman primates may serve as a better model for stereotyped behavior in individuals with autism or intellectual disability than for compulsions in individuals with obsessive-compulsive disorder. Because animal models may not be exact in all features of the disorder being studied, it is important to investigate the strengths and weaknesses of using a nonhuman primate model for stereotyped behavior in people with psychological disorders.