Corrine K Lutz’s research while affiliated with The National Academies of Sciences, Engineering, and Medicine and other places

Promoting welfare should be a goal of all facilities housing nonhuman primates. However, determining whether that goal has been met can be challenging. One means of measuring primate welfare is by assessing the animal’s behavior. Herein, we review commonly used behavioral indices for measuring welfare. The first is abnormal behavior, which is defined as behavior that differs in kind or degree from natural behavior. Abnormal behavior can indicate past or present adverse experiences, but it is also impacted by intrinsic factors such as species, temperament, age, and sex. Although abnormal behavior may in some way help an animal to cope with its environment, the presence of abnormal behavior is of concern and interventions may be warranted. Low well-being can also be measured by the display of anxiety-related self-directed behaviors such as scratching and yawning, as well as fear-related facial expressions and vocalizations, freezing, and fleeing. The benefit of utilizing normal species-appropriate anxiety behaviors is that, unlike with abnormal behavior, they are ubiquitous and can function as a “warning system,” which allows for earlier identification of environmental deficiencies and intervention. Species normative behaviors that are reflective of positive emotional states can be used to identify animals experiencing positive welfare, but determining appropriate levels of these behaviors in captivity can be challenging. Regardless of the behaviors being assessed, an understanding of the species’ behavioral repertoire is critical when using behavior as a measure of welfare. When accurately assessed, an animal’s behavior, whether normal or abnormal, can be utilized as an indicator of well-being in nonhuman primates.

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.

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.

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.

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.

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.

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.

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 x sex interaction for abnormal appetitive behavior (b =-2.379, p<0.01) and a genus x 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.

Behavioral assessment is an essential element of chimpanzee care. Behavioral data were compiled from four chimpanzee laboratory facilities (N=522; 286 females, 236 males) using differing methods of assessment including quantitative data collection, animal records and observations by behavioral management staff. The subjects were 46.4% mother-reared (MR), 46.9% non-mother-reared (NONMR), and 6.7% wild-born (WB). Mean group size was 5.9, 100% had access to outdoor space all year, and 59.2% had daily access to natural substrate. Species-typical behaviors were surveyed: 95.4% used tools to acquire food; 50% built nests; 94.4% initiated grooming; and 68% copulated. Forty-two percent showed abnormal behavior; most commonly stereotypic rocking and coprophagy. Ninety-seven percent generally voluntarily cooperate with requests to shift and 64.2% present for an injection. Chi-square analyses (df = 2) revealed MR chimpanzees were more likely than NONMR to use tools (Chi-square = 16.73, p < .001) and to initiate grooming (Chi-square = 22.59, p < .001). WB were more likely to build nests than MR and MR more likely than NONMR (Chi-square = 82.25, p < .001). MR and WB were more likely than NONMR to copulate (Chi-square = 30.43, p < .001). MR were more likely than NONMR to display coprophagy (Chi-square = 11.74, p = .003). This analysis will help guide future improvements in behavioral management to address existing behavioral problems or deficits.