Standard growth and diarrhea-associated growth faltering in captive infant rhesus macaques (Macaca mulatta).

Reference growth studies of captive rhesus macaque infants have not accounted for diarrhea and the potential for growth stunting or growth faltering. Healthy infants without diarrhea could be used to build a standard growth chart and a tool used to detect growth faltering associated with diarrhea. We hypothesized infants who develop diarrhea during the first year of life would experience decreased linear weight gain compared to healthy infants, and we used healthy infants to establish standard growth of male and female infants. We hypothesized the lower 3rd percentile of standard growth would be cut-off criteria used in screening for diarrhea-associated growth faltering. Using a retrospective cohort of 6,510 infant weight records in a multiple linear regression, daily weight gain through the first year of life was determined by sex, housing type, and health status. Male standard growth was 4.1 g/day (95%CI: 4.0-4.2 g/day) in corrals and 4.7 g/day (95%CI: 4.5-4.8 g/day) in shelter housing. Female standard growth was 4.0 g/day (95%CI: 3.8-4.2 g/day) in corrals and 4.4 g/day (95%CI: 4.0-4.7 g/day) in shelter housing. Diarrhea was significantly associated with decreased linear weight gain by up to 34% during the first year of life. Odds of growth faltering of infants, defined as those falling below the 3rd percentile of standard growth, were at least 8.9 higher given a history of diarrhea compared to healthy. The growth faltering cut-off criteria had a sensitivity of at least 53% for males and females to screen for diarrhea in infants between 6 and 12 months in shelters housing. Interinstitutional collaborations of infant rhesus macaque weight records would refine the standard growth charts and cut-off criteria, and additional morphometric data would provide a more nuanced picture of growth stunting.

Personality, environmental stressors, and diarrhea in Rhesus macaques: An interactionist perspective.

Previous research has repeatedly shown both personality and psychological stress to predict gastrointestinal disorders and chronic diarrhea in humans. The goal of the present research was to evaluate the role of personality, as well as psychological stressors (i.e., housing relocations and rearing environment), in predicting chronic diarrhea in captive Rhesus macaques, with particular attention to how personality regulated the impact of such stressors. Subjects were 1,930 R. macaques at the California National Primate Research Center reared in a variety of environments. All subjects took part in an extensive personality evaluation at approximately 90-120 days of age. Data were analyzed using generalized linear models to determine how personality, rearing condition, housing relocations, and personality by environment interactions, predicted both diarrhea risk (an animal's risk for having diarrhea at least once) and chronic diarrhea (how many repeated bouts of diarrhea an animal had after their initial bout). Much like the human literature, we found that certain personality types (i.e., nervous, gentle, vigilant, and not confident) were more likely to have chronic diarrhea, and that certain stressful environments (i.e., repeated housing relocations) increased diarrhea risk. We further found multiple interactions between personality and environment, supporting the "interactionist" perspective on personality and health. We conclude that while certain stressful environments increase risk for chronic diarrhea, the relative impact of these stressors is highly dependent on an animal's personality.

Rhesus macaque personality, dominance, behavior, and health.

Previous studies of nonhuman primates have found relationships between health and individual differences in personality, behavior, and social status. However, despite knowing these factors are intercorrelated, many studies focus only on a single measure, for example, rank. Consequently, it is difficult to determine the degree to which these individual differences are independently associated with health. The present study sought to untangle the associations between health and these individual differences in rhesus macaques (Macaca mulatta). We studied 85 socially housed macaques at the Oregon and California National Primate Research Centers, and used veterinary records to determine the number of injuries and illnesses for each macaque. We measured personality using 12 items from a well-established primate personality questionnaire, performed focal observations of behaviors, and calculated dominance status from directional supplant data. All twelve personality questionnaire items were reliable and were used to represent five of the six personality dimensions identified in rhesus macaques-Dominance, Confidence, Openness, Anxiety, and Friendliness (also known as Sociability). Following this, we fit generalized linear mixed effects models to understand how these factors were associated with an animal's history of injury and history of illness. In the models, age was an offset, facility was a random effect, and the five personality dimensions, behavior, sex, and dominance status were fixed effects. Number of injuries and illnesses were each best represented by a negative binomial distribution. For the injury models, including the effects did improve model fit. This model revealed that more confident and more anxious macaques experienced fewer injuries. For the illness models, including the fixed effects did not significantly improve model fit over a model without the fixed effects. Future studies may seek to assess mechanisms underlying these associations.

Social hair pulling in captive rhesus macaques (Macaca mulatta).

Alopecia is common among captive populations of nonhuman primates. There are many potential causes of alopecia, including physiological conditions such as hormonal imbalance and infection, features of the captive environment such as housing type, ground substrate, and group density, as well as behavioral abnormalities such as self-plucking. A potential behavioral cause of alopecia in group-housed primates is social hair pulling, where one animal pulls hair from a conspecific. While social hair pulling has been conflated with overgrooming in some of the alopecia literature, other authors have categorized it as a form of aggression rather than a form of excessive grooming. In this study, we examined social hair pulling, grooming, and aggression within seven groups of rhesus macaques (Macaca mulatta) (N = 319). We took weekly 30-min behavioral observations on each group for one year to assess the patterns of hair pulling and grooming, which monkeys were receiving and initiating these behaviors, as well as aggression and other behaviors indicating dominance. We also assessed the amount of alopecia on each individual monthly. While grooming tended to be directed "up" the hierarchy (i.e., monkeys were more likely to groom animals of a higher rank than lower rank), most hair pulling was directed "down" the hierarchy. Further, hair pulling seldom co-occurred with aggressive behaviors, suggesting that it was not a form of aggression. Hair pulling also usually resulted in ingestion of the pulled hair. Hair pulling was correlated with alopecia; monkeys who were frequent recipients of hair pulling scored higher on monthly alopecia ratings than those who were less often observed having hair pulled. Our results suggest that social hair pulling is a behavior distinct from either grooming or aggressive behavior, and that it may contribute to alopecia in socially housed macaques.

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.

Evaluation of environmental and intrinsic factors that contribute to stereotypic behavior in captive rhesus macaques (Macaca mulatta).

Full body repetitive behaviors, known as motor stereotypic behaviors (MSBs), are one of the most commonly seen abnormal behaviors in captive non-human primates, and are frequently used as a behavioral measure of well-being. The main goal of this paper was to examine the role of environmental factors (i.e., foraging enrichment and socialization) and intrinsic factors (i.e., temperament and origin) in the development of MSB in rhesus macaques living in cages. MSB was assessed during short annual observations in which a trained observer recorded a monkey's behavior for 5 min, followed by a 3-min novel object test. Data were collected over 11 years, totaling 9805 observations. We compared MSB for animals with and without foraging enrichment, and across three socialization conditions: full contact pairing, protected contact socialization (partners physically separated by widely spaced bars), and single housing. In addition, we evaluated whether individual differences in response to a novel object and ancestral origin (i.e., China vs. India), predicted MSB expression during the annual observations. Data were analyzed using generalized mixed effects modeling, with the best fitting models chosen using Akaike Information Criterion. Subjects were at lowest risk for MSB when a foraging device was present (p < 0.05), and when in full contact social housing (p < 0.001). There was no statistically significant difference in MSB between subjects that were single housed and subjects housed in protected contact pairs. In addition, subjects that never touched the novel object were significantly less likely to exhibit MSB than those that touched the object immediately (p < 0.001) or within 3 min (p < 0.001). Finally, monkeys with some degree of Chinese ancestry were significantly more likely to display MSB than Indian-origin monkeys (p < 0.05). These results add to the growing body of literature on factors that can contribute to the development of MSB.

Using porches to decrease feces painting in rhesus macaques (Macaca mulatta).

The goal of this project was to evaluate the efficacy of a porch in decreasing feces painting in captive rhesus macaques. The porch is a small extension that is hung on the outside of a monkey's primary home cage. Porches provide many potential benefits to indoor-housed macaques, including opportunities to perch above the ground, additional space, and increased field of view. Rates of feces painting, an abnormal behavior in which the animal smears or rubs feces on a surface, were compared in 3 situations: with porch enrichment, with 'smear board' enrichment (a foraging device commonly used to decrease feces painting), and without either enrichment item. Feces painting was evaluated daily by using a 5-point scale that ranged from 0, no feces present, to 4, multiple large areas of feces. We found that subjects received significantly lower feces painting scores when given porch enrichment or smear board enrichment compared with baseline. Furthermore, subjects received significantly lower feces painting scores with porch enrichment than smear board enrichment. These results demonstrate that the porch is an effective tool to decrease feces painting in captive macaques.

Risk factors for stereotypic behavior and self-biting in rhesus macaques (Macaca mulatta): animal's history, current environment, and personality.

Captive rhesus macaques sometimes exhibit undesirable abnormal behaviors, such as motor stereotypic behavior (MSB) and self-abuse. Many risk factors for these behaviors have been identified but the list is far from comprehensive, and large individual differences in rate of behavior expression remain. The goal of the current study was to determine which experiences predict expression of MSB and self-biting, and if individual differences in personality can account for additional variation in MSB expression. A risk factor analysis was performed utilizing data from over 4,000 rhesus monkeys at the California National Primate Research Center. Data were analyzed using model selection, with the best fitting models evaluated using Akaike Information Criterion. Results confirmed previous research that males exhibit more MSB and self-biting than females, MSB decreases with age, and indoor reared animals exhibit more MSB and self-biting than outdoor reared animals. Additionally, results indicated that animals exhibited less MSB and self-biting for each year spent outdoors; frequency of room moves and number of projects positively predicted MSB; pair separations positively predicted MSB and self-biting; pair housed animals expressed less MSB than single housed and grate paired animals; and that animals expressed more MSB and self-biting when in bottom rack cages, or cages near the room entrance. Based on these results we recommend limiting exposure to these risk factors when possible. Our results also demonstrated a relationship between personality and MSB expression, with animals low on gentle temperament, active in response to a human intruder, and high on novel object contact expressing more MSB. From these results we propose that an animal's MSB is related to its predisposition for an active personality, with active animals expressing higher rates of MSB.

The Effects of Predictability in Daily Husbandry Routines on Captive Rhesus Macaques (Macaca mulatta).

Rhesus macaques (Macaca mulatta) housed indoors experience many routine husbandry activities on a daily basis. The anticipation of these events can lead to stress, regardless of whether the events themselves are positive or aversive in nature. The specific goal of this study was to identify whether increasing the predictability of husbandry events could decrease stress and anxiety in captive rhesus macaques. This study was conducted on 39 single-housed subjects in four indoor rooms at the Oregon National Primate Research Center. Temporal and signaled predictability were added to four daily husbandry events: morning and afternoon feeding, enrichment distribution, and room cleaning. Temporally predictable husbandry events occurred reliably at the same time daily, while signaled predictable husbandry events were preceded by a distinct event-specific signal in the form of a doorbell. Informal tests prior to study onset found the doorbells not to be aversive to the subjects. Subjects received each of four treatments: unpredictable events, temporally predictable events, signaled predictable events, and temporally and signaled predictable events. Change in stress was evaluated by monitoring changes in motor stereotypies and displacement behaviors. Our results showed that subjects displayed less stress and anticipatory behaviors related to feeding and enrichment events when the events were temporally predictable (P < 0 .0001). When husbandry events were preceded by a reliable signal, subjects vocalized less prior to the event and were less responsive to activity outside of the room (P < 0 .01). However this may have come at a cost as the animals were extremely reactive to the doorbell signals and showed a heightened stress response during the actual husbandry events (P < 0 .01). Similar to temporal predictability alone, when temporal predictability was combined with signaled predictability subjects displayed less stress and anticipatory behaviors related to feeding and enrichment events (P < 0 .0001). In addition, when both forms of predictability were combined subjects showed less stress behaviors while waiting for daily room cleaning (P < 0 .01). When signaled predictability was paired with temporal predictability subjects no longer had the negative response to the doorbell signal, as they were able to predict and anticipate when the events would occur. Because these results are not necessarily applicable to animals that are given control over their environment or housed in a group setting, the management recommendation that can be made from this study is that temporal predictability of feeding reduces stress and anxiety and is thus beneficial to captive indoor single-housed rhesus macaques.

Latent variables affecting behavioral response to the human intruder test in infant rhesus macaques (Macaca mulatta).

The human intruder test is a testing paradigm designed to measure rhesus macaques' behavioral responses to a stressful and threatening situation. In the test, an unfamiliar human positions him/herself in various threatening positions relative to a caged macaque. This paradigm has been utilized for over 20 years to measure a variety of behavioral constructs, including fear and anxiety, behavioral inhibition, emotionality, and aggression. To date, there have been no attempts to evaluate comprehensively the structure of the behavioral responses to the test. Our first goal was to identify the underlying latent factors affecting the different responses among subjects, and our second goal was to determine if rhesus reared in different environments respond differently in this testing paradigm. To accomplish this, we first performed exploratory and confirmatory factor analyses on the behavioral responses of 3- to 4-month-old rhesus macaques, utilizing data from over 2,000 separate tests conducted between 2001-2007. Using the resulting model, we then tested to see whether early rearing experience affected responses in the test. Our first analyses suggested that most of the variation in infant behavioral responses to the human intruder test could be explained by four latent factors: "activity," "emotionality," "aggression," and "displacement." Our second analyses revealed a significant effect of rearing condition for each factor score (P < 0.001); most notable socially reared animals had the lowest activity score (P < 0.001), indoor mother-reared animals had the highest displacement score (P < 0.001), and nursery-reared animals had the highest emotionality (P < 0.001) and lowest aggression scores (P < 0.001). These results demonstrate that this standardized testing paradigm reveals multiple patterns of response, which are influenced by an animal's rearing history.

Efficacy of 3 types of foraging enrichment for rhesus macaques (Macaca mulatta).

Primate facilities provide environmental enrichment to improve animal wellbeing, increase opportunities for expression of species-typical behaviors, and decrease the occurrence of stereotypic behaviors. The current study assessed the efficacy of 3 types of foraging enrichment: puzzle balls, supertubes, and shakers. We assigned 48 rhesus macaques to 3 experimental groups, each of which received (after a 3-wk baseline observation period) 1 of the 3 enrichment devices intermittently for 3 wk. Observations were collected during 10-min sessions by using 1-0 sampling with 15-s intervals (480 h total). Observations were collected at the same 10 specified time points each week during the baseline period and after enrichment. Data were analyzed by using generalized linear mixed-effects modeling under the assumption that the underlying response followed a Poisson distribution. Foraging behavior increased significantly in all 3 groups and remained increased in some groups when enrichment was removed after 43 h. The 3 enrichment devices had different effects on individual expression of stereotypy: supertubes decreased it, shakers increased it, and puzzle balls led to a decrease followed by an increase. We present potential reasons for the changes in stereotypy and postulate a likely balance between the beneficial and negative effects of enrichment in any given environment.

The effects of four nursery rearing strategies on infant behavioral development in rhesus macaques (Macaca mulatta).

Nursery rearing is the single most important risk factor in the development of severe forms of abnormal behavior, such as self-biting, in rhesus macaques. This practice is common in research laboratories and typically involves continuous pair housing of infants without maternal contact. We examined the effects of variation in peer socialization on the behavioral development of rhesus infants by exposing 32 newborn infants to 4 different socialization routines: continuously paired; intermittently paired; continuously paired rotationally (partners rotated within the group once a week); and intermittently paired rotationally. Analyses revealed that infants paired intermittently exhibited 'floating limb' and self-biting behavior at significantly higher frequencies than those reared by using any other strategy. Results also suggested that continuous pairing was most effective in reducing the development of abnormal behaviors (that is, self-bite and floating limb), whereas intermittent pairing significantly reduced partner clinging and geckering. A principal component analysis revealed that floating limb behavior and self-biting are strongly associated. Self-biting began as early as 32 d of age, and a negative binomial regression on data of floating limb and self-biting revealed that early development of floating limb behavior predicts self-biting behavior later in development. Despite the significant effects of rearing strategies on the frequency of abnormal behaviors, we note that animals in all 4 treatment groups developed these traits to some degree. We suspect that the solitary incubator environment may be a trigger for the development of abnormal behaviors.