Early-in-life isoflurane exposure alters resting-state functional connectivity in juvenile non-human primates.

BACKGROUND: Clinical studies suggest that anaesthesia exposure early in life affects neurobehavioural development. We designed a non-human primate (NHP) study to evaluate cognitive, behavioural, and brain functional and structural alterations after isoflurane exposure during infancy. These NHPs displayed decreased close social behaviour and increased astrogliosis in specific brain regions, most notably in the amygdala. Here we hypothesise that resting-state functional connectivity MRI can detect alterations in connectivity of brain areas that relate to these social behaviours and astrogliosis. METHODS: Imaging was performed in 2-yr-old NHPs under light anaesthesia, after early-in-life (postnatal days 6-12) exposure to 5 h of isoflurane either one or three times, or to room air. Brain images were segmented into 82 regions of interest; the amygdala and the posterior cingulate cortex were chosen for a seed-based resting-state functional connectivity MRI analysis. RESULTS: We found differences between groups in resting-state functional connectivity of the amygdala and the auditory cortices, medial premotor cortex, and posterior cingulate cortex. There were also alterations in resting-state functional connectivity between the posterior cingulate cortex and secondary auditory, polar prefrontal, and temporal cortices, and the anterior insula. Relationships were identified between resting-state functional connectivity alterations and the decrease in close social behaviour and increased astrogliosis. CONCLUSIONS: Early-in-life anaesthesia exposure in NHPs is associated with resting-state functional connectivity alterations of the amygdala and the posterior cingulate cortex with other brain regions, evident at the juvenile age of 2 yr. These changes in resting-state functional connectivity correlate with the decrease in close social behaviour and increased astrogliosis. Using resting-state functional connectivity MRI to study the neuronal underpinnings of early-in-life anaesthesia-induced behavioural alterations could facilitate development of a biomarker for anaesthesia-induced developmental neurotoxicity.

OpenMonkeyChallenge: Dataset and Benchmark Challenges for Pose Estimation of Non-human Primates.

The ability to automatically estimate the pose of non-human primates as they move through the world is important for several subfields in biology and biomedicine. Inspired by the recent success of computer vision models enabled by benchmark challenges (e.g., object detection), we propose a new benchmark challenge called OpenMonkeyChallenge that facilitates collective community efforts through an annual competition to build generalizable non-human primate pose estimation models. To host the benchmark challenge, we provide a new public dataset consisting of 111,529 annotated (17 body landmarks) photographs of non-human primates in naturalistic contexts obtained from various sources including the Internet, three National Primate Research Centers, and the Minnesota Zoo. Such annotated datasets will be used for the training and testing datasets to develop generalizable models with standardized evaluation metrics. We demonstrate the effectiveness of our dataset quantitatively by comparing it with existing datasets based on seven state-of-the-art pose estimation models.

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.

Improving transparency-A call to include social housing information in biomedical research articles involving nonhuman primates.

The social setting of animal subjects in the research environment has known effects on a variety of dependent measures used in biomedical research. Proper evaluation of the robustness of published research is dependent upon transparent, detailed, and accurate reporting of research methods, including the animals' social housing conditions. However, to date, most research articles utilizing nonhuman primates (NHPs) provide only partial data on this topic, hampering transparency, and reproducibility. Therefore, we call for the inclusion of information pertaining to the social aspects of the animals' housing conditions in publications involving NHPs to improve transparency. We argue that including this information in scientific publications is crucial for the interpretation of research findings in the appropriate context and for understanding unexplained variability in study findings. Finally, the inclusion of this information in publications will additionally familiarize scientists with how other researchers conducting similar studies are housing their animals and will encourage them to consider the implications of various housing conditions on their research outcomes.

Infant isoflurane exposure affects social behaviours, but does not impair specific cognitive domains in juvenile non-human primates.

BACKGROUND: Clinical studies show that children exposed to anaesthetics for short times at young age perform normally on intelligence tests, but display altered social behaviours. In non-human primates (NHPs), infant anaesthesia exposure for several hours causes neurobehavioural impairments, including delayed motor reflex development and increased anxiety-related behaviours assessed by provoked response testing. However, the effects of anaesthesia on spontaneous social behaviours in juvenile NHPs have not been investigated. We hypothesised that multiple, but not single, 5 h isoflurane exposures in infant NHPs are associated with impairments in specific cognitive domains and altered social behaviours at juvenile age. METHODS: Eight Rhesus macaques per group were anaesthetised for 5 h using isoflurane one (1×) or three (3×) times between postnatal days 6 and 12 or were exposed to room air (control). Cognitive testing, behavioural assessments in the home environment, and provoked response testing were performed during the first 2 yr of life. RESULTS: The cognitive functions tested did not differ amongst groups. However, compared to controls, NHPs in the 3× group showed less close social behaviour (P=0.016), and NHPs in the 1× group displayed increased anxiety-related behaviours (P=0.038) and were more inhibited towards novel objects (P<0.001). CONCLUSIONS: 5 h exposures of NHPs to isoflurane during infancy are associated with decreased close social behaviour after multiple exposures and more anxiety-related behaviours and increased behavioural inhibition after single exposure, but they do not affect the cognitive domains tested. Our findings are consistent with behavioural alterations in social settings reported in clinical studies, which may guide future research.

Behavioral predictors of pairing success in rhesus macaques (Macaca mulatta).

Pair housing is one of the most important components of behavioral management for caged macaques; however, it can result in aggression and injury if partners are incompatible. Knowing when to proceed and when to stop social introductions can be challenging, and can have consequences for the partners. We examined whether behavior early in social introductions predicted success (i.e., partners remained cohoused with full contact for at least 28 days) in 724 female-female and 477 male-male rhesus macaque pairs. We took cage side one-zero focal observations on pairs during the first 2 days of full contact, recording social and aggressive behaviors. The majority of pairs (79.6% of female and 83.0% of male) were successful. The most common behaviors exhibited by pairs during these observations were maintaining proximity, tandem threats, and anxiety. Mounting was also relatively common in male pairs. Grooming and close social contact (e.g., touching) were not common in our study. Several behaviors observed on Day 1 significantly predicted pairing success. For females, these included proximity, tandem threat, rump present, mount, and groom. Day 1 predictors of success for male pairs included proximity, tandem threat, rump present, mount, and social contact. Fewer behaviors predicted success on Day 2. Maintaining proximity on Day 2 predicted success for both sexes, but tandem threat predicted success only for females. Behaviors that predicted incompatibility for females on Day 1 included displace, grimace, threat, bite, and other aggressive contacts. Day 1 predictors of separation for male pairs were displaced, grimace, and abnormal behavior. The only Day 2 behavior that correlated with incompatibility was grimace, which was predictive for males. Interestingly, aggression did not predict incompatibility for male pairs. Identifying behaviors exhibited by monkeys early in the pair introduction that are predictive of long-term compatibility can shape pairing decisions, reducing later stress and potential injury.

Oxytocin and pair compatibility in adult male rhesus macaques (Macaca mulatta).

Pair housing is considered one of the best ways of promoting psychological wellbeing for caged macaques. However, incompatible partnerships can result in stress or aggression. Though previous studies have analyzed the role of variables such as age, weight, gender, and temperament on pair compatibility, few have examined the relationship between physiological parameters and pair compatibility. Oxytocin is known to promote prosocial nonsexual behavior in various primate species and may serve as an indicator of pair compatibility. In this study, we examined the association between peripheral oxytocin levels and prosocial behaviors in isosexual pairs of male rhesus macaques. We hypothesized that animals that demonstrated high levels of prosocial behaviors would have higher oxytocin levels than those showing low levels of the behavior. In addition, to elucidate the relationship between oxytocin and compatibility, we compared peripheral oxytocin between the highly affiliative animals and single-housed males identified as having multiple unsuccessful pair attempts with multiple partners. We collected plasma oxytocin on 40 pairs of monkeys that had lived together for at least 1 month and 20 single-housed animals. Further, we simultaneously collected behavioral data on the pairs, recording prosocial interactions (e.g., groom, play). Oxytocin varied among individuals, but was highly correlated between members of a pair (r = 0.58, p < .001). Additionally, prosocial behavior was positively correlated with plasma oxytocin (r = 0.38, p < .02). However, contrary to our expectations, oxytocin did not differ between single and highly affiliative pair-housed animals (F(1,38) = 0.71, p = .40). Our results suggest that oxytocin may be associated with the quality of isosexual pairs of male macaques. More work is needed to determine the nature of this relationship.

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.

Isoflurane Anesthesia Has Long-term Consequences on Motor and Behavioral Development in Infant Rhesus Macaques.

BACKGROUND: Experimental evidence correlates anesthetic exposure during early development with neuronal and glial injury and death, as well as behavioral and cognitive impairments, in young animals. Several, although not all, retrospective human studies of neurocognitive and behavioral disorders after childhood exposure to anesthesia suggest a similar association. Few studies have specifically investigated the effects of infant anesthesia exposure on subsequent neurobehavioral development. Using a highly translational nonhuman primate model, the authors investigated the potential dose-dependent effects of anesthesia across the first year of development. METHODS: The authors examined the effects of single or multiple early postnatal isoflurane exposures on subsequent behavioral development in 24 socially reared rhesus macaques. Infants were exposed to 5 h of isoflurane anesthesia once, three times (ISO-3), or not at all (control). The authors assessed reflex development and anxiety using standardized tests. At approximately 1 yr, infants (n = 23) were weaned and housed indoors with 5 to 6 other subjects. The authors recorded their response to this move and reassessed anxiety. RESULTS: Compared to controls, animals exposed to repeated isoflurane (ISO-3) presented with motor reflex deficits at 1 month (median [range]: ISO-3 = 2 [1 to 5] vs. control = 5 [3 to 7]; P < 0.005) and responded to their new social environment with increased anxiety (median [range]: ISO-3 = 0.4 bouts/min [0.2 to 0.6]; control = 0.25 bouts/min [0.1 to 0.3]; P = 0.05) and affiliative/appeasement behavior (median [range]: ISO-3 = 0.1 [0 to 0.2]; control = 0 bouts/min [0 to 0.1]; P < 0.01) at 12 months. There were no statistically significant behavioral alterations after single isoflurane exposure. CONCLUSIONS: Neonatal exposure to isoflurane, particularly when repeated, has long-term behavioral consequences affecting both motor and socioemotional aspects of behavior.

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.

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.

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.

Effects of Seasonality and Pregnancy on Hair Loss and Regrowth in Rhesus Macaques.

Several studies have examined the etiology of alopecia, or hair loss, in rhesus macaques. While outcomes differ across studies, some commonalities have emerged. Females, particularly pregnant females, show more alopecia than males, and alopecia follows a seasonal pattern. Much research has explored causes of hair loss; however, alopecia can result from lack of hair growth in addition to hair loss. To better understand how sex, reproductive state, and season affect alopecia, we followed 241 rhesus macaques (Macaca mulatta) in outdoor breeding groups over one year, recording both alopecia severity and presence of hair regrowth. We found that both alopecia and hair regrowth followed a seasonal pattern; alopecia was highest in spring and lowest in late summer, while regrowth started in spring and peaked in late summer. Reproductive state also correlated with both alopecia and hair growth. Females in their third trimester had the highest average level of alopecia and the lowest amount of hair regrowth. Regrowth resumed postpartum, regardless of whether females were rearing an infant. Results indicate that the seasonal pattern of alopecia is due in part to the seasonal limitations on hair regrowth, and that breeding, which also occurs seasonally in rhesus macaques, may further suppress hair regrowth.

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.

Individual differences in temperament and behavioral management practices for nonhuman primates.

Effective behavioral management plans are tailored to unique behavioral patterns of each individual species. However, even within a species behavioral needs of individuals can vary. Factors such as age, sex, and temperament can affect behavioral needs of individuals. While some of these factors, such as age and sex, are taken into account, other factors, such as an individual's temperament, are rarely specifically provided for in behavioral management plans. However, temperament may affect how animals respond to socialization, positive reinforcement training and other forms of enrichment. This review will examine how individual differences in temperament might affect, or be affected by, behavioral management practices for captive primates. Measuring temperament may help us predict outcome of social introductions. It can also predict which animals may be difficult to train using traditional methods. Further, knowledge of temperament may be able to help identify individuals at risk for development of behavioral problems. Taken together, understanding individual differences in temperament of captive primates can help guide behavioral management decisions.

Video Conference Technology as a Tool for Pair Introduction in Rhesus Macaques.

Pair housing is known to promote welfare for macaques in captivity. However, finding compatible partners can be challenging, particularly when animals are not located near one another. Because macaques show interest in videos of conspecifics, we examined the use of video conference technology (Zoom) as a potential tool to assess compatibility in 84 rhesus macaques (2-22 years old) prior to pair introduction. Monkeys involved in the pairs (12 female-female, 21 male-male, 9 female-male) were unfamiliar with each other. We set up a 10 min Zoom session between potential partners (on an iPad in front of the cage). We scored attention to the screen, anxiety, and prosocial behaviors and examined whether these behaviors predicted future pair success. Monkeys spent relatively little time attending to the tablet (median = 13.3%), and attention did not predict pair success (B = -0.06, NS). However, pairs in which attention was primarily shown by one animal had a higher chance of success than those in which both individuals showed similar levels (B = -4.66. p = 0.03). Neither prosocial (B = 0.89, NS) nor anxiety (B = -1.95, p = 0.07) behavior correlated with pair success. While preliminary, our data suggest that video conferencing technology may be useful as a tool for introducing unfamiliar partners prior to a socialization attempt.

Bedding as an Enrichment Strategy in Group-housed Mauritian Cynomolgus Macaques (Macaca fascicularis).

The research community is committed to improving the well-being of nonhuman primates by providing opportunities to express species-specific behaviors such as foraging. In the wild, macaques spend a large part of their day foraging; this behavior is greatly limited in captivity. Bedding (wood shavings substrate) has been shown to promote foraging in rhesus macaques. However, the amount of bedding needed to affect these changes is unknown. Further, few studies have examined other benefits of bedding, including its potential to reduce noise levels, which can negatively impact welfare. We examined the use of bedding substrate in male Mauritius cynomolgus macaques (2-3-y-old) living in one of 2 social groups with either a full bale of bedding (that is, approximately 6 in of substrate) or a half bale (approximately 3 in) added to the pens for 10 d, followed by 4 d without bedding. We performed focal observations on 8 monkeys biweekly for 8 wk and used a dosimeter to measure sound in the room for 42 d. As expected, monkeys spent significantly more time foraging and less time self-grooming when bedding was present than when it was not. The amount of bedding did not make a difference. The presence of bedding did not affect social grooming or aggression, although it did help to dampen sound. Both peak and mean sound levels were lower with a full bale of bedding than with no bedding. Taken together, these results suggest that bedding is an effective enrichment strategy that can improve welfare of group-housed macaques.

Chronic consumption of a high-fat diet during pregnancy causes perturbations in the serotonergic system and increased anxiety-like behavior in nonhuman primate offspring.

Childhood obesity is associated with increased risk of behavioral/psychological disorders including depression, anxiety, poor learning, and attention deficient disorder. As the majority of women of child-bearing age are overweight or obese and consume a diet high in dietary fat, it is critical to examine the consequences of maternal overnutrition on the development of brain circuitry that regulates offspring behavior. Using a nonhuman primate model of diet-induced obesity, we found that maternal high-fat diet (HFD) consumption caused perturbations in the central serotonergic system of fetal offspring. In addition, female infants from HFD-fed mothers exhibited increased anxiety in response to threatening novel objects. These findings have important clinical implications as they demonstrate that exposure to maternal HFD consumption during gestation, independent of obesity, increases the risk of developing behavioral disorders such as anxiety.

Caring for nonhuman primates in biomedical research facilities: scientific, moral and emotional considerations.

Animal care for nonhuman primates (NHPs) in biomedical facilities has undergone major changes in the past few decades. Today, most primate facilities have dedicated and highly trained animal care technicians who go to great efforts to ensure the physiological and psychological well being of the primates in their charge. These caretakers work closely with the animals and, as a result, often develop strong relationships with them. Once discouraged and considered a potential threat to scientific objectivity, such positive relationships are now seen as important components to animal care. Positive interactions between caretakers and primates can benefit the primates by reducing their stress and improving their overall well being which can, in turn, help the scientific endeavor. Further, providing the best possible care is our moral responsibility. However, there can also be emotional costs associated with caring for NHPs in research facilities, particularly when animals become ill or have to be euthanized. Facilities can do much to help ease this conflict. High-quality and conscientious animal care is good for the animals, science, and public perception of research facilities.