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.

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.

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.

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.

Prevalence of enteric bacterial parasites with respect to anthropogenic factors among commensal rhesus macaques in Dehradun, India.

There has been a recent surge in research on primate infectious disease ecology. Two major areas remain relatively unaddressed to date-the prevalence of enteric bacterial parasites and the role of anthropogenic environmental factors in parasite acquisition in commensally living primate populations. In this preliminary assessment, we address both these gaps by assessing the prevalence, and the role of anthropogenic factors in shaping this prevalence, of three enteric bacterial parasites-E . coli O157:H7, Salmonella sp., Shigella sp.-across populations of rhesus macaques (M. mulatta) that live commensally with humans in Dehradun, northern India. Across 10-week study period, we collected data on (1) human-macaque behavioral interactions, (2) macaque and human demographic and activity scans, and (3) macaque fecal samples from the environment at four different locations in Dehradun. Biochemical tests and morphology-based confirmations clearly established the presence of all three enteric bacterial parasites in rhesus macaques. Overall prevalence ranged from 2 to 5 %, with Shigella sp. being the most prevalent. Regression analyses linking anthropogenic factors to bacterial prevalence showed a positive association between rates of macaques eating human garbage and E. coli O157:H7 (ß = 0.23, p = 0.083), but a negative association with Salmonella sp. (ß = -0.17, p = 0.026). Rather, the prevalence of Salmonella sp. was positively linked to rates of macaque eating provisioned food (ß = 0.0012, p = 0.058). Finally, we found no relationship between anthropogenic factors and the prevalence of Shigella sp. Our findings establish the prevalence of enteric bacterial parasites in commensal populations of primates and suggest that although anthropogenic factors are linked to bacterial prevalence, the nature of the relationships may depend on the socioecological/foraging strategies of macaques and the food sources that facilitate the environmental survival of particular types of enteric bacteria over others.

Human-wildlife conflict: proximate predictors of aggression between humans and rhesus macaques in India.

Macaques live in close contact with humans across South and Southeast Asia, and direct interaction is frequent. Aggressive contact is a concern in many locations, particularly among populations of rhesus and longtail macaques that co-inhabit urbanized cities and towns with humans. We investigated the proximate factors influencing the occurrence of macaque aggression toward humans as well as human aggression toward macaques to determine the extent to which human behavior elicits macaque aggression and vice versa. We conducted a 3-month study of four free-ranging populations of rhesus macaques in Dehradun, India from October-December 2012, using event sampling to record all instances of human-macaque interaction (N = 3120). Our results show that while human aggression was predicted by the potential for economic losses or damage, macaque aggression was influenced by aggressive or intimidating behavior by humans as well as recent rates of conspecific aggression. Further, adult female macaques participated in aggression more frequently than expected, whereas adult and subadult males participated as frequently as expected. Our analyses demonstrate that neither human nor macaque aggression is unprovoked. Rather, both humans and macaques are responding to one another's behavior. Mitigation of human-primate conflict, and indeed other types of human-wildlife conflict in such coupled systems, will require a holistic investigation of the ways in which each participant is responding to, and consequently altering, the behavior of the other.

Risk factors and remediation of self-injurious and self-abuse behavior in rhesus macaques.

Considered signs of decreased welfare--abnormal behaviors such as self-injury and self-abuse among nonhuman primates housed in the laboratory--may put into question the validity and reliability of scientific research using these animals as models. Providing environmental enrichment decreases the incidence of some undesirable behaviors but is often unsuccessful at ameliorating the most severe types of abnormal behaviors. To prevent such behaviors from developing, it is important to identify risk factors that provide insight into the causes of certain abnormal behaviors. This study confirmed previous research identifying nursery rearing, single housing, and time spent in single housing as important risk factors. Results also indicate that the number of cage relocations affects the development of these behaviors. In addition, this study presents new data on comorbidity of several abnormal behaviors and discusses possible reasons for these patterns.