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.     

Early predictors of self-biting in socially-housed rhesus macaques (Macaca mulatta)

The development of self-biting behavior in captive monkeys is little understood and poses a serious risk to their well-being. Although early rearing conditions may influence the expression of this behavior, not all animals reared under similar conditions self-bite. The purpose of this study was to examine the effects of three rearing conditions on biting behavior and to determine whether early infant behavior can predict later self-biting. The subjects were 370 rhesus macaques born at the National Institutes of Health (NIH) Animal Center between 1994 and 2004. They were reared under three conditions: mother-reared in social groups (n=183), peer-reared in groups of four (n=84), and surrogate-peer-reared (n=103). Significantly more surrogate-peer-reared animals self-bit compared to peer-only or mother-reared animals. There was no sex difference in self-biting, but this result may have been affected by a sex bias in the number of observations. The durations of behaviors exhibited by the surrogate-peer-reared subjects were recorded in 5-min sessions twice a week from 2 to 6 months of age while the animals were in their home cages and play groups. In the play-group situation, surrogate-peer-reared subjects who later self-bit were found to be less social and exhibited less social clinging than those that did not self-bite. Home-cage behavior did not predict later self-biting, but it did change with increasing age: surrogate clinging and self-mouthing decreased, while environmental exploration increased. Our findings suggest that surrogate rearing in combination with lower levels of social contact during play may be risk factors for the later development of self-biting behavior.     

Social responding to mirrors in rhesus macaques (Macaca mulatta): Effects of changing mirror location

Two rhesus macaques (Macaca mulatta) with a lifetime of continuous exposure to mirrors showed a dramatic and reliable reinstatement of social behavior directed toward the mirror when it was simply moved to a new location. These data are discussed in the context of repeated failures to find self-recognition in monkeys and several recent claims that a cessation of social behavior directed toward mirrors can be used as evidence for the beginning of self-recognition in nonhuman primates.     

Normative nerve conductions in the tail of rhesus macaques (Macaca mulatta)

BACKGROUND: The aim of this study was to test the feasibility of using the tail of Macaca mulatta for neurophysiological testing of the peripheral nervous system. METHODS: Motor and sensory nerve conduction studies (NCS) of the tail were obtained by surface stimulation and recording. The technique utilized was novel. Unlike other NCS obtained from other peripheral nerves, this technique did not require any special neurophysiological expertise. RESULTS: The latency of the motor and sensory response was 2.5 +/- 0.71 and 1.1 +/- 0.27 ms respectively. The amplitude of the motor and sensory response was 8.1 +/- 5.1 mV and 14.6 +/- 9.4 microV respectively. Similar to human beings, there was a statistically significant relationship between age and motor amplitude, motor latency and sensory latency. CONCLUSIONS: Based on our results, a relatively simple, reproducible neurophysiological monitoring technique of the peripheral nervous system is possible.     

Demodex spp. in the hair follicles of rhesus macaques (Macaca mulatta)

The perineal or perineal and facial skin were evaluated on 53 rhesus macaques as part of a necropsy protocol. Microscopic evaluation of H & E stained skin sections revealed 19 animals positive for Demodex spp. Mites were seen within all portions of the hair follicles. Infestation varied from minimal to severe. Mites were found in macaques of all ages and in both sexes. Reaction to the mites ranged from no reaction, to minimal follicular epidermal hyperplasia to furunculosis. Immune status of the animal did not determine infestation but immune compromised macaques had more severe lesions. This is the first known report of Demodex spp. in rhesus macaques.     

Social interactions among female rhesus macaques (Macaca mulatta) during the nonbreeding season: Responses to the introduction of males

When rhesus monkeys are observed in social groups during the breeding season, increases in interfemale aggression coincide with midcycle increases in sexual activity between males and females. However, some investigators have suggested that both aggressive and affiliative interactions between females are influenced by the presence or absence of males, irrespective of menstrual cycle stage. In the present study, social interactions among members of a captive group of rhesus females were measured during the non-breeding season in response to the introduction of rhesus males. Ovariectomized rhesus females (estrogen-treated or untreated) served as stimulus controls. Tests with males were characterized by significantly decreased interfemale proximity and grooming and significantly increased aggression from that seen in tests with stimulus females or in the absence of stimulus animals. Only interfemale proximity declined significantly during stimulus female tests, but results suggest that this may merely reflect a decline in this behavior that occurs across the course of the day. Estrogen treatment did not alter either the aggressive or affiliative behavior of stimulus females or group female response to stimulus females. The possibility is discussed that changes in interfemale interactions during tests with males reflect female interest in interacting with the male, particularly under social conditions that may limit such interactions.     

Behavioral,immunological, and hormonal responses associated with social change in rhesus monkeys (Macaca mulatta)

Twelve animals to be socially reorganized in a group of 49 animals were compared with ten animals in a socially stable group (n = 51) for reproductive hormones, cortisol concentrations, immune function, and behavioral patterns for a 6 week baseline and 16 week postreorganization period. Cortisol values, mitogen-induced lymphocyte blastogenesis, and rates of behavior reflected social events. Increased cortisols, increased noncontact aggression, and decreased mitogen response were associated with animal introductions. Increased cortisol concentration and decreased mitogen response correlated significantly only in animals removed from the group for trauma, and females successful at group membership exhibited lower cortisol concentrations. High-ranking animals in small stable groups exhibited significantly higher lymphocyte proliferation than middle- or low-ranking animals. While relative ranks established in small groups were maintained following reorganization, baseline cortisol values, immune measures, or male testosterone values did not predict success at group membership. © 1996 Wiley-Liss, Inc.     

Improved behavioral indices of welfare in continuous compared to intermittent pair-housing in adult female rhesus macaques (Macaca mulatta)

Limiting opportunities for captive nonhuman primates (NHPs) to express species-specific social behaviors may disrupt the adaptive drive for social companionship and may lead to increases in coping behaviors and inactivity. While captive NHPs show improved welfare when moving to pair-housing from single-housing, the impact of daily separation of pair-mates, as is implemented in intermittent pair-housing, is not fully understood. We compared behavioral indices of welfare exhibited by adult female rhesus macaques (Macaca mulatta) in two conditions: (1) intermittent pair-housing, involving daily overnight separation of pair-mates, and (2) continuous pair-housing, involving little separation of pair-mates. A within-subjects study design tested two groups of females experiencing both pairing conditions in an alternate order, switching either from continuous to intermittent pair-housing, or from intermittent to continuous pair-housing. Behavioral observations, recording activity state, self-directed, abnormal, and social behaviors, were conducted at midday when all females were paired, and in the afternoon when intermittent pairs were separated. Females exhibited higher levels of inactivity and self-directed behavior when separated due to intermittent pair-housing in comparison to continuous pair-housing. In addition, intermittently paired females showed higher levels of grooming and other types of affiliation when paired, than during the same time frame when they were continuously paired. These results suggest that females in the continuous presence of a social partner experience improved levels of activity and do not need to elevate levels of behavioral coping mechanisms (e.g., self-scratching, increased affiliation) as they receive the benefits associated with social companionship consistently throughout the day. Overall, this study provides the first evidence that continuous pair-housing affords better welfare than intermittent pair-housing in adult female rhesus macaques. Pair-housing options, such as continuous pairing, that reduce reliance on behavioral coping mechanisms and promote adaptive social behavior throughout the entirety of the day should be prioritized over husbandry care scheduled for convenience.     

Influences of blood sampling procedures on basal hypothalamic-pituitary-adrenal hormone levels and leukocyte values in rhesus macaques (Macaca mulatta)

Abstract: The influences of housing location and temporal factors on the results of blood sampling were examined to determine their contributions to levels of hypothalamic-pituitary-adrenal hormones, as well as leukocyte subset counts from peripheral blood in rhesus monkeys. Differences in housing location and the amount of room disturbance associated with blood sampling have a significant impact on cell counts, but not on ACTH or Cortisol levels.     

The effect of inter-opponent distance on the occurrence of reconciliation in stumptail (Macaca arctoides) and rhesus macaques (Macaca mulatta)

Several studies have shown that affiliative contact between opponents increases after conflicts in a number of primate species. This study investigated the effect of inter-opponent distance on the occurence of reconciliation in stumptail and rhesus macaques. Both species were represented by multi-male, multi-female groups housed in large outdoor compounds. Ten-minute focal animal observations during post-conflict (PC) and matched control (MC) samples were collected in which affiliative interactions and the inter-opponent distance at the beginning of each sample were recorded. A total of 251 and 561 PC-MC opponent pairs were obtained for stumptail and rhesus macaques, respectively. Inter-opponent distance was smaller in PC than in MC observations for both stumptail and rhesus macaques. Conciliatory tendency varied as a function of the initial PC-MC inter-opponent distance. In particular, the closer opponents were in PC compared to MC periods, the more likely they were to reconcile. When the inter-opponent distance was the same in PC and MC periods the conciliatory tendency of both species was notably reduced. These findings have implications for the estimation of conciliatory tendency and its use in comparative studies.     

Evaluation of the use of coconut to treat chronic diarrhea in rhesus macaques (Macaca mulatta)

Background Chronic diarrhea can be challenging to manage in captive rhesus macaques (Macaca mulatta) leading to ongoing diagnostics, medications, monitoring, and potential euthanasia. Coconut has been used as a dietary supplement for people with inflammatory bowel disease, with anecdotal reports of decreased diarrhea following the dietary addition. A dietary trial in rhesus macaques was initiated to evaluate the hypothesis that dietary coconut decreases symptoms of chronic diarrhea in rhesus macaques. Methods Ten rhesus macaques with chronic diarrhea were selected for the trial. Five of the subjects were fed coconut macaroons and five of the subjects were fed a sham cookie. Stool consistency was monitored daily for both groups. Results and conclusions Data of chi‐squared analysis obtained from eight rhesus macaques with chronic diarrhea showed that the use of coconut macaroons as a dietary supplement did not have a statistically significant effect on their diarrhea.     

A comparison of the mating behavior of adolescent and adult female rhesus macaques (Macaca mulatta)

This study compares adult and adolescent female rhesus macaques with regard to (1) characteristics of their copulatory partners, (2) their proceptive behaviors, and (3) adult male behaviors toward them during estrus. We conducted focal follows of 24 adolescent and 65 adult free-ranging estrous female rhesus macaques on Cayo Santiago during two mating seasons. Compared to adult females, adolescents presented sexually to males at higher rates; copulated more frequently with rankless young male, and extra-group males; and, in one of two mating seasons, were ignored more frequently by males to whom they presented sexually. Adolescents tended to copulate with ranked, resident males at higher frequencies on days when the operational sex ratio (adult males:estrous adult females) was high. Males directed “muzzle-up” signals to adolescents at lower rates than to adults in one of two mating seasons, although this effect vanished when males who might have fathered adolescent females were excluded from analysis. Adolescents did not differ consistently from adults in strength of the correlation between proximity maintenance (dyadic Hinde's Index) and copulation rate, or in approach rate to males. Adolescent females, relative to adult females, presented sexually more to rankless young males, but did not present more to ranked, resident males. Both proximate (e.g. endocrine) and ultimate (e.g. differential fecundity; female-female mate competition) explanations may account for the reported differences between adult and adolescent female rhesus macaque sexuality.     

Natural and experimental infection of immunocompromised rhesus macaques (Macaca mulatta) with the microsporidian Enterocytozoon bieneusi genotype D

Microsporidia are obligate intracellular parasites that cause opportunistic infections in AIDS and other immunocompromised patients. Eight simian immunodeficiency virus (SIV)-infected rhesus macaque monkeys (Macaca mulatta) were inoculated orally with Enterocytozoon bieneusi spores isolated from intestinal lavage fluid of an AIDS patient (genotype D) to study the natural history of this infection. Four monkeys were already naturally infected with E. bieneusi (also genotype D), and were included to determine if a second inoculum affected the course of illness. Spore shedding was detected in feces of all eight monkeys within the first week of experimental infection. Five monkeys died within 3.5 months of experimental E. bieneusi inoculation. Three of these five monkeys began the study with CD4+CD29+ T cell levels well below 20% of total T lymphocytes. Deaths were due to a variety of AIDS-related manifestations. Microsporidia did not appear to directly contribute to mortality but may have contributed to morbidity. At necropsy, microsporidia were found in bile and tissue sections of the gallbladder but not in the gut, kidneys, or liver. The percent CD4+CD29+ levels of the last three monkeys remained near the level observed at the time of inoculation. These monkeys lived more than 2 years after the end of the study and continued to shed spores. This study corroborates previous reports that E. bieneusi can be reliably transmitted to SIV-infected rhesus monkeys but indicates that the use of SIV-infected monkeys for the study of microsporidiosis is complicated by the confounding effect of other opportunistic or AIDS-related infections.     

Early hematologic changes in rhesus macaques (Macaca mulatta) infected with pathogenic and nonpathogenic isolates of SIVmac

Early hematologic changes were studied over a 14 day period in three groups of six rhesus macaques intravenously infected with pathogenic and nonpathogenic isolates of SIVmac. Abnormalities in blood included a mild blood loss anemia, sporadic lymphopenia, and variable CD4+ and CD8 + T lymphocyte numbers. Prominent bone marrow findings in macaques inoculated with pathogenic uncloned SIVmac and molecularly cloned pathogenic SIVmac-239 were hypercellularity, myeloid and megakaryocytic hyperplasia, and lymphoid aggregates. Infrequent mild morphologic abnormalities were present in macaques infected with a nonpathogenic molecular clone, SIVmac-1A11.     

环境和社会因素对喀斯特石山猕猴日活动节律和活动时间分配的影响

2007年9月至2008年8月,以广西弄岗国家级自然保护区内的一大群野生猕猴为研究对象进行连续的跟踪观察,采用瞬时扫描取样法收集其食物组成、活动节律和活动时间分配的数据,旨在探讨影响石山猕猴活动节律及活动时间分配的环境和社会因素。结果表明：研究猴群的日活动节律表现为上午和下午的觅食高峰以及中午的休息高峰,这与白天温度和日照强度的变化有关。日活动时间分配中,休息42.1%,移动34.5%,觅食15.1%,玩耍2.0%,理毛5.2%,其他行为1.3%。猴群依据食物的变化调整活动时间分配,其中用于移动的时间与食物中果实的比例成显著的正相关性。不同性别年龄组个体的活动时间分配表现出显著差异,主要表现为成年雄性花费更多的时间休息,而成年雌性花费更多的时间觅食和社会性理毛,未成年个体则花费更多的时间玩耍。与同域分布的小群猕猴相比,本研究群花费更多的时间休息,较少的时间觅食。这些差异可能与盗食农作物有关。     

Computed tomography or necropsy diagnosis of multiple bullae and the treatment of pneumothorax in rhesus macaques (Macaca mulatta)

Pulmonary bullae and pneumothorax have various etiologies in veterinary medicine. We diagnosed multiple pulmonary bullae combined with or without pneumothorax by computed tomography (CT) or necropsy in seven rhesus macaques (Macaca mulatta) imported from China. Two of seven rhesus macaques accompanied by pneumothorax were cured by fixation of ruptured lung through left or right 3rd intercostal thoracotomy. Pneumonyssus simicola, one of the etiologies of pulmonary bullae, was not detected from tracheobronchiolar lavage. To the best of our knowledge, this is the first case report on the CT‐aided diagnosis of pulmonary bullae and the successful treatment of combined pneumothorax by thoracotomy in non‐human primates (NHPs).     

The hemogram,serum biochemistry,and electrolyte profile of the free-ranging Cayo Santiago rhesus macaques (Macaca mulatta)

Sixty-four male and 33 female free-ranging rhesus monkeys (Macaca mulatta) from one of six social groups on the island of Cayo Santiago, Puerto Rico, were surveyed to establish normal values for the hemogram and serum biochemical and electrolytes for the colony. Mean values (± 1 SD) are reported by sex for each of three age groups (2–3, 4–9 and ≥ 10 years). All adult females (≥ 4 years) were pregnant. There were significant differences for a number of variables compared to the range reported in the existing literature, and among the age and sex groups in the sampled population.