The relationship of agonistic and affiliative behavior patterns to cellular immune function among cynomolgus monkeys (Macaca fascicularis) living in unstable social groups

Considerable recent interest has focused on the possibility that behavioral factors may influence immune competence, and hence, potentially, patterns of disease. We report here the relationship between the aggressive and affiliative behavior and the cellular immune responses of 30 adult male cynomolgus monkeys (Macaca fascicularis) living in small (n = 5) social groups whose members were periodically redistributed over 26 months. Animals also were subjected to behavioral observation, allowing them to be categorized as either high or low in aggressiveness and affiliation. At the end of the 26 months, lymphocyte proliferation tests were performed on blood samples from all monkeys, using both concanavalin A (ConA) and phytohemagglutinin (PHA) in concentrations of 1, 5, and 10 ug/ml. Two-by-two (Aggressiveness [high, low] X Affiliation [high, low]) analyses of variance performed on these data showed lymphocyte proliferation in response to both ConA and PHA to be greatest (at 1 ug/ml) among highly affiliative animals, albeit only if they were also low in aggressiveness (ConA: Affiliation x Aggression, P < 0.02; PHA: Affiliation x Aggression, P < 0.03). An additional finding was that natural killer cell activity (at an effector to target ratio of 100:1) was highest among highly affiliative animals, regardless of their aggressiveness (P < 0.05). These results indicate that immune competence may be enhanced among monkeys which, in response to a disrupted social environment, spend large amounts of time in affiliation with other animals. Social status, a phenomenon known to influence many aspects of nonhuman primate physiology, was unassociated with nonspecific lymphocyte blastogenesis or natural killer cell activity in this experiment.     

Positional behavior of long-tailed macaques (Macaca fascicularis) in northern Sumatra

Although the majority of extant primates are described as "quadrupedal," there is little information available from natural habitats on the locomotor and postural behavior of arboreal primate quadrupeds that are not specialized for leaping. To clarify varieties of quadrupedal movement, a quantitative field study of the positional behavior of a highly arboreal cercopithecine, Macaca fascicularis, was conducted in northern Sumatra. At least 70% of locomotion in travel, foraging, and feeding was movement along continuous substrates by quadrupedalism and vertical climbing. Another 14-25% of locomotion was across substrates by pronograde clambering and vertical clambering. The highest frequency of clambering occurred in foraging for insects, and on the average smaller substrates were used in clambering than during quadrupedal movement. All postural behavior during foraging and feeding was above-substrate, largely sitting. Locomotion across substrates requires grasping branches of diverse orientations, sometimes displaced away from the animal's body. The relatively low frequency of across-substrate locomotion appears consistent with published analyses of cercopithecoid postcranial morphology, indicating specialization for stability of limb joints and use of limbs in parasagittal movements, but confirmation of this association awaits interspecific comparisons that make the distinction between along- and across-substrate forms of locomotion. It is suggested that pronograde clambering as defined in this study was likely a positional mode of considerable importance in the repertoire of Proconsul africanus and is a plausible early stage in the evolution of later hominoid morphology and locomotor behavior.     

抱崽与否对笼养雌性食蟹猴个体社会行为的影响

目的比较笼养雌性食蟹猴抱崽与否,是否对其社会行为有影响。方法从2010年5月开始,在江苏省苏州中科实验动物有限公司猴场可观察的个体中,随机抽取观察对象40个;同年10月开始正式拍摄,样本中,11个个体抱崽,29个个体未抱崽。三名观察员采用焦点观察法,使用高清摄像机,对所有个体每天跟踪拍摄7个时间片段,每个时间段为30分组,每个个体观察4 d,共计完成有效累积观察时间560 h;将每天所拍摄视频汇总而后随机分配给NOLDUS分析员分析转换成为行为数据。结果抱崽个体多数时间是怀抱住幼崽,社会友好行为较多,比如为其他个体理毛或被其他个体理毛;社会地位较高,如与猴王共坐于制高点(悬于空中的板子或链子上,依据各个猴场饲养条件而议)时间较长;通讯行为较多,即努嘴行为;运动行为和交配行为较多;而未抱崽个体聚温行为较多,即与其他个体相互怀抱聚温;两组在摄食行为、发情行为、休息行为、冲突行为、警戒行为和各种自我行为差异无显著性。结论抱崽对雌性食蟹猴的社会行为有影响。     

Adoption success under single-cage conditions by cynomolgus macaque mothers (Macaca fascicularis)

Retrospective data were studied to determine the success of experimental adoption by 122 cynomolgus macaques kept in individual cages at the Tsukuba Primate Center. The four types of adoption procedures included (1) singletons adopted after weaning (SAW)—21 cases; (2) singletons adopted after stillbirth (SAS)—20 cases; (3) singletons adopted after forced separation of the biological infant during the nursing period (SAF)—4 cases; and (4) adoption of a second “twin” while still nursing a biological infant (TA)—77 cases. Adoption was defined as successful if the mother nursed the foster infants for at least 7 days. Success rates (percent) were 47.6 for SAW, 75 for SAS, 100 for SAF, and 74 for TA. Success was affected by the postbirth stage of foster mothers at adoption but not by foster infant age or sex.     

Effects of ovarian hormones on the behavior of captive Macaca fascicularis

To examine the effects of ovarian hormones on the behavior of female Macaca fascicularis and their male partners, daily 1-hr behavior tests were conducted while ovariectomized females were (1) untreated, (2) given estradiol benzoate (EB) (5 μg subcutaneously [s.c.]/day), (3) given estradiol benzoate together with increasing doses of progesterone (P) (5 mg, 10 mg, and 20 mg. s.c./day), and (4) given testosterone propionate (TP) (0.25 mg s.c./day) (six pairs, 540 tests). Weekly blood samples were analyzed by radioimmunoassay for plasma hormone levels (81 samples). Estrogen treatment produced plasma estradiol levels similar to those of intact females during the late follicular phase of the menstrual cycle. Additional progesterone at the lowest dose produced plasma progesterone levels similar to or somewhat higher than those during the midluteal phase, while higher doses produced supraphysiological levels. Androgen treatment resulted in plasma levels well above the physiological range. Hormone treatments produced highly significant effects on the sexual, social, and aggressive interactions of the pairs. As in rhesus monkeys, estrogen increased male and female sexual activity, and increasing doses of additional progesterone reversed these effects. Unlike in rhesus monkeys, testosterone propionate increased both female sexual motivation (invitations) and also male sexual activity and ejaculatory performance. The direction of the hormone-dependent changes in grooming and aggressive interactions confirmed earlier results with intact females and indicated that aggressive interactions and male grooming times were highest, and female grooming times were lowest, when copulatory activity was at its height.     

A comparison of the behavior of Macaca fascicularis and Macaca mulatta in relation to the menstrual cycle

Observations on oppositely sexed pairs of M. fascicularis and M. mulatta revealed certain differences. M. fascicularis showed single-mount copulations, higher potency, less grooming activity, and milder but more frequent aggressive exchanges than the rhesus monkey. These differences might be due to the lower dominance gradient between the sexes and less sexual dimorphism in M. fascicularis than in M. mulatta. There were changes in the sexual, grooming, and aggressive interaction in relation to the menstrual cycle, indicating the suitability of M. fascicularis for hormone-behavior studies. Comparison of data from 30 and 60 min tests showed that important behavioral changes did not become apparent unless animals were given enough time to interact.     

Bridging behavior and other affiliative interactions among male tibetan macaques (Macaca thibetana)

I describe bridging behavior and social relationships between adult males and infants in a free- ranging group of Tibetan macaques (Macaca thibetana)at Mt. Huangshan, China. The subjects performed bridging in which two adult males simultaneously lifted up an infant, sucked or touched its genitalia, and then groomed each other in nonagonistic contexts. Males also expressed social behaviors with other males, such as mounting, penis-sucking, and embracing while touching each other’s penes. Males also employ bridging while exploiting an infant as a social tool, not only to reduce the probability of an aggressive response from dominant males (agonistic buffering), but also to develop and to maintain affiliative social relationships with other males. Use of male infants in bridging contributed to frequent male-infant interactions such as holding,grooming, and penis-sucking. Although these interactions might not have a positive influence on infant survival, they may facilitate the maintenance of affiliative relationships with adult males until they reach maturity. The development of bridging might have a close relation to the high socionomic sex ratio (adult male/adult female) and frequent affiliative interactions between males, especially among the adolescents and adults.     

The influence of rearing conditions on maternal behavior in cynomolgus macaques (Macaca fascicularis)

We studied the influence of rearing on the adequacy of maternal behavior by comparing 20 harem-reared and 15 peer-reared primiparous cynomolgus monkeys. We used them plus 11 wild-caught females to extend this comparison to multiparous subjects and also to compare primiparae with multiparae. We observed no behavioral effect of rearing and parity. Primiparous maternal adequacy amounted to 93% in peer-reared subjects and to 95% in harem-reared monkeys. We extensively discuss theories concerning rearing effects. Leitmotifs throughout the discussion are survival value of maternal behavior immediately after parturition and predictive value of this behavior for the further course of maternal behavior. Support is accumulated for the hypothesis that certain tactile and visual experiences suffice for the development of adequate maternal behavior.     

Effects of group composition on agonistic behavior of captive pigtail macaques,Macaca nemestrina

We surveyed agonistic behaviors of 20 captive groups of pigtail macaques (Macaca nemestrina) housed under identical spatial conditions. Fifteen groups contained one male each; the other five groups contained no adult males. Groups included six to twelve adult females, some of which had infants with them. We found no relationship between social density of groups and incidence of agonistic behavior, but significantly more contact aggression (grab, hit, push, bite) and noncontact aggression (chase, open-mouth “threat,” bark vocalization) occurred among females in groups containing no males than in those containing one male each. Apparently, males played an important role in the inhibition of intragroup conflict. We also found that females in groups containing males exhibited less noncontact aggression if infants were present than if no infants resided in their groups. Thus, competition of females over infants must not have been an important constituent of intragroup conflict under the conditions of this survey.     

Pregnancy-induced sclerosis in the myometrial vessels of cynomolgus monkeys (Macaca fascicularis)

Sclerotic changes were found histologically in the myometrial vessels of 27 out of 33 cynomolgus monkeys (Macaca fascicularis). The sclerosis was composed of fibrous proliferations and intimal thickening. These changes were not observed in nulliparous cases, but were found only in multiparous ones. The findings suggest that the sclerotic changes in the myometrial vessels of cynomolgus monkeys are a pregnancy-induced phenomenon.     

Acute changes in social composition and agonistic behavior in male vervet monkeys (Cercopithecus aethiops sabaeus)

Among nonhuman primates the composition of social groups influences the interactions of group members. We assessed the effects of acute changes in social composition on behavior among 15 adult male vervet monkeys (Cercopithecus aethiops sabaeus). Subjects were observed in their basal social groups which comprised 3 adult males, 2–4 adult females, and offspring; and in two subgroups consisting of either two or three adult males. Agonism and vigilance increased in smaller groups relative to basal conditions, while subjects in two-male groups displayed more aggression than those in three-male groups. These findings suggest that, among male vervet monkeys, acute disruption of stable social groups increases aggressive behavior, and that the amount of agonism is influenced by the composition of the consequent subgroups. © 1992 Wiley-Liss, Inc.     

A natural model of behavioral depression in postpartum adult female cynomolgus monkeys (Macaca fascicularis)

Within the postpartum period, both mothers and infants are susceptible; but because PPD typically occurs for short durations and has moderate symptoms, there exists challenges in exploring and addressing the underlying cause of the depression. This fact highlights the need for relevant animal models. In the present study, postpartum adult female cynomolgus monkeys(Macaca fascicularis) living in breeding groups were observed for typical depressive behavior. The huddle posture behavior was utilized as an indicator of behavioral depression postpartum(BDP) as it has been established as the core depressive-like behavior in primates. Monkeys were divided into two groups: A BDP group(n=6), which were found to spend more time huddling over the first two weeks postpartum than other individuals that formed a non-depression control group(n=4). The two groups were then further analyzed for locomotive activity, stressful events, hair cortisol levels and for maternal interactive behaviors. No differences were found between the BDP and control groups in locomotive activity, in the frequencies of stressful events experienced and in hair cortisol levels. These findings suggested that the postpartum depression witnessed in the monkeys was not related to external factors other than puerperium period. Interestingly, the BDP monkeys displayed an abnormal maternal relationship consisting of increased infant grooming. Taken together, these findings suggest that the adult female cynomolgus monkeys provide a natural model of behavioral postpartum depression that holds a number of advantages over commonly used rodent systems in PPD modeling. The cynomolgus monkeys have a highly-organized social hierarchy and reproductive characteristics without seasonal restriction—similar to humans—as well as much greater homology to humans than rodents. As such, this model may provide a greater translational efficiency and research platform for systematically investigating the etiology, treatment, prevention of PPD.     

Immunohistochemical distribution of leucocyte antigens in lymphoid tissues of cynomolgus monkeys (Macaca fascicularis)

Crossreactivity of antibodies to human leucocyte antigens with lymphoid tissues of cynomolgus monkeys was studied by immunohistochemistry and immunoblotting. Of a total of 54 clusters of differentiation (CD) antigens, 39 were expressed essentially with the same immunostaining patterns in the monkey as in human lymphoid tissues. By immunoblotting L26 (CD20) detected a 35 Kd molecule in the monkey lymph node. Our observations indicated that most of the CD antigens are expressed and can be studied in lymphoid tissues of cynomolgus monkeys.     

Evaluation of caged mating behavior in Macaca fascicularis.

Studies were undertaken to characterize the basic behavioral parameters of a breeding colony of Macaca fascicularis under caged conditions. The female Reproduction Performance Index and the Success Ratio were found to correlate with mating behavior relating to cyclicity in females with cycles of less than 30 days. These evaluations proved to be useful in the selection of animals based on sexual vigor.     

Hormonal regulation of agonistic and affiliative behavior in female mongolian gerbils (Meriones unguiculatus)

Ovarian steroids and oxytocin (OT) have been implicated in the regulation of social behaviors. The purpose of the present study was to examine hormonal substrates of aggression and affiliation in the female Mongolian gerbil (Meriones unguiculatus), a highly social, monogamous rodent. Sexually naive adult females were paired with sexually experienced males for 48 h and their interactions videotaped. Females were gonadally intact and tested during vaginal estrus (INT) or ovariectomized and observed after the following treatments, administered by means of sc injections: EBEB (7 days of estradiol-benzoate); EBP (2 days of EB followed by progesterone), SALEB (saline, days 1-5 then 2 days of EB), OTEB (OT for days 1-5 then 2 days of EB); OTOIL (OT for days 1-5 then 2 days of OIL); or SALOIL (saline days 1-5 then 2 days of OIL). During the first hour of pairing INT females displayed higher levels of affiliation and lower levels of sniffing and agonistic behavior than SALOIL females. All hormonal treatments reduced agonistic behaviors when compared to SALOIL, although none of the hormonal treatments restored affiliation to INT levels. During the 48-h test overt aggression varied by treatment with INT, EBEB, EBP, and OTEB females displaying lower levels than SALOIL, while all groups displayed similar levels of affiliation. The results indicate that OT and E play a significant role in regulating male-directed aggressive behavior in females and that the presence of ovarian hormones as well as OT can increase affiliation during initial contact. Over a sustained period of cohabitation social cues appear to be more important in regulating affiliation than gonadal hormones.     

Operant behavior and colonic temperature of Macaca mulatta exposed to radio frequency fields at and above resonant frequencies

Five food-deprived rhesus monkeys were exposed to 225-MHz continuous-wave, and 1.3-GHz, and 5.8-GHz pulsed radiation to determine the minimal power densities affecting performance. The monkeys were trained to press a lever (observing-response) thereby producing signals that indicated availability of food. In the presence of the aperiodically appearing food signals, a detection response on a different lever was reinforced by a food pellet. Continuous, stable responding during 60-min sessions developed and was followed by repeated exposures to radiofrequency radiation. The subjects, restrained in a Styrofoam chair, were exposed to free-field radiation while performing the task. Colonic temperature was simultaneously obtained. Observing-response performance was impaired at increasingly higher power densities as frequency increased from the near-resonance 225 MHz to the above-resonance 5.8 GHz. The threshold power density of disrupted response rate at 225 MHz was 8.1 mW/cm²; at 1.3 GHz it was 57 mW/cm², and at 5.8 GHz it was 140 mW/cm². These power densities were associated with reliable increases in colonic temperatures above sham-exposure levels. The mean increase was typically in the range of 1°C, and response-rate changes were not observed in the absence of concomitant temperature increases. In these experiments increase of colonic temperature was a much better predictor of behavioral disruption than was either the power density of the incident field or estimates of whole-body-averaged rates of energy absorption.     

Neighbor effect: evidence of affiliative and agonistic social contagion in captive chimpanzees (Pan troglodytes)

Previous studies of captive chimpanzees have demonstrated the "neighbor effect," or social contagion, with respect to agonistic vocalizations and behaviors. The present study considers whether there is a relationship between behavior patterns in focal animals and the auditory signals of neighboring social groups. Using focal-group sampling, we collected 172.5 hr of data on 51 subjects (25 females and 26 males) housed in 10 social groups. We performed two-tailed Wilcoxon matched-pairs signed-rank tests to determine whether the relative frequency of the vocalizations (high vs. low) affected the behaviors. In keeping with past research, we found that agonistic noises and vocalizations from neighboring social groups had a significant effect on the rates of focal-group bluff displays, pant-hoots, and aggression (P<0.05). In addition, we also found significant relationships between grooming behavior and vocalizations in focal groups, and grooming vocalizations from neighboring groups (P<0.05). The results suggest that social contagion is not limited to aggressive behaviors, but also occurs for affiliative behavior patterns.     

Sequential analysis of the social behavior of infants in groups of Japanese monkeys (Macaca fuscata fuscata)

We employed techniques of behavioral entropy to carry out a quantitative analysis of sequences of behavioral patterns evident in the interaction between infants and other members of a group of Japanese monkeys (Macaca fuscata fuscata). The group concerned included examples both of monkeys in captivity and in the wild state. The results were examined as a function of the animal age and environmental differences (cage-field). An example is given to illustrate the use of information theory. Findings partially confirmed that the variability of social behavior decreases as the age of the animals increases.