Social enrichment of the environment with infants for singly caged adult rhesus monkeys

The practicability of social enrichment for singly caged adult rhesus monkeys was examined. Twenty-nine weaned rhesus monkey infants were removed from breeding troops to avoid overcrowding and were placed with unfamiliar singly caged adults. An adult-infant pair was considered compatible when (1) the two animals started huddling with each other within the first 5 days after pair formation and (2) the infant showed no signs of depression and took its share from a limited amount of favored food. Adult-infant pairs were compatible in 90% (26/29) of cases. Compatibility depended neither on the sex, age, and origin of the adult nor on the sex of the infant. There was no evidence that partners lost interest in each other during 7–11 months of follow-up observations. Three adults exhibiting stereotypical behavior abandoned their peculiar habits after they had lived with their young companions for 4 months. It was concluded that the often-heard notion that rhesus monkeys are highly aggressive should not prevent simple attempts to provide singly caged animals with a companion.     

Elemental hair analysis of Japanese macaques transplanted to the United States

One of the world’s best studied troops of Japanese macaques (Macaca fuscata) was captured intact at Arashiyama, Japan and transplanted to a brushland savannah area near Laredo, Texas, in 1972. The transplantation provided a unique opportunity to study the biological responses of this troop to a drastically different environment than the one in which it evolved. We investigated one biological response, the metabolism of nutrient, and non-nutrient elements, by neutron activation analysis (NAA) of hair from 88 of the transplanted monkeys nine months after transplantation. Many of the elements mammals metabolize are deposited in hair. Hair analysis is therefore a measure of these elements the mammal encounters in its environment. Hair concentration of S and Cl were found to increase with animal age at the 95% confidence level, and hair concentrations of Hg, Se, and I were found to decrease with animal age at the 95% confidence level. Male hair had more Zn and less Se than female hair at the 95% confidence level. Comparison of this information with similar information on the sister troop in Japan and on other troops will provide some indication of the homeostatic ability of this primate species to cope with different exposure regimes of certain elements. Such information is of general interest where pollution and other cultural activities are changing environmental levels of many elements.     

Alopecia scoring: the quantitative assessment of hair loss in captive macaques

Many captive animals show forms of pelage loss that are absent in wild or free-living conspecifics, which result from grooming or plucking behaviours directed at themselves or at other individuals. For instance, dorsal hair loss in primates such as rhesus macaques (Macaca mulatta) in research facilities, results from excessive hair-pulling or over-grooming by cage-mates. This behaviour appears to be associated with stress, and is controllable to some extent with environmental enrichment. Quantifying alopecia in primates (as in many species) is therefore potentially useful for welfare assessment. A simple system for scoring alopecia was developed and its reliability was tested. Study 1 showed high interobserver reliability between two independent scorers in assessing the state of monkeys coats from photographs. Study 2 showed that there were no significant differences between the scores derived from photographs and from direct observations. Thus, where hair loss due to hair pulling exists in captive primates, this scoring system provides an easy, rapid, and validated quantitative method, for use in assessing the success of attempts to reduce it via improved husbandry. In the future, such scoring systems might also prove useful for quantifying barbering in laboratory rodents.     

Age-related diffuse chronic telogen effluvium- type alopecia in female squirrel monkeys (Saimiri boliviensis boliviensis)

We investigated the diffuse alopecia affecting some female squirrel monkeys (Saimiri boliviensis boliviensis) housed in a breeding facility. We randomly selected 100 female and 10 male animals and performed a complete physical exam and a hair assessment on all animals; blood tests, trichograms, hair density; and skin biopsies in representative cases; and a dominance behavioral assessment of 50 animals. Hair coat was normal in 35 female monkeys and all 10 male animals. Of the 65 females with diffuse alopecia, 17 had mild, 22 moderate, and 26 severe hair loss. The alopecia group had a mean age of 9.6 +/- 0.6 years, whereas that of the normal group was 4.7 +/- 0.6 years (P < 0.05). The parity in the alopecia group was 4.2 +/- 0.6 but 2.0 +/- 0.6 (P < 0.05) in the normal group. There were no statistically significant differences in body weight, hemoglobin, blood urea nitrogen, serum glucose, liver aspartate aminotransaminase, or free thyroxine. The trichogram demonstrated 20.8% +/- 1.6% (mean +/- standard error) of telogen hairs in the alopecia group compared with 9.5% +/- 2.8% of the control group (P < 0.05). The hair density in the alopecia group was 52.8 +/- 4.1/cm2 and 79.6 +/- 14.3/cm2 in the control group. Skin biopsies in affected monkeys demonstrated increased telogen follicles, with no fibrosis or inflammation. There were no statistically significant differences in the dominance behavioral analysis. The findings are consistent with chronic telogen effluvium (CTE). A number of organic, behavioral, and dominance-related stress causes of CTE were excluded. CTE appears to be predominantly age-related in this population. CTE in female squirrel monkeys may serve as an animal model for human diffuse alopecia.     

Social interactions between adult male and infant rhesus monkeys in Nepal

In 1,506 hours of field observations on free-ranging rhesus monkeys in Kathmandu Valley, Nepal, in 1974 and 1975 18 cases of favorable social interactions between adult males and infants were observed. Eleven of these were brief encounters of play or grooming; seven were more extended cases of male care. One of the latter was a complete adoption of a neonatal orphan by a dominant male. This adoption was possessive and restrictive and it resulted in the death of the infant by starvation within three days. A similar adoption involving the same male occurred in 1976 and it also resulted in the death of the infant. Most of the favorable male-infant interactions occurred during the winter and spring when the infants were 6 to 12 months of age. These favorable social interactions involved eight males in six different troops, out of a total of about 48 males in 12 troops in our study population of approximately 600 monkeys. These observations are discussed in light of current sociobiological theories.     

中国现生六种非人灵长类和树鼩大脑两半球不对称性的比较研究

对中国现生六种灵长类动物：懒猴、猕猴、灰叶猴、川金丝猴、滇金丝猴、长臂猿以及与灵长类关系密切的树鼩的大脑两半球形态,功能的不对称性以及由此引起的行为不对称性进行了研究。结果表明：大脑两半球不对称现象均存在于上述几种动物中。因而,这种不对称性可能经历了一个长期演化历程。     

Exploration and play in howler monkeys (Alouatta palliata)

Exploration and play were observed in eight troops of howler monkeys (Alouatta palliata) containing 56 young and 95 adults. The behavior patterns of seven age classes are described. There was a clear trend for animals to spend less time in nonsocial exploration with increasing age, and for the frequency of social play to follow an inverted “U” pattern, peaking in the early juvenile stage at 15–30 min per day. The howlers' specialization for eating large quantities of difficult to digest plant matter affected their play: as the young became increasingly dependent on plant food around the infants stage, there was a shift in their playtimes to allow for the energy demanding activity of digestion. This and other aspects of howler behavior are related to a reinforcement theory of exploration and play.     

Copper,iron, manganese,and zinc content of hair from two populations of rhesus monkeys

The concentrations of the elements copper (Cu), iron (Fe), manganese (Mn), and zinc (Zn) in hair of caged (in Maryland) and freeranging (in Puerto Rico) rhesus monkey populations were determined. Significant chronological age-related decreases were evident for the trace elements Mn and Zn in both populations (P<0.01) and for Cu and Fe in free-ranging monkeys (P<0.005). The only overall gender difference was higher hair Mn concentration in freeranging males than in females (P<0.03). There were no significant differences in hair Cu, Fe, or Mn related to pregnancy status. Hair Zn was lower in samples from pregnant than from nonpregnant monkeys from the caged monkeys (P≤0.05), but did not differe in the freeranging monkeys. Comparison of the two populations revealed that hair Zn levels were significantly higher in caged vs free-ranging animals (P<0.001). We attribute this higher hair Zn in the caged monkeys to contact and ingestion of Zn from their galvanized enclosures. Hair iron levels were significantly higher (P<0.001) in free-ranging monkeys, possibly as a result of Fe-rich soil ingestion from their environment. These data support continued investigation of the use of hair as an indicator of the exposure of large groups or populations to potentially high levels of specific minerals, and the use of nonhuman primates as models for the study of trace element deficiency and/or toxicity in humans. Prelliminary reports of portions of these data were presented at the 69th Annual Meeting of the Federation of American Societies for Experimental Biology, April 1982, New Orleans, LA (B. M. Marriott, J. C. Smith, R. Jacobs, A. O. Jones, M. J. Kessler, and R. Rawlins,Fed. Proc. 41:770, [1982]) and in a symposium at the 6th Annual Meeting of the American Society of Primatologists, 1983, East Lansing, MI (B. Marriott, J. C. Smith, R. Jacobs, A. O. Lee Jones, R. Rawlins, and M. J. Kessler,Am. J. Primatol. 4(3): 157 [1983]; B. Marriott, J. C. Smith, Jr., R. M. Jacobs, A. O. Lee Jones, R. Rawlins, and M. J. Kessler, inThe Cayo Santiago Macaques, R. Rawlins and M. J. Kessler, eds., SUNY Press, Albany, NY, pp. 219–231 [1986]).     

Life history variables of wild troops of formosan macaques (Macaca cyclopis) in Kenting,Taiwan

A study on population dynamics of wild Formosan macaques (Macaca cyclopis) in Kenting, southern Taiwan, was conducted from March 1985 to August 1990. At first, only one monkey troop was studied. It fissioned in 1987 and both of the daughter troops have been observed since then. Total number of animals increased from 10 to 29 over the years, but the sizes of individual troops have never been more than 20. Seasonality in breeding has been detected: copulations were concentrated in the period from November to January and 75% of all the 28 births occurred between April and June. Time of birth by parous females without offspring from the preceding year was earlier than that of lactating females. Young females gave their first births at 4 or 5 years of age. Total birth rate over the study period was 0.8 infant per female per year. Hunting was the main cause of death while natural mortality rate was low for the animals. There was only one adult male in each troop for most of the time. Troop males in the two daughter troops have been replaced two or three times in the three years by some solitary males that moved around in the area. The reproductive parameters of Formosan macaques in Kenting were found to be more similar to that of rhesus monkeys than to Japanese macaques. And a case of higher reproductive success in a high-ranking matriline was reported.     

Does intermale mounting function as a dominance demonstration in rhesus monkeys?

The relationship between dominance and intermale mounting was analyzed in two troops of captive rhesus monkeys (Macaca mulatta). The data did not support the assumption that mounting among males functions as a dominance demonstration as described in the literature because mounting commonly (63% of 65 dyads) occurred in a bidirectional fashion, and mounting not only was performed by dominant males but also was shown with regularity (36% of 521 cases) by subordinate males. Intermale mounting was often (37% of 521 cases) associated with amicable interactions--commonly preceding them--but it was only rarely (2%) associated with dominance-subordination behaviors. It was concluded that intermale mounting may serve as a socially cohesive behavior in rhesus monkeys by promoting nonagonistic contact.     

The efficacy of diazepam treatment for the management of acute wounding episodes in captive rhesus macaques

The spontaneous development of self-injurious behavior (SIB) in singly housed monkeys poses a challenge for their management and well-being in captivity. Relatively little information is available on effective treatments for SIB. This study examined the effects of diazepam (Valium) on self-wounding and other abnormal behaviors in eight individually housed male rhesus monkeys (Macaca mulatta). Each monkey's response to an anxiolytic dose of diazepam (1 mg/kg or greater orally) was compared with the animal's behavior during drug-free periods. When examined across all animals, treatment with diazepam did not significantly alter wounding frequency or rates of self-directed biting without wounding. However, closer examination of the data revealed that four of the animals showed significant decreases in self-biting and wounding frequency (positive responders, PR group), whereas the remaining monkeys showed a trend towards increased wounding frequency (negative responders, NR group). Subsequent examination of colony and veterinary records demonstrated that compared with NR monkeys, PR monkeys had spent significantly more years in individual cage housing and had experienced a greater number of minor veterinary procedures. PR animals also were significantly less likely to have a documented history of self-biting behavior. Our findings suggest that SIB is not a homogeneous disorder in rhesus monkeys; rather, distinct subtypes exist that require different treatment approaches.     

Stereotypic and self-injurious behavior in rhesus macaques: a survey and retrospective analysis of environment and early experience

Abnormal behavior in captive rhesus monkeys can range from active whole-body and self-directed stereotypies to self-injurious behavior (SIB). Although abnormal behaviors are common in singly-housed rhesus monkeys, the type and frequency of these behaviors are highly variable across individual animals, and the factors influencing them are equally varied. The purpose of this investigation was to survey abnormal behavior in a large population of rhesus macaques, to characterize the relationship between stereotypies and self-injury, and to identify potential risk factors for these aberrant behaviors. Behavioral assessments of 362 individually housed rhesus monkeys were collected at the New England Regional Primate Research Center (NERPRC) and combined with colony records. Of the 362 animals surveyed, 321 exhibited at least one abnormal behavior (mean: 2.3, range: 1-8). The most common behavior was pacing. Sex differences were apparent, with males showing more abnormal behavior than females. SIB was also associated with stereotypies. Animals with a veterinary record of self-injury exhibited a greater number of self-directed stereotypies than those that did not self-injure. Housing and protocol conditions, such as individual housing at an early age, longer time housed individually, greater number of blood draws, and nursery rearing, were shown to be risk factors for abnormal behavior. Thus, many factors may influence the development and maintenance of abnormal behavior in captive primates. Some of these factors are intrinsic to the individual (e.g., sex effects), whereas others are related to colony management practices, rearing conditions, and research protocols.     

Hair pulling: a review

Hair pulling has been reported in humans, six different non-human primate species, mice, guineapigs, rabbits, sheep and muskox, dogs and cats. This behaviour seems to occur only in subjects who are confined in an artificial environment. It has been classified as a mental disorder in humans, as a behavioural pathology in animals. The hair is not only pulled but also, in most species, ingested. Hair pulling can be both self-directed and partner-directed, contains elements of aggression, manifests more often in females than in males, is associated with psychogenic distress, and resists treatment. Research data collected from affected animals are probably not normative, hence scientifically unreliable. The preemptive correction of husbandry deficiencies causing long-term stress may prevent the development of this bizarre behaviour in healthy subjects.     

Behavior of nursery/peer-reared and mother-reared rhesus monkeys from birth through 2 years of age

The behavior of 8 nursery/peer-reared and 16 mother-only reared rhesus macaques was observed between birth and 5 months of age, with follow-up studies conducted when the animals were 10–21 months old and living in large social groups. Nursery-reared neonates were more awake, active, and irritable than mother-only reared monkeys. From 1 to 5 months of age the nursery/peer-reared animals exhibited a greater variety of behaviors than the mother-only reared infants, which spent the majority of the time in ventral contact with mothers. As juveniles the groups were indistinguishable with the exception of more self-directed behaviors observed in the nursery/peer-reared monkeys. Both rearing conditions, by virtue of their atypicality, imposed restrictions on social development. The behavioral similarity of the juveniles while in the large social group may be a function of maturation or due to the rehabilitative effect of the large social group.     

Effect of nasal instillation of female urine or vaginal exudate on testosterone secretion in isolated and anesthetized male rhesus monkeys (Macaca mulatta)

Two male adult rhesus monkeys were individually placed in cages with a pulling device in order to immobilize the animals for anesthesia. The room was temperature-controlled having a light/dark period of 12/12 hours. The animals were rapidly immobilized and immediately anesthetized with ketamine i. m. (10 mg/kg of body weight). They were bled four times at 15, 30, 45, and 60 mins after the ketamine injection, twice a week during 6 weeks. When necessary, maintenance doses of ketamine were administered. The levels of serum testosterone in experimental conditions (nasal instillation of female urine or a suspension of vaginal exudate) showed significant lower values with respect to those in control conditions (saline instillation). The control levels of testosterone tend to increase up to 60 mins. The testosterone from samples obtained in experimental conditions did not show such an increase, remaining similar during the sampling and similar to the 15 min control levels that could be considered as basal. These results seem to point out some chemical information from females capable of modifying the pattern of secretion of testosterone of the males in the above mentioned experimental conditions.     

Effects of testosterone on the behavior of male cynomolgus monkeys (Macaca fascicularis)

To determine the threshold doses of testosterone propionate (TP) that cause clear-cut behavioral changes in the sexual behavior of castrated male cynomolgus monkeys, observations were made on three males during successive 5-week treatment periods while they received daily subcutaneous doses of 100 μg TP increasing in octaves to 25.6 mg TP. Males were tested with each of the same two ovariectomized, estrogen-treated females (6 pairs, 330 1-hr behavior tests). To mimic the diurnal plasma testosterone rhythm, TP injections were given at 1600 hr and blood samples were obtained at 0800 hr (141 samples). Male ejaculatory activity increased at the threshold dose of 200 μg TP per day giving plasma testosterone levels of 830 ng/100 ml, which is in the physiological range of 600–1600 ng/100 ml for intact males. This threshold dose was eight times higher than in rhesus monkeys on a dose per kilogram body weight basis. There was a further marked increase in ejaculatory performance at higher doses (6.4 to 25.6 mg) giving supraphysiological plasma levels of 4000–9000 ng/100 ml. There were individual differences in the behavioral changes occurring with TP treatment, and the female partner modulated the effects. These findings were generally similar to those obtained with male rhesus monkeys, but certain species differences were noted.     

Squirrel monkeys (Saimiri) in natural habitats in Panama,Colombia, Brazil,and Peru

Troops ofSaimiri (squirrel monkeys) were observed in 31 locations in natural habitats in Panama, Colombia, Brazil, and Peru. Troop size varied from 10 to 35 animals in Panama and Colombia and from 120 to 300 or more in the unaltered rainforests of Amazonia. Troop size correlated with forest size in all areas.Saimiri associated withCebus (capuchin monkeys) in several areas.Saimiri troops showed different responses to man, fear and flight or neutral responses or curiosity; and these correlated with local environmental conditions. Social behavior varied significantly between the large and small troops. Social interactions were much more frequent and individual distances were much smaller in the large troops than in the small troops. Several factors that may relate to these differences in sociability are discussed in light of data from this and other studies.     

Xenogeneic immunotherapy of transplantable guinea pig hepatoma with primate leukocyte lysates

Summary Injection of leukocyte lysates prepared from rhesus monkeys xenografted with syngeneic strain-2 guinea pig line 10 hepatoma cells had the ability to increase survival times in guinea pigs receiving lethal, metastasizing doses of the tumor cells. Immunotherapy of the line 10 hepatoma with these xenogeneic anti-line 10 leukocyte lysates resulted in 5 out of 11, or 45.4%, of the animals surviving tumor challenge. Substantially increased survival times were observed in groups of animals treated with lysates from normal or anti-line 1 hepatoma sensitized rhesus monkeys as well. All survivors possessed in vivo skin reactivity and in vitro positive cell-migration inhibition against the line 10 antigen and purified protein derivative. The survivors exhibited negative or marginal immune reactivity against line 1 antigen, strain-2 salt-extracted liver antigen, and a nonspecific antigen, keyhole limpet hemocyanin (KLH). Intact leukocyte lysates from line 10 xenografted baboons, rhesus monkey lysate dialysates, RNA extracts of leukocyte lysates, or lysates of nonlymphoid liver cells obtained from line 10 sensitized rhesus monkeys all failed to extend survival times significantly in strain-2 guinea pigs bearing the line 10 tumor.     

重组霍乱毒素B亚基与疟原虫多表位融合蛋白的免疫保护作用研究

对以霍乱毒素B亚基为载体蛋白的重组疟疾多价抗原在小鼠及恒河猴中的免疫原性及对相应疟原虫感染的免疫保护作用进行了研究。结果表明：该抗原免疫小鼠后,对约氏疟子孢子攻击的保护率在50%左右;恒河猴免疫后用1×10⁸食蟹疟裂殖子攻击,对照组2只动物在攻击后4d感染,感染持续30d以上;免疫组2只动物中,两只动物在感染6～7d后完全恢复,且1只推迟3d感染,说明该抗原具有免疫保护作用。     

A functional analysis of social grooming patterns through direct comparison with self-grooming in rhesus monkeys

Social grooming in primates is a complex behavior in which monkeys stroke, pick, or otherwise manipulate a companion’s body surface. While grooming has been associated with important social functions, researchers who have examined its physical characteristics, such as body site preferences, have focused on its role in skin care and ectoparasite removal. Whether the form of social grooming is constrained primarily by utilitarian or social functions was empirically tested by directly comparing this behavior with self-grooming, which was assumed to have primarily utilitarian functions. Predictions made concerning social grooming, based on a comparison with self-grooming, were tested by examining site preferences, duration of grooming (overall and to specific body sites), and method of grooming (stroking, picking, or a combination of the two) in rhesus monkeys. None of these predictions was verified. The physical characteristics of social grooming could not be predicted from the way an animal groomed itself. There was no relationship between site preferences in these two types of grooming. Animals groomed others for longer periods of time than they groomed themselves, both overall and when grooming specific sites. The methods these animals used differed markedly in self-and social grooming: they primarily picked at their own hair or skin but, when grooming others, varied their technique across sites, stroking the hair where it was thickest and picking where the hair was sparse. These results suggest that utilitarian functions are not the most important factors constraining the form of social grooming.