Rearing infant monkeys (Macaca nemestrina) in pairs produces deficient social development compared with rearing in single cages

Many scientists and colony managers assume that social housing is a beneficial living condition for all captive primates. Several older studies of primate development question the generality of this assumption. We recently tested this assumption by comparing the social development of pigtailed macaque infants raised in pairs and those that were raised in individual cages. All animals received 30 min of daily socialization in a playroom. Infants paired from postnatal week 3 through month 4 developed a playroom behavioral repertoire consisting largely of mutual clinging, fear, and social withdrawal. This was especially true of females. Unlike the singly caged infants, pair-reared monkeys did not successfully adapt to living in a large social group at 8–10 months of age. In this situation, pair-reared infants were subordinate and spent almost all of their time huddling on the pen floor. It was concluded that rearing macaque infants in pairs produces a behavioral repertoire that is maladaptive with respect to social development.     

人工饲养条件下死亡实验恒河猴肠道病理改变特点分析

目的观察人工饲养条件下实验恒河猴肠道病理改变,探讨实验猴肠道疾病分布规律和病理改变特点,丰富实验猴自发病变基本研究资料。方法对1998-2008年云南地区饲养的自然死亡的155只恒河猴（年龄2-20岁）的肠道进行病理检查,按年龄分为幼年组、成年组、老年组,并对观察结果进行统计学分析。结果155例恒河猴中58例检出肠道病变,有慢性肠炎、急性肠炎、黏膜充血水肿、出血、糜烂、溃疡、穿孔、寄生虫共8种主要病变,出现率最高的为急性肠炎（20．00％）。实验猴不同年龄组肠道病变类型分布基本相同,肠道病变率随年龄增长而增高,不同年龄组间统计学分析差异无显著性。结论人工饲养条件下死亡实验猴肠道病变检出率较高,急性肠炎是实验猴的主要致死原因之一,实验猴肠道病理改变随年龄增长而病变加重。对实验猴饲养和研究时,应重视肠道病变因素,尤其是急性肠炎。死亡实验猴肠道病变研究对实验猴的质量控制和相关动物实验有重要指导价值。     

人工饲养条件下死亡恒河猴肺脏病理改变分析

目的观察人工饲养条件下实验恒河猴肺脏病理改变,探讨实验猴呼吸系统疾病分布规律和病理改变特点,丰富实验猴自发病变基本研究资料。方法对1998～2008年云南地区饲养的自然死亡的155只恒河猴（年龄2～20岁）的肺脏进行病理检查,按年龄分为幼年组、成年组、老年组,并对观察结果进行统计学分析。结果实验猴肺脏主要病变有大叶性肺炎、支气管肺炎、间质性肺炎、肺气肿、支气管扩张症、胸膜炎、肺肉芽肿性炎等12种,出现率最高的为支气管肺炎（18.71%）和大叶性肺炎（16.74%）。恒河猴肺脏病变在不同年龄阶段均有发生,老年猴组肺脏病变发生率最高,疾病类型和发生率在不同年组中分布不相同,统计学分析显示：支气管炎病变成年组发病率明显高于幼年组;肺气肿病变老年组明显高于成年组和幼年组,（P〈0.05）。结论人工饲养条件下死亡实验猴肺脏病变检出率较高,实验猴肺脏病变在不同年龄阶段存在差异,实验猴肺脏病理改变结果丰富了实验猴的基本研究资料,对实验猴的质量控制和相关动物实验有重要价值。     

Effects of manipulatable objects on the activity of captive capuchin monkeys (Cebus apella)

The aim of this study was to evaluate simple behavioral enrichment procedures for a captive group of tufted capuchin monkeys (Cebus apella). We examined the effects of providing a manipulatable substrate (straw) and a variety of portable objects in the monkeys' home cage. The animals were observed across three conditions in two replications: 1) No portable objects were present; 2) a set of six identical portable objects was present; and 3) a set of six varied portable objects was present. The cage floor was bare in the first replication; straw was uniformly spread on the cage floor in the second replication. An 18-month period of qualitative note taking followed completion of the initial data collection phase. The presence of straw and portable objects affected patterns of affiliation by decreasing quiet contact and close proximity. Providing additional manipulative opportunities affected both the form and frequency of object-directed activities. Object contacts were directed toward a greater variety of targets, and some objects were spontaneously used as tools. Manipulation of provided objects and use of objects as tools have become routine activities in this group of monkeys. We conclude that providing straw and portable objects in an already well equipped cage is an effective means of long-term behavioral enrichment for captive capuchin monkeys. Enabling captive capuchins to express species-typical manipulative tendencies is apparently conducive to the monkeys' optimal physical and psychological well-being as well as interesting to the human observer.     

Voluntary progression order in captive rhesus macaques

The sequence in which 14 laboratory rhesus macaques left their home enclosure during a routine catching procedure was recorded on 30 occasions during 6 weeks. The animals were trained to voluntarily exit one by one and enter a transport cage for weighing and/or treatment. Mean weekly exit orders cross-correlated significantly, and individuals retained their exit positions with remarkable consistency throughout the study period. An animal's position did not depend on its sex, age, or dominance rank. The oldest female never failed to enter the transport cage as number 1. When she was prevented from taking the lead, the group was hesitant but eventually proceeded in the usual order. Food was a strong, yet not absolute, incentive for the monkeys to cooperate. If they could not expect a reward, they took more time before proceeding, but did so in the habitual order. The predictability of the exit sequence has practical managerial value because it makes it possible for a single person to quickly catch a selected group member when necessary.     

The effect of roads on spider monkeys’ home range and mobility in a heterogeneous regenerating forest

Arboreal fauna living in tropical ecosystems may be particularly affected by roads given their dependency on forest cover and the high vulnerability of such ecosystems to changes. Over a period of 4 yr, we followed subgroups of spider monkeys living in a regenerating dry tropical forest with 8.2 km of roads within their home range. We aimed to understand whether roads shaped the home range of spider monkeys and which road features affected their movement. Only 18 percent (3 km) of the spider monkeys’ home range perimeter bordered with roads; these roads had greater habitat disparity between road sides than roads inside the home range. Although monkeys were reluctant to be close to roads, and roadside habitat contained low proportions of mature forest, spider monkeys crossed roads at 69 locations (7.5 crossings per kilometer). The main road characteristic affecting crossings was canopy opening size, with greater probability of crossing where canopy openings were smaller. Our findings support the importance of canopy opening size for road crossing of arboreal taxa, but they also indicate the relevant role roadside forest structure may have. Minimizing canopy opening size and forest disturbance along roads can facilitate the movement of arboreal fauna and preserve the important role of spider monkeys and other arboreal taxa in seed dispersal and thus the maintenance and regeneration of forest diversity.     

Nutrient Balancing by Captive Golden Snub-Nosed Monkeys <Emphasis Type="Italic">(Rhinopithecus roxellana</Emphasis>)

An organism’s fitness is tied closely to its ability to obtain food. However, many foods are nutritionally suboptimal on their own, forcing an individual to develop a feeding strategy that actively manages both type and amount of food consumed. Animals in captivity are additionally limited to human provisioned diets, which may be nutritionally inadequate and negatively affect behavior and health. We studied the nutritional intake of captive golden snub-nosed monkeys (Rhinopithecus roxellana) at two locations in China (132 days of continuous, sunrise to sunset focal samples of 7 individuals at each site) and used the Geometric Framework for nutrition to identify their feeding strategy and evaluate diet variation across sites, seasons, and age–sex classes. Captive golden snub-nosed monkeys had a mean nutrient intake of 75% carbohydrates (15% neutral detergent fiber, 60% total nonstructural carbohydrates), 12% fat, and 13% protein (by energy) that differed by location and season owing to differences in the type and amount of food items offered and consumed. Intake at one location differed from that of wild golden snub-nosed monkeys, suggesting that the captive diet was inadequate. These results highlight the importance of developing nutritionally adequate diets for captive animals based on an understanding of their nutritional requirements.     

Reproductive performance in a breeding colony of Brazilian squirrel monkeys (Saimiri sciureus).

In a captive colony of Brazilian squirrel monkeys (Saimiri sciureus) a discrete birth season has been retained for 5 years although its duration increased from 3 months in 1972 to 6 months in 1976. The ages of breeder females in this colony ranged from 3 to 14 years, and within this range reproductive performance was not affected by age, although it was significantly better in feral than in colony-born females. The latter had a lower pregnancy rate and a higher incidence of neonatal and fetal deaths than did the feral monkeys. It is our belief that the reproductive and maternal capabilities of the colony-born females were adversely affected by the practice of removing neonates from their mothers at weaning and raising them with age-mates.     

Fecal Bacterial Composition of Sichuan Snub-Nosed Monkeys (<Emphasis Type="Italic">Rhinopithecus roxellana</Emphasis>)

The intestinal microbiota plays an important role in maintaining the health of its host, including human and nonhuman primates. Little is known about the intestinal bacterial composition of the Sichuan snub-nosed monkey (Rhinopithecus roxellana), which has been classified as Endangered on the International Union for Conservation of Nature Red List since 2003. We evaluated the fecal bacterial compositions of 11 Sichuan snub-nosed monkeys, including six young captive individuals (one sample from each), three adult captive individuals (four samples each), and two adult provisioned free-ranging individuals (four samples each). We also quantified fecal Bacteroides vulgatus, Bifidobacterium spp., and Lactobacillus spp., which are defined as probiotics in humans, using real-time polymerase chain reaction. We identified five major phyla in the collected samples, including Firmicutes (32.4 %), Bacteroidetes (14.7 %), Verrucomicrobia (8.8 %), Actinobacteria (4.4 %), and unclassified microbacteria (39.7 %). Fecal bacteria composition varied with age and different seasons. The fecal bacterial composition of the captive monkeys was less variable than that of provisioned free-ranging monkeys. B. vulgatus amounts were almost 100 times higher in the provisioned free-ranging monkeys (10¹²) than in the captive monkeys (10¹⁰). Our results provide an initial catalogue of gut microbiota in the Sichuan snub-nosed monkey, which helps to enrich our knowledge of gut microbiota in nonhuman primates.     

Factors influencing reproductive success and litter size in captive island foxes

A severe decline of island foxes (Urocyon littoralis) on the northern Channel Islands in the 1990s prompted the National Park Service to begin a captive breeding program to increase their numbers. Using detailed records of all the fox pairs (N = 267) that were part of the program on San Miguel, Santa Rosa, and Santa Cruz Islands from its inception in 2000 through 2007, we identified factors influencing the breeding success of pairs in captivity in the interest of formulating strategies that could increase captive productivity. We compiled a database of variables including litter size, reproductive success, distance to nearest occupied pen during the breeding season, subspecies, exposure, female age, male age, age difference, female and male origin (wild vs. captive born), same versus different origin, years paired, previous reproductive success by the pair, previous reproductive success by the female, mate aggression-related injuries, male previous involvement in a pair with mate aggression, and female previous involvement in a pair with mate aggression. We used multiple linear regression to identify factors predictive of litter size, and logistic regression to predict the probability of reproductive success. A larger inter-pen distance, older male age, less exposure, and a smaller intra-pair age difference positively affected litter size. The probabilities of reproductive success increased with fewer years paired and less exposure. Comparatively, pairs with wild born females (vs. captive born females), and previously successful pairs (vs. previously unsuccessful and new pairs) were most likely to be successful. These results indicate that the optimal situation was to pair wild-caught females with older males in sheltered pens that were as far from other pens as possible, to maintain successful pairs and repair unsuccessful ones. Published 2013. This article is a U.S. Government work and is in the public domain in the USA.     

Compound grips in tufted capuchin monkeys (Sapajus spp and Sapajus libidinosus)

An experimental study with captive individuals and study of video recordings of wild monkeys explored whether and how tufted capuchin monkeys use onehand to hold one or more objects with multiple grips (compound grips). A task designed to elicit compound grip was presented to five captive tufted capuchin monkeys (Sapajus spp). The monkeys held one to four balls in onehand and dropped the balls individually into a vertical tube. Multiple simple grips and independent digit movements enabled separate control of multiple objects in one hand. Monkeys always supported the wrist on the horizontal edge of the tube before releasing the ball. Increasing the number of balls decreased the likelihood that the monkeys managed the task. Wild bearded capuchins (Sapajus libidinosus) used compound grips spontaneously to store multiple food items. Compound grips have been described in macaques, gorillas, chimpanzees, and humans, and now in a New World primate. We predict that any primate species that exhibits precision grips and independent digit movement can perform compound grips. Our findings suggest many aspects of compound grip that await investigation.     

Mirror reactions in a zoo colony of Cebus monkeys

The extensive research investigating the reactions of a number of species of nonhuman primates to their mirror images has revealed that monkeys have never been observed to react with self-directed behaviors, as have some species of higher apes. The intermittent exposure of captive Cebus monkeys to a mirror over a 5-week period produced species-specific social reactions to the mirror, supporting the suggestion that at least in some instances the monkeys were viewing their mirror image as a conspecific. The variability in the duration and expression of mirror-directed behaviors observed in the study appeared to be related to the age and past experience of the monkeys. The duration of mirror viewing of subadults was over twice that of the adults, while the young, hand-reared animals exhibited more manipulative and fewer social behaviors than did the young animals raised in the zoo. The average viewing time of the zoo colony decreased substantially over the course of the study but the monkeys were still spending an appreciable time at the mirror after 5 weeks.     

Changes in blood chemistry and hematology variables during aging in captive rhesus macaques (Macaca mulatta)

Identifying changes with age in physiological variables of captive nonhuman primates will aid in the proper treatment and clinical diagnosis of these animals, as well as enhance our understanding of nonhuman primate models for human aging. Information for 33 physiological variables was obtained from the Primate Aging Database, a multi-centered database being developed for clinical and research use. Using multiple regression analyses, we investigated the relationship of age to hematological variables, blood chemistry and body weight in 345 captive rhesus monkeys (age range 7-30 years) from three different primate research facilities. The analyses revealed that 15 of these variables show a significant relationship with chronological age and are altered in older as compared with adult animals. Here we present the first phase of a project that will: a) identify changes with age in physiological variables among adult captive rhesus macaques; and b) characterize normative values for the aging rhesus population.     

Influence of vertical panels on use of space by domestic fowl

In the wild, cover is used by animals to seek shelter from the elements, protection from predators and aggressive conspecifics and as a way to reduce inter-animal communication. Rearing environments for captive raised fowl often contain open areas that are lacking in complexity and that are greatly underused. As a result, use of space within pen-type enclosures is often not uniform. This paper investigates the effect of increased environmental complexity on the use of space by broilers. The experiment consisted of three cover treatments (mesh panels, frame panels and no cover) and three group sizes (80, 110 and 140). The vertical panels, constructed of PVC piping, were positioned in pen centers, while the pen centers in the no cover treatment were left empty. It was hypothesized that the provision of vertical panels to pen centers would attract birds into the central space and would lead to a more uniform distribution of birds. Using a grid-coordinate system set up in each pen, scan samples were taken on the use of space in each pen four times per day, 3 days per week from 5 to 44 days of age. Use of space in the central region for the two cover treatments was significantly higher than for the no cover treatment (P<0.0001). The effect of cover treatment on the mean percentage of birds using the central space was influenced by age (P<0.0001) and by group size (P<0.05). Differences in the use of space between the frame and mesh treatment were only found during week 1. In the side, end and middle regions surrounding the panels, use of space was influenced by cover treatment and age (P<0.0001). Over 80% of the use of pen center occurred at the ends and sides of the panels. These results support the hypothesis that the presence of vertical panels results in a more uniform distribution of birds within the pen by increasing the number of birds using the center.     

Influence of regional crossbreeding between rhesus macaques on the rate of weight gain of their offspring

To evaluate potential heterosis resulting from breeding between rhesus macaques of Chinese and Indian origin in a captive social group, the rates of weight gain of Indian (nonhybrid) rhesus monkeys were compared with those of their hybrid (half Chinese/half Indian) peers. The coefficients for the linear regression of age on weight were estimated for each animal for each exact age between 1 and 4, when that regression is strictly linear, at which he/she lived in the group. The average rates of weight gain of hybrids and nonhybrids were compared using the t statistic. Both male and female hybrids exhibited statistically significantly higher rates of weight gain than their nonhybrid peers before, but not after, age 4. No evidence could be found that either hybrid status or rate of weight gain increases fitness, at least under captive conditions. © 1994 Wiley-Liss, Inc.     

Movement out of home range and disturbed behavior patterns in a group of bonnet monkeys: Macaca radiata

A free living group of bonnet monkeys unnaturally and unusually moved far out of its established home range. The movement in this new habitat made the behavior of these monkeys abnormal. They did not follow any ordered pattern of group movement and any regular pattern of everyday activities. The social behavior and social communications were highly disturbed. The monkeys appeared to be scared, shy and suspicious. The death of four members during a 37-day-trip was an abnormally high rate of mortality.     

Effects of positive interaction with caretakers on the behaviour of socially housed common marmosets (Callithrix jacchus)

Every aspect of the life of the captive non-human primates should be carefully attended to, as updated refinement concept recommends. Interaction with humans as environmental enrichment for these animals is believed to be of value, but it has been subject to little quantitative evaluation. This study investigates the effects of positive interaction with humans on the behaviour of a captive colony of common marmosets (Callithrix jacchus). The study was composed of two phases: baseline condition, where the interaction with humans was represented by routine care and management; and a second phase (‘Human Interaction Effects’), in which a familiar caretaker spent additional 20 min per day with each family, interacting actively and positively with the monkeys. In order to assess potential durable effects of such interaction, data were collected only when caretaker was absent. Between the two phases, a period of interaction 4 weeks long per family took place with the caretaker. The sampling method used was a 10 s scan sampling, with daily sessions 30 min long. Following the period of additional interaction with caretaker, the marmosets showed an increased level of grooming and playful activities, generally considered signs of increased level of welfare; however, they also showed lower levels of self-scratching and locomotion. A trend towards reduced contact vocalizations was also observed. These results suggest that simple, unstructured positive interactions between humans and marmoset monkeys may be part of a program aimed at maximising the level of welfare of captive non-human primates.     

Relationship between the behaviour of sows at 6 months old and the behaviour and performance at farrowing

Piglet crushing remains a major problem in pig production. Reduced crushing might be obtained through genetic selection on sow behavioural traits. The aim of the study was to assess the relationship between behavioural responses at 6 months of age, around farrowing, and sows' reproductive performance including crushing levels. At 6 months of age, behavioural responses of 75 nulliparous sows were observed both during behavioural tests to human presence and to the presence of a novel object in their home pen, and their responses when placed in a weighing device. At first farrowing, nervousness of the sows was observed when placed in the farrowing crate 1 week before and the day of farrowing, as well as their fear responses when approached by a human from behind or at the front of the farrowing crate. At 6 months of age, escape from a human tended to be correlated with the reactivity in the weighing device (rs = 0.21, P = 0.09). Around first farrowing, the withdrawal reaction when a human approached at the front was correlated with the fear response when approached from behind and the nervousness of the sow in the crate (rs = 0.29, P < 0.05; rs = 0.37, P < 0.01). The fear response when approached from behind was correlated with nervousness in the crate and around farrowing (rs = 0.70, P < 0.001; rs = 0.25, P < 0.05), and nervousness in the crate was significantly correlated with the nervousness around farrowing (rs = 0.34, P < 0.01). The escape from a human at 6 months was correlated with withdrawal when approached from the front before farrowing (rs = 0.38, P < 0.01) and with nervousness of the sow in the crate (rs = 0.24, P < 0.05). The number of piglets crushed at first farrowing was correlated with the latency to approach a novel object at 6 months and nervousness around farrowing (rs = -0.27, P < 0.05; rs = 0.28, P < 0.05), and tended to be correlated with the escape behaviour from human at 6 months and withdrawal away from human presence before farrowing (rs = 0.21, P = 0.09; rs = 0.22, P = 0.08). These results suggest that behavioural responses to humans and during management practices of nulliparous sows at 6 months of age are, to some extent, related with their behaviour around farrowing and crushing levels of piglets at farrowing.     

Reproduction of the owl monkey (Aotus spp.) in captivity

Abstract: The reproduction performance of captive owl monkeys, a breed used extensively in biomedical research, was observed at the Battelle Primate Facility (BPF). The colony grew through captive breeding, imports from the Peruvian Primatological Project, and others to a peak size of 730. It included seven karyotypes of Aotus sp. Results showed that owl monkeys can breed successfully in a laboratory in numbers sufficient to sustain modest research programs. Reproductive success increases when pairs are compatible, of the same karyotype, and stabilized; however, mated pairs of different karyotype are also productive. Under conditions of controlled lighting and heating, owl monkeys at BPF showed no birth peak nor birth season.     

Computer-task testing of rhesus monkeys (Macaca mulatta) in the social milieu

Previous research has demonstrated that a behavior and performance testing paradigm, in which rhesus monkeys (Macaca mulatta) manipulate a joystick to respond to computer-generated stimuli, provides environmental enrichment and supports the psychological well-being of captive research animals. The present study was designed to determine whether computer-task activity would be affected by pair-housing animals that had previously been tested only in their single-animal home cages. No differences were observed in productivity or performance levels as a function of housing condition, even when the animals were required to “self-identify” prior to performing each trial. The data indicate that cognitive challenge and control are as preferred by the animals as social opportunities, and that, together with comfort/health considerations, each must be addressed for the assurance of psychological well-being.