Adjustments and adaptations to indoor and outdoor environments: Continuity and change in young adult rhesus monkeys

Optimal environments for captive primates are assumed to be those which simulate certain ecological features and elicit a wide range of species-typical behavior patterns. Outdoor environments are often thought to be more suitable than indoor environments in that they provide more space and potentially higher levels of stimulation. The purpose of this study was to compare the long-term behavioral responses of several groups of animals that had been reared identically during the first two years of life and then exposed to different environments. Two groups were moved into separate “enriched” indoor pens while one group was moved to an outdoor area covering approximately 5 acres. The monkeys were observed during the first year of life and again in these different environments between the ages of 6 and 10. Although behaviorally similar during the first year of life, monkeys developed different response patterns to indoor and outdoor environments. Contrary to commonly held views, indoor monkeys were not more aggressive, nor did they show higher levels of stereotypical behavior. Instead, indoor monkeys exhibited higher levels of grooming, sexual posturing, tactile/oral exploration, and passive visual behavior than their outdoor counterparts. These differences are consistent with the reconciliation model of de Waal. Individual monkeys also showed remarkable stability in certain traits over the 5-year period. © 1992 Wiley-Liss, Inc.     

Nature Needs Nurture: The Interaction of Hormonal and Social Influences on the Development of Behavioral Sex Differences in Rhesus Monkeys

Thirty years of research on early social and hormonal environments and their relationship to the expression of behavioral sex differences in rhesus monkeys are reviewed. These studies demonstrate that whether aggressive and submissive behaviors are sexually dimorphic depends primarily on the social and not the hormonal environment. Early rearing environments without mothers or allowing brief periods of peer interaction produced higher levels of male aggression and female submission. Presenting behavior was expressed more by females than males in environments with high male aggressivity and female submissiveness. No sex differences in presenting occurred in low aggressivity environments, unless monkeys were reared isosexually, when males presented more than females. Rough and tumble play and foot-clasp mounting were consistently exhibited more by males than females across all rearing environments studied, but rearing environment affected the degree of the sex difference. When reared isosexually males displayed less, and females more, foot-clasp mounting than when heterosexually reared. No social environment increased the low frequency of female rough and tumble play. Suppressing neonatal androgen in males did not effect any sexually dimorphic behavior. Prenatal androgen administration to genetic females masculinized many aspects of their juvenile behavior, consistently increasing rough and tumble play and foot-clasp mounting across different social environments. Thus the sexually dimorphic behaviors which showed the smallest variability across social contexts were the most profoundly affected by the prenatal hormonal environment. These studies demonstrate that the expression of consistent juvenile behavioral sex differences results from hormonally induced predispositions to engage in specific patterns of juvenile behavior whose expression is shaped by the specific social environment experienced by the developing monkey.     

Social interactions of monkeys reared in a nuclear family environment versus monkeys reared with mothers and peers

Four-year-old laboratory-born rhesus monkeys that had been reared in a nuclear family social environment consisting of mothers, fathers, siblings, peers, and other adults of both sexes were permitted to interact in various combinations with equal-aged monkeys that had been reared in an environment consisting of only mothers and peers. It was found that in most interaction sessions nuclear family subjects exhibited significantly higher levels of dominance and activity behaviors and significantly lower levels of submissive and passive behaviors than the mother-peer-reared subjects. These differences were not evident when subjects were tested within their own rearing groups. The significance of the results with respect to previous and future studies of social development in differential social environments is discussed.This research was supported by grant No. MH-11894 from the National Institute of Mental Health to the University of Wisconsin Primate Laboratory, by the Grant Foundation, and by grant No. RR-0167 from the National Institutes of Health to the University of Wisconsin Primate Research Center.     

Sexual behavior of laboratory- and wild-born male Rhesus monkeys.

Rearing method has an important influence on the sexual performance of adult male rhesus monkeys. Testosterone levels and sexual behavior of laboratory-born and -reared adult males were compared with those of males born in the wild and brought to the laboratory as adults. The mean sexual performance level of colony-reared animals was significantly below that of males born in the wild but testosterone levels in the two groups did not differ significantly. Not all laboratory-reared males were sexually inadequate but less than 30% ejaculated in tests of sexual behavior. The sexual behavior and testosterone levels of adult males treated prenatally with testosterone propionate were found not to differ from those of untreated males reared in the same way. Conclusions about sexual adequacy based on 10-mm tests of sexual behavior differed very little from those based on 1-hr tests.     

Effects of rearing on aggression and subordination in papio monkeys

The objective of this study is to assess the effects of short-term maternal deprivation (birth to 12 weeks) followed by peer group rearing on the development of aggressive and subordinate behaviors in papio monkeys (superspecies – Papio cynocephalus). Nursery reared monkeys (34 males and 30 females) were compared with mother-peer reared monkeys (11 males and 12 females) in late infancy (6 to 12 months of age) and at the end of their juvenile stage (36 to 42 months of age) in social groups composed of 75% nursery reared subjects and 25% mother reared subjects. Focal animal data were analyzed with a repeated measure ANOVA model. In general, the nursery reared infants tended to be less aggressive than mother-peer reared infants and performed less dominance behaviors, such as displace. Significant sex differences were present in the performance of aggressive (♂ > ♀) and subordinate (♂ > ♀) behaviors. Significant age differences were observed, with infants having consistently higher rates of performance.     

A preliminary study of food transfer in Sichuan snub-nosed monkeys (Rhinopithecus roxellana)

Food transfer happens regularly in a few nonhuman primates species that are also characterized by remarkable social tolerance. Sichuan snub-nosed monkeys (Rhinopithecus roxellana), or golden monkeys, which exhibit high social tolerance in their social relationships are thus of interest to see whether tolerance would extend to food transfer. In this study, branch feeding activity was observed in a semi-captive group of Sichuan snub-nosed monkeys, which consisted of 10 subjects that included a one-male unit (OMU) and an all-male unit (AMU). We recorded 1,275 food interactions over 27 days, and 892 instances of food transfer. The most commonly observed types of food transfer behavior were co-feeding (62.1%) and relaxed claim (22.8%). Of 892 food transfers, 756 (84.8%) took place in the OMU, most of which were among adults (34.7%) and among juveniles (42.1%). The transfer success rate was high in both the cases (87.9% for adults and 78.9% for juveniles). Food transfer in the AMU took place less often than that among adults in the OMU though with similar high transfer success. Food transfer between the OMU and AMU was limited to juvenile males from the OMU and adults from the AMU. These results provide the first evidence of food transfer in golden monkeys and suggest that tolerant social relationships in golden monkeys make transfer possible.     

The influence of rank on affect perception by pigtailed macaques (Macaca nemestrina)

Previous studies of affect perception in nonhuman primates have involved young animals and/or manipulations of early experience. Based upon data suggesting that middle-ranked monkeys in small social groups show patterns of behavior different from their low- or high-ranked counterparts, the current study examined the role of social rank in affect perception by normally reared, adult female pigtailed macaques. Employing color videotapes as the presentation medium, we observed animals as they watched unfamiliar animals display social (aggressive or submissive) or nonsocial behavior. Virtually all threats were recorded as the subjects watched the submissive presentations, and most submissive signals occurred while watching aggressive behavior tapes. Middle-ranked monkeys were most attentive during all presentations, and levels of disturbance behavior were related to rank of the watcher and type of presentation observed. The results suggest that dominance status is an influence in the process of affect perception.     

Sex differences in play behavior in juvenile tufted capuchin monkeys (Cebus apella)

According to the motor training hypothesis, play behavior in juvenile primates improves motor skills that are required in later adult life. Sex differences in juvenile play behavior can therefore be expected when adult animals assume distinct sexually dimorphic roles. Tufted capuchin monkeys show sexually dimorphic levels of physical antagonism in both inter- and intra-group encounters. Accordingly, it can be predicted that juvenile capuchins also show sex differences in social play behavior. To test this hypothesis, the play behavior of nine juvenile and two infant capuchins was examined. As predicted, juvenile males showed significantly higher levels of social play (wrestle, chase) than juvenile females, but no differences were found in nonsocial play (arboreal, object). Levels of infant play behavior were comparable to that of juveniles. These results lend support to the motor training hypothesis and highlight the need for more detailed investigations of individual differences in play behavior. An erratum to this article can be found at     

Space use selectivity by chimpanzees and gorillas in an indoor-outdoor enclosure

Understanding the relationship between physical environments and nonhuman primate behavior is a key element for effective care and management in a range of settings. The physical features of the captive environment, including not only gross useable space but also environmental complexity, can have a significant influence on primate behavior and ultimately, animal welfare. But despite this connection, there remains relatively little conclusive data on how captive primates, especially great apes, use the spaces provided to them, especially in modern, indoor-outdoor enclosures that have become more prevalent in recent years. In this study, we used four years of detailed data on where 23 great apes (chimpanzees and gorillas) positioned themselves within a modern, indoor-outdoor zoo enclosure to determine not only how the apes utilized their space but also how access to outdoor areas affected their spatial selectivity. We found that both species used relatively little of their available space: chimpanzees and gorillas spent half their time in only 3.2 and 1.5% of their useable three-dimensional space, respectively. Chimpanzees utilized the outdoor space more than gorillas, but access to the outdoors did not affect space selectivity in the indoor area for either species. Although both species of ape were highly selective in their space use, consideration should be given to the importance of providing the choice to locate in a variety of spaces, including outdoor areas. These data represent an extremely detailed account of space selectivity by great apes in an indoor-outdoor environment and have substantial implications for future facility design and captive primate management.     

Behavioral effects of enrichment on pair-housed juvenile rhesus monkeys

Among captive primates, inanimate environmental enrichment can lead to measurable changes in behavior indicative of an improvement in psychological well-being. Although this has been demonstrated repeatedly for singly caged primates, the relationship is not as well studied for pairhoused animals. Study of the pair-housed setting has become increasingly relevant because of the social housing mandate of the Animal Welfare Act regulations. We therefore observed 68 juvenile rhesus monkeys born in 1988 and 1989 and living in mixed-sex pairs from the ages of 2 to 3 years. All pairs were compatible. Half of the pairs received two types of enrichment, while the remaining pairs served as controls. Enriched and control juvenile subjects differed in the amount of time that they spent being inactive, playing, and drinking, but did not differ in the amount of time they spent interacting with their partner. Grooming and play were the two most common socially directed activities in both groups, a species-appropriate pattern. Males played more and vocalized less than did females. Overall, enriched and control subjects spent equivalent amounts of time located within a social distance of one another, but there was some difference between groups in allocation of behaviors while near the pairmate. Environmental enhancers were frequently utilized, and led to relatively small changes in behavior between control and enriched subjects, suggesting that the presence of a partner for juvenile rhesus monkeys acts as a form of enrichment that may dilute the effects of inanimate environmental enhancements. © 1994 Wiley-Liss, Inc.     

Foraging Ontogeny is not Linked to Delayed Maturation in Squirrel Monkeys (Saimiri sciureus)

The acquisition of complex foraging behaviors by young is a proposed cause of a prolonged juvenile phase in many vertebrates, including primates. I compared the foraging behaviors of infant, juvenile and adult squirrel monkeys to determine if significant age‐related differences in foraging behavior and efficiency were present. Infants and juveniles differed from each other in patterns of prey and fruit foraging, but few differences existed between juveniles and adults. Despite differing in the use of foraging substrates, young juveniles (8–12 mo) were as efficient as older juveniles (1–4 yr) and adults at capturing and processing large prey. Young juveniles (<1 yr) were limited in their ability to consume husked palm fruits due to an inability to peel them to obtain pulp. By 1 yr of age, however, foraging behaviors of adults and juveniles were nearly indistinguishable. The absence of meaningful differences between adults and juvenile foraging is not consistent with the hypothesis that the need to develop foraging skills accounts for the pattern of extended juvenility in squirrel monkeys.     

The Development of Local Song Preferences in Female Cowbirds (Molothrus ater): Flock Living Stimulates Learning

We carried out two experiments across 2 yr on song perception in female cowbirds (Molothrus ater). In the first experiment, juvenile and adult female brown‐headed cowbirds, living in same‐sex flocks in outdoor aviaries, were periodically tutored with recordings of local male cowbirds’ songs. In the spring, four adult male cowbirds were placed with half of the females for a 12‐d period. We then tested song preferences of all females by measuring copulation solicitation displays during the breeding season. We found that the females exposed only to tape‐tutor songs preferred those songs to those of the unfamiliar males used as companions and that the females allowed to interact with males preferred their songs over the familiar tape‐tutor songs. These data establish the modifiability of female cowbirds’ song preferences at the level of local song. In a second experiment, we studied the playback responses of juvenile females, hand‐reared from the egg, who were tape‐tutored only in the spring in the presence or absence of adult females. There were no differences between the responses of juveniles housed with or without adult females and the hand‐reared juveniles were significantly less responsive to song than adult females. Adult females responded more to familiar songs than to the unfamiliar songs: juvenile females made no such distinction. Taken as a whole, these data are the first to document that female cowbirds’ song preferences for local song can be reshaped by post‐natal experience. These data complement recent study in cowbirds and other species showing that socially more complex contexts reveal plasticity in female song preferences that are not apparent when learning opportunities are constrained by impoverished laboratory settings.     

Interleukin-1 induces sleep-like behavior and alters call structure in juvenile rhesus macaques

To date, there have been no investigations of the behavioral effects of interleukin-1 (IL-1) in nonhuman primates. In this study the locomotor behavior and vocalizations of juvenile rhesus monkeys were monitored for 45 minutes following intravenous injections of recombinant human IL-1 alpha. In addition, their reaction to a broadcasted recording of infant monkey distress calls was determined 20 minutes after the beginning of each test session. IL-1 induced sleep-like inactivity and significantly diminished the monkey's behavioral and vocal responses to the broadcasted calls. The coo calls uttered by the monkeys following IL-1 treatment also had a longer duration and lower fundamental frequency than calls during the control condition. As several studies have indicated that behavioral effects of IL-1 may be mediated by corticotropin-releasing hormone (CRH), a second group of rhesus monkeys was given injections of CRH. CRH did not alter behavior or call structure at the dose administered. These results extend previous research on the behavioral effects of IL-1 to include the nonhuman primate and provide the first evidence that cytokines can affect vocal communication in rhesus monkeys. © 1995 Wiley-Liss, Inc.     

Rearing conditions required for behavioral compensation after unilateral cercal ablation in the cricket Gryllus bimaculatus

The rearing condition necessary for behavioral compensation after sensory deprivation was investigated in the cricket Gryllus bimaculatus. The right-cercus-ablated cricket was reared in a glass vial with a slightly larger diameter than the body length of the cricket. After two weeks of rearing in the vial, the air-puff-evoked escape behavior of the cricket was investigated. The response rate (relative occurrence of the escape behavior after a standard air puff) obtained was identical with that of crickets reared in a large cage. On the other hand, unlike crickets reared in a large cage, the distorted escape directional property of the cricket reared in the vial was not compensated at all. Control experiments proved that the restraint in the vial did not affect the motor system, and the air motion from environments was not essential for the compensational recovery of the escape direction. Therefore, the ablated crickets required spontaneous walking in order to compensate the directionality of their escape. A self-generated wind caused by spontaneous walking appears necessary for the crickets to realize the defect of their sensory system and to compensate the related escape behavior. A hypothesis for the compensation mechanism based on the efference copy signal is proposed.     

Swarming and mating activity of Anopheles gambiae mosquitoes in semi‐field enclosures

Anopheles gambiae Giles sensu stricto (Diptera: Culicidae) is the major Afro‐tropical vector of malaria. Novel strategies proposed for the elimination and eradication of this mosquito vector are based on the use of genetic approaches, such as the sterile insect technique (SIT). These approaches rely on the ability of released males to mate with wild females, and depend on the application of effective protocols to assess the swarming and mating behaviours of laboratory‐reared insects prior to their release. The present study evaluated whether large semi‐field enclosures can be utilized to study the ability of males from a laboratory colony to respond to natural environmental stimuli and initiate normal mating behaviour. Laboratory‐reared males exhibited spatiotemporally consistent swarming behaviour within the study enclosures. Swarm initiation, peak and termination time closely tracked sunset. Comparable insemination rates were observed in females captured in copula in the semi‐field cages relative to females in small laboratory cages. Oviposition rates after blood feeding were also similar to those observed in laboratory settings. The data suggest that outdoor enclosures are suitable for studying swarming and mating in laboratory‐bred males in field‐like settings, providing an important reference for future studies aimed at assessing the comparative mating ability of strains for SIT and other vector control strategies.     

Ethogram of Celebes monkeys (Macaca nigra) in two captive habitats

A well-composed and stable group of Celebes monkeys in captivity (one dominant adult male, one sub-adult male, three juvenile males, three adult females, and two juvenile females; housed together for several years) were studied in three successive 10-week periods. The first two periods consisted of a preliminary study and replication of the animals' behaviors while in a large cage enclosure. In the third period, observations were gathered on the same animals while they were on a simulated island to which they had been permanently moved. The study was designed to obtain an ethogram on the monkeys as well as to compare their social behaviors in these two captive environments. With respect to the latter, the acquisition of an acculturated social behavior involving a water-filled moat surrounding their new island environment was observed.     

饥饿对中华倒刺鲃幼鱼代谢、个性和集群的影响

在自然界中,环境变化、季节更替和人为因素造成食物资源时空分布的不均一性,导致鱼类经常面临食物资源短缺的环境胁迫,对其能量代谢和行为造成一定影响。为考察食物资源短缺下暖水性鲤科鱼类能量代谢、个性与集群行为的应对策略及其可能的内在关联,选取中华倒刺鲃(Spinibarbus sinensis)幼鱼为实验对象,分别测定饥饿组(2周)和对照组(维持日粮)在处理前后实验鱼的标准代谢率(Standard metabolic rate,SMR)、个性行为(勇敢性、探索性和活跃性)以及实验处理后的集群行为(凝聚力和协调性)。研究发现:(1)饥饿组和对照组实验过程中实验鱼SMR均显著下降,但仅饥饿组实验鱼SMR具有重复性;(2)饥饿导致中华倒刺鲃幼鱼勇敢性、探索性、活跃性均显著增加;(3)饥饿导致群体成员间距离缩短,游泳速度及其同步性上升。研究表明:饥饿后的中华倒刺鲃不仅适应性降低SMR以减少能量消耗,而且呈现出更高的勇敢性、探索性和活跃性以利于获取食物资源;饥饿迫使中华倒刺鲃群体提高凝聚力和协调性,可能有助于提高群体的生存能力。     

Monomorphic Region of the Serotonin Transporter Promoter Gene in New World Monkeys

Genetic variation in the human serotonin system has long been studied because of its functional consequences and links to various neuropsychiatric and behavior‐related disorders. Among non‐human primates, the common marmosets (Callithrix jacchus) and tufted capuchins monkeys (Cebus apella) are becoming increasingly used as models to study the effects of genes, environments, and their interaction on physiology and complex behavior. In order to investigate the independent functions of and potential interactions between serotonin‐related genes, anxiety and neuropsychiatric disorders, we analyzed the presence and variability of the serotonin transporter gene‐linked polymorphic region (5‐HTTLPR) in marmoset and capuchin monkeys. By PCR and using heterologous primers from the human sequence, we amplified and then sequenced the corresponding 5‐HTT region in marmosets and capuchins. The resulting data revealed the presence of a tandem repeat sequence similar to that described in humans, but unlike humans and other Old World primates, no variable length alleles were detected in these New World monkeys, suggesting that if serotonin transporter is involved in modulating behavior in these animals it does so through different molecular mechanisms. Am. J. Primatol. 74:1028‐1034, 2012. © 2012 Wiley Periodicals, Inc.     

Primate Location Preference in a Double-Tier Cage: The Effects of Illumination and Cage Height

Nonhuman primates are frequently housed in double-tier arrangements with significant differences between the environments of the upper and lower-row cages. Although several studies have investigated whether this arrangement alters monkeys' behavior, no studies have addressed the two most notable differences, light and height, individually to determine their relative importance. This experiment examined how rhesus and long-tailed macaques allocated their time between the upper and lower-row cages of a 1-over-1 apartment module under different lighting conditions. In Condition A, monkeys' baseline degree of preference for the upper- and lower-row was tested. In Condition B, the lighting environment was reversed by limiting illumination in the upper-row cage and increasing illumination in the lower-row cage. In both conditions, monkeys spent more time in the upper-row cage, thus indicating a strong preference for elevation regardless of illumination. The amount of time that monkeys spent in the lower-row cage increased by 7% under reversed lighting, but this trend was not significant. These results corroborate the importance of providing captive primates with access to elevated areas.     

Social organization and ecology of proboscis monkeys (Nasalis larvatus) in mixed coastal forest in Sarawak

Data are presented from a 16-month study of proboscis monkeys in an area of mixed coastal forest in Sarawak. The population density, social organization, and feeding and ranging behavior are described in detail. Results are compared with those from other primates in an attempt to understand why females of certain species (including proboscis monkeys) transfer between social groups. The scarcity of available food and reasons for the limited habitat preferences of proboscis monkeys are also discussed.