Enclosure environment affects the activity budgets of captive Japanese macaques (Macaca fuscata)

Individuals adapt to changes in their environment, such as food availability and temperature, by adjusting the amount of time spent in different behavioral activities. These adjustments in behavior should vary across age-sex class according to specific physiological and social needs. We studied the activity budgets of three social Japanese macaque groups inhabiting either vegetated or nonvegetated enclosures in order to compare the effects of access with vegetation, as both food and substrate on resting, feeding, grooming and moving activities over a 12-month period. Daily access to natural foods for monkeys in the vegetated enclosure seems to be largely responsible for the differences in daily time budgets of these three groups. Resting time in all three groups was longer than the time devoted to other activities. Resting and moving time in the two nonvegetated enclosures was significantly longer than in the vegetated enclosure. In contrast, feeding and grooming time was significantly longer in the vegetated enclosure. Seasonal variation in time spent feeding, resting and grooming was significantly effected by enclosure type. In all three enclosures, immatures, particularly females, spent more time feeding and moving, whereas adults spent more time resting. Significant monthly variation in time spent by age-sex class was noted only for feeding and resting. Interestingly, in the vegetated enclosure, time spent feeding on natural vegetation was equal to the amount of time spent feeding on provisioned food. This suggests that factors other than energetic and nutritional needs may be important determinants of the activity budget of the species. These results have important implications for the enrichment of captive primates and our understanding of the maintenance of activity patterns by primates in the wild.     

Encouraging natural feeding behavior in captive-bred black and white ruffed lemurs (Varecia variegata variegata)

Captive breeding of endangered species is commonly proposed as a means of conserving biodiversity. The suggestion is that captive populations can be built up to provide individuals to reinforce or re-establish wild populations. However, there is evidence to suggest that captive-bred animals lack the skills necessary for survival in their natural habitat. This research was designed to assess whether a group of captive-bred Varecia variegata variegata exhibit such behavioral deficiencies in relation to feeding behavior compared to two wild groups. A further aim was to determine which of four methods of food presentation and two captive environments were most effective in encouraging the exhibition of natural feeding behavior. An identical focal animal, instantaneous time-sampling technique was used to collect data from the wild groups in the Betampona Reserve, Madagascar, and the captive group at Chester, UK. Results from Betampona confirm the highly frugivorous and arboreal nature of V. v. variegata. Under all captive conditions, except the rooftop feed in the cage environment, the captive V. v. variegata spent significantly less time feeding than their wild conspecifics. Suspensory feeding postures are an important adaptation enabling wild V. v. variegata to harvest fruit in the small-branch setting. Similar frequencies of use of such postures to those observed at Betampona were most effectively encouraged among captive V. v. variegata in the cage environment by the rooftop food presentation method and on a naturalistic island exhibit by the suspended method of food presentation. Differences in feeding behavior between the wild and captive V. v.variegata can be explained in terms of structural differences between their environments. As naturalistic captive environments allow lemurs to experience the challenges associated with feeding in the wild, it is strongly recommended that zoos endeavor to provide them with such conditions. Zoo Biol 17:379–392, 1998. © 1998 Wiley-Liss, Inc.     

Japanese macaques (Macaca fuscata) social development: Sex differences in Juvenile behavior

We have quantitatively documented the development of sex differences in the behavior of juvenile Japanese macaques (1 to 2 years of age). Mothers treated their offspring differently by sex, i.e., mothers of males broke contact with them more frequently than did mothers of females. Juvenile males played more, and mounted other macaques more frequently; juvenile females groomed their mothers more and were also punished by other group members more frequently than were males. Males showed a pattern of decreasing interactions with their mothers, but females increased the frequency of their maternal interactions. These patterns appear to presage the life histories of the sexes. However, comparisons with other species of nonhuman primates indicate that although sex differences in behavior are common, the variability among species severely limits cross-specific generalizations.     

Play behavior in immature moor macaques (Macaca maura) and Japanese macaques (Macaca fuscata)

Play is widespread across mammalian taxa, but species strongly vary in the ways they play. In less despotic primate species (i.e., with less steep dominance hierarchies, less severe conflicts, and more reconciliation), play has been described as being more frequent, cooperative, and freely expressed. To study the link between social play and dominance style, we compared play behavior in free-ranging infants, juveniles and subadults of more despotic Japanese macaques (Macaca fuscata, N = 24) and less despotic moor macaques (Macaca maura, N = 17). We found interspecific differences in play behavior that corresponded with the contrasting dominance styles of the study species, largely confirming our predictions. In particular, moor macaques spent a larger proportion of time in solitary and social play than Japanese macaques, while Japanese macaques spent a larger proportion of time in grooming interactions. In moor macaques, play sessions included more players, a larger variety of play behaviors, greater play face rates, a greater proportion of time in contact play, and a higher rate of reciprocal play-biting than in Japanese macaques. Aggressive escalations were not common, but more frequent in Japanese macaques. Finally, a higher frequency of play faces during play sessions predicted the occurrence of more reciprocal play-bites, but not the proportion of time spent in contact play behaviors. Additional studies on other groups and species will allow a better understanding of the link between dominance style and social play.     

Factors affecting aggression among females in captive groups of rhesus macaques (Macaca mulatta)

Captive groups of primates often exhibit higher rates of aggression than wild, free-ranging groups. It is important to determine which factors influence aggression in captivity because aggression, particularly intense aggression, can be harmful to animal health and well-being. In this study, we investigated the effect of ground substrate as well as season, rank, age, and group size on rates of agonistic interactions per female in seven captive groups of rhesus macaques (n = 70 females, 1,723 focal samples) at the California National Primate Research Center. Agonistic interactions were divided into three categories: displacements, mild aggression, and intense aggression. Females living in enclosures with gravel substrate were 1.7 times more likely to be involved in intense aggression (e.g. chases and physical contact) than females living in enclosures with grass (Poisson regression model: P < 0.001). High-ranking females were at least 1.3 times more likely to be involved in mild (e.g. threats and lunges) aggression than lower-ranking females (low rank: P = 0.03; mid rank: P = 0.001). Females of all ranks were 1.5-1.9 times more likely to be involved in both intense and mild aggression during the breeding season than other seasons. Age and group size did not affect rates of mild or intense aggression. These findings indicate that although some aggression appears to be natural and unavoidable, i.e. aggression during the breeding season, the well-being of captive macaques can be improved by developing grass substrate in outdoor enclosures.     

Use of foraging racks and shavings as enrichment tools for groups of rhesus monkeys (Macaca mulatta)

Searching for and processing food are important activities of free-ranging primates. In contrast, captive primates spend little time foraging. Their food is readily available, easily obtained, and can be consumed quickly. The present study compared the use of foraging racks and a shavings substrate as two manipulations used to alter feeding behavior in nonhuman primates. Each method was tested in between two baseline periods (no racks or shavings present). Behavioral data were collected using a 30-sec scan sampling procedure for 1 hr during the feeding period. Both the rack conditions and the shavings condition decreased passive feeding behavior in the subjects. The use of racks also resulted in increased cage usage, activity, and movement, and decreased social proximity; the use of shavings resulted in decreased agonism. This study suggests that foraging racks and shavings are useful devices for environmental enrichment. © 1995 Wiley-Liss, Inc.     

The effects of temporary cover on the behavior of socially housed stumptailed macaques (Macaca arctoides)

To examine the effects of the provision of temporary cover on the behavior of stumptailed macaques (Macaca arctoides), a single group of 26 animals was observed during 25 testing periods over 7.5 months. During each testing period, the group was observed under two conditions. In the Cover condition, two solid temporary walls 9.6 m in length, were erected within the animals' living compound. In the No-Cover condition, the wall materials were stacked against one solid exterior wall of the compound. The provision of cover significantly reduced the levels of contact aggression, proximity between animals, and locomotion, and reduced the ability of the dominant male to monopolize copulations. It did not effect other measures of affiliation. Inconsistencies between these results and those of other published studies suggest that, while cover can have a significant influence on some kinds of social behavior in some situations, generalizations about the benefits of providing cover to captive animals may be premature.     

Female sexual behavior in the absence of male-male competition in captive Japanese macaques (Macaca fuscata)

A captive group of Japanese macaques (Macaca fuscata). consisting of one adult male and three adult females, was observed for 88 hr during the 1988 mating season. We focused on the group's sexual activities because understanding how social dynamics affect reproductive behavior may enhance our ability to establish self-sustaining captive populations. The adult male exhibited distinct preferences in copulation partners, although all females were receptive and cycled during the study period. The dominant female participated in the most copulations and successfully harassed and disrupted copulations between the male and the other females. The alpha female, therefore, actively constrained the formation of mating pairs. Further, the male did not consort with his year-round female grooming partner. This female, the least dominant member of the group, engaged in the most autosexual and homosexual behavior. Birth season data show that only the dominant female bore offspring. This study emphasizes the influence of social dynamics on a group's reproductive potential and suggests an alternative means by which females can influence consort formation.     

Close bonds and social rank similarities favor non-random mating in captive stump-tailed macaques (Macaca arctoides)

Assortative mating is non-random mating by the mutual choice of phenotypes or behavioral types. In polygynandrous species, competition for mating by social rank can lead to assortative mating. However, although not an individual trait, social bonds also influence mating opportunities resembling assortative mating. Stump-tailed macaques form long-term close bonds and organize in a linear dominance–subordination hierarchy. Therefore, we studied whether the strength of the social bond and rank closeness influenced mating decisions and increased mating opportunities, particularly for low- and middle-ranking animals. Firstly, we observed whether females directed proceptive behavior to close-bonded or adjacent rank males. Secondly, we measured whether successful copulations were related to the strength of social bonds and close ranking. Thirdly, to ensure that copulations owed mainly to the aforementioned factors, we also evaluated whether sexual coercion was unrelated to social bonds and rank similarities. Finally, we assessed whether close bonds mediated agonistic support to females. The study subjects were 12 adult female and 11 male captive stump-tailed macaques. We monitored daily females' reproductive status by vaginal cytology. Sexual behavior was recorded by all occurrences sampling and scan sampling to collect the agonistic and affiliative instances required to calculate social ranks, social bond strength, and agonistic support. The results indicated that the probability of females displaying proceptivity increased during the follicular phase toward close-bonded and high-ranking males. Copulation chances increased with male–female social bonds and rank closeness. Forced copulation decreased in close-bonded individuals, while agonistic support increased in close-ranking strong-bonded animals. In conclusion, close social bonds and similar social rank result in non-random mating in stump-tailed macaques.     

The foraging behavior of Japanese macaques Macaca fuscata in a forested enclosure:Effects of nutrient composition,energy and its seasonal variation on the consumption of natural plant foods

In the wild, primate foraging behaviors are related to the diversity and nutritional properties of food, which are affected by seasonal variation. The goal of environmental enrichment is to stimulate captive animals to exhibit similar foraging behavior of their wild counterparts, e.g. To extend foraging time. We conducted a 12-month study on the foraging behavior of Japanese macaques in a semi-naturally forested enclosure to understand how they use both provisioned foods and naturally available plant foods and what are the nutritional criteria of their consumption of natural plants. We recorded time spent feeding on provisioned and natural plant foods and collected the plant parts ingested of their major plant food species monthly, when available.We conducted nutritional analysis (crude protein, crude lipid, neutral detergent fiber-'NDF', ash) and calculated total non-slructural carbohydrate - 'TNC' and total energy of those food items. Monkeys spent 47% of their feeding time foraging on natural plant species. The consumption of plant parts varied significantly across seasons. We found that leaf items were consumed in months when crude protein, crude protein-to-NDF ratio, TNC and total energy were significantly higher and NDF was significantly lower, fruit/nut items in months when crude protein and TNC were significantly higher and crude lipid content was significantly lower, and bark items in months when TNC and total energy were higher and crude lipid content was lower. This preliminary investigation showed that the forested enclosure allowed troop members to more fully express their species typical flexible behavior by challenging them to adjust their foraging behavior to seasonal changes of plant item diversity and nutritional content, also providing the possibility for individuals to nutritionally enhance their diet.     

猕猴不同性别年龄组个体时间分配和姿态行为的差异分析

2005 年11 月至2006 年10 月,对生活在广西桂林七星公园内的一群半野生猕猴进行观察,采用瞬时扫描取样法收集不同性别-年龄组个体的活动时间分配、活动高度和姿态行为的数据。研究结果表明:七星公园猕猴属半地栖性灵长类动物,花费较多的时间休息(41.5% );坐是猕猴最主要的休息姿态
(85. 5% )和觅食姿态(85. 4% ),四足行走是最主要的移动模式(64.5% )。成年个体的活动时间分配表现出明显的性别差异,主要表现为成年雌猴花费更多的时间相互理毛。不同年龄组个体的活动时间分配也表现出显著差异。休息时间随年龄的增长而增加,而玩耍时间则表现出相反的趋势。猕猴的活动高度和移动模式也表现出明显的年龄差异。成年个体花费更多的时间在地面活动。在移动过程中,成年个体采用四足行走的频率明显高于其它年龄组个体;亚成年个体跳跃最多;少年个体采用攀爬和架桥的频率明显高于成年个体。这些差异可能与个体在不同发育阶段的体型和活动水平差异以及林冠的不连续性有关。本研究结果将有助于了解猕猴不同性别年龄组个体对其栖息的社会和自然环境的行为适应机制。     

Relationship between sexual interactions and the timing of the fertile phase in captive female Japanese macaques (Macaca fuscata)

Japanese macaques live in multi‐male/multi‐female social groups in which competition between males, female mate choice, and alternative male mating strategies are important determinants of mating and reproductive success. However, the extent to which adult males rely on female behavior to make their mating decisions as well as the effect of social rank on mating success are not clear as results are inconclusive, varying from study to study. In this study, we combined behavioral and endocrine data of 14 female Japanese macaques to examine the relationship between ovarian cycle phase and frequency of sexual behaviors, and to investigate how social rank influences sexual behavior in this species. We found that there was no increase in female proceptive behaviors during the fertile phase of the ovarian cycle, suggesting that female behaviors did not clearly signal the probability of conception. In spite of that, the frequencies of ejaculatory copulations were highest during this phase, indicating that the attractivity of females increased significantly during the period with higher probability of conception. Males, and especially the highest ranking male, were able to discriminate females nearing ovulation and to concentrate their mating effort, implying that the timing of ovulation was not concealed from them. The α male seemed able to monopolize most female matings, which is probably due in part to the low number of females simultaneously ovulating and to the limited number of inconspicuous places that the lower ranking males have to mate with females and avoid α male aggression. All together, these results suggest that different males may have access to different signals of ovulation and/or are differentially restrained as to how they can act on that information. The exact nature of the estrogen‐related cues males use to recognize female reproductive status, and to what extent males use them warrants further investigation. Am. J. Primatol. 71:868–879, 2009. © 2009 Wiley‐Liss, Inc.     

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.     

The development of behavioural sex differences in infant rhesus macaques (Macaca mulatta)

Studies of infant rhesus macaques have generally reported sex differences in the frequency of expression of some behaviour patterns, such as rough-and-tumble play and socio-sexual mounting. In contrast, sex differences in other behaviour patterns, such as proximity to the mother, have been less consistantly reported. Using data on the behavioural development of infant rhesus macaques living in captive social groups, we have attempted to provide further evidence for, or against, sex differences in behaviour and to investigate the possible influence of maternal rank and parity on sex differences in infant behaviour and mother-infant interactions. The behaviour of 14 male and 20 female infants and their mothers was studied during the first six months of life, including measures of play behaviour socio-sexual mounting, and mother-infant interactions. Our data reveal that, on average, male infants exhibited more rough-and-tumble play and mounting than female infants, and also exhibited stationary play, chasing play, and initiated play more frequently than females. Such sex differences appear to be robust in macaques and have been reported in a variety of housing conditions. male and female infants did not differ in the amount of time spent at particular distances from their mothers, and mothers were not found to behave differently towards sons and daughters, using measures of restraint, rejection, and grooming. These results are in contrast to previous studies on singly-housed mother-infant pairs but similar to those on free-ranging populations. Mothers did behave differently towards their infants depending upon the mother's rank and previous number of offspring. These maternal characteristics may have significant consequences for the behavioural development of both male and female infant primates.