Hormonal Correlates of Maternal Style in Captive Macaques (Macaca fuscata and M. mulatta)

Previous studies on nonhuman primate maternal styles showed that variation in infant-directed behavior falls along two dimensions, traditionally labeled as protectiveness and rejection. We investigated maternal styles in rhesus (Macaca mulatta) and Japanese (M. fuscata) macaques living in analogous captive social groups, and correlated them with the levels of estrogen metabolites excreted in female feces during the perinatal period. We focally observed mother-infant pairs 3 hours per week during the first 12 weeks of infant life. We collected fecal samples twice a week from each mother, starting 4 weeks before delivery and ending 4 weeks after delivery. Three significant components were extracted by principal component analysis from 15 different infant directed behaviors, each reflecting a different aspect of mothering style: rejection is correlated with behavioral measures of maternal opposition to contact; protectiveness is correlated with maternal solicitude; and independence is correlated with time in contact, grooming and cradling. Levels of estrogen metabolites are significantly correlated to rejection but not to protectiveness or independence, indicating that, in nonhuman primates, individual endocrine changes related to maternal behavior might specifically affect the timing of contact interruption.     

大熊猫的刻板行为及其矫正对策——丰富圈养环境举措

由于生活环境单一、活动空间狭小等阻碍了正常行为的表达,圈养大熊猫经常发生一种谓之“刻板行为”的机械、呆板行为。所谓刻板行为,是指圈养大熊猫无明显目的的、不变的、以固定频率反复重复的无任何功能效果的简单行为。丰富圈养环境举措(环境富集)是矫正刻板行为的一种重要的行之有效的对策。介绍了圈养大熊猫刻板行为的表现、特点、发生机制及富集化矫正对策。     

Social Behavior of Captive Indochinese and Insular Long-Tailed Macaques (Macaca fascicularis) Following Transfer to a New Facility

There are measurable differences in behavior, physiology, social organization, and geographic distribution within and between various species of macaques. We collected information on the social behavior of captive Macaca fascicularis from Indochina and island populations after they had been transferred to a new environment and new social groups. While some changes in behavior occurred over time, we found no decrease in high levels of agonistic behaviors. We interpret this finding in light of previous research reporting that long-tailed macaques show low levels of habitatuation to novelty and are highly aroused in comparison to other macaque species. We found predictable differences in behavior for males, females, and infants, in which infants played more, females had higher levels of contact proximity to other individuals, and males exhibited more sexual and threat behavior. A comparison of social behavior in long-tailed macaques from different origins indicate that Indochinese macaques are generally less affiliative and Indochinese males are more aggressive than their insular counterparts. Differences among macaque species, and within the fascicularis-group, should be considered in management of captive colonies and when interpreting research data.     

Birth Patterns in Wild and Captive Lion-Tailed Macaques (Macaca silenus)

During a 5-yr study of lion-tailed macaques in their natural habitat, we found that: 1) most births occurred from January to April (70%) and from September to December (19%), showing a bimodal pattern with a major and a minor birth peak; 2) the period of peaks remained the same over 5 yr; and 3) a similar pattern of birth peaks occurred both in groups in large forest complexes that had overlapping home ranges with other groups and in single groups that were isolated in forest fragments in the same region but with similar ecological conditions. The results suggest more of a birth seasonality than mere breeding synchronization in the wild lion-tailed macaques. We also analyzed data on births in captivity in European Zoos for 10 yr. We observed no seasonality or peaks in births, and the pattern was the same over the years. Data on rainfall suggest that resource availability in the wild habitat may not be uniform throughout the year; hence, ecological factors may play an important role in determination of birth patterns in the natural habitats of lion-tailed macaques.     

笼养雌性短尾猴月经周期及性行为

在多雄多雌的灵长类社会中,成年雌雄个体的性行为并不局限于雌性受孕期,但仍认为性行为在受孕期最为活跃.对于雌性隐藏发情的灵长类物种,雌雄个体的性行为与雌性月经周期的相关性尚不清楚.本研究以短尾猴(Macaca thibetana)为研究对象,研究雌性隐藏发情灵长类的性行为与月经周期阶段的关系.在短尾猴繁殖季节,从2019...     

Improving the Welfare of Captive Macaques (Macaca sp.) Through the Use of Water as Enrichment

This review evaluates the use of water as a tool for enriching the environments of macaques (Macaca sp.) in captivity. Many macaque species are known to swim and forage in water in the wild, and in-situ reports suggest that access to water promotes activity and cultural behavior. Yet, there is a relative dearth of information on water enrichment, covering only a small number of macaque species in both laboratory and zoo settings. Previous studies in captivity report high levels of usage of water enrichment as well as further behavioral benefits, including increases in play, exploratory behavior, and tool use. Subsequently, there is a clear need for more research on the potential benefits of water enrichment for both macaques and other primate species, especially given that small water troughs and pools provide an inexpensive method for enriching nonhuman primate lives in captivity.     

促进人工饲养实验猕猴心理康乐

目的促进实验猕猴心理康乐,既能减少动物异常行为的发生、获得可靠的科学数据,同时也是实现这一珍贵非人灵长类实验动物福利的重要内容。实验猕猴社会化集群、环境优化、婴猴饲养方式是影响动物心理康乐几个较大的因素,本文对其研究进展进行了综述,对推进我国灵长类实验动物福利具有积极作用。     

四川马尔康圈养林麝的刻板行为

在圈养环境下,迁地保育野生动物易发育刻板行为,刻板行为的发育可直接影响圈养野生动物的繁殖和存活,从而影响迁地保育。2016年5月1日至7月31日间,采用焦点取样及所有事件记录法对四川马尔康林麝繁育场的75头圈养林麝(Moschus berezovskii)进行了刻板行为取样,分析了性别、年龄、圈区环境、圈群结构等因素对其刻板行为的效应。结果表明,四川马尔康麝场的圈养林麝在单位取样时间(10 min)内展现的刻板行为持续时间占比为20.53%±2.43%(n=75);雌麝刻板行为持续时间占比(18.14%±3.26%,n=46)略低于雄麝(20.89%±3.98%,n=25);随圈养年限(本研究中的圈养林麝"年龄"即是"被圈养年数")增加,林麝展现刻板行为的持续时间显著增加(P0.05);圈区环境设施对刻板行为存在显著效应(P0.05),裸地基底圈舍中林麝的刻板行为持续时间占比最高(33.11%±6.16%,n=24);圈群结构对林麝刻板行为持续时间的影响不显著(P0.05),混合圈群的刻板行为持续时间(19.31%±3.18%,n=53)最小;圈群密度对刻板行为持续时间的效应不显著(P0.05)。增加圈养环境的植被覆盖,进行混合圈养,可有效降低圈养林麝的刻板行为强度,并可提升林麝迁地保育的有效性。     

Environmental Enrichment Effect on Fecal Glucocorticoid Metabolites and Captive Maned Wolf (Chrysocyon brachyurus) Behavior

Environmental enrichment is a technique that may reduce the stress of nonhuman animals in captivity. Stress may interfere with normal behavioral expression and affect cognitive decision making. Noninvasive hormonal studies can provide important information about the stress statuses of animals. This study evaluated the effectiveness of different environmental enrichment treatments in the diminution of fecal glucocorticoid metabolites (stress indicators) of three captive maned wolves (Chrysocyon brachyurus). Correlations of the fecal glucocorticoid metabolite levels with expressed behaviors were also determined. Results showed that environmental enrichment reduced fecal glucocorticoid metabolite levels. Furthermore, interspecific and foraging enrichment items were most effective in reducing stress in two of the three wolves. No definite pattern was found between behavioral and physiological responses to stress. In conclusion, these behavioral and physiological data showed that maned wolves responded positively from an animal well being perspective to the enrichment items presented.     

Stereotypic behavior and fecal cortisol level in captive giant pandas in relation to environmental enrichment

Stereotypic behavior is exhibited by a wide range of captive animals. Its association with hormones, especially elevated cortisol level and lack of naturalistic stimuli in the environment, has been little studied. This study hypothesizes that stereotypic behavior is caused by stress due to lack of appropriate, naturalistic stimuli in the environment. Using four adult pandas (Ailuropoda melanoleuca) in the Beijing Zoo from March–July in 2003, we tested the following predictions: 1) stereotypic behavior and fecal cortisol level will not change associated with the progress of reproductive state; 2) there is a positive correlation between the occurrence of stereotypic behavior and fecal cortisol level; and 3) environmental enrichment by adding a naturalistic stimulus will reduce both stereotypic behavior and fecal cortisol level. We did not find any significant differences in the occurrence of stereotypic behavior and fecal cortisol level but did find a significant difference in the total time engaged in displaying the stereotypic behavior among the three estrous periods. The level of stereotypic behavior was correlated with elevated fecal cortisol level. Enrichment simply by adding a naturalistic stimulus did not show significant effects on stereotypic behavior, or on fecal cortisol level. Our results supported the second prediction, but did not completely support the first and the third ones perhaps because of the small sample size. Additionally, our results showed that stereotypic behavior might be a response to a heightened level of cortisol. Zoo Biol 0:1–15, 2006. © 2006 Wiley‐Liss, Inc.     

Behavior and Welfare of Domestic Cats Housed in Cages Larger than U.S. Norm

The effect of providing additional floor space on cat behavior and welfare is not well documented. This study involved replication of an investigation of cats’ responses to enhanced cage and room environments using cages of 0.56 m² with the same methodology but an increased space allowance of 1.1 m². Singly housed adult cats (n = 59) were randomly assigned to a treatment group that was a combination of a managed or unmanaged room and an enriched or unenriched cage environment. Cats were observed for 2 days for maintenance, affiliative, and avoidant behaviors using scan sampling and 5-min, continuous focal sampling. At the end of Day 2, cats’ reactions to the approach of an unfamiliar person were assessed. Cats housed in enriched/managed environments exhibited more maintenance and affiliative behaviors and fewer avoidant behaviors than cats in unmanaged/unenriched environments, suggesting that macro and micro environments may be equally relevant to the cat. Increased space did not enhance the cats’ welfare outcomes, suggesting that the provision of additional cage space may not be as important to the cat as a managed housing environment.     

Tourism and Infant-Directed Aggression in Tibetan Macaques (Macaca thibetana) at Mt. Huangshan,China

ABSTRACT

Previous studies of habituated Tibetan macaques (Macaca thibetana) at Mt. Huangshan, China demonstrated the negative impact that some tourism management strategies had on monkeys' annual infant mortality, but data on precise causes and perpetrators of infant injuries were not available. We worked at the same site and recorded rates of aggression that older monkeys directed toward group infants as a function of tourist numbers and proximity. We found a negative correlation between the number of people on the viewing platform and the frequency of monkeys' aggression toward the group's infants, but the effect is slight. We noted that infant-directed aggression (IDA) was more likely to occur in the provisioning zone where tourists bounded the monkeys on two sides, despite the fact that infants spent very little time in that location. The alpha and beta males engaged in more IDA than expected, while the other three adult males, adult females, and juveniles exhibited less IDA than expected. Males' IDA included biting, chasing, grabbing, and pushing. Adult females bit and grabbed mostly their own infants in the contexts of punishment and weaning. Juveniles' IDA was uncommon and consisted mostly of open-mouth threats. To minimize the severity and frequency of male-toinfant IDA, we recommend that sections of the tourist viewing platform be closed off so that tourists do not surround the monkeys, particularly when infants are near the viewing platforms and tourist numbers are few. The rule against tourists feeding monkeys should also be strictly enforced, so that altercations between the highest-ranked males and other group members, particularly infants, are less likely to occur.     

Male-female mating tactics and paternity of wild Japanese Macaques (Macaca fuscata yakui)

For Japanese macaques, visits by nontroop males (NTMs) often diminish the immediate copulation success of high-ranking males, although few studies have conducted a genetic analysis to show their contribution to the gene pool. I used noninvasively collected samples of semen, blood, urine and feces for the analysis of paternity in nine offspring born in two troops living on the island of Yakushima, Japan. I found that five of the nine offspring were sired by NTMs. It is argued that social change, small troop size and the timing of conception are all factors contributing to the NTM's reproductive success.     

Male-Induced Sociosexual Behavior by Vaginal Secretions in Macaca arctoides

Odor communication in Old World monkeys and apes is controversial, because most females have evolved visual and behavioral cues to signal fertility, e.g., sexual swellings. Female stump-tailed macaques (Macaca arctoides) do not have swellings, and mediation of chemical communication likely occurs because males engage in sexual behavior mostly throughout the periovulatory phase of the menstrual cycle. We tested whether vaginal secretions from different cycle phases, with saline solution as a control, promote changes in the frequency of male genital exploration, copulation, and coercive behavior toward females different from the donors, while female donors were apart from the group. Males explored more female genitals when exposed to follicular, periovulatory, and early luteal secretions in comparison to saline or menstrual or late luteal secretions. The increase in coercive behavior after exposure to follicular and periovulatory secretions most likely was a male response to the lack of cooperation of target females in engaging in copulation, as the latter were not receptive during the tests. The strength of male response to vaginal secretions varied significantly as a result of individual variability between donor females, yet the variability does not correlate either to dominance rank or to female age. Exploratory behavior of males correlates significantly with their social rank. Our results suggest that vaginal secretions are among the cues that male Macaca arctoides use to acknowledge the reproductive status of females in the absence of visual signals.     

Parity Modifies Endocrine Hormones in Urine and Problem-Solving Strategies of Captive Owl Monkeys (Aotus spp.)

Parental behavior modifies neural, physiologic, and behavioral characteristics of both maternal and paternal mammals. These parenting-induced modifications extend to brain regions not typically associated with parental responses themselves but that enhance ancillary responses, such as foraging efficiency and predator avoidance. Here we hypothesized that male and female owl monkeys (Aotus spp.) with reproductive experience (RE) would demonstrate more adaptive ancillary behavioral and neuroendocrine responses than those of their nonRE counterparts. To assess cognitive skills and coping flexibility, we introduced a foraging strategy task, including a set of novel objects (coin holders) marked with different symbols representing different food rewards, to the animals. To assess endocrine responses, urine samples were assayed for cortisol and dehydroepiandrosterone (DHEA) levels and their ratios to determine physiologic measures of emotional regulation in RE and nonRE owl monkeys. Compared with nonRE monkeys, experienced parents had higher DHEA:cortisol ratios after exposure to habituation training and on the first day of testing in the foraging task. Both hormones play critical roles in the stress response and coping mechanisms, and a high DHEA:cortisol ratio usually indicates increased coping skills. In addition, RE monkeys exhibited more efficient foraging responses (by 4-fold) than did the nonRE mating pairs. We conclude that RE modifies relevant behavioral and hormonal responses of both maternal and paternal owl monkeys exposed to a challenging cognitive paradigm. Corroborating previous research demonstrating adaptive modifications in foraging efficiency and emotional responses in reproductively experienced rodents, the current results extend these findings to a monogamous primate species.Abbreviations: DHEA, dehydroepiandrosterone; MDS, multidimensional scaling; RE, reproductive experiencePast research has elucidated the fundamental components of pregnancy and motherhood,^39,57,58,78 not only emphasizing the crucial role of the quality of maternal care on infant development^9,27,34 but also revealing how pregnancy and motherhood can reshape the neural, physiologic, and behavioral characteristics of animals.^2,11,36,53 These parent-induced modifications also extend to brain regions that are not directly associated with maternal responses^46,60,63 but instead are involved in enhancing the mother''s efficiency in ancillary parental responses, such as foraging efficiency and predator avoidance. Interestingly, evidence of these maternally related neurobiologic modifications has been confirmed in several species, including humans.^{12,13,39,47,50} For example, compared with animals that lacked reproductive experience (RE), maternal rats exhibited enhanced foraging abilities in a spatial task^37,40 as well as less behavioral and neural evidence of fear reactivity in an open-field task, as expressed by reduced c-fos immunoreactivity in the basolateral amygdala.⁷²Prior research suggests that stress hormones play an integrative role in parent-induced neurobiologic adaptations. Glucocorticoids, for example, have been shown to be suppressed in lactating females, due to blunted activity of the hypothalamic–pituitary–adrenal axis.^6,24,64 Accordingly, the current study assessed the integrative role of both cortisol and dehydroepiandrosterone (DHEA) on adaptive parental responses. Both hormones play critical roles in the stress response and coping mechanisms.¹⁵ DHEA has been shown to be released parallel to cortisol during physical stress²⁸ and has been associated with providing protection against the negative effects of prolonged exposure to glucocorticoids.⁵⁴ Potentially related to the cognitive modifications observed in maternal animals, DHEA can act centrally to decrease glucocorticoid-induced neuronal death in the hippocampus and to promote neurogenesis in the dentate gyrus of the hippocampus and in sensory dorsal root ganglion neurons.⁴⁹ Furthermore, the ratio between DHEA and cortisol has been found to be a reliable index of neuroprotection, because DHEA can increase the proliferation of progenitor cells in the adult hippocampus and also have antidepressant activity.^49,61,70 Accordingly, in the current study, we hypothesized that an increased DHEA:cortisol ratio would be advantageous in parental owl monkeys (Aotus spp.) presented with the metabolically expensive challenges associated with caring for offspring.Although females demonstrate more pronounced parent-induced effects, males experience hormonal alterations associated with copulation, pair-bonding, and paternal care, such as increased vasopressin levels.^{16,41,42,51,55} Research has identified specific neurobiologic modifications that accompany various degrees of paternal responsiveness, including distinct patterns of vasopressin receptor-binding sites and enhanced arginine-, vasopressin-, and oxytocin-immunoreactive cell bodies and fibers, as well as increased neuronal restructuring in the hippocampus.^30,41,79,80 Increased levels of oxytocin and prolactin have been reported in paternal males as well.^{29,67,79,81,82}Owl monkeys (Aotus) are New World monkeys that are characterized by the extensive involvement of fathers in the care of the infant. These primates are small (weight, approximately 1 kg), nocturnal, generalist omnivores that consume fruits, leaves, flowers, insects, and small vertebrate prey.^18,75 Owl monkeys possess prolonged, and probably exclusively, monogamous relationships between the mating pair, enforced through a high level of intrasexual competition.^18,19,53 In biomedical research, owl monkeys have been studied primarily because of their high resistance to parasites, and they are comparative model of herpes virus infection in humans. Consequently, very little is known about the physiologic correlates of their paternal behavior. Due to these characteristics, owl monkeys represent an ideal species in which to investigate the role of RE in the cognitive and emotional responses of animals in captivity.In light of past research emphasizing adaptive effects in reproductively experienced (RE) rodents, we hypothesized that adaptive ancillary behavioral and neuroendocrine responses would be greater in RE male and female owl monkeys than in their nonRE counterparts. To assess the monkeys’ cognitive skills and coping flexibility, we introduced a set of novel objects (coin holders) marked with different symbols representing different food rewards. Arguably, cognitive skills related to foraging are among the most critical adaptations in primates.¹⁷ Furthermore, cortisol and DHEA were evaluated to determine emotional responsivity and resilience in parental owl monkeys. Extending these parental investigations to a nonhuman primate species is necessary to determine the robustness of previously reported findings from laboratory rodents as well as to provide a reliable animal model of the effects of parity on the behavior of captive primates involved in biomedical research.     

Social stimulation and the resumption of copulation in Rhesus (Macaca mulatto) and stumptail (Macaca arctoides) Macaques

Copulatory data derived from observations of social groups of rhesus and stumptail macaques were analyzed to test the hypothesis that pairs of animals would resume copulation significantly sooner if a second male copulated with the female shortly after the first male’s ejaculation. Data from both groups supported the hypothesis. These results, extending previous studies in Macaca nemestrina,suggest that the shortening of copulatory intervals by social stimuli occurs in several species, both in social groups and in experimentally created triads. These findings also are consistent with the hypothesis that socially mediated resumption of mating is related to intrasexual competition among males.     

Sneaky Monkeys: An Audience Effect of Male Rhesus Macaques (Macaca mulatta) on Sexual Behavior

Males and females have different sexual interests and subsequently may show conflicting sexual strategies. While dominant males try to monopolize females, promiscuity benefits females and subordinate males. One way to escape monopolization by dominant males is to copulate in their absence. We tested this inhibitory effect of males on the sexual behavior of their group members in captive group‐living Rhesus macaques. Copulations between females and nonalpha males almost exclusively took place when the alpha male was out of sight. Furthermore, the inhibiting effect was not unique for the alpha male. An upcoming nonalpha male also inhibited copulations of its group members, and three other nonalpha males inhibited female copulation solicitations. Females adjusted their behavior to the presence of bystander males, as they initiated and accepted initiations more often in absence than in presence of bystander males. Although not significant, in males, a similar pattern was found. The observed reduction in mating behavior in presence of bystander males is in accordance with an “audience effect,” in which the behavior is modulated in relation to the presence or absence of third parties. This audience effect may serve as an important mechanism to reduce (aggressive) interruptions of subordinate male copulations.     

Male Migration in Barbary Macaques (Macaca sylvanus) at Affenberg Salem

We analyzed male migration during a 20-year period in the free-ranging Barbary macaque population of Affenberg Salem. Most natal migrations occurred around puberty, but only one third of all males left the natal group. Secondary group transfers were rare. All males immediately transferred to other bisexual groups. Migration rates were highest during periods with high adult female/male ratios within social groups. Immigrants highly preferred groups with fewer males of their own age than in the natal group, and many males immigrated into groups that had no male their own age. These groups originated from a skewed distribution of resident males during group fissions. A comparison of emigrants with their natal peers supports the inbreeding avoidance hypothesis as cause of emigration rather than the male competition avoidance hypothesis. Emigrants had no lower individual rank position and did not come from lower-ranking matrilines. Emigrants had more female maternal relatives, especially sisters. Males without female relatives almost never emigrated. Conversely, there is virtually no indication that emigrants were evicted from the natal group. Emigrants had no increased mortality. Paternity data revealed that the reproductive success of emigrants and natal males is similar, indicating that emigration had no reproductive cost. Many similarities between emigrants and natal males that separated from female maternal kin during group fissions suggest that inner migration during fissions is an alternative way to avoid maternal inbreeding. The mating system resulted in a genetic structure within social groups that largely diminished the chances for paternal inbreeding even without recognizing paternal kin.