Critically endangered blonde capuchins fish for termites and use new techniques to accomplish the task

We report the spontaneous modification and use of sticks to fish for termites, above the ground, in wild blonde capuchins (Cebus flavius). These critically endangered Neotropical primates inhabit remnants of the Atlantic Forest. They used two previously undescribed techniques to enhance their termite capture success: nest tapping and stick rotation. The current ecologically based explanation for tool use in wild capuchins (i.e. terrestrial habits and bipedalism) must be viewed cautiously. Instead, remarkable manual skills linked to a varied diet seem important in promoting tool use in different contexts. The repertoire of tool-using techniques employed by wild capuchins has been expanded, highlighting the behavioural versatility in this genus.     

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     

Why Be Vigilant? The Case of the Alpha Animal

We compared patterns of vigilance behavior in a male- and a female-dominant species—white-faced capuchins and ring-tailed lemurs—and used the results to test four hypotheses to explain vigilance behavior in primates. Adult male white-faced capuchins spent significantly more time vigilant than females did, and much male vigilance appeared to be directed toward males from other social groups. This finding supports the protection of paternity hypothesis. No sex difference existed in vigilance behavior among the ring-tailed lemurs, and subjects of both sexes exhibited more vigilance toward predators/potential predators than toward extragroup conspecifics, which supports the predator detection hypothesis. A trade-off argument, suggesting that females tolerate males in a group in return for greater male vigilance, does not apply to ring-tailed lemurs in our study. In both the male-dominant capuchins and the female-dominant ring-tailed lemurs, the alpha subject in the majority of the study groups was significantly more vigilant than other group members were. In white-faced capuchins, the alpha male mates more often than subordinate males do; therefore, the greater degree of vigilance exhibited by the alpha male may correspond to the protection of his reproductive investment. In ring-tailed lemurs, there can be more than one matriline in a group. Thus, the greater amount of vigilance behavior exhibited by the alpha female may be related to protection of her matriline, which could ultimately lead to greater inclusive fitness. Alpha subjects in our study groups exhibited certain behaviors more frequently or exclusively. Accordingly, there may be a constellation of behaviors characteristic of alpha animals.     

云南拉沙山黑白仰鼻猴交配行为和出生季节

灵长类的交配模式对于了解和掌握雄性的交配策略和社群的稳定机制非常重要,但是目前有关亚洲灵长类交配模式的数据较少;因此,该研究于2011年1—12月,分别采用全事件取样法和焦点动物瞬时扫描取样法收集了拉沙山黑白仰鼻猴群的交配行为和出生数据。猴群全年交配,有2个峰期,一个是繁殖交配高峰期(8一10月);另一个在出生季节,但其非繁殖交配的生物学意义尚不清楚。雌性通过俯卧/注视雄性或跳落邀配。爬跨射精比为8.8,射精交配稀少(11.4%),这说明雄性并非每次交配都射精,因而支持黑白仰鼻猴交配模式的主体为多次爬跨射精或处于从单次爬跨射精到多次爬跨射精连续谱上段的观点。雄性邀配的射精爬跨多于雌性,说明多次爬跨射精不仅是雄性的一个交配策略,而且可以决定交配模式在连续谱的位置。交配时间后延6~7个月,交配频次与婴猴出生率相关。拉沙山猴群出生模式为严格的季节性,这进一步证实了前人的观点。婴猴出生具有一定的同步性,且不同猴群婴猴出生的同步模式不同。     

Coping with Acute Crowding by Cebus apella

Traditionally, scientists believed that crowded housing conditions increased aggression in animals. Recent research on captive primates fails to support a linear relationship between population density and aggressive behavior. Our study is the first to investigate the effects of acute crowding on a New World primate. We observed brown capuchins (Cebus apella) under 2 different spatial conditions: a control that offered the full indoor space in the enclosure and a short-term experimental condition that restricted the capuchins to approximately half the amount of space of the control condition. We compared rates of self-grooming, aggression, contact sitting, social grooming, and play between both conditions. We conducted a mixed factorial ANOVA at the individual level while taking subject sex and age class into account. Intense aggression, play, and social grooming decreased significantly in crowded conditions, suggesting that capuchins avoid social encounters if spatially confined. Their strategy for coping with acute crowding via a decrease in all forms of social behavior is intermediate between chimpanzee and macaque strategies in similar experiments. The only behavior to increase under crowding was a nonsocial, self-directed behavior with the potential of reducing arousal: self-grooming.     

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.     

中国滇南-东南亚跨境动物多样性监测平台概述

中国滇南-东南亚跨境动物多样性监测平台由中国科学院西双版纳热带植物园“动物行为与环境变化研究组”和中国科学院东南亚生物多样性研究中心“动物多样性与保护研究组”共建共管。平台始建于2012年6月, 覆盖的区域包括中国滇南和东南亚邻国, 致力于完善滇南和东南亚地区生物多样性本底资料, 了解重点保护动物的分布、种群大小、保护现状, 提出保护建议并制定保护方案。截至2019年9月, 在国内外22个监测点(包括保护区内、外)共布设了1,493个红外相机位点, 收回了国内外部分监测点照片。现已鉴定国内纳板河(2012-2016)、勐腊(2014-2019)、勐仑(2015-2019)和尚勇(2018-2019) 289个有效位点的718,995张照片, 调查工作量97,444个相机日, 记录到兽类48种, 鸟类80种。国外收回红外相机照片的鉴定工作正在推进。基于平台, 我们取得了一些重要成果, 例如: 报道了中国西南地区野猪(Sus scrofa)的种群生态, 发现了纳板河北豚尾猴(Macaca leonina)和猕猴(M. mulatta)的时空生态位分化, 结合分子生物学证据对麂属(Muntiacus)、斑羚属(Naemorhedus)、比氏鼯鼠属(Biswamoyopterus)进行了分类修订等。后续将在现有基础上扩大监测范围, 在国内与更多滇南保护区开展合作, 国外与更多东南亚国家合作。     

Significance of kin relations and individual preferences in the social behaviour of Cebus apella

Captive tufted capuchins (Cebus apella) formed a group characterized by greater affiliative behaviour within matrilines. Affiliation within the matriline is dependent upon social intimacy during infancy with matriline members. Courtship and mating are not identically distributed: subordinate and subadult males participate in a larger proportion of matings than of courtships. In all these aspects of social behaviour, variability across individuals contributes to the complex dynamics of the social group.     

Behavioral adaptations to heat stress and water scarcity in white-faced capuchins (Cebus capucinus) in Santa Rosa National Park, Costa Rica

We examined thermoregulatory behaviors in a wild population of white-faced capuchins (Cebus capucinus) inhabiting a highly seasonal dry forest in Santa Rosa National Park (SRNP), Costa Rica. The dry season in SRNP lasts approximately 5 months and is characterized by high ambient temperatures regularly exceeding 37 degrees C, low relative humidity, and the near absence of precipitation. This study demonstrates that capuchins rest more and travel shorter distances during the hottest and driest hours of the day, and suggests that they extend their tongues to lower body temperature via evaporative cooling. Seasonal weather patterns and group movement data reported here are based on 940 h of observations on three social groups of capuchins (wet season: 370 h, dry season: 570 h). In the dry season, the proportion of time spent resting increased at higher temperatures whereas the proportion of time spent traveling decreased. Distance traveled between location points taken at half-hour intervals decreased significantly as temperature increased, although the correlation was not strong. Capuchins exposed their tongues during hot, dry, windy conditions, and this behavior was much more frequent in the dry season. Temperature was significantly higher and humidity significantly lower for "tongue-out" events than expected for a random event in the dry season. Finally, as surface water became scarce, home-range areas of heavy use became increasingly centered on the remaining permanent water sources. These results suggest that heat stress and water scarcity are significant influences on the behavior of capuchins in hot, dry conditions.     

Reunion displays in captive male brown capuchins (Cebus apella)

Separation and subsequent reintroduction of brown capuchins (Cebus apella) can lead to reunion displays during which individuals will embrace and emit high-pitched, loud vocalizations. These displays were investigated in three male capuchins: two adults and one juvenile. These subjects were part of a larger captive social group held at the Capuchin Laboratory, Hiram College, OH, USA. We hypothesized that males would engage in reunion displays following separation regardless of the order of reintroduction, as evidence of an affiliative bond judged by concurrent social behavior. Sixty separations were conducted as part of weekly husbandry over a period of 13 months. Occurrence of reunion displays between the males was recorded with the initiator also noted. Reunion displays among males were found to occur only between the juvenile and alpha male, and all displays were initiated by the juvenile. Displays were highly influenced by the order of reintroduction. We suggest that reunion displays operate to reaffirm social relationships, particularly during situations of social tension.     

Calibrating a camera trap–based biased mark–recapture sampling design to survey the leopard population in the N'wanetsi concession,Kruger National Park,South Africa

Estimating large carnivore abundance can be challenging. A biased leopard (Panthera pardus) population survey was conducted in the N'wanetsi concession in the Kruger National Park (KNP), South Africa, using motion‐sensitive camera traps from April to August 2008. Survey effort included 88 trapping occasions and 586 trap days. The survey yielded 24 leopard photographs, comprising fourteen adults of eleven males and three females. The capture rate was determined to be 24.4 trap days per leopard. Estimates of population abundance stabilized at approximately 500 trap days. Precision of population estimates began to stabilize after 378 trap days. We estimated that there were nineteen leopards in an area of 150 km². Leopard density was estimated at 12.7 leopards per 100 km². We explore the possibility of employing the methods used in this study to survey the leopard population in the KNP and surrounding areas.     

Wild Capuchins Show Male-Biased Feeding Tool Use

Relatively few studies have explored sex differences in the use of foraging tools among primates other than apes. Although male primates are thought to be more innovative, researchers have reported a female sex bias in the use of feeding tools in wild chimpanzees. We investigate here the nature and extent of sex differences in foraging tool use over 12 mo in a free-ranging group of bearded capuchins (2 males, 5 females, and 3 juveniles) living in the dry Caatinga forests of the Serra da Capivara National Park, Piaui, Brazil. These capuchins used 3 major types of feeding tools: 1) tools for probing; 2) tools for pounding/cracking; and 3) digging stones to extract tubers or roots. Adult males performed 63% (n = 134) of all events of tool use and used tools significantly more frequently than did females, although male bout lengths across all tools (57 s ± 7.9 SE) were equivalent to those of adult females (47.3 s ± 12.6 SE). Both sexes used digging and cracking tools, although at different rates, whereas adult males used sticks to probe for prey and other rewards far more than females. Differential opportunities to use tools were not apparent: >71% of tool-use events occurred on the ground, and males and females spent equal time on the ground. We suggest that sex differences in tool use may function as opportunities for male signaling of investment quality.     

千岛湖片段化栖息地地栖哺乳动物的红外相机监测及最小监测时长

作为典型的陆桥岛屿, 千岛湖成为检验栖息地片段化理论的自然研究平台。2011年5月1日至2014年3月31日, 我们在千岛湖32个岛屿和1个大陆对照样点布设了60台红外相机, 对千岛湖体型较大的地栖兽类及其最小监测时长进行了监测和研究。在27,798个相机日的监测中, 共获得动物影像照片23,639张, 照片清晰、可进行物种鉴定的有2,414张, 占照片总数的10.2%; 其中体型较大的地栖兽类独立照片988张, 识别为9个物种: 穿山甲(Manis pentadactyla)、黄麂(Muntiacus reevesi)、野猪(Sus scrofa)、华南兔(Lepus sinensis)、马来豪猪(Hystrix brachyuran)、猪獾(Arctonyx collaris)、鼬獾(Melogale moschata)、花面狸(Paguma larvata)和豹猫(Prionailurus bengalensis), 平均独立照片拍摄率为40.9%。种-面积曲线研究表明, 岛屿上的地栖兽类物种丰富度随着岛屿面积的增大而增大, 曲线的z值为0.27。大岛(>10 ha)中, 最小监测时长随面积增加而增加, 而小岛没有明显趋势; 最小监测时长随隔离度增加而减小, 但关系不显著(d.f. = 20, F = 3.067, P = 0.095), 表明建湖后栖息地的片段化与岛屿化导致了一些对面积或栖息地较为敏感的大型兽类在小岛屿上的局部灭绝。因此, 我们建议对于面积较大的片段化栖息地, 红外相机应保证较长的最小监测时长, 而面积较小的片段化栖息地在监测中应根据隔离度、基质性质、物种种类适时调整调查强度, 以完整反映当地物种实际情况。     

Identification of individual adult female Javan lutungs (Trachypithecus auratus sondaicus) by using patterns of dark pigmentation in the pubic area

In a series of field surveys of wild Javan lutungs (Trachypithecus auratus sondaicus) conducted at Pangandaran Nature Reserve in West Java, Indonesia, from 2011 to 2012, we tried to use a method of individual identification by using individual-specific patterns of dark pigmentation in the pubic area. During the 2011 dry season, we used a digital SLR camera with a 400-mm telephoto lens to photograph the pubic area of each individual of a habituated group. These photographs were the basis for identifying 14 different adult females. During the rainy season of 2011 and the dry season of 2012, we checked the presence/absence of each of the identified individuals and found that these patterns were stable, at least during our study period. We found that two adult females and one adult female disappeared from the subject group between the first and second and between the second and third surveys, respectively, and that one adult female gave birth between the first and second surveys, but the infant had disappeared from the group between the second and third surveys. We could not confirm the validity of the method for juvenile females because of the dense white hair in their pubic areas and the fact that few individuals had clear patterns. Furthermore, we could not use this method for males because of the lack of pigmentation in the pubic area. As patterns of pigmentation in the pubic area are known to be present in other Trachypithecus species, our method can be useful for identification of individual adult females of these species, on which few individual-based behavioral studies have been conducted. Collecting individual-based behavioral data would enable us to track the presence of individuals in groups or movements between groups; determine the effects of social rank and age on within-group competition and copulation; and examine population data.     

Attending to the outcome of others: disadvantageous inequity aversion in male capuchin monkeys (Cebus apella)

Brosnan and de Waal [Nature 425:297-299, 2003] reported that capuchin monkeys responded negatively to unequal reward distributions between themselves and another individual when comparing their own rewards with that of their partner. It was suggested that social emotions provided the underlying motivation for such behavior and that this inequity aversion is specific to the social domain. However, alternative hypotheses such as the "frustration effect" or the "food expectation hypothesis" may provide more parsimonious explanations for Brosnan and de Waal's [Nature 425:297-299] results, while others have argued that these findings are not congruent with the Fehr-Schmidt inequity aversion model cited by the authors. The claim that inequity aversion behavior is specific to the social domain has also been questioned, as primates also develop expectations about rewards in the absence of partners, and react negatively when those expectations are violated. In this study, a modified Dictator game was used to investigate whether capuchins would exhibit either disadvantageous inequity aversion behavior or reference-dependent expectancy violation in social and nonsocial conditions, respectively. When given the choice between an equitable and an inequitable outcome, the subjects showed disadvantageous inequity aversion behavior, choosing the equitable outcome significantly more in the social condition. In the nonsocial condition, however, subjects did not show negative expectancy violation resulting from the formation of reference-dependent expectations, choosing the equitable outcome at chance levels. These results suggest that capuchins attend to differential payoffs and that they are averse to inequity, which is disadvantageous to themselves.     

Advancing Primate Research and Conservation Through the Use of Camera Traps: Introduction to the Special Issue

Effective conservation and management of primates depend on our ability to accurately assess and monitor populations through research. Camera traps are proving to be useful tools for studying a variety of primate species, in diverse and often difficult habitats. Here, we discuss the use of camera traps in primatology to survey rare species, assess populations, and record behavior. We also discuss methodological considerations for primate studies, including camera trap research design, inherent biases, and some limitations of camera traps. We encourage other primatologists to use transparent and standardized methods, and when appropriate to consider using occupancy framework to account for imperfect detection, and complementary techniques, e.g., transect counts, interviews, behavioral observation, to ensure accuracy of data interpretation. In addition, we address the conservation implications of camera trapping, such as using data to inform industry, garner public support, and contributing photos to large-scale habitat monitoring projects. Camera trap studies such as these are sure to advance research and conservation of primate species. Finally, we provide commentary on the ethical considerations, e.g., photographs of humans and illegal activity, of using camera traps in primate research. We believe ethical considerations will be particularly important in future primate studies, although this topic has not previously been addressed for camera trap use in primatology or any wildlife species.     

The Ontogeny of Prehensile‐Tail Use in Cebus capucinus and Alouatta palliata

A study of the platyrrhine prehensile tail provides an opportunity to better understand how ecological and biomechanical factors affect the ability of primates to distribute mass across many different kinds of arboreal supports. Young individuals experience ontogenetic changes in body mass, limb proportions, and motor skills that are likely to exert a strong influence on foraging strategies, social behaviors, support use, and associated prehensile‐tail use. In this research, I examine ontogenetic patterns of prehensile‐tail use in Cebus capucinus and Alouatta palliata. I collected behavioral data on activity, positional context, support size, and prehensile‐tail use in five age categories of white‐faced capuchins and mantled howlers during a 12‐month period at Estación Biológica La Suerte in northeastern Costa Rica. Infant and juvenile howlers and capuchins were found to use their prehensile tails significantly more often than adults during feeding, foraging, and social behavior. Prehensile‐tail use did not show predictable increases during growth. In both species, adults used their prehensile tails in mass‐bearing modes significantly less often than juveniles. Despite differences in tail anatomy in Cebus and Alouatta, prehensile‐tail use was observed to follow an increasing trajectory from infancy, peaking during juvenescence, and then decreasing in older juveniles and adults. In both species, it appeared that adult patterns of prehensile‐tail use reflected the demands placed on young juveniles. Am. J. Primatol. 74:770‐782, 2012. © 2012 Wiley Periodicals, Inc.     

A population study of the japanese wood mouse,Apodemus speciosus (Mammalia: Muridae), with reference to its social behavior

The role of social behavior on the population regulation of the Japanese wood mouse, Apodemus speciosus, was studied in the Ashu Experimental Forest of Kyoto University by monthly trapping and direct observation on the social behavior at the artificial feeding site. The census was carried out from May to October in 1974 and 1975, and the direct observation in June, August and October, 1975. In the study area, the Japanese wood mouse has two breeding seasons in a year: in spring and in autumn. Minimum survival rate was high in the non-breeding season and low in the breeding season. It was negatively correlated to the number of sexually active adults in both sexes. Home ranges of females tended to be mutually exclusive, and female residents prevented the settlement of female immigrants. On the other hand, home ranges of males overlapped largely and males had a straight social hierarchy. Subordinate males tended to disappear more often than dominant males did, but male residents did not hinder the settlement of male immigrants. Males may regulate their number by driving out the subordinate males, while females by spacing behavior.     

黄山短尾猴不同顺位等级雄性个体友好行为的比较研究

社会顺位等级制度在灵长类动物中普遍存在,它对动物个体的繁殖和社会行为有广泛的影响.本研究对黄山短尾猴鱼鳞坑YA2群6个不同顺位成年雄性个体,根据顺位高低,将它们分成3组:高顺位组(2只个体)、中等顺位组(2只个体)、低顺位组(2只个体),采用目标动物取样法对它们的社会行为进行研究,结果表明,3组之间(1)接收和发出架桥行为频次差异显著,高顺位组接收架桥次数最多;(2)接收和发出爬跨行为频次差异显著;低顺位组接收爬跨次数最多;(3)发出呈臀行为频次差异显著,但接收呈臀行为频次差异不显著;高顺位组是接收呈臀次数最多,低顺位组发出呈臀次数最多;(4)摇树行为频次差异显著,高顺位组发出摇树行为最多.因此雄性黄山短尾猴友好行为可以体现出社群顺位等级关系,这种社群顺位等级关系和这些友好行为在维持社群稳定上有重要作用.     

Social Aspects of Fur-rubbing in <Emphasis Type="Italic">Cebus capucinus</Emphasis> and <Emphasis Type="Italic">C. apella</Emphasis>

Capuchins rub particular plant materials into their pelage, a behavior for which most authors have proposed a medicinal function (Baker in American Journal of Primatology 38:263–270, 1996, Baker, M. (1998). Fur Rubbing as Evidence for Medicinal Plant Use by Capuchin Monkeys (Cebus capucinus): Ecological, Social, and Cognitive Aspects of the Behavior. Dissertation thesis. University of California Riverside; DeJoseph et al. in Journal of the American Academy of Dermatology 46:924–925, 2002). Individuals fur-rub solitarily or in groups, but researchers have not conducted studies to understand the differences. We investigated the link between the form of fur-rubbing and other social variables in 2 capuchin species. We supplied 2 captive groups —white-faced capuchins and tufted capuchins— with citrus fruit and onions and explored the behavioral processes and social aspects underlying the activity. We documented the occurrence, number of participants, and effect of recruitment behaviors in fur-rubbing subgroups. We investigated the role of kinship, affiliation, and dominance relationships in accounting for fur-rubbing groups. There is a significant difference in the form of fur-rubbing between white-faced and tufted capuchins. White-faced capuchins fur-rubbed mainly in subgroups and performed a particular behavior to recruit prospective participants, whereas tufted capuchins fur-rubbed mainly alone, and showed no particular motivation to be joined by other group members. White-faced capuchins could fur-rub together frequently, whatever their degree of kinship, affiliation, or dominance interval. In tufted capuchins, fur-rubbing appeared to be significantly affected by kinship and dominance.