Young Primates Research Articles

Repeatability of measures of behavioral organization over two years in captive infant rhesus macaques, Macaca mulatta.

Individual differences of infant temperament have been associated with future health outcomes that provide explanatory power beyond adult personality. Despite the importance of such a metric, our developmental understanding of personality-like traits is poor. Therefore, we examined whether young primates show consistency in personality traits throughout development. We replicated a Biobehavioral Assessment (BBA) at three time periods: 3-4 months, 1 year, and 2 years of age in 47 rhesus macaque (Macaca mulatta) subjects from large mixed-sex outdoor social housing units at the California National Primate Research Center. We report results for tests focused on responses and adaptation to the temporary separation and relocation, responses to a threatening stimulus, and ratings of overall temperament. We found consistently repeatable associations in measures of Emotionality; these associations were stronger in males, but also present in females, and broadly consistent between Years 1 and 2. We also explored whether behavioral responses to this experimental relocation might be influenced by their experience being relocated for other reasons (i.e., hospitalizations) as individuals' responses might be influenced by similar experiences to the BBA procedure. Only locomotion, during one of the assessments, was associated with past hospitalization events. Overall, repeatability in Emotionality-associated behaviors was evident across the 2 years, in both sexes. We did, however, find evidence of the emergence of sex differences via differentiated expression of behavioral responses during the BBA. We emphasize that there is likely contextual nuance in the use of these BBA factor-associated behaviors. Further research is required to determine whether and how shifts occur in underlying factor structure and the expression of associated behaviors.

Inhibitory neuron map of sevoflurane induced neurotoxicity model in young primates.

Sevoflurane, one of the most commonly used anesthetic agents in children, may induce neuronal dysfunction and cognitive impairment. Exposure to sevoflurane might induce an imbalance between neural excitation and inhibition which could be a mechanism behind anesthesia-induced cognitive and affective dysfunctions. However, the underlying mechanisms remain unclear. In this study, we used two rhesus macaques in the control group, and one rhesus macaques in the anesthesia group. We employed single-nucleus RNA sequencing (snRNA-seq) technology to explore alterations in distinct types of inhibitory neurons involved in the long-term cognitive impairment caused by sevoflurane in young macaques. Following sevoflurane treatment, an upregulation was observed in the SST+ inhibitory neuron in the LHX6+ neighborhood in the hippocampus of rhesus macaques. This alteration might impact brain development by influencing interneuron migration and maturation. Additionally, we proposed a novel classification of inhibitory neurons, defined by CNR1 and LHX6 applicable to both humans and macaques. Our study proposed a novel classification of inhibitory neurons defined by LHX6 and CNR1, relevant in macaques and humans. We also provide evidence that sevoflurane upregulated the SST+ inhibitory neuron in the LHX6+ neighborhood in the hippocampus of rhesus macaques, which may underlie the potential neurotoxic effects induced by general anesthetics. Our results also offer a more reliable approach for studying the structure and function of the human brain.

Asymmetric dimethyl arginine in captive owl monkeys(Aotussp).

Only four of 40 animals had measurable asymmetric dimethyl arginine (ADMA) levels. The young primate had the lowest value (53.4ng/ml) when compared with the two adults (218.8 ± 9.3ng/ml) and the elderly one (320.5ng/ml). The ADMA levels in this study may relate to the echocardiographic abnormalities found, and possible hypertensive individuals.

К проблеме социальной обусловленности орудийного поведения высших животных: структура и особенности «социальных контекстов»

The article provides a review and critical analysis of recent primate wild population research revealing the significance of social interactions ("social contexts") for the development and maintenance of tool behavior in animals from the perspective of the Vygotsky — Leontiev school. As social contexts, we consider the role of "skilled" group members, primarily maternal individuals, as well as artifacts of animal tool activity. We argue that these new data don’t contradict the main statements of cultural and activity psychology regarding the fundamental differences between the psychological mechanisms underlying the process of social determination of animal and humans tool activity: namely, "skilled" animals, unlike humans, do not teach or encourage intentionally the attempts of naive individuals to develop tool actions, nor form their specific ways of handling tools; young primates do not seek help and support in acquiring and performing these actions. In addition, artifacts are perceived by animals primarily as preferred objects that have certain physical characteristics, for example, for extracting food, in contrast to human children, who adopt socially accepted techniques for handling them.

Maternal stress effects on infant development in wild Verreaux's sifaka (Propithecus verreauxi)

Maternal effects mediated by nutrients or specific endocrine states of the mother can affect infant development. Specifically, pre- and postnatal maternal stress associated with elevated glucocorticoid (GC) output is known to influence the phenotype of the offspring, including their physical and behavioral development. These developmental processes, however, remain relatively poorly studied in wild vertebrates, including primates with their relatively slow life histories. Here, we investigated the effects of maternal stress, assessed by fecal glucocorticoid output, on infant development in wild Verreaux’s sifakas (Propithecus verreauxi), a group-living Malagasy primate. In a first step, we investigated factors predicting maternal fecal glucocorticoid metabolite (fGCM) concentrations, how they impact infants’ physical and behavioral development during the first 6 months of postnatal life as well as early survival during the first 1.5 years of postnatal life. We collected fecal samples of mothers for hormone assays and behavioral data of 12 infants from two birth cohorts, for which we also assessed growth rates. Maternal fGCM concentrations were higher during the late prenatal but lower during the postnatal period compared to the early/mid prenatal period and were higher during periods of low rainfall. Infants of mothers with higher prenatal fGCM concentrations exhibited faster growth rates and were more explorative in terms of independent foraging and play. Infants of mothers with high pre- and postnatal fGCM concentrations were carried less and spent more time in nipple contact. Time mothers spent carrying infants predicted infant survival: infants that were more carried had lower survival, suggesting that they were likely in poorer condition and had to be cared for longer. Thus, the physical and behavioral development of these young primates were impacted by variation in maternal fGCM concentrations during the first 6 months of their lives, presumably as an adaptive response to living in a highly seasonal, but unpredictable environment.Significance statementThe early development of infants can be impacted by variation in maternal condition. These maternal effects can be mediated by maternal stress (glucocorticoid hormones) and are known to have downstream consequences for behavior, physiology, survival, and reproductive success well into adulthood. However, the direction of the effects of maternal physiological GC output on offspring development is highly variable, even within the same species. We contribute comparative data on maternal stress effects on infant development in a Critically Endangered primate from Madagascar. We describe variation in maternal glucocorticoid output as a function of ecological and reproductive factors and show that patterns of infant growth, behavioral development, and early survival are predicted by maternal glucocorticoids. Our study demonstrates how mothers can influence offspring fitness in response to challenging environmental conditions.

S27. Investigating Anxiety-Related Behavior in Young Primates: A Novel, Computer-Automated Approach

Anxiety disorders affect millions of people worldwide, are more common in females, and often develop early in life (Bandelow & Michaelis, 2015; Rice & Miller, 1995). Our group examines the neurobiology of early life anxiety using a well-validated rhesus-monkey model (Macaca mulatta). The scalability of this approach, however, is limited by the need for human experts to score primates’ behavior.

How primates acquire their gestures: evaluating current theories and evidence.

Mechanisms underlying gesture acquisition in primates are largely unstudied, yet heavily debated. While some studies suggest that gestural repertoires are largely innate, others emphasize that gestures emerge and are shaped in social interactions with other conspecifics. There is agreement, however, regarding the negligible role of imitation for the acquisition of gestures. The aim of this paper is to provide an overview of the current knowledge about gesture acquisition in nonhuman primates, to introduce the corresponding mechanisms suggested to be involved, and to discuss how findings from current studies support the different theories of gesture acquisition. We suggest that seemingly inconsistent findings across different research groups can be reconciled by pointing to differences between their research foci as well as methods of data collection. The additional comparison of the developmental pathways of gestural and facialcommunication highlights thecomplex interplay of genetic as well as social factors involved in shaping a species repertoire. We close by proposing that extending longitudinal studies, which capture the onset and usage of gestures in young primates, and which include the comparisons of severalspecies and groups in different environments, will enable us to better understand developmental pathways of gestural communication in primates.

T12. Prefrontal Regulatory Pathways in Young Non-Human Primates That Modulate the Function of the Neural Circuitry Underlying Anxious Temperament

T12. Prefrontal Regulatory Pathways in Young Non-Human Primates That Modulate the Function of the Neural Circuitry Underlying Anxious Temperament

Developments in development: What have we learned from primate locomotor ontogeny?

The importance of locomotion to evolutionary fitness has led to extensive study of primate locomotor behavior, morphology and ecology. Most previous research has focused on adult primates, but in the last few decades, increased attention to locomotor development has provided new insights toward our broader understanding of primate adaptation and evolution. Here, we review the contributions of this body of work from three basic perspectives. First, we assess possible determinants on the timing of locomotor independence, an important life history event. Significant influences on timing of locomotor independence include adult female body mass, age at weaning, and especially relative brain size, a significant predictor of other primate life history variables. Additionally, we found significant phylogenetic differences in the timing of locomotor independence, even accounting for these influences. Second, we discuss how structural aspects of primate growth may enhance the locomotor performance and safety of young primates, despite their inherent neuromotor and musculoskeletal limitations. For example, compared to adults, growing primates have greater muscle mechanical advantage, greater bone robusticity, and larger extremities with relatively long digits. Third, focusing on primate quadrupedalism, we provide examples that illustrate how ontogenetic transitions in morphology and locomotion can serve as a model system for testing broader principles underlying primate locomotor biomechanics. This approach has led to a better understanding of the key features that contribute to primates' stride characteristics, gait patterns, limb force distribution, and limb postures. We have learned a great deal from the study of locomotor ontogeny, but there is much left to explore. We conclude by offering guidelines for future research, both in the laboratory and the field.

Primate Positional Behavior Development and Evolution

Positional behavior (posture and locomotion) studies are a category of primatological and anthropological field research that attempts to describe movement capabilities and expressed behavior within an evolutionary, ecological, and/or morphological context. This area of research is appealing because it allows the integration of morphological data (capabilities) with expressed behaviors and provides a basis for understanding fossil reconstruction. Because positional behavior acts as a mediator between the biology and the environment, it offers information about virtually all aspects of a primate's life. We are currently undergoing an increase in the number of field projects focusing on the development of positional behaviors in immature primates, and results suggest that in many species positional competence develops relatively early. In this review, I present information on recent positional behavior studies with a focus on how positional behavior develops in young primates. Research on immature primates suggests that natural selection operates at all life stages to influence survival and that the adult positional repertoire likely reflects the challenges confronted by younger individuals.

Rank acquisition in rhesus macaque yearlings following permanent maternal separation: The importance of the social and physical environment.

Rank acquisition is a developmental milestone for young primates, but the processes by which primate yearlings attain social rank in the absence of the mother remain unclear. We studied 18 maternally reared yearling rhesus macaques (Macaca mulatta) that differed in their social and physical rearing environments. We found that early social experience and maternal rank, but not individual traits (weight, sex, age), predicted dominance acquisition in the new peer-only social group. Yearlings also used coalitions to reinforce the hierarchy, and social affiliation (play and grooming) was likely a product, rather than a determinant, of rank acquisition. Following relocation to a familiar environment, significant rank changes occurred indicating that familiarity with a physical environment was salient in rank acquisition. Our results add to the growing body of literature emphasizing the role of the social and physical environment on behavioral development, namely social asymmetries among peers.

No evidence for loss of short-wavelength sensitive cone photoreceptors in normal ageing of the primate retina

In old world primates including humans, cone photoreceptors are classified according to their maximal sensitivity at either short (S, blue), middle (M, green) or long (L, red) wavelengths. Colour discrimination studies show that the S-cone pathway is selectively affected by age and disease, and psychophysical models implicate their loss. Photoreceptors have high metabolic demand and are susceptible to age or disease-related losses in oxygen and nutrient supply. Hence 30% of rods are lost over life. While comparable losses are not seen in cones, S-cones comprise less than 10% of the cone population, so significant loss would be undetected in total counts. Here we examine young and aged primate retinae stained to distinguish S from M/L-cones. We show there is no age-related cone loss in either cone type and that S-cones are as regularly distributed in old as young primates. We propose that S-cone metabolism is less flexible than in their M/L counterparts, making them more susceptible to deficits in normal cellular function. Hypoxia is a feature of the ageing retina as extracellular debris accumulates between photoreceptors and their blood supply which likely impacts S-cone function. However, that these cells remain in the ageing retina suggests the potential for functional restoration.

Grasping primate development: Ontogeny of intrinsic hand and foot proportions in capuchin monkeys (Cebus albifrons and Sapajus apella).

Young primates have relatively large hands and feet for their body size, perhaps enhancing grasping ability. We test the hypothesis that selection for improved grasping ability is responsible for these scaling trends by examining the ontogeny of intrinsic hand and foot proportions in capuchin monkeys (Cebus albifrons and Sapajus apella). If selection for improved grasping ability is responsible for the observed patterns of hand and foot growth in primates, we predicted that fingers and toes would be longer early in life and proportionally decline with age. We measured the lengths of manual and pedal metapodials and phalanges in a mixed-longitudinal radiographic sample. Bone lengths were (a) converted into phalangeal indices (summed non-distal phalangeal length/metapodial length) to test for age-related changes in intrinsic proportions and (b) fit to Gompertz models of growth to test for differences in the dynamics of phalangeal versus metapodial growth. Manual and pedal phalangeal indices nearly universally decreased with age in capuchin monkeys. Growth curve analyses revealed that metapodials generally grew at a faster rate, and for a longer duration, than corresponding phalanges. Our findings are consistent with the hypothesis that primates are under selection for increased grasping ability early in life. Relatively long digits may be functionally adaptive for growing capuchins, permitting a more secure grasp on both caregivers and arboreal supports, as well as facilitating early foraging. Additional studies of primates and other mammals, as well as tests of grasping performance, are required to fully evaluate the adaptive significance of primate hand and foot growth.

Editorial: Frontiers in Synaptic Plasticity: Dendritic Spines, Circuitries and Behavior.

Editorial: Frontiers in Synaptic Plasticity: Dendritic Spines, Circuitries and Behavior.

Escherichia coli Enteropatógena en Crías de Primate Aotus (Aotidae) con Diarrea en Cautiverio

<p>La diarrea es el signo más frecuente de enfermedad gastrointestinal en crías de primates mantenidas en cautiverio. El estudio tuvo como objetivo aislar e identificar especies bacterianas presentes en crías de <em>Aotus </em>con diarrea que son criadas en cautiverio con fines experimentales. Se tomaron muestras de heces mediante hisopado rectal a 78 ejemplares de 1 a 7 meses de edad de <em>A. nancymae </em>(n=65) y <em>A. vociferans</em> (n=13) con diarrea y a 29 ejemplares de 1 mes de edad, aparentemente sanos de <em>A. nancymae </em>(n=21)<em> </em>y <em>A. vociferans</em> (n=8), durante el periodo de 2002 a 2005. En el grupo control se identificó principalmente <em>E. coli</em>, además de <em>Proteus vulgaris</em>, <em>P. mirabilis</em> y <em>Citrobacter freundii</em>. Resultado similar fue registrado en el grupo con diarrea, además de <em>Klebsiella oxitoca y Enterobacter aerogenes. </em>Los serotipos de <em>E. coli</em> enteropatógena (EPEC) identificados en el grupo con diarrea fueron siete: O158, O142, O86, O125, O126, O55 y O111. Los resultados indican que las crías con diarrea tienen bacterias que corresponden a la flora intestinal normal, siendo <em>E. coli </em>la de mayor frecuencia.</p>

Abstract 246: Thoracic versus Abdominal Aortic Stiffness in Young and Old Non-Human Primates

We demonstrated that thoracic aortic stiffness is increased in aging monkeys, with the mechanism involving increased vascular smooth muscle cell (VSMC) stiffness. In view of the importance of increased abdominal aortic stiffness to greater incidence of abdominal aortic aneurysms, the goal of this investigation was to determine differences in thoracic vs. abdominal aortic stiffness in young and old monkeys (fascicularis and rhesus). Most prior studies on aortic stiffness have been conducted in vitro or in anesthetized animals with indirect measurements of stiffness. A novel feature of the current investigation was to measure aortic diameter and pressure instantaneously and continuously in chronically instrumented, conscious young (n=25, 5-12yrs) and old male (n=21, >24yrs) monkeys, instrumented with aortic pressure gauges and ultrasonic aortic diameter crystals on the thoracic and abdominal aorta. The aortic stiffness index, β[[Unable to Display Character: ]][[Unable to Display Character: ]]calculated as a ratio of systolic and diastolic aortic pressures and diameters, was markedly greater, p<0.05, in abdominal, compared with thoracic, aorta in both young (33±5.0 in abdominal vs. 14±2.2 in thoracic) and old monkeys (57±6.3 in abdominal vs. 34±0.4 in thoracic). Although both thoracic and abdominal aortic stiffness were greater in old monkeys, p<0.05, surprisingly, abdominal aortic stiffness in young monkeys (33±5.0) was equal to thoracic aortic stiffness in old monkeys (34±0.4). Using atomic force microscopy, aortic VSMC stiffness was 2 fold greater, p<0.05, in old monkeys vs. young monkeys, but there were no differences in abdominal vs. thoracic aortic VSMC stiffness in either young or old monkeys. In summary, as expected, aging increased aortic stiffness, with the mechanism, in part, due to increased VSMC stiffness. However, aortic stiffness was increased more in the abdominal than thoracic aorta both in young and old monkeys, with the magnitude of the increase in the abdominal aorta of the young monkeys, similar to that which occurs with aging in the thoracic aorta. These findings point out the major differences in stiffness along the aorta and have relevance to the greater frequency of abdominal aortic aneurysms.

Differentially methylated plasticity genes in the amygdala of young primates are linked to anxious temperament, an at risk phenotype for anxiety and depressive disorders.

Children with an anxious temperament (AT) are at a substantially increased risk to develop anxiety and depression. The young rhesus monkey is ideal for studying the origin of human AT because it shares with humans the genetic, neural, and phenotypic underpinnings of complex social and emotional functioning. Heritability, functional imaging, and gene expression studies of AT in young monkeys revealed that the central nucleus of the amygdala (Ce) is a key environmentally sensitive substrate of this at risk phenotype. Because epigenetic marks (e.g., DNA methylation) can be modulated by environmental stimuli, these data led us to hypothesize a role for DNA methylation in the development of AT. To test this hypothesis, we used reduced representation bisulfite sequencing to examine the cross-sectional genome-wide methylation levels in the Ce of 23 age-matched monkeys (1.3 ± 0.2 years) phenotyped for AT. Because AT reflects a continuous trait-like variable, we used an analytical approach that is consistent with this biology to identify genes in the Ce with methylation patterns that predict AT. Expression data from the Ce of these same monkeys were then used to find differentially methylated candidates linked to altered gene regulation. Two genes particularly relevant to the AT phenotype were BCL11A and JAG1. These transcripts have well-defined roles in neurodevelopmental processes, including neurite arborization and the regulation of neurogenesis. Together, these findings represent a critical step toward understanding the effects of early environment on the neuromolecular mechanisms that underlie the risk to develop anxiety and depressive disorders.

Central amygdala nucleus (Ce) gene expression linked to increased trait-like Ce metabolism and anxious temperament in young primates.

Children with anxious temperament (AT) are particularly sensitive to new social experiences and have increased risk for developing anxiety and depression. The young rhesus monkey is optimal for studying the origin of human AT because it shares with humans the genetic, neural, and phenotypic underpinnings of complex social and emotional functioning. In vivo imaging in young monkeys demonstrated that central nucleus of the amygdala (Ce) metabolism is relatively stable across development and predicts AT. Transcriptome-wide gene expression, which reflects combined genetic and environmental influences, was assessed within the Ce. Results support a maladaptive neurodevelopmental hypothesis linking decreased amygdala neuroplasticity to early-life dispositional anxiety. For example, high AT individuals had decreased mRNA expression of neurotrophic tyrosine kinase, receptor, type 3 (NTRK3). Moreover, variation in Ce NTRK3 expression was inversely correlated with Ce metabolism and other AT-substrates. These data suggest that altered amygdala neuroplasticity may play a role the early dispositional risk to develop anxiety and depression.

Cortisol predicts decreased cerebral cortical volume in 592 young non-human primates

Cortisol predicts decreased cerebral cortical volume in 592 young non-human primates

灵长类社会玩耍的行为模式、影响因素及其功能风险

PDF HTML阅读 XML下载 导出引用 引用提醒 灵长类社会玩耍的行为模式、影响因素及其功能风险 DOI: 10.5846/stxb201103210345 作者: 作者单位: 陕西省动物研究所,西北大学生命科学院、陕西省动物研究所,西北大学生命科学学院;西北大学生命科学学院,陕西省动物研究所,陕西省动物研究所,陕西省动物研究所、 西北大学生科院、 作者简介: 通讯作者: 中图分类号: 基金项目: 陕西省科学院基金(2009K-08);陕西省自然科学基金(2010JM3006);国家自然科学基金(30970444,30900168,30970379);日本Cosmo石油环保卡基金(2005-2011) Behavioral patterns, influencing factors, functions and risks of social play in primates Author: Affiliation: Shannxi institute of zoolgy,,,,,shannxi institute of zoology Fund Project: 摘要 | 图/表 | 访问统计 | 参考文献 | 相似文献 | 引证文献 | 资源附件 | 文章评论 摘要:社会玩耍是指两个或两个以上个体共同参与的一种互作性玩耍行为,个体间的行为彼此适应并相互影响。 社会玩耍行为在灵长类物种的社会交往过程中普遍发生,作为未成年个体一种重要的发育行为,其对个体的生存技能和成年后的繁殖成功具有重要影响。灵长类物种的社会玩耍不仅仅表现为追逐、摔跤、跳跃等一些常见行为,部分物种还发展出自己特有的行为。一般而言,社会玩耍在婴儿后期和青少年早期的发生频率最高,然后随着年龄增长直到成年时期,这类行为的平均发生频率将逐渐下降。未成年雄性个体要比同年龄段的雌性个体更喜欢玩耍,但常因物种、研究对象年龄等因素表现不同甚至相反;很多物种的个体喜欢与有亲缘关系的个体玩耍,或者与性别相同、年龄相仿、等级相近的个体玩耍。总之,非人灵长类个体社会玩耍的发育不但受环境参量如食物、场地等的影响,而且还与个体的年龄、性别、等级、亲缘关系等社群因素紧密相关。未成年个体在玩耍过程中,获得了身体机能的快速发育、完善了生存技能、建立了个体间的友好关系、增强了认识自身及适应周围环境的能力,从而为顺利过渡到成年期和履行自己的职能打好基础,但有时却需要承担玩耍过程中受伤甚至死亡的风险。玩耍作为灵长类社会的一种行为文化,对其研究有助于对人类自身行为进化的不断认识,相信这方面的理论将会得到后来者的不断创新和丰富,也期望这方面的理念及经验能被及时运用到保护繁育等实践活动中。 Abstract:This article discusses the behavioral patterns, influencing factors, functions and risks of social play in primates, including information from published references and a study of Rhinopithecus roxellana by the authors. Social play involves the interaction between two or more individuals who often adjust to or influence the others' behavior. Play behavior is common among immature primates and can affect present individual survival and future reproductive success. The categories of social play in primates include common behaviors such as chasing, wrestling and jumping. Some species have developed novel behaviors such as play panting in chimpanzees (Pan troglodyte), spinning in vervet monkeys (Cercopithecus aethiops) and bridging in Tibetan macaques (Macaca thibetana). Generally, primates play most during late infancy and early juvenility, after which the average frequency of play behavior will gradually decline through adolescence to adulthood. The play behaviors of species which are evolutionarily closest to humans are more complicated and human-like than those of less developed species. Immature males often engage more in social play than females of the same age, but this varies with species, age and other factors, and in some cases the opposite is true. When selecting play partners, young primates appear to have a preference for partners who are kin, of the same sex, of similar age, and of similar dominance status because of the similarity in play motivation, less risk of being hurt, and the opportunity to form social allies. Individuals who prefer playing with partners of high dominance have increased access to food, water resources and opportunities for copulation. The frequency of play behavior of individuals living in high quality habitat is usually higher than that of individuals with low quality habitat. The same is true for individuals in larger groups and with an abundance of food compared to those in smaller groups and with a scarcity of food, respectively. Play behavior is also affected by play area, ambient temperature, familiarity among play partners and other environmental factors. For example, the play frequency of young golden monkeys (Rhinopithecus roxellana) changes with the season. In conclusion, the development of social play in non-human primates is thought to be related not only to environmental parameters such as availability of food, configuration of the play area, group size and season but also to factors related to the community itself such as age, sex, kinship and relative dominance of play partners. While engaging in play behavior, immature primates can develop improved physical fitness and survival skills, establish social relationships, enhance cognitive ability, develop troop culture and adapt to changes in the surrounding environment. These skills facilitate the transition from infant to juvenile to adult and the ability to perform the social responsibilities expected at each stage. However, social play is also risky because individuals may get injured, disabled, or even die during play. Social play, as a kind of behavioral culture in primates, should be further studied, especially in less developed species. We believe future studies on primate play will be more innovative and of higher scientific rigor. What is currently known about social play in primates should be applied to their protection and utilization. 参考文献 相似文献 引证文献