Celebrating a Life by Recognizing Realities

This special issue on nonhuman primate behavior and welfare, the proceedings of a special Animal Behavior Society session, celebrates the life of Dr. Sylvia Taylor (1963-2005). Sylvia's premature death reminded her friends to recognize the reality that life is short, but one can make the most of it. Many individuals and organizations have also recognized the reality that an educational venture such as this one requires adequate funding and support. Their generosity has made this undertaking a success. The idea behind the session was to recognize the reality that one cannot ensure nonhuman animal welfare without understanding animal behavior, and to explore the ways in which this principle applies to primates. One must also recognize the reality that nonhuman primate welfare depends on understanding the behavior of the human primate as well as the nonhuman primate. Ensuring the welfare of the nonhuman primate sometimes requires educating and motivating the human primate. This special issue will hopefully provide helpful information to increase the reader's knowledge of primate behavior and welfare and to help the reader educate others on these important topics.     

Stereotypies in Captive Primates and the Use of Inositol: Lessons from Obsessive–Compulsive Disorder in Humans

Animal stereotypies have long been used in the study of obsessive–compulsive disorder (OCD) in humans. These studies have led to the understanding of some of the molecular pathways in the disorder and the use of selective serotonin reuptake inhibitors and myo-inositol in the treatment of these conditions. If animal models, especially nonhuman primate models, were used to study human disorders and if the resulting treatments were successful, then conversely one should be able to treat nonhuman primate stereotypies with similar methods. We here summarize animal models of OCD (including nonhuman primate models) and human OCD treatments, and using successful human treatment by myo-inositol as models, recommend the use of myo-inositol in good captive management practice and the treatment of nonhuman primate stereotypies. We believe that this would be particularly useful in the treatment of stereotypies in nonhuman primates because they are physiologically so similar to humans.     

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。     

Editor's introduction to the Journal of Applied Animal Welfare Science

Animal welfare names a science in which investigators ask the general question: What are the capacities, sensibilities, needs, and interests of animals as they relate to their welfare? The objects of study in this emerging field are exclusively animals other than humans. Numerous contexts give rise to this interest in nonhuman animal welfare: The intensification of the use of animals since World War II, particularly on the farm and in the laboratory. The development of moral philosophies that establish nonhuman animals as objects of moral consideration. The advances in science in fields that have added to our understanding of animals, such as cognitive ethology. Advances in technology that give us more direct access to human physiology and psychology and undercut the tradition of using animal models. The success of the contemporary animal rights movement in placing the issue of the treatment of animals before the public.     

The relevance of non-human primate and rodent malaria models for humans

At the 2010 Keystone Symposium on "Malaria: new approaches to understanding Host-Parasite interactions", an extra scientific session to discuss animal models in malaria research was convened at the request of participants. This was prompted by the concern of investigators that skepticism in the malaria community about the use and relevance of animal models, particularly rodent models of severe malaria, has impacted on funding decisions and publication of research using animal models. Several speakers took the opportunity to demonstrate the similarities between findings in rodent models and human severe disease, as well as points of difference. The variety of malaria presentations in the different experimental models parallels the wide diversity of human malaria disease and, therefore, might be viewed as a strength. Many of the key features of human malaria can be replicated in a variety of nonhuman primate models, which are very under-utilized. The importance of animal models in the discovery of new anti-malarial drugs was emphasized. The major conclusions of the session were that experimental and human studies should be more closely linked so that they inform each other, and that there should be wider access to relevant clinical material.     

Willingness to Pay: Animal Welfare and Related Influencing Factors in China

Personal willingness to pay, an important research aspect on nonhuman animal welfare, is the foundation of animal welfare legislation. As China has no special laws on the issue, it is important to study animal welfare. This article assesses personal willingness to pay for animal welfare in China, using the Contingent Valuation Method. Based on collected data of 229 visitors from Heilongjiang Northeast Tiger Garden (Harbin), Beijing Zoo, Changchun Zoo and Botanical Garden, Dalian Forest Zoo, and Harbin North Forest Zoo, the study researched willingness to pay for animal welfare and associated influence factors in China. Results showed a high rate of personal willingness to pay (89.5%). Factors such as age, education, and income had obvious effects on personal willingness to pay; however, gender and career had only slight effects.     

Role of the nonhuman primate for research related to women's health

This overview of the current status of medical problems that affect women is related to current studies on pathophysiology and therapeutic interventions using nonhuman primates to demonstrate the utility of the primate model for the study of disease processes in women. The current medical literature on women's health is compared with the literature on nonhuman primate research. The findings reviewed in the articles of ILAR Journal Volume 45 Issue 2 of 2004 are evaluated in the context of the scope and problems associated with disease entities in women. Nonhuman primate research with known information regarding women's disease is discussed, and the utility of the animal model for the study of human disease is highlighted, based on its significant relevance due to similarities of nonhuman primate and human subjects' physiology, metabolism, and responses to therapeutic interventions. Additional advantages of the animal model include the ability to control the experimental environment and the capacity to perform chronic study procedures. These findings allow us to utilize the nonhuman primate as the most relevant model in the animal world for the study of human disease processes.     

Willingness to pay: animal welfare and related influencing factors in China

Personal willingness to pay, an important research aspect on nonhuman animal welfare, is the foundation of animal welfare legislation. As China has no special laws on the issue, it is important to study animal welfare. This article assesses personal willingness to pay for animal welfare in China, using the Contingent Valuation Method. Based on collected data of 229 visitors from Heilongjiang Northeast Tiger Garden (Harbin), Beijing Zoo, Changchun Zoo and Botanical Garden, Dalian Forest Zoo, and Harbin North Forest Zoo, the study researched willingness to pay for animal welfare and associated influence factors in China. Results showed a high rate of personal willingness to pay (89.5%). Factors such as age, education, and income had obvious effects on personal willingness to pay; however, gender and career had only slight effects.     

An hourly variation in zoo visitor interest: measurement and significance for animal welfare research

A methodological difficulty facing welfare research on nonhuman animals in the zoo is the large number of uncontrolled variables due to variation within and between study sites. Zoo visitors act as uncontrolled variables, with number, density, size, and behavior constantly changing. This is worrisome because previous research linked visitor variables to animal behavioral changes indicative of stress. There are implications for research design: Studies not accounting for visitors' effect on animal welfare risk confounding (visitor) variables distorting their findings. Zoos need methods to measure and minimize effects of visitor behavior and to ensure that there are no hidden variables in research models. This article identifies a previously unreported variable—hourly variation (decrease) in visitor interest—that may impinge on animal welfare and validates a methodology for measuring it. That visitor interest wanes across the course of the day has important implications for animal welfare management; visitor effects on animal welfare are likely to occur, or intensify, during the morning or in earlier visits when visitor interest is greatest. This article discusses this issue and possible solutions to reduce visitor effects on animal well-being.     

Primate archaeology 3.0

The new field of primate archaeology investigates the technological behavior and material record of nonhuman primates, providing valuable comparative data on our understanding of human technological evolution. Yet, paralleling hominin archaeology, the field is largely biased toward the analysis of lithic artifacts. While valuable comparative data have been gained through an examination of extant nonhuman primate tool use and its archaeological record, focusing on this one single aspect provides limited insights. It is therefore necessary to explore to what extent other non-technological activities, such as non-tool aided feeding, traveling, social behaviors or ritual displays, leave traces that could be detected in the archaeological record. Here we propose four new areas of investigation which we believe have been largely overlooked by primate archaeology and that are crucial to uncovering the full archaeological potential of the primate behavioral repertoire, including that of our own: (1) Plant technology; (2) Archaeology beyond technology; (3) Landscape archaeology; and (4) Primate cultural heritage. We discuss each theme in the context of the latest developments and challenges, as well as propose future directions. Developing a more “inclusive” primate archaeology will not only benefit the study of primate evolution in its own right but will aid conservation efforts by increasing our understanding of changes in primate-environment interactions over time.     

非人灵长类糖尿病动物模型研究进展

糖尿病是继心血管疾病和肿瘤之后的另一种严重危害人类健康的重要慢性疾病,据世界卫生组织(WHO)报道,2009年全世界约有2.2亿糖尿病患者。对糖尿病发病机理的研究、预防和诊断、治疗药物的筛选和评价都需要合适的动物模型。在已报道的糖尿病动物模型中,非人灵长类动物糖尿病病程、病症与人类的糖尿病最为相似。该文从糖尿病动物模型的来源归纳了目前报道的主要的非人灵长类糖尿病模型,重点介绍了猕猴、食蟹猴和树鼩糖尿病模型及其特征,并对该领域的发展提出了一些思考。     

An Hourly Variation in Zoo Visitor Interest: Measurement and Significance for Animal Welfare Research

A methodological difficulty facing welfare research on nonhuman animals in the zoo is the large number of uncontrolled variables due to variation within and between study sites. Zoo visitors act as uncontrolled variables, with number, density, size, and behavior constantly changing. This is worrisome because previous research linked visitor variables to animal behavioral changes indicative of stress. There are implications for research design: Studies not accounting for visitors' effect on animal welfare risk confounding (visitor) variables distorting their findings. Zoos need methods to measure and minimize effects of visitor behavior and to ensure that there are no hidden variables in research models. This article identifies a previously unreported variable—hourly variation (decrease) in visitor interest—that may impinge on animal welfare and validates a methodology for measuring it. That visitor interest wanes across the course of the day has important implications for animal welfare management; visitor effects on animal welfare are likely to occur, or intensify, during the morning or in earlier visits when visitor interest is greatest. This article discusses this issue and possible solutions to reduce visitor effects on animal well-being.     

U.S. laws, regulations, and policies important to managers of nonhuman primate colonies

The various animal welfare laws, regulations, policies, accreditation standards, and welfare groups have an obvious impact on the activities of managers of nonhuman primate colonies. Federal organizations such as the Department of Health and Human Services, Department of Interior, the Department of Agriculture, the Department of Transportation, and the Justice Department regulate many aspects of animal management. Pertinent guidance is available through scientific organizations such as the American Association for Accreditation of Laboratory Animal Care and the National Academy of Sciences. Finally, the recommendations of responsible animal welfare organizations should also receive careful consideration.     

中国非人灵长类物种的行为偏侧研究进展

行为偏侧是指动物进行某一行为时偏好使用某一侧肢体或感觉器官。行为偏侧作为脑偏侧所对应的可观测的行为指标,是动物行为适应性进化的代表性特征之一,它在个体水平上影响着个体适合度,在群体水平上是社会性物种的一种进化稳定策略,具有重要的生态和进化意义。中国非人灵长类资源丰富,而中国非人灵长类的行为偏侧研究起步较晚,始于二十世纪八十年代。本文系统归纳中国非人灵长类物种的行为偏侧研究进展,并基于当前研究现状,为今后发展提出积极建议。     

Equine Welfare in England and Wales: Exploration of Stakeholders' Understanding

Investigating how those responsible for the care of nonhuman animals understand the concept of animal welfare is important for animal welfare improvement. In-depth interviews with 31 equine stakeholders were used to explore their perceptions and understanding of welfare. The results showed the stakeholders understood the concept of welfare in 4 ways. Firstly, welfare was understood in terms of the provision of resources—for example, food. Secondly, a “horse-centered” understanding of welfare was articulated; this understanding included the horses' mental state and was linked to natural behavior. Thirdly, the word welfare had negative connotations, and for some, good welfare was achieved through avoidance of negative states. Finally, interviewees discussed incidents that occurred in their own familiar contexts but suggested that these were not welfare problems. Evidence indicated that the ways in which equine stakeholders understood the concept of welfare might have been acting as a barrier to the alleviation of some equine welfare problems. There is a need for strategies aimed at improving equine welfare to consider stakeholder constructs of welfare and the ways in which these constructs are generated and acted upon.     

Current status and future directions of applied behavioral research for animal welfare and conservation

The papers that follow in this special issue reflect the state of knowledge and theory in the fields of animal welfare and conservation behavior. A particular focus is placed on how enrichment can be used judiciously to improve welfare and to prepare captive animals for release back to the wild. However, my purpose here is not simply to reiterate what the contributors of this special issue have said, but to provide an overview of the major themes, problems, and opportunities in applied animal behavior related to conservation and welfare. I review major issues in three interrelated areas: captive welfare, captive breeding, and conservation behavior research for wild populations. Despite many advancements in welfare science, one of the most significant impediments to a predictive science of welfare is the need to further refine theories advanced to explain environment–welfare relationships. I provide a brief overview of ten theories that have been proposed to explain good or poor welfare and suggest that they need to be made more conceptually distinct so that clear hypotheses can be articulated, and predictions made and tested. Captive breeding programs for ex situ conservation have borrowed and applied many of the concepts involved in welfare science to great advantage. Other keys to successful breeding programs include applying knowledge of social organization and processes to enhance reproduction; for example, finding the right combination of individuals to get animals breeding. However, behaviorists are only recently learning how to manipulate behavioral mechanisms, such as signaling behavior and mate choice, to optimize captive breeding for conservation. The emerging field of conservation behavior has played a role in captive breeding, but also is poised to play a major role in in situ conservation. Applied behavioral research can illuminate a number of issues important to conservation, including behavioral responses to habitat fragmentation and human disturbance (e.g., pollutants, noise, and light), and human–animal conflict (e.g., crop-raiding). Behavioral decisions made when animals are dispersing and selecting habitat for settlement determine the distribution of animals on the landscape and are important to understand for improving reserve and habitat corridor design. Captive–release and translocation programs require detailed behavioral knowledge to predict responses to novel environments and ensure that animals are adequately prepared for environmental change. This review underscores that many of the behavioral processes of interest to welfare science are also important for conservation behavior: perception, stress, assessment and decision-making rules, and other behavioral and physiological mechanisms. If properly understood, these mechanisms can be manipulated in the service of conservation goals, moving the field of conservation behavior from implication to application. A better integration of the disciplines of animal welfare and conservation behavior – together tackling problems at multiple levels of analysis – will further these goals.     

Empty Nest: A Case Study of Maternal Response to Separation From a Juvenile Offspring in a Captive Sumatran Orangutan (Pongo pygmaeus abelii)

Improving the welfare of captive nonhuman primates requires evaluating the stressors created by the captive environment and reducing their negative effects. Social separation, although sometimes necessary for managing the genetic diversity of captive populations of animals, causes both psychological and physiological stress in human and primate monkey infants. Few studies have examined the maternal response of great ape mothers to separation from their offspring. This article describes the behavioral changes of a mother orangutan (Pongo pygmaeus abelii) after separation from her juvenile daughter. We collected data on measures of proximity and social behavior before the separation of the mother-infant dyad and of locomotion, arboreality, abnormal behavior, solitary behavior, and vocalization both before and after separation. We observed no behavioral indications of protest but observed some indications of despair after separation: decreased locomotion, increased inactivity, and increased self-directed behavior. In addition, we observed increases in arboreality and object-oriented behavior during morning sessions. These findings suggest that mother-juvenile separation in orangutans might be less stressful for mothers than might be expected. Such research has implications for the welfare and management of captive animals.     

Empty Nest: A Case Study of Maternal Response to Separation From a Juvenile Offspring in a Captive Sumatran Orangutan (Pongo pygmaeus abelii)

Improving the welfare of captive nonhuman primates requires evaluating the stressors created by the captive environment and reducing their negative effects. Social separation, although sometimes necessary for managing the genetic diversity of captive populations of animals, causes both psychological and physiological stress in human and primate monkey infants. Few studies have examined the maternal response of great ape mothers to separation from their offspring. This article describes the behavioral changes of a mother orangutan (Pongo pygmaeus abelii) after separation from her juvenile daughter. We collected data on measures of proximity and social behavior before the separation of the mother-infant dyad and of locomotion, arboreality, abnormal behavior, solitary behavior, and vocalization both before and after separation. We observed no behavioral indications of protest but observed some indications of despair after separation: decreased locomotion, increased inactivity, and increased self-directed behavior. In addition, we observed increases in arboreality and object-oriented behavior during morning sessions. These findings suggest that mother-juvenile separation in orangutans might be less stressful for mothers than might be expected. Such research has implications for the welfare and management of captive animals.     

The Implications of Primate Behavioral Flexibility for Sustainable Human–Primate Coexistence in Anthropogenic Habitats

People are an inescapable aspect of most environments inhabited by nonhuman primates today. Consequently, interest has grown in how primates adjust their behavior to live in anthropogenic habitats. However, our understanding of primate behavioral flexibility and the degree to which it will enable primates to survive alongside people in the long term remains limited. This Special Issue brings together a collection of papers that extend our knowledge of this subject. In this introduction, we first review the literature to identify past and present trends in research and then introduce the contributions to this Special Issue. Our literature review confirms that publications on primate behavior in anthropogenic habitats, including interactions with people, increased markedly since the 2000s. Publications concern a diversity of primates but include only 17% of currently recognized species, with certain primates overrepresented in studies, e.g., chimpanzees and macaques. Primates exhibit behavioral flexibility in anthropogenic habitats in various ways, most commonly documented as dietary adjustments, i.e., incorporation of human foods including agricultural crops and provisioned items, and as differences in activity, ranging, grouping patterns, and social organization, associated with changing anthropogenic factors. Publications are more likely to include information on negative rather than positive or neutral interactions between humans and primates. The contributions to this Special Issue include both empirical research and reviews that examine various aspects of the human–primate interface. Collectively, they show that primate behavior in shared landscapes does not always conflict with human interests, and demonstrate the value of examining behavior from a cost–benefit perspective without making prior assumptions concerning the nature of interactions. Careful interdisciplinary research has the potential to greatly improve our understanding of the complexities of human–primate interactions, and is crucial for identifying appropriate mechanisms to enable sustainable human–primate coexistence in the 21st century and beyond.     

Application of microarray technology in primate behavioral neuroscience research

Gene expression profiling of brain tissue samples applied to DNA microarrays promises to provide novel insights into the neurobiological bases of primate behavior. The strength of the microarray technology lies in the ability to simultaneously measure the expression levels of all genes in defined brain regions that are known to mediate behavior. The application of microarrays presents, however, various limitations and challenges for primate neuroscience research. Low RNA abundance, modest changes in gene expression, heterogeneous distribution of mRNA among cell subpopulations, and individual differences in behavior all mandate great care in the collection, processing, and analysis of brain tissue. A unique problem for nonhuman primate research is the limited availability of species-specific arrays. Arrays designed for humans are often used, but expression level differences are inevitably confounded by gene sequence differences in all cross-species array applications. Tools to deal with this problem are currently being developed. Here we review these methodological issues, and provide examples from our experiences using human arrays to examine brain tissue samples from squirrel monkeys. Until species-specific microarrays become more widely available, great caution must be taken in the assessment and interpretation of microarray data from nonhuman primates. Nevertheless, the application of human microarrays in nonhuman primate neuroscience research recovers useful information from thousands of genes, and represents an important new strategy for understanding the molecular complexity of behavior and mental health.