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Common Husbandry, Housing, and Animal Care Practices
Abstract
Animal care in facilities housing nonhuman primates has undergone a transformation in the past two decades, as the scientific community has learned more about the effects of husbandry practices on behavior and physiology of captive nonhuman primates. Today, husbandry consists of more than simply feeding animals and removing waste. Husbandry practices cover all aspects of animal care, from ensuring the animals’ nutritional needs to providing adequate shelter, monitoring the health of the animals, and refining procedures so that they reduce stress and distress. As such, husbandry is integral to providing optimal animal welfare. This chapter will summarize four main areas of husbandry (health monitoring, nutrition, shelter, and humane handling) and discuss how each can influence aspects of the welfare of captive nonhuman primates living in a research environment.
Chimp Haven is a private, nonprofit organization that serves as the largest chimpanzee sanctuary in the world. The National Institutes of Health supports the federal sanctuary system, which is operated by Chimp Haven, to provide lifetime care for chimpanzees who have retired from biomedical research. Chimp Haven is home to over 300 chimpanzees, with a wide variety of individual health needs including infectious diseases. The chimpanzees live in large, mixed-sex social groups within corrals, multi-dimensional enclosures, and naturally forested habitats, which presents challenges for monitoring and balancing individual versus group needs. Primate veterinarians and animal behavior directors have an obligation to collaborate for the best possible health and welfare outcomes for the species in their care. This manuscript details how veterinarians and behavioral staff at Chimp Haven interface to enhance clinical management and improve chimpanzee welfare using two clinical cases to illustrate this relationship. This is accomplished through the development of individual care plans that include the utilization of welfare assessment metrics and positive reinforcement training programs collaboratively developed between the veterinarians and behaviorists to facilitate voluntary medical procedures without the need for social isolation. Specifically, welfare metrics such as monitoring chimpanzee wounding levels and severity, as well as targeted assessments, involve the input of both the veterinarians and behaviorists. Positive reinforcement training initiatives such as weight loss, heart health, and wound care also require the interface between the two disciplines. The authors aim to demonstrate that working together provides optimal levels of expert care for both the physical and mental health of the chimpanzees in our care.
Simple Summary
At the California National Primate Research Center (CNPRC), rhesus macaques are kept in large, complex social groups outdoors because this environment helps them behave naturally and cope well. However, living in groups can lead to problems, such as fights that sometimes result in injuries. To handle these situations, a team of experts from different fields regularly meets to discuss and decide if any macaques need to be moved to protect them from repeated attacks. The team uses a careful process to identify which animals might be at risk and decide whether the individual should stay in the social group or be relocated, keeping in mind both the animal’s well-being and the stability of the whole group. This paper includes real-life examples to show how they make these tough decisions, aiming to keep all the animals physically and mentally healthy while maintaining harmony in the group.
Abstract
At the California National Primate Research Center (CNPRC), the preferred housing for rhesus macaques involves maintaining them in complex social groups outdoors, primarily for breeding purposes. This functionally appropriate environment promotes effective coping through the expression of species-typical behaviors and important aspects of species-typical social structure, thus enabling normal animal development, higher reproductive success, and the production of high-quality biological models. Despite the benefits, social housing introduces challenges like trauma from aggressive interactions. These challenges necessitate a delicate balance between tolerating some aggression and preventing repeated targeting of individuals. Therefore, the CNPRC has established a multidisciplinary working group of behavioral management experts, veterinarians, animal care, and researchers that meets regularly to review cases of animals that may need to be removed from their social group. We discuss the criteria and decision-making processes employed to manage and mitigate aggression. We describe the systematic approach to identifying at-risk individuals and the comprehensive evaluation process that guides whether to relocate an animal from their groups or not. Considerations include the welfare of the individual and the group’s social stability. This paper provides case studies demonstrating how the working group applies these criteria and processes in practical scenarios, highlighting the complexities and challenges of such decisions.
Where once it was common to house primates singly in concrete enclosures, it has since been recognized that nonhuman primates have complex behavioral needs. The purpose of this chapter is to provide an overview of the main housing and husbandry considerations for zoo-housed primates. We first address the need to balance zoo goals, ensuring good animal welfare, conservation, education, research, and entertainment within enclosure design. We then discuss some specific design considerations such as space and complexity. We end on a brief discussion regarding diet and nutrition as this is perhaps an area which requires further investigation when considering the welfare of primates in zoos.
One challenge facing zoos is balancing welfare needs with other primary goals, which include conservation, education, research, and entertainment. Managing primates in zoos involves similar welfare challenges faced by primates in other environments, which are covered elsewhere in this volume. In this chapter we identify and discuss welfare challenges that are unique to zoo-housed primates. All captive primates experience the presence of familiar humans (animal care staff), however the presence of unfamiliar humans (visitors) is common in zoo environments. In addition to providing a resource to zoo visitors, zoo primates also have an important conservation role that may involve intensive social management to facilitate captive breeding. We first discuss the influence of both familiar and unfamiliar humans on the welfare of zoo primates. We then examine the impact of different methods of social management on primate welfare.
Promoting welfare should be a goal of all facilities housing nonhuman primates. However, determining whether that goal has been met can be challenging. One means of measuring primate welfare is by assessing the animal’s behavior. Herein, we review commonly used behavioral indices for measuring welfare. The first is abnormal behavior, which is defined as behavior that differs in kind or degree from natural behavior. Abnormal behavior can indicate past or present adverse experiences, but it is also impacted by intrinsic factors such as species, temperament, age, and sex. Although abnormal behavior may in some way help an animal to cope with its environment, the presence of abnormal behavior is of concern and interventions may be warranted. Low well-being can also be measured by the display of anxiety-related self-directed behaviors such as scratching and yawning, as well as fear-related facial expressions and vocalizations, freezing, and fleeing. The benefit of utilizing normal species-appropriate anxiety behaviors is that, unlike with abnormal behavior, they are ubiquitous and can function as a “warning system,” which allows for earlier identification of environmental deficiencies and intervention. Species normative behaviors that are reflective of positive emotional states can be used to identify animals experiencing positive welfare, but determining appropriate levels of these behaviors in captivity can be challenging. Regardless of the behaviors being assessed, an understanding of the species’ behavioral repertoire is critical when using behavior as a measure of welfare. When accurately assessed, an animal’s behavior, whether normal or abnormal, can be utilized as an indicator of well-being in nonhuman primates.
The use of primates in regulated research and testing means that they are intentionally subjected to scientific procedures that have the potential to cause pain, suffering, distress, or lasting harm. These harms, combined with keeping primates in restricted laboratory conditions, are balanced against the potential (primarily human) benefits gained from their use. In this chapter, we provide a brief overview of the use of primates in laboratories, the estimated number, and purpose of use, and summarize the evidence that primates are especially vulnerable and deserve special protection compared to other animals. The 3Rs (replacement, reduction, and refinement) framework, underpinning humane science, is described, and we emphasize both the ethical and scientific needs for refinement. Refinement refers to all approaches used (by humans responsible for their care) to minimize harms and improve welfare for those primates that are still used in research after the application of the replacement and reduction principles. There is a growing body of evidence demonstrating an interplay between animals’ welfare and experimental parameters, and that this interplay affects the validity and reliability of scientific output. With this perspective, we argue that it is better to collect no data than to collect poor (e.g., invalid, unreliable) data. It is, after all, unacceptable for primates to suffer in vain and violates utilitarian principles underlying animal use. Furthermore, inconsistency in experimental approach may introduce conflicting results, increasing the likelihood of using more animals, and delaying delivery of promising therapies to the clinic. We focus on mitigating the major welfare issues faced by primates housed in laboratories through coordinated refinements across their life spans. Drawing on examples from cynomolgus macaques (Macaca fascicularis), an Old World monkey commonly used during the development of medical products, we highlight the importance of understanding the critical role humans play in the laboratory, providing environments, performing husbandry, and undertaking procedures that promote welfare and decrease harms. Our theoretical premise is that if primates are to be “fit for purpose” (i.e., well suited for the designated role), we need a proactive, concerted approach for implementing refinement that spans their lifetime.Keywords3RsFit for purposeRegulated research
Macaca fascicularis
ReliableValid data
We describe the basic and specialized requirements specifically for primate breeding colonies, including veterinary care, housing, welfare and enrichment, and management of social behavior. We emphasize that all four areas are of critical importance to the ethical and healthy productions of these animals. We explore in detail the needs for record keeping and pedigree maintenance when breeding primates, including genetic and demographic management.KeywordsNonhuman primateColony managementWelfareEnrichmentHousingPedigree managementGenetic managementInfant rearingNursery rearing
Nonhuman primates (henceforth, primates) are among the most extensively studied animal species on the planet. In this chapter I provide a brief overview of the reasons why primatology is a popular and thriving science, why primates are valuable research subjects, the scientific disciplines in which they are used, and the species and numbers involved. Globally, an estimated 100,000 to 200,000 primates are used in research every year, the majority (an estimated two-thirds) being long-tailed and rhesus macaques used mainly for pharmaceutical development, neuroscience, and infectious disease studies. I give examples of what primates may experience as part of their involvement in regulated and unregulated scientific procedures and outline how the associated ethical and welfare issues are typically addressed. Although primate research projects are conducted in a variety of settings, special attention is given in this chapter to laboratory- and zoo-based research. The role of zoos in primate conservation and education is also discussed. I conclude with some broad principles for good practice in the design, conduct, and reporting of primate research, aimed principally at students and early career scientists. Adoption of high scientific and ethical standards is important for continued funding and public support for primate research, and for garnering maximum value from it.
Primates have been kept in captivity for at least 5000 years, but only in the last 200 years they have been maintained in facilities that we would regard as zoos. During those 200 years, many important advances have been made both in zoo practice and philosophy and in the housing and husbandry of primates. Initially, zoos attempted to display many different species in a way that followed taxonomic principles. Modern zoos concentrate on a smaller number of species, many of which are of conservation importance, housed according to habitat or ecological principles. Housing has changed, too, from relatively barren cages with little furniture to naturalistic and sometimes semi-free-ranging designs. Husbandry has moved from being based on ideas of what has worked in the past to a more evidence-based scientific approach, and this has resulted in better health and longevity, and improved breeding success in the animals. At the same time, zoos have become a significant resource for researchers interested in primate biology. This chapter surveys these changes through the recent history of primates in zoos.
Rhesus monkeys (Macaca mulatta) either of wild origin or mother-reared in the laboratory were housed along in small caged from birth to 6½ yrs. Observations were made on 24 Ss that were introduced singly into a small and a large test cage. Both the laboratory mother-reared and the wild-reared Ss showed abnormal behavior. The extent of the normal behavior repertoire was not smaller in Ss showing a relatively large degree of abnormal behavior. In a large cage, more normal but less stereotyped locomotion was shown than in a small cage. However, nonlocomotory abnormal patterns were not influenced by cage dimensions. The various abnormal behaviors were randomly associated. (16 ref)
We must ensure the welfare of captive chimpanzees. One way to do so is by building environments that enable chimpanzees to express evolved cognitive abilities and skills. These environments must therefore include “cognitive enrichment” that resemble daily challenges that chimpanzees in the wild must meet if they are to survive and reproduce. In the Kumamoto Sanctuary of Kyoto University, Japan, we introduced fission–fusion emulation, a dynamic group management system in which the spatiotemporal cohesion within a group in terms of space, group size, and group membership was changed by human caretakers. Kumamoto Sanctuary also instituted a new experimental system that balances the needs of human experimenters and the chimpanzee participants by ensuring that the chimpanzees do not experience stress during experimental procedures. Moreover, because conservation has become an increasingly important consideration, the cognitive challenges at Kumamoto Sanctuary are designed to allow captive chimpanzees to engage in decision making on a daily basis. Conservation activities also need to consider the needs of local people and their chimpanzee neighbors. A plantation project in a fragmented habitat with anthropogenic activity can be regarded as environmental enrichment on a large scale, in chimpanzees’ natural habitat. These enrichment designs, one in Kumamoto Sanctuary and one in chimpanzees’ natural habitat, not only maximize chimpanzee welfare, but also enable chimpanzees to express their natural behaviors to the fullest extent possible.
Population density has been suggested to affect social interactions of individuals, but the underlying neural mechanisms remain unclear. In contrast, neurotransmission of monoamines such as serotonin (5-HT) and dopamine (DA) has been demonstrated to play important roles in social behaviors. Here, we investigated whether housing density affected social interactions of rodents and non-human primates housed in groups, and its correlations with monoamines. Japanese macaques exhibited higher plasma 5-HT, but not DA, concentrations than rhesus macaques. Similarly, C57BL/6 mice exhibited higher plasma and brain tissue 5-HT concentrations than DBA2 mice. Under crowding, C57BL/6 mice and Japanese macaques exhibited more prominent social avoidance with mates than DBA2 mice and rhesus macaques, respectively. Although DBA2 mice and rhesus macaques in crowding exhibited elevated plasma stress hormones, such stress hormone elevations associated with crowding were absent in C57BL/6 mice and Japanese macaques. Administration of parachlorophenylalanine, which inhibits 5-HT synthesis, increased social interactions and stress hormones in C57BL/6 mice under crowding. These results suggest that, animals with hyperserotonemia may exhibit social avoidance as an adaptive behavioral strategy to mitigate stress associated with crowding environments, which may also be relevant to psychiatric disorder such as autism spectrum disorder.
Animal welfare is a key issue for industries that use or impact upon animals. The accurate identification of welfare
states is particularly relevant to the field of bioscience, where the 3Rs framework encourages refinement of
experimental procedures involving animal models. The assessment and improvement of welfare states in animals
is reliant on reliable and valid measurement tools. Behavioural measures (activity, attention, posture and
vocalisation) are frequently used because they are immediate and non-invasive, however no single indicator can
yield a complete picture of the internal state of an animal. Facial expressions are extensively studied in humans
as a measure of psychological and emotional experiences but are infrequently used in animal studies, with the
exception of emerging research on pain behaviour. In this review, we discuss current evidence for facial
representations of underlying affective states, and how communicative or functional expressions can be useful
within welfare assessments. Validated tools for measuring facial movement are outlined, and the potential of
expressions as honest signals are discussed, alongside other challenges and limitations to facial expression
measurement within the context of animal welfare. We conclude that facial expression determination in animals is
a useful but underutilised measure that complements existing tools in the assessment of welfare.
Link to paper (Open Access): http://www.altex.ch/resources/epub_Descovich_of_170208.pdf
The behavioral management of laboratory nonhuman primates in the United States has not been thoroughly characterized since 2003. This article presents the results of a survey behavioral management programs at 27 facilities and covering a total of 59,636 primates, 27,916 housed in indoor cages and 31,720 in group enclosures. The survey included questions regarding program structure, implementation, and methodology associated with social housing, positive reinforcement training, positive human interaction, exercise enclosures, and several categories of inanimate enrichment. The vast majority of laboratory primates are housed socially (83%). Since 2003, the proportion of indoor-housed primates reported to be housed singly has fallen considerably, from 59% to 35% in the facilities surveyed. The use of social housing remains significantly constrained by: 1) research protocol requirements, highlighting the value of closely involved IACUCs for harmonizing research and behavioral management; and 2) the unavailability of compatible social partners, underscoring the necessity of objective analysis of the methods used to foster and maintain compatibility. Positive reinforcement training appears to have expanded and is now used at all facilities responding to the survey. The use of enrichment devices has also increased in the participating facilities. For most behavioral management techniques, concerns over the possibility of negative consequences to animals are expressed most frequently for social housing and destructible enrichment, while skepticism regarding efficacy is limited almost exclusively to sensory enrichment. Behavioral management program staffing has expanded over time in the facilities surveyed, due not only to increased numbers of dedicated behavioral management technicians but also to greater involvement of animal care technicians, suggesting an increase in the integration of behavioral care into animal husbandry. Broad awareness of common practice may assist facilities with program evaluation and assessment of progress in the field can generate recommendations for continuing the advancement of primate behavioral management programs. Am. J. Primatol.
The separate influences of spatial density and housing quality on the behavior of captive animals are difficult to measure because the two factors are often intrinsically linked. Here, we recorded affiliative and agonistic behavior in adult sooty mangabeys in various housing situations, testing spatial density and housing quality changes separately (N = 26 experienced spatial density changes; N = 12 experienced housing quality changes). We varied spatial density by 50% while holding housing quality constant and we varied housing quality while holding spatial density constant (achieved by comparing two types of run-housing that varied in the amount of visual privacy and outdoor access). Each housing condition was one month in duration. Prior to collecting data in each housing condition, we evaluated the subjects' initial responses to the change in housing environment during 2-week novelty periods. Affiliative behavior did not change during the novelty periods. Agonistic behavior initially increased slightly when spatial density increased and it decreased significantly when spatial density decreased; it also decreased when subjects moved to housing that offered more visual privacy and outdoor space, indicating that the mangabeys were sensitive to these housing changes. After the novelty periods, affiliative behavior increased under higher spatial density, but remained unchanged across housing quality conditions; agonistic behavior remained unchanged across all conditions. Results suggest that a prolonged increase in spatial density led the mangabeys to adopt a tension-reduction coping strategy, in which the increase in affiliative behavior alleviates a presumed increase in social tension. Reducing visual privacy and choice did not affect the mangabeys' behavior, post-novelty period. Thus, like many other primates, the mangabeys managed tension by flexibly adapting to changes in their housing environment in ways that reduce the risk of severe aggression. This study highlights the importance of controlled behavioral studies in facilitating data-driven management decisions that promote animal welfare. Am. J. Primatol. © 2015 Wiley Periodicals, Inc.
© 2015 Wiley Periodicals, Inc.
Chronic pain and distress are universally accepted conditions that may adversely affect an animal's quality of life (QOL) and lead to the humane euthanasia of an animal. At most research institutions and zoological parks in the USA, a veterinarian, who has physically examined the animal and reviewed the clinical records, ultimately decides when an animal has reached a humane endpoint. To aid in the difficult process of interpreting pain and distress, we have developed specific behavioural guidelines, in addition to standard clinical information, to help define unique characteristics and traits of primates to assess and promote discussion of an individual primate's QOL, and thereby, to assist in the decision-making process regarding euthanasia. These guidelines advocate the creation of a QOL team when the animal is diagnosed with a life-threatening or debilitating chronic condition, or at the time the animal is entered into a terminal study. The team compiles a list of characteristics unique to that individual animal by utilising a questionnaire and a behavioural ethogram. This list enables the team to quantitatively assess any deviations from the established normal behavioural repertoire of that individual. Concurrently, the QOL team determines the number of behavioural deviations that are needed to trigger an immediate discussion of the necessity for humane euthanasia of the animal. The team remains intact once created, and revisits the animal's condition as frequently as deemed necessary. This process improves animal welfare by continuing the quest to optimally define QOL for captive primates, and potentially for all captive animals.
Animal care in biomedical facilities housing nonhuman primates has undergone a dramatic transformation in the past two decades, with increasing emphasis on behavioral management, psychological well-being, and animal welfare. Today, providing for the psychological well-being of nonhuman primates is an integral part of animal care. Behavioral management is a comprehensive management strategy that includes enrichment, positive reinforcement training, facilities and enclosure design, positive staff–animal interactions, and behavioral monitoring in an effort to promote psychological well-being and animal welfare. Successful behavioral management strategies are tailored to the natural behavior of the species and include both social and nonsocial forms of enrichment. An increasing number of behavioral management programs include positive reinforcement training, a significant refinement to animal care practices. Appropriate behavioral management strategies can help reduce stress for nonhuman primates and prevent behavioral problems from occurring, which ultimately enhances the utility of the primate model in biomedical research. This chapter briefly summarizes several concepts that are integral to the appropriate behavioral management of laboratory primates and to the promotion of their psychological well-being and welfare.
Omega-3 fatty acids are essential for healthy brain and retinal development and have been implicated in a variety of neurodevelopmental disorders. This study used resting-state functional connectivity MRI to define the large-scale organization of the rhesus macaque brain and changes associated with differences in lifetime ω-3 fatty acid intake. Monkeys fed docosahexaenoic acid, the long-chain ω-3 fatty acid abundant in neural membranes, had cortical modular organization resembling the healthy human brain. In contrast, those with low levels of dietary ω-3 fatty acids had decreased functional connectivity within the early visual pathway and throughout higher-order associational cortex and showed impairment of distributed cortical networks. Our findings illustrate the similarity in modular cortical organization between the healthy human and macaque brain and support the notion that ω-3 fatty acids play a crucial role in developing and/or maintaining distributed, large-scale brain systems, including those essential for normal cognitive function.
Worldwide there is large variation in the age at which young macaques destined for use in research are permanently separated from their mothers, and in the subsequent social environment in which they are reared. This stems from variation in minimum weaning ages and rearing practices in guidelines on laboratory animal care and use, as well as from scientific, business and other considerations. This article summarises the literature on the effects of weaning policy on the behavioural and physical development of macaques, supplemented with production data from breeding colonies of rhesus and long-tailed macaques. The aim is to help guide decision-making to improve animal welfare and quality of science. On the basis of the evidence reviewed here, unless there is strong justification for artificial weaning on scientific or animal health grounds, it is preferable for young macaques to remain with their mothers until they have become behaviourally independent. Minimum weaning age should therefore not normally be less than 10-14 months old, but weight, health and behavioural criteria should be used to determine the most appropriate weaning age for the welfare of each individual monkey.
Promoting welfare should be a goal of all facilities housing nonhuman primates. However, determining whether that goal has been met can be challenging. One means of measuring primate welfare is by assessing the animal’s behavior. Herein, we review commonly used behavioral indices for measuring welfare. The first is abnormal behavior, which is defined as behavior that differs in kind or degree from natural behavior. Abnormal behavior can indicate past or present adverse experiences, but it is also impacted by intrinsic factors such as species, temperament, age, and sex. Although abnormal behavior may in some way help an animal to cope with its environment, the presence of abnormal behavior is of concern and interventions may be warranted. Low well-being can also be measured by the display of anxiety-related self-directed behaviors such as scratching and yawning, as well as fear-related facial expressions and vocalizations, freezing, and fleeing. The benefit of utilizing normal species-appropriate anxiety behaviors is that, unlike with abnormal behavior, they are ubiquitous and can function as a “warning system,” which allows for earlier identification of environmental deficiencies and intervention. Species normative behaviors that are reflective of positive emotional states can be used to identify animals experiencing positive welfare, but determining appropriate levels of these behaviors in captivity can be challenging. Regardless of the behaviors being assessed, an understanding of the species’ behavioral repertoire is critical when using behavior as a measure of welfare. When accurately assessed, an animal’s behavior, whether normal or abnormal, can be utilized as an indicator of well-being in nonhuman primates.
The use of primates in regulated research and testing means that they are intentionally subjected to scientific procedures that have the potential to cause pain, suffering, distress, or lasting harm. These harms, combined with keeping primates in restricted laboratory conditions, are balanced against the potential (primarily human) benefits gained from their use. In this chapter, we provide a brief overview of the use of primates in laboratories, the estimated number, and purpose of use, and summarize the evidence that primates are especially vulnerable and deserve special protection compared to other animals. The 3Rs (replacement, reduction, and refinement) framework, underpinning humane science, is described, and we emphasize both the ethical and scientific needs for refinement. Refinement refers to all approaches used (by humans responsible for their care) to minimize harms and improve welfare for those primates that are still used in research after the application of the replacement and reduction principles. There is a growing body of evidence demonstrating an interplay between animals’ welfare and experimental parameters, and that this interplay affects the validity and reliability of scientific output. With this perspective, we argue that it is better to collect no data than to collect poor (e.g., invalid, unreliable) data. It is, after all, unacceptable for primates to suffer in vain and violates utilitarian principles underlying animal use. Furthermore, inconsistency in experimental approach may introduce conflicting results, increasing the likelihood of using more animals, and delaying delivery of promising therapies to the clinic. We focus on mitigating the major welfare issues faced by primates housed in laboratories through coordinated refinements across their life spans. Drawing on examples from cynomolgus macaques (Macaca fascicularis), an Old World monkey commonly used during the development of medical products, we highlight the importance of understanding the critical role humans play in the laboratory, providing environments, performing husbandry, and undertaking procedures that promote welfare and decrease harms. Our theoretical premise is that if primates are to be “fit for purpose” (i.e., well suited for the designated role), we need a proactive, concerted approach for implementing refinement that spans their lifetime.Keywords3RsFit for purposeRegulated research
Macaca fascicularis
ReliableValid data
Many, but not all, countries and jurisdictions around the world have laws, regulations, policies, and other systems of oversight relating to the use of animals in science. There are variations in scope, scale, approach; in legal basis; in social and cultural perspectives; and in implementation. There is increasing convergence of the features of this oversight. In particular, there is increased emphasis on a wider scope of oversight to include all facets of animal use, in particular on ethical aspects and on standards and approaches to animal care and welfare. As the use of nonhuman primates in research requires special consideration of their welfare, many countries have adopted special requirements to achieve that objective. In addition, numerous professional organizations have published guidance documents designed to optimize the welfare of nonhuman primates in captive environments. The purpose of this chapter is to provide an introduction to the range of legislative approaches and to highlight associations that are impactful in this area.
The development of positive reinforcement animal training methods has been an important refinement in the care of primates living in research settings. Using operant conditioning techniques, research primates have been taught to cooperate with veterinary, husbandry, and research procedures. Successfully trained behaviors include moving to locations on cue, body examination behaviors, biological sample collection, cooperating with restraint, and promoting social housing. Classical conditioning techniques have also been used, particularly counter-conditioning, to reduce fear. This chapter describes these training accomplishments and reviews the scientific evidence for the enhancement of animal welfare associated with training. Animal training can improve the quality of the science being conducted with primate subjects and increase the ease with which people can work with the animals. Opportunities to make further progress are discussed, including more incorporation of applied behavior analysis, and thoughts on how best to develop training programs and select trainers. The use of positive reinforcement training is continuing to grow in the primate research community, and its full potential has not yet been achieved.
This volume reviews the broad topic of welfare in nonhuman primates under human care. Chapters detail the history of primates in captivity, ethical and legal issues surrounding the use of nonhuman primates as entertainment or in research, the different approaches that welfare are measured, and how housing, enrichment, and other conditions can foster or degrade welfare.
Since humans began keeping nonhuman primates we have made vast strides in understanding their cognitive abilities, strong social bonds, vibrant personalities, and their capacity for joy and suffering. With an increasing number of countries banning the use of great apes in biomedical research, the welfare of primates in zoos and research facilities has gained increasing attention.
This interdisciplinary work features contributors from many of the fields involved and those on both sides of the issue, thus providing an exhaustive overview of primate welfare. Readers from animal welfare science, primatology, animal testing, veterinary medicine, conservation to ethics and legislation will find this an important account.
Animal care in biomedical facilities has undergone major changes in the past few decades, including having dedicated and highly trained caretakers to oversee the physiological and psychological well-being of the animals in their charge. An important outcome of this high quality animal care is the close relationship that can develop between the caretaker and the animal. Once discouraged and considered a potential threat to scientific objectivity, such positive interactions are now encouraged by many facilities. This chapter summarises the current use of animals in scientific research, and the types of human–animal interactions that are typically found in the research environment. It then examines effects of such interactions and relationships on both the animal and the caretaker. Lastly, suggestions for facilitating positive interactions while reducing the potential costs, as well as directions for future research are provided.
Environmental enrichment plans for captive nonhuman primates often include provision of foraging devices. The rationale for using foraging devices is to promote species-typical activity patterns that encourage physical engagement and provide multi-sensory stimulation. However, these devices have been shown to be ineffective at sustaining manipulation over long periods of time, and often produce minimal cognitive engagement. Here we use an evidence-based approach to directly compare the amount of object-directed behavior with a foraging device and a computer-based videogame system. We recorded 11 adult male rhesus monkeys' interactions with a foraging device and two tasks within a joystick videogame cognitive test battery. Both techniques successfully produced high levels of engagement during the initial 20 min of observation. After 1 hr the monkeys manipulated the foraging device significantly less than the joystick, F(2,10) = 43.93, P < 0.0001. Subsequent testing showed that the monkeys engaged in videogame play for the majority of a 5 hr period, provided that they received a 94 mg chow pellet upon successful completion of trials. Using a model approach, we developed previously as a basis for standardized cost:benefit analysis to inform facility decisions, we calculated the comprehensive cost of incorporating a videogame system as an enrichment strategy. The videogame system has a higher initial cost compared to widely-used foraging devices, however, the ongoing labor and supply costs are relatively low. Our findings add to two decades of empirical studies by a number of laboratories that have demonstrated the successful use of videogame-based systems to promote sustained non-social cognitive engagement for macaques. The broader significance of the work lies in the application of a systematic approach to compare and contrast enrichment strategies and encourage evidence-based decision making when choosing an enrichment strategy in a manner that promotes meaningful cognitive enrichment to the animals.
Background:
Alopecia can occur in captive non-human primates, but its etiology is poorly understood. The purpose of this study was to assess alopecia and hair cortisol in rhesus monkeys and to identify the potential risk factors.
Methods:
Subjects were 117 rhesus monkeys at two National Primate Research Centers. Photographs and hair samples were obtained during routine physicals. Photographs were analyzed using Image J software to calculate hair loss, and hair samples were assayed for cortisol.
Results:
Age, days singly housed, and their interactions contributed to the alopecia model for both facilities. Sex and location changes contributed to the hair cortisol model for Facility 1; sedations contributed for Facility 2. Alopecia and hair cortisol were associated at Facility 1.
Conclusions:
Captive management practices can affect alopecia and hair cortisol. However, there are facility differences in the relationship between alopecia and hair cortisol and in the effect of intrinsic variables and management procedures.
This chapter highlights design issues related to animal-use space in an animal facility. Animal-use support space is one of the primary functional areas of an animal research facility. This is separate from, but contiguous with the animal housing space, the other primary functional area of the facility. Control of unwanted variables is paramount for research animal facilities because the data obtained from research animals can otherwise be affected, confounding interpretation of research results. In general, animal-use procedures should be conducted in areas separated from animal-care and housing rooms because, besides competing with ongoing animal husbandry activities, many use procedures may also affect research animal metabolic, physiologic, and behavioral parameters via stimulation of visual, auditory, and/or olfactory processes. There are no specific rules regarding the numbers, sizes, or types of space that must be included in a facility; these are driven by the anticipated needs that must be accommodated by an institution's research programs. Different facilities can vary appreciably depending on the programmatic requirements.
This chapter focuses on specific design and construction features of nonhuman primates (NHP) housing facilities, with descriptions of both indoor and outdoor housing structures. Facilities that house NHP incorporate many of the same design features as housing facilities for other laboratory animal species. Recognition of the specialized needs of NHP species is critical to the incorporation of design features that will streamline daily operations in these facilities by providing for a safe environment for personnel, as well as opportunities for the provision of environmental enrichment for NHP. When planning the construction of a new NHP facility, particular attention should be paid to site location. These facilities should be isolated from spaces housing other species because NHP generate significant noise. For outdoor or indoor/outdoor housing, it is important that a perimeter buffer zone be present to decrease the levels of noise and odors from impacting neighbors. The provision of environmental enrichment to promote psychological well-being, which is mandated by federal law, is an important consideration during the design phase of an NHP housing facility. Moreover, NHP facilities must be constructed to minimize vermin infestation. Of particular concern for NHP is the volume of food waste that is generated daily as a consequence of normal foraging behavior in these species.
The majority of procedures carried out during the course of biomedical research studies do not require anesthesia. However, when required, it is essential that the most appropriate and effective methods of anesthesia and analgesia be employed. As in other species, refining research procedures for nonhuman primates by careful selection of anesthesic and analgesic methods not only contributes to improving animal welfare, but also improves the quality of scientific data that is obtained. The aim of this chapter is to provide a guide to the general principles of good anesthetic practice, indicate how this needs to be integrated into an overall plan of perioperative care, and highlight some of the challenges specific to anesthetizing nonhuman primates.
Establishing a thorough preventive medicine program is crucial to protecting and maintaining the health of captive nonhuman primate colonies. A variety of components contribute to an adequate preventive medicine program and their implementation should be based on a careful risk assessment. These components are discussed in and include an occupational health and safety program to protect and monitor personnel, a comprehensive quarantine program to limit the introduction of new pathogens to an established colony, good animal husbandry to maintain the health and well-being of colony animals, thorough disease surveillance to monitor for unexpected outbreaks of disease, and an animal vaccination program.
General biologyGeneral husbandryLaboratory proceduresUse in researchWelfareFuture developmentsEuthanasiaRecord keepingReferences
Animals kept in captivity are reliant on humans for their care and welfare. Enclosure design, and choice of group mates as well as routine husbandry events such as feeding, cleaning, and health care are in the hands of human keepers. It is therefore important to understand how external human-related husbandry events affect daily behaviour routines for animals, to help promote good welfare. Predictability (or lack thereof) of these routines can have profound effects on behaviours of captive animals. This study investigates whether providing a reliable predictable signal indicating entry into indoor brown capuchin (Sapajus apella) enclosures can increase welfare. All day focal follows of 12 zoo-housed capuchins were performed, recording behaviour in relation to husbandry events. The Baseline data show that unreliable sounds of door openings and closings outside the enclosure increase anxiety-related behaviours such as self-scratching, vigilance and jerky motions, and that the capuchins were startled by keepers entering the enclosure. A reliable signal (knocking) was subsequently introduced before enclosure entry and the monkeys given two weeks to associate the signal prior to Treatment condition data collection. The results indicate that the anxiety-related behaviours were reduced in the Treatment condition compared to Baseline frequencies. We conclude that making certain husbandry events reliable and predictable through the introduction of a unique signal can have a significant positive impact on the welfare of animals. Such an approach is not time consuming and costs nothing to implement, yet can result in significant advancements in animal welfare that can be implemented in a wide range of captive settings.
Naming research animals may improve their well-being—or bias experiments.
The goal of this project was to evaluate the efficacy of a porch in decreasing feces painting in captive rhesus macaques. The porch is a small extension that is hung on the outside of a monkey's primary home cage. Porches provide many potential benefits to indoor-housed macaques, including opportunities to perch above the ground, additional space, and increased field of view. Rates of feces painting, an abnormal behavior in which the animal smears or rubs feces on a surface, were compared in 3 situations: with porch enrichment, with 'smear board' enrichment (a foraging device commonly used to decrease feces painting), and without either enrichment item. Feces painting was evaluated daily by using a 5-point scale that ranged from 0, no feces present, to 4, multiple large areas of feces. We found that subjects received significantly lower feces painting scores when given porch enrichment or smear board enrichment compared with baseline. Furthermore, subjects received significantly lower feces painting scores with porch enrichment than smear board enrichment. These results demonstrate that the porch is an effective tool to decrease feces painting in captive macaques.
Reduced space can lead to crowding in social animals. Crowding increases the risk of agonistic interactions that, in turn, may require additional physiological defensive coping mechanisms affecting health. To determine the stress induced from increased social density in a group of nineteen baboons living in an indoor/outdoor enclosure, saliva cortisol levels and rates of anxiety-related behavior were analyzed across two unique crowding episodes. Initially, mean salivary cortisol levels when animals were restricted to their indoor quarters were compared to those when they also had access to their larger outdoor enclosure. Then, mean cortisol levels were compared before, during, and after two distinct crowding periods of long and short duration. Crowding resulted in significantly elevated cortisol during crowding periods compared to non-crowded periods. Cortisol levels returned to baseline following two crowding episodes contrasting in their length and ambient climate conditions. These cortisol elevations indicate greater metabolic costs of maintaining homeostasis under social stress resulting from reduced space. Self-directed behavior, conversely, was not reliably elevated during crowding. Results suggest that the potential for negative social interactions, and/or the uncertainty associated with social threat can cause physiological stress responses detected by salivary cortisol. Self-directed behavioral measures of stress may constitute inadequate indicators of social stress in colony-housed monkeys or represent subjective emotional arousal unrelated to hypothalamic-pituitary adrenal axis activation. Am. J. Primatol. © 2015 Wiley Periodicals, Inc
The effects of controllable versus uncontrollable appetitive stimulation on socioemotional development were studied in 20 infant rhesus monkeys reared in 5 peer groups consisting of 4 monkeys each. In 2 groups (Masters), subjects had access to operant manipulanda that permitted them to control the delivery of food, water, and treats. In 2 other groups (Yoked), subjects received access to these reinforcers noncontingently. In a fifth group (Standard Rearing Control), subjects were reared in a standard laboratory cage without access to the manipulanda and the variety of reinforcers available in the Master and Yoked groups. Subjects were introduced to these rearing environments during the second month of life; during the second half of the first year, tests of socioemotional behavior commenced. Results indicated that Master subjects displayed less fear, as measured by reactions to a mechanical toy robot, and exhibited more exploratory behavior, as measured by responses to a standard primate playroom, than did Yoked subjects. Master and Yoked subjects did not differ on measures of response to social separation from peers, unless opportunities to make active coping attempts were provided, in which case Master subjects appeared to adapt or cope better. On most measures, Yoked subjects did not differ from Standard Rearing Controls. Thus the above results could be attributed to the effects of experience with increased control over appetitive environmental events rather than to the effects of prolonged exposure to noncontingent or uncontrollable appetitive stimulation.
This study addresses a recommendation in The Guide for the Care and Use of Laboratory Animals to provide singly housed nonhuman primates with intermittent access to large, enriched (play) caging. Research on the potential benefits of this type of caging is limited. The present study examines the effects of play caging on behavior, activity, and enrichment use. Singly housed, adult male, rhesus macaques (n = 10) underwent a baseline phase in their home cages, a 2-wk treatment phase with housing in play cages, and a posttreatment phase after returning to their home cages. Each subject underwent focal behavioral observations (n = 10; duration 30 min each) during each study phase, for a total of 150 h of data collection. Results showed increases in locomotion and enrichment use and a trend toward decreased abnormal behavior while subjects were in the play cage, with the durations of these behaviors returning to baseline levels after treatment. Anxiety-related behaviors decreased between the treatment and posttreatment phases but not between baseline and treatment, suggesting that outside factors may have influenced the decline. During the treatment phase, subjects spent more time in the upper quadrants of the play caging and preferred a mirror and forage boards as forms of enrichment. The greatest behavioral improvement occurred during the first week in the play cage. This study provides evidence to support the benefits of play caging for singly housed rhesus macaques.
Responses to different feeding schedules in group living capuchins (Cebus apella) were evaluated. Animals were fed on a predictable schedule for 6 weeks followed by 6 weeks on an unpredictable schedule (varied by early, on-time, or late feedings). Behavior was sampled via scan sampling at 1min intervals 1h pre-feed and 1h post-feed. It was hypothesized that meal unpredictability would alter behavior and fecal cortisol concentrations. Major differences in behavior typically associated with stress or anticipation (e.g. abnormal behavior, self-directed behavior) were not observed when feedings were switched to an unpredictable schedule. However, differences in other behavioral measures suggest that a predictable schedule is better for the well being of the animals. In the predictable schedule animals spent more time in proximity, activity, and social behavior. Though some changes in behavior during the unpredictable phase were positive (e.g. more foraging, less tension), they were restricted to on-time and early feeds. More negative changes in behavior were seen in the unpredictable phase, specifically on on-time and late feed days. In particular, in the hour before feeding animals spent less time in proximity, less time engaged in social behavior, and more time inactive. This pattern suggests that anticipation of feeding is particularly pronounced when feeding times are delayed in an unpredictable manner. Cortisol concentrations were significantly higher during the unpredictable phase than the predictable phase. Subjects did not habituate to the unpredictable feeding schedule, as evidenced by sustained elevated cortisol concentrations during the sixth week of the unpredictable feeding schedule when compared to cortisol concentrations during the predictable phase. The results of both the behavioral and physiological data suggest that predictable feeding schedules may be most beneficial to the well being of captive capuchins.
Dry bedding has been shown to be an effective enrichment strategy for small groups of captive nonhuman primates housed in cages or in small enclosures with concrete flooring. However, dry bedding is used infrequently for large groups because of the perception that its use is time- and resource-intensive. We investigated the cost-effectiveness of this enrichment strategy in large groups (30 to 50 subjects) of rhesus macaques. Macaques were housed under 3 comparison conditions for 4 wk: pine shavings (n = 4), aspen and pine shaving mixture (n = 4), and nonbedded control (n = 4). As measures of resource consumption, husbandry tasks were documented by using time-in-motion methodology, and water usage was determined. In addition, groups underwent behavioral observations to assess the effect of dry bedding. The time required to care for units did not differ between bedded and nonbedded units. However, significantly less water was used for sanitization of bedded compared with nonbedded units. Monkeys housed in bedded units showed more foraging (13.8% ± 1.6% of time in bedded compared with 4.0% ± 0.3% of time in nonbedded units) and less aggression and self-grooming. Dry bedding benefited the macaques, reduced water usage and costs, and did not affect human resources.
A group of captive of white-faced capuchin monkeys (Cebus capucinus) was observed in the absence and in the presence of four different types of deep litter: woodchips, dried ground corncob, woodwool and garden peat. In addition to baseline and litter phases, food (grain) was scattered either on the bare floor or on the litter, which was spread across the floor of a large indoor room. Behaviour was affected in different ways by the litters. Woodwool and peat had the largest range of positive effects, including in use of the floor area and in manipulatory foraging activity. The ground corncob was associated with some negative effects and the monkeys avoided using this substrate. Positive behavioural changes were also recorded when grain was scattered on the bare floor or on litter. Apart from some increases in social contacts in the presence of the two most effective litters, social behaviour was relatively unaffected by the provision of litter.
One factor not often studied in the design of feeding enrichment programs is the timetable according to which enrichments are offered. This study was performed to lend a quantitative basis to primate colony management decisions concerning feeding schedules. The objective was to determine whether feeding fresh produce meals on a predictable schedule was preferable to doing so on an unpredictable schedule from the perspective of promoting psychological well-being of chimpanzees. The subjects were 30 adult or adolescent chimpanzees (Pan troglodytes) living in four different social groups. Feeding practices were changed to a more unpredictable schedule for two of these groups, 5 or 6 months prior to the initiation of data collection; feeding of the other two groups continued on a more predictable schedule. The predictable meal was always fed within a 30 min period and the unpredictable meal was fed within a 150 min period. Observational data were collected during prefeeding and baseline periods. A mixed model multivariate analysis of variance for repeated measures revealed that inactivity was more prevalent in the prefeeding period for the chimpanzees fed on the predictable schedule than in the other study phases, and abnormal behavior showed a similar trend. These findings indicate that feeding on a more unpredictable schedule may lead to increased species-appropriate behavior. The scheduling of animal care routines deserves closer attention from those conducting research on improving care and well-being of captive primates.
Numerous studies have demonstrated that the behavior of singly caged laboratory primates can be positively affected by inanimate enrichment within the cage. The environment outside of the cage may also influence the behavior of singly caged rhesus monkeys. To test this, we compared two cohorts of yearling rhesus (Macaca mulatta); one that had only limited stimulation in the environment outside of the cage (singly caged in indoor rooms), and one that had considerable naturalistic and social stimulation in the extra-cage environment (singly caged in an outdoor building). Half the animals in each housing condition received a three-phase enrichment program and the rest served as controls. Subjects that had sensory access to social groups of conspecifics spent significantly more time drinking, feeding, and behaving abnormally, and significantly less time inactive and playing than did subjects that only had sensory access to other singly caged rhesus. Enriched subjects in both settings spent significantly more time playing and less time self-grooming than did controls. There was also a significant interaction for time spent in play, with enriched subjects living indoors playing the most. Although subjects that received considerable stimulation from outside of the cage spent more time engaged in abnormal behavior, most was pacing; usually in response to human manipulations of the other monkeys in the colony. Subjects housed indoors, with limited extra-cage stimulation spent less time pacing, but more time in potentially injurious abnormal activities. Among enriched subjects only, those housed indoors spent less time drinking and behaving abnormally and more time playing and using enrichment. Inanimate enrichment within the cage led to consistent positive changes in behavior for singly housed rhesus. Although the environment outside of the cage was shown to influence behavior, it was not clear whether exposure to numerous social and naturalistic stimuli was preferable to more limited stimulation for promoting well-being. Although the increased stimulation associated with a complex extra-cage environment is usually considered beneficial, not all such stimulation is positive. Frequent disturbances to social groups in view of singly caged subjects resulted in increased pacing, but the complex extra-cage environment also provided subjects with more opportunities to express and observe components of the species-typical behavioral repertoire.
Newly proposed federal regulations will mandate that singly caged non-human primates be kept in cages larger than the current minimum standard, or be given 4 hours in an exercise cage per week. In order to evaluate the effectiveness of increasing cage size in improving well-being, the behavioral and heart rate responses of 10 female rhesus monkeys (Macaca mulatta) to three different cage sizes were measured. With the exception of vocalizations, no significant differences in behavior were obtained. Grunts increased in the largest cage, following the birth of an infant in a cage within view of the test cages. No differences with respect to cage size were found in heart rate or activity level, although there were significant variations at different times of day. We conclude that modest increases in cage size are less likely to enrich the environment of singly caged laboratory primates than are changes in social opportunities or increases in environmental complexity.
We investigated the effects of a six-fold increase in cage size on the behaviour of individually housed male rhesus monkeys. Limitations of previous studies included the magnitude of change in cage size, the length of the observation period, and the potential confounds of relocation. Prior to this study, eight male monkeys were individually housed in pens (6.77m3) for varying lengths of time before moving to baboon cages (1.24m3) located within their pens. After 2 years in baboon cages, monkeys were returned to their pen environment (6.77m3). Monkeys were observed for forty 5min observation periods representing four phases: short (first 4 months) and long-term (after 23 months) exposure to the baboon cage followed by short (first month) and long-term (after 8 months) exposure to the pen environment. Contrary to expectations, general activity decreased and abnormal behaviour remained unchanged when the monkeys were returned to their pens. However, tension-related behaviour decreased significantly with exposure to a larger cage. The results of this study suggest that cage size does not have a detectable impact on habitual kinds of abnormal behaviour but may significantly affect the level of tension.
The aim of this study was to analyse the influence of the presence of seeds and litter on the time budget of a family group of red-capped mangabeys, to improve animal welfare. Five experimental situations were tested in succession: (1) bare ground (without making any particular modifications of the cage), (2) seeds added to fruits ration (seeds were dispersed over the bare ground), (3) litter on the ground and seed added to food ration, (4) litter added without seed, (5) bare ground as in first situation. Addition of seeds and litter modified to various degrees the behaviour of these animals. The addition of both litter and seeds induced a significant decline in self-directed activities and a significant increase in search for food. The presence of litter, with or without seeds, induced diversification of occupation of space. Behavioural responses to the different modifications of the environment in the cage varied between individuals with females varied more than males.
Young rhesus monkeys exposed to conditions of social restriction are subject to stress. The physiological indicator, plasma cortisol, can be used to measure this stress. A technique using dexamethasone suppression-adrenocorticotropic hormone (ACTH) challenge was used to determine whether inanimate enrichment and social housing condition affected plasma cortisol levels in juvenile rhesus monkeys. Cortisol levels in two cohorts of monkeys (N = 64) were determined first while monkeys were caged singly and then while caged in pairs. Both control and enriched subjects received the dexamethasone suppression-ACTH challenge procedure and, for each cohort, cortisol samples were obtained after 10 and 12 months of single-caging and subsequently after 2 and 4 months of pair-housing. Compared with controls, experimental subjects receiving inanimate environmental enrichment did not show lower levels of plasma cortisol. Although environmental enrichment may lead to behavioural improvements, it did not affect adrenal function in this study. Social housing condition (single vs. pair) also did not affect cortisol. Monkeys in most conditions responded appropriately to the dexamethasone suppression-ACTH challenge, indicating that levels of stress were not extreme. There were a number of significant interaction effects that were due to an atypical set of results for one of the control groups in one of the singly housed test sessions. Monkeys that spent their year of single-caging in indoor rooms showed higher activations of the hypothalamic-pituitary-adrenal system than did monkeys that spent their year of single-caging in outdoor buildings. This suggests that aspects of the environment outside of the cage (conspecific activity, environmental variation, etc.) may influence plasma cortisol. This is surprising, considering that inanimate and social enhancements within the cage had little effect.
Captive rhesus macaques sometimes exhibit undesirable abnormal behaviors, such as motor stereotypic behavior (MSB) and self-abuse. Many risk factors for these behaviors have been identified but the list is far from comprehensive, and large individual differences in rate of behavior expression remain. The goal of the current study was to determine which experiences predict expression of MSB and self-biting, and if individual differences in personality can account for additional variation in MSB expression. A risk factor analysis was performed utilizing data from over 4,000 rhesus monkeys at the California National Primate Research Center. Data were analyzed using model selection, with the best fitting models evaluated using Akaike Information Criterion. Results confirmed previous research that males exhibit more MSB and self-biting than females, MSB decreases with age, and indoor reared animals exhibit more MSB and self-biting than outdoor reared animals. Additionally, results indicated that animals exhibited less MSB and self-biting for each year spent outdoors; frequency of room moves and number of projects positively predicted MSB; pair separations positively predicted MSB and self-biting; pair housed animals expressed less MSB than single housed and grate paired animals; and that animals expressed more MSB and self-biting when in bottom rack cages, or cages near the room entrance. Based on these results we recommend limiting exposure to these risk factors when possible. Our results also demonstrated a relationship between personality and MSB expression, with animals low on gentle temperament, active in response to a human intruder, and high on novel object contact expressing more MSB. From these results we propose that an animal's MSB is related to its predisposition for an active personality, with active animals expressing higher rates of MSB. Am. J. Primatol. 9999:XX-XX, 2013. © 2013 Wiley Periodicals, Inc.
Seventy-five percent of rhesus macaques at national primate research centers are housed outside. Annually, 15–39% of these animals experience diarrhea and require veterinary treatment for dehydration, electrolyte imbalance, or weight loss. An estimated 21–33% of these patients will die or be euthanized. Many studies have explored the various infectious etiologies of non-human primate diarrhea. However, there is little published information on diarrhea incidence rates and risk factors in outdoor-housed rhesus macaques. Without this information, it is challenging to determine endemic and epidemic diarrhea levels, or to develop and evaluate mitigation strategies. Using electronic medical records, we conducted a retrospective cohort study to calculate diarrhea incidence rates for rhesus macaques (N = 3,181) housed in three different outdoor housing types (corrals, shelters, and temporary housing) at the Oregon National Primate Research Center between November 1, 2009 and October 31, 2010. With multiple logistic regression analysis, we determined the relative risk of housing type, sex, and age on development of diarrhea. Diarrhea incidence and mortality in our population was lower than many published ranges. Type of outdoor housing, age, and previous diarrhea episode were positively correlated with diarrhea risk. Younger animals in smaller shelters and temporary housing had a greater risk of acquiring diarrhea, with juvenile animals (0.7–3.9 years) having the highest mortality rate. Sex was not a risk factor, but adult females with diarrhea were more likely to develop life-threatening complications than adult males. We also constructed a predictive model for diarrhea-associated mortality using Classification and Regression Tree. Findings from this study will be used to develop and evaluate mitigation strategies in our outdoor-housed population and to provide a foundation for genetic susceptibility and immune function testing. Am. J. Primatol. 75:872–882, 2013.
Rhesus macaques (Macaca mulatta) housed indoors experience many routine husbandry activities on a daily basis. The anticipation of these events can lead to stress, regardless of whether the events themselves are positive or aversive in nature. The specific goal of this study was to identify whether increasing the predictability of husbandry events could decrease stress and anxiety in captive rhesus macaques. This study was conducted on 39 single-housed subjects in four indoor rooms at the Oregon National Primate Research Center. Temporal and signaled predictability were added to four daily husbandry events: morning and afternoon feeding, enrichment distribution, and room cleaning. Temporally predictable husbandry events occurred reliably at the same time daily, while signaled predictable husbandry events were preceded by a distinct event-specific signal in the form of a doorbell. Informal tests prior to study onset found the doorbells not to be aversive to the subjects. Subjects received each of four treatments: unpredictable events, temporally predictable events, signaled predictable events, and temporally and signaled predictable events. Change in stress was evaluated by monitoring changes in motor stereotypies and displacement behaviors. Our results showed that subjects displayed less stress and anticipatory behaviors related to feeding and enrichment events when the events were temporally predictable (P < 0 .0001). When husbandry events were preceded by a reliable signal, subjects vocalized less prior to the event and were less responsive to activity outside of the room (P < 0 .01). However this may have come at a cost as the animals were extremely reactive to the doorbell signals and showed a heightened stress response during the actual husbandry events (P < 0 .01). Similar to temporal predictability alone, when temporal predictability was combined with signaled predictability subjects displayed less stress and anticipatory behaviors related to feeding and enrichment events (P < 0 .0001). In addition, when both forms of predictability were combined subjects showed less stress behaviors while waiting for daily room cleaning (P < 0 .01). When signaled predictability was paired with temporal predictability subjects no longer had the negative response to the doorbell signal, as they were able to predict and anticipate when the events would occur. Because these results are not necessarily applicable to animals that are given control over their environment or housed in a group setting, the management recommendation that can be made from this study is that temporal predictability of feeding reduces stress and anxiety and is thus beneficial to captive indoor single-housed rhesus macaques.
It has been suggested that housing of laboratory primates in two-tiered racks adversely affects the psychological well-being of those primates housed on the lower row. Excessive darkness and its consequences are among the factors suggested to account for the supposed diminished well-being of lower-row inhabitants. Additionally, two-tiered housing has been suggested to introduce unacceptable variation into experimental designs, potentially necessitating additional subjects and/or invalidating results. Only recently have data been published to address these issues, but all studies have involved small numbers of subjects. In the present study, we compared the behaviour of 45 yearling rhesus macaques (Macaca mulatta) housed in upper-row cages with the behaviour of 48 yearling rhesus macaques housed in lower-row cages during a year of single housing. There were no significant differences across cage locations for time spent performing behaviours indicative of diminished psychological well-being (abnormal behaviour, inactivity, vocalisation, self-directed grooming) or for species-typical activities (feeding, playing). The difference in time spent exploring between macaques housed on the lower row and those housed on the upper row approached significance, with lower-row-housed animals spending more time exploring. Although lower-row cages are significantly darker than upper-row cages at our facility, the data from the present study demonstrate that the diminished lighting and other supposed disadvantages experienced by lower-row-housed monkeys have few behavioural consequences. Thus, there are now additional empirical data that suggest that lower-row-housed monkeys are not suffering in a "monkey cave", and that the findings of research projects using two-tiered housing systems are unlikely to be compromised.