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5 Adult male rhesus macaque (Macaca mulatta) with arm in blood sleeve. The monkey was trained to put his arm in the blood sleeve and hold onto the peg at the distal end until released by the trainer. (Photo reprinted from Coleman et al. (2008, figure 1, p. 38) with permission from the Journal of the American Association of Laboratory Animal Science.)
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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 managem...
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... , although other studies have not found this relationship (K.Baker et al., 2010). While PRT is often time-consuming, and thus may not be feasible in all situations, it confers several other advantages to both humans and primates, including compliance with procedures, increased safety, and decreased stress (e.g.,Bliss-Moreau et al., 2013;Coleman et al., 2012;Graham et al., 2012;Veeder et al., 2009). Treatment success relies heavily on the working understanding of animal training techniques by the trainer and the provision of the time and tools from managers ...
Across captive settings, nonhuman primates may develop an array of abnormal behaviors including stereotypic and self-injurious behavior. Abnormal behavior can indicate a state of poor welfare, since it is often associated with a suboptimal environment. However, this may not always be the case as some behaviors can develop independently of any psychological distress, be triggered in environments known to promote welfare, and be part of an animal's coping mechanism. Furthermore, not all animals develop abnormal behavior, which has led researchers to assess risk factors that differentiate individuals in the display of these behaviors. Intrinsic risk factors that have been identified include the animal's species and genetics, age, sex, temperament, and clinical condition, while environmental risk factors include variables such as the animal's rearing, housing condition, husbandry procedures, and research experiences. To identify specific triggers and at-risk animals, the expression of abnormal behavior in captive nonhuman primates should be routinely addressed in a consistent manner by appropriately trained staff. Which behaviors to assess, what assessment methods to use, which primates to monitor, and the aims of data collection should all be identified before proceeding to an intervention and/or treatment. This article provides guidance for this process, by presenting an overview of known triggers and risk factors that should be considered, steps to design a comprehensive evaluation plan, and strategies that might be used for prevention or treatment. It also outlines the tools and processes for assessing and evaluating behavior in an appendix. This process will lead to a better understanding of abnormal behavior in captive primate colonies and ultimately to improved welfare.
... However, the increased safety is likely also due to the behavior of the monkeys themselves. As mentioned above, the monkeys were calmer in the CBC than the ORC, and working with a calm, cooperative monkey is safer than working with an anxious monkey [39]. ...
Collaborative semen collection in monkeys is a valuable tool in research, animal collection management, and conservation efforts. To obtain samples, monkeys are often restrained in open restraint chairs (ORC) with the “pole and collar” technique. While commonly used, this restraint is not tolerated by all individuals; some become anxious or aggressive towards the poles and people. In an effort to refine this procedure and improve welfare of the monkeys, we examined the use of a “closed box chair” (CBC), a clear, plexiglass box in which the monkey is trained to sit for sperm collection. The CBC does not require pole and collar, and although legs are secured, the arms and neck are not restrained. The use of CBCs has increased in recent years; however, there are few studies demonstrating its effects on scientific outcomes. We used positive reinforcement techniques to train 34 adult male rhesus macaques (Macaca mulatta) to provide semen samples using either the ORC or the CBC. While all CBC monkeys (n = 14) were reliably trained for this procedure, only 75% of ORC (n = 20) males completed the training (p = 0.04). It took significantly less time to train animals in the CBC than the ORC (201.0 vs. 412.4 min; p <0.001). In a controlled subset, males restrained with ORC (n = 7) produced a significantly lower ejaculatory volume than those collected by CBC (n = 10) (297.6 µL vs 522.1 µL respectively; p = 0.04) and had a lower concentration of sperm (186.0 × 106/mL vs 367.5 × 106/mL respectively; p = 0.017), although there were no differences with respect to sperm motility (p = 0.15). Our data suggest the closed box chair technique reduces stress on the animals while enhancing semen quality, supporting the use of the CBC as an important refinement.
... Strategies that are categorized as sensory stimulation alone are those that: 1) primarily focus on enhancement of sensory stimulation (e.g., provision of radio is categorized as sensory, but not manipulative, or cognitive although it could be made to be so); and 2) occur without a corresponding activity related explicitly to manipulation or cognitive stimulation (i.e., supplementary feeding of various fruits, vegetables, or other foods, but absent significant foraging requirement). As discussed more fully below in integration with the proposed assessment framework, there is little specific evidence to guide relative weighting, or priority, of stimulation via the different sensory modalities with respect to direct assessment of impact on NHP wellbeing (see also , Coleman, Bloomsmith, Crockett, Weed, & Schapiro, 2012). Thus, the overall goal of enhancing the sensory environment may initially be addressed by simply noting whether the enrichment primarily engages one sensory modality (e.g., radio, aural) or multiple senses (e.g., television, aural and visual). ...
... For NHP, foraging is a large part of their daily activity budget in natural settings. Given that the explicit goal of EE programs, one emphasized in the AWA and many organizational guidelines, is to increase species-typical behavior and given that food is motivating factor for NHP, many enrichment devices do incorporate dietary components (i.e., puzzle feeders, foraging devices; for review, (Bennett et al., 2014;Clark, 2011;Coleman et al., 2012) Some studies have aimed at disentangling motivational factors related to food vs curiosity that affect animals' engagement with various EE. Several studies show that increases in species-typical behavior and other positive effects persist after the food component of an enrichment strategy is consumed (Honess & Marin, 2006;Schapiro et al., 1996). ...
Nonhuman primates (NHP) are housed in captivity for a variety of purposes. In the US the housing and care for the majority of primates fall under federal regulation with additional guidelines and means of evaluation provided by various accreditation organizations. There is a gap, however, between the policy, common practices, and the findings of a large empirical literature on the effectiveness of care strategies aimed at ensuring the animals' psychological wellbeing. Uniform assessment tools to guide decisions about selection and refinement of standards and practices are largely missing. In two consecutive publications, we propose a novel approach to evaluation and refinement of environmental enrichment (EE) programs that: 1) is based on empirical evidence; 2) permits flexibility to balance facility goals (or purpose) with consideration of animal wellbeing; 3) provides a systematic framework for assessment; and 4) identifies priority areas for hypothesis-driven research. We focus on one area of EE that is relatively neglected with respect to consistency in practice and detail in standards yet is well-supported both theoretically and empirically. The non-social, non-structural EE domain includes practices that promote sensory, manipulative (motor), and cognitive (SMC) engagement which often are less constrained by space, geography, resources, and any conflicts with the facilities' varying purposes. This first paper provides the theoretical background for our proposed EE evaluation technique; whereas, the second describes the technique in detail. The systematic approach to categorization and assessment of the relevant components of facilities' federally-required NHP EE plans (EEP) proposed here can readily accommodate new evidence and is adaptable for different species and facility types. In turn, the approach can assist consideration of refinement, changes in EE, and development of best practices that transcend facility type.
... Strategies that are categorized as sensory stimulation alone are those that: 1) primarily focus on enhancement of sensory stimulation (e.g., provision of radio is categorized as sensory, but not manipulative, or cognitive although it could be made to be so); and 2) occur without a corresponding activity related explicitly to manipulation or cognitive stimulation (i.e., supplementary feeding of various fruits, vegetables, or other foods, but absent significant foraging requirement). As discussed more fully below in integration with the proposed assessment framework, there is little specific evidence to guide relative weighting, or priority, of stimulation via the different sensory modalities with respect to direct assessment of impact on NHP wellbeing (see also , Coleman, Bloomsmith, Crockett, Weed, & Schapiro, 2012). Thus, the overall goal of enhancing the sensory environment may initially be addressed by simply noting whether the enrichment primarily engages one sensory modality (e.g., radio, aural) or multiple senses (e.g., television, aural and visual). ...
... For NHP, foraging is a large part of their daily activity budget in natural settings. Given that the explicit goal of EE programs, one emphasized in the AWA and many organizational guidelines, is to increase species-typical behavior and given that food is motivating factor for NHP, many enrichment devices do incorporate dietary components (i.e., puzzle feeders, foraging devices; for review, (Bennett et al., 2014;Clark, 2011;Coleman et al., 2012) Some studies have aimed at disentangling motivational factors related to food vs curiosity that affect animals' engagement with various EE. Several studies show that increases in species-typical behavior and other positive effects persist after the food component of an enrichment strategy is consumed (Honess & Marin, 2006;Schapiro et al., 1996). ...
Nonhuman primates (NHP) are housed in captivity for a variety of purposes. In the US the housing and care for the majority of primates fall under federal regulation with additional guidelines and means of evaluation provided by various accreditation organizations. There is a gap, however, between the policy, common practices, and the findings of a large empirical literature on the effectiveness of care strategies aimed at ensuring the animals’ psychological wellbeing. Uniform assessment tools to guide decisions about selection and refinement of standards and practices are largely missing. In two consecutive publications, we propose a novel approach to evaluation and refinement of environmental enrichment (EE) programs that: 1) is based on empirical evidence; 2) permits flexibility to balance facility goals (or purpose) with consideration of animal wellbeing; 3) provides a systematic framework for assessment; and 4) identifies priority areas for hypothesis-driven research. We focus on one area of EE that is relatively neglected with respect to consistency in practice and detail in standards yet is well-supported both theoretically and empirically. The non-social, non-structural EE domain includes practices that promote sensory, manipulative (motor), and cognitive (SMC) engagement which often are less constrained by space, geography, resources, and any conflicts with the facilities’ varying purposes. This first paper provides the theoretical background for our proposed EE evaluation technique; whereas, the second describes the technique in detail. The systematic approach to categorization and assessment of the relevant components of facilities’ federally-required NHP EE plans (EEP) proposed here can readily accommodate new evidence and is adaptable for different species and facility types. In turn, the approach can assist consideration of refinement, changes in EE, and development of best practices that transcend facility type.
... 1,4 Pair housing is widely used for NHP involved in some types of research studies, given that pairs can be maintained in standard indoor caging, allowing access for research procedures while meeting the need for social housing. 22 Pair housing facilitates more precise monitoring of food and water intake and elimination of waste, compared with group housing, 11 and pair-housed NHP require less frequent veterinary treatment than those maintained in other housing conditions. 36 However, for research, clinical, or animal management needs, separation of NHP from their partners and subsequent individual housing is required at times. ...
Literature-based recommendations regarding how to separate pairs of laboratory-housed NHP when required for research,veterinary, or management needs are unavailable. This study assessed 2 separation techniques—rapid and stepwise—to determine whether a period of limited social access mitigates the behavioral stress response after complete separation.Researchers observed 12 pairs of mother-reared, adolescent male rhesus macaques before and after separation with a solid divider; 6 of the pairs experienced a transitional week of limited social access through a perforated panel. Observers collected 30-min focal animal scans during study phase, totaling 144 h of behavioral data. Target behaviors included those classified as protest, agitation, tension, and withdrawn or self-directed. Social separation resulted in a significant change in behavior. Separated monkeys displayed more withdrawn or self-directed behaviors (for example, huddling, self-directed stereotypies) than when pair-housed. Stepwise separation resulted in increased agitation behaviors in the limited contact phase and did not mitigate separation effects. Adverse behavioral changes during the limited contact phase support continuous pair housing until required individual housing.
... The breeding systems of swine in Brazil are currently mostly intensive, where animals are kept in restricted areas, making it impossible to express their natural behaviors (BAXTER et al., 2011).Because of this, several researches have been carried out in order to improve the physical, psychological and social conditions of animals raised in confinement and/or captivity. As a technique to improve the biological functioning of the animal created in intensive systems by the modification of the environment, there is the environmental enrichment (COLEMAN et al., 2012). ...
Studies have shown that the benefits from music can improve the welfare conditions of laboratory, pet and production animals. The study aimed to evaluate the influence of music (Antonio Lucio Vivaldi compositions) on behavior aspects (position, activity, stereotypes, social and agonistic behavior) and physiological responses (respiratory rate and rectal temperature) in gestating sows in individual cages (stage 1), and collective stalls (stage 2). 28 animals were studied, 14 belonged to music group, and 14 to the control group (without music).The respiratory rate had the lowest averages in the group with music, for example, in stage 1, time 1, values of 19.28 and 21.50 mov.min−1. In stage 2, the values found in the same time were 20.36 and 24.16, and in time 2, values of 24.37 and 27.18 mov.min−1. These findings follow in stage 2 until time 4.Behaviors position, activity, stereotypes and agonistic interaction with the researcher were also influenced by the music. We concluded from the results that music influenced the behavior of animals, providing greater relaxing and reduce stereotypes aspects related to a better welfare.
... Defining good versus poor welfare for laboratory NHPs, as well as measuring and assessing changes to it, generally follows standards established by a combination of regulation, enforcement, the scientific literature, and facility practices [Coleman et al., 2012]. In general, NHPs are considered to have good, even optimal, welfare when they have a healthy body condition and coat quality (weight to height ratio that accounts for distribution of fat and fur that uniformly covers skin), are free of injury or disease, exhibit species typical behavior, and have a low occurrence of abnormal, anxious, depressive, and aggressive behaviors [Capitanio, 1986;Keeling & Wolf, 1975]. ...
... Changes to these metrics are typically used to monitor captive populations for declining welfare and identify and evaluate methods for improving it. While some conditions clearly constitute poor welfare if untreated (e.g., self-injurious behavior, serious illness), many others are in a gray area of change toward or away from optimal welfare [Coleman et al., 2012]. The welfare consequences associated with social housing changes are often assessed from any combination of the above measures. ...
Macaque species, specifically rhesus (Macaca mulatta), are the most common nonhuman primates (NHPs) used in biomedical research due to their suitability as a model of high priority diseases (e.g., HIV, obesity, cognitive aging), cost effective breeding and housing compared to most other NHPs, and close evolutionary relationship to humans. With this close evolutionary relationship, however, is a shared adaptation for a socially stimulating environment, without which both their welfare and suitability as a research model are compromised. While outdoor social group housing provides the best approximation of a social environment that matches the macaque behavioral biology in the wild, this is not always possible at all facilities, where animals may be housed indoors in small groups, in pairs, or alone. Further, animals may experience many housing changes in their lifetime depending on project needs, changes in social status, management needs, or health concerns. Here, we review the evidence for the physiological and health effects of social housing changes and the potential impacts on research outcomes for studies using macaques, particularly rhesus. We situate our review in the context of increasing regulatory pressure for research facilities to both house NHPs socially and mitigate trauma from social aggression. To meet these regulatory requirements and further refine the macaque model for research, significant advances must be made in our understanding and management of rhesus macaque social housing, particularly pair-housing since it is the most common social housing configuration for macaques while on research projects. Because most NHPs are adapted for sociality, a social context is likely important for improving repeatability, reproducibility, and external validity of primate biomedical research. Am. J. Primatol. © 2016 Wiley Periodicals, Inc.
... Therefore, smaller labs, often without dedicated behavioral management teams, may be the primary users of these animals. Many facilities employ introduction methodology developed for the social management of macaques [Coleman et al., 2012;DiVincenti and Wyatt, 2011]. However, the effectiveness of managing vervet introductions using methodology developed for macaque species has not been evaluated. ...
... At the TNPRC and WF, a step-wise introduction plan was employed. As Carlson [2008], Coleman et al. [2012], DiVincenti andWyatt [2011], andTruelove et al. [2015] have described, typical socialization attempts with macaques proceed in a step-wise fashion allowing "pair familiarization" during which both members of the pair are allowed to establish a dominant-subordinate relationship with little to no physical or tactile contact. The animals are allowed to see each other without contact, and the amount of tactile access is steadily increased until the animals are in full contact. ...
Vervets, also known as African green monkeys, are a nonhuman primate species widely used in biomedical research. However, there are currently few references available describing techniques and rates of success for pair-housing this species. We present data from four cohorts of vervets from three different facilities: (i) the Wake Forest Vervet Research Colony (VRC; n = 72 female pairs, n= 52 male pairs), (ii) the University of Louisiana at Lafayette-New Iberia Research Center (UL-NIRC; n = 57 female pairs, n = 54 male pairs), (iii) the Tulane National Primate Research Center (TNRPC; n = 18 male pairs), and (iv) a cohort of imported males (n = 18 pairs) at Wake Forest. Compatibility was measured at 14, 30, and 60 days following introduction. Success rates for pair-housing at 14 days ranged from 96% to 98% for females and 96% to 100% for males at the VRC and UL-NIRC but were lower in the smaller imported male cohorts (TNPRC: 50%; WF: 28%). Among the UL-NIRC cohort and VRC male cohort, most of the pair separations after 14 days were due to reasons unrelated to social incompatibility. In contrast, a large proportion of TNPRC and imported male pairs successful at 14 days required separation within 60 days due to incompatibility. Multiple logistic regressions were performed using cohort, mean age of pair and weight difference between pair-mates as potential predictors of compatibility at 14 days. All three predicted the 14-day outcome in males but not females. A separate analysis in the VRC cohort found no evidence that prior familiarity in a group setting influenced outcomes. Variations in success rates across cohorts may have been influenced by introduction methodology. Behavioral differences between vervets and macaques, coupled with our findings, lead us to theorize that the gradual introduction techniques commonly implemented to pair house macaques may not be beneficial or suitable for this species. Am. J. Primatol. © 2015 Wiley Periodicals, Inc.
... 10,24,26,27 The behavior of NHP, including rhesus macaques (Macaca mulatta), can be especially difficult to interpret due to their relatively stoic nature and tendency to mask clinical signs of illness in the presence of human observers. 8,10,12,14,17 Two explanations for the tendency to mask pain, which is also observed in other species, are their status as a prey species and the need to hide weaknesses from group members. 3,17,22,23 According to the 2009 Institute for Laboratory Animal Research (ILAR) recommendations for recognizing pain and distress in nonhuman primates, " [v] iewing an animal from a distance or by video can aid in detecting subtle clinical changes." ...
Understanding the behavior of laboratory NHP facilitates health assessment and clinical care. We sought to characterize the behavior of critically ill rhesus macaques (Macaca mulatta) and determine whether specific behaviors or behavioral changes might facilitate the determination of prognosis and clinical endpoints. Twenty-two critically-ill subjects were videorecorded after they were removed from the outdoor breeding colony for diagnostic work-up and treatment. Subjects were categorized as survivors (n = 15) and those that were euthanized according to existing clinical endpoints (n = 7). Behavior before, during, and after cageside examination was compared between these groups with regard to the presence or absence of direct observation. This approach allowed us to determine whether these settings revealed differences between groups or masking of behaviors during direct observation. Before cageside examination, several behaviors (for example, self-grooming and anxiety behaviors) were significantly more common in surviving subjects than in euthanized subjects. Few significant differences in behavior were detectable during or after the examination. Subjects that were eventually euthanized showed more illness-related behaviors; however, not all animals requiring euthanasia showed these signs when an observer was present. Furthermore, euthanized animals spent more time in an alert posture during direct observation than at other times. Therefore, direct observation of critically ill rhesus macaques may not yield the most accurate assessment of illness severity, and using video to assess behavior may be helpful for prognosis.
... As Coleman et al. (7) have noted, the term 'enrichment' has been used variously to refer to specific items placed in the cage with the animals, or, more broadly, to describe a process to improve animal welfare. Mench (8) notes that environmental enrichment is 'often defined in terms of its purposes rather than simply as a process or a phenomenon'. ...
It has been widely accepted for some time that species-appropriate environmental enrichment is important for the welfare of research animals, but its impact on research data initially received little attention. This has now changed, as the use of enrichment as one element of routine husbandry has expanded. In addition to its use in the care of larger research animals, such as nonhuman primates, it is now being used to improve the environments of small research animals, such as rodents, which are used in significantly greater numbers and in a wide variety of studies. Concern has been expressed that enrichment negatively affects both experimental validity and reproducibility. However, when a concise definition of enrichment is used, with a sound understanding of the biology and behaviour of the animal as well as the research constraints, it becomes clear that the welfare of research animals can be enhanced through environmental enrichment without compromising their purpose. Indeed, it is shown that the converse is true: the provision of suitable enrichment enhances the well-being of the animal, thereby refining the animal model and improving the research data. Thus, the argument is made that both the validity and reproducibility of the research are enhanced when proper consideration is given to the research animal's living environment and the animal's opportunities to express species-typical behaviours.
