Introduction to Behavioral Management

Animal care in research, teaching, and testing facilities has undergone a remarkable transformation in the past two decades, and there is a heightened emphasis on the psychological status of animals living in these institutions. Today, providing for the psychological well-being of research animals is an integral part of animal care programs and is key to promoting a “culture of caring” within our facilities. This change occurred as the scientific community realized that animals have many behavioral needs, which, if not met, can adversely affect their behavior, physical health, and research utility. Programs to address the well-being of laboratory animals by providing them with more complex and interesting environments are now common across all taxa, including primates, dogs, cats, pigs, sheep, rodents, rabbits, birds, and fish.

The term behavioral management refers to a comprehensive approach to improving the welfare of captive animals by employing social housing, environmental enrichment, animal training, facility design, and the assessment of behavior and behavioral problems. Behavioral management builds from a foundation of understanding the behavior of the target species (or of closely related species) in natural conditions, with the aim of improving animal care and enhancing animal welfare. An important premise of behavioral management is that the individual components of enrichment, animal training, social housing, and behavioral assessment can be integrated to achieve behavioral goals for captive animals better and more completely than any one technique applied in isolation. Behavioral management practices that improve psychological well-being and reduce stress for research subjects are important refinements in animal care.

Social housing of laboratory animals is fundamental to effective behavioral management programs since the most commonly used laboratory animals are social species. The Guide for the Care and Use of Laboratory Animals (hereafter referred to as the Guide) states, “Appropriate social interactions among members of the same species (conspecifics) are essential to normal development and well-being” (National Research Council 2011, p. 64). Social housing in compatible groupings or pairs offers the animals opportunities for engaging in a variety of species-typical behaviors, such as grooming, affiliation, agonism, play, and rearing of offspring. Social housing also reduces the occurrence of abnormal behaviors in many species, and it generally is especially important to socially house young animals.

Environmental enrichment enhances the well-being of animals by providing them with species-specific opportunities for exercise and manipulating objects, and cognitive challenges (Guide, p. 53). Enrichment is classified into broad and overlapping categories, including four types of nonsocial enrichment: feeding, physical, sensory, and cognitive and occupational enrichment (Keeling et al. 1991). When used together, these different categories of enrichment can improve many different facets of the animals’ behavioral repertoire.

Animal training, and especially positive reinforcement training (PRT), is another component of behavioral management programs. PRT is a form of conditioning in which the subjects are given positive reinforcement (e.g., food treat or social interaction) following their performance of a desired behavior. PRT relies on the voluntary cooperation of animals, rather than on compelling them to comply through manual restraint or chemical restraint. PRT is generally seen as preferable to negative reinforcement training, in which the subject performs a desired behavior to avoid or escape from a negative stimulus (e.g., loud sound). While PRT has been used most often with nonhuman primates, it is now being applied to a variety of other laboratory animal species.

Behavioral assessment and monitoring are important aspects of behavioral management programs, as they are needed to identify behavioral problems, determine needed treatments for those problems, and assess whether treatments are effective. Behavioral assessment can be based on quantitative behavioral data collection and formal studies of behavioral change, or on a systematic application of less rigorous methods.

Specialized positions in behavioral management are becoming more common as research facilities are employing more individuals with expertise in behavior and animal welfare. When this type of focused position is not in place, others in the organization should be designated to take on the behavioral responsibilities, and this should be included as part of their job descriptions; performance of these responsibilities should be measured in their performance reviews; and they should be given the resources to learn about behavioral management.

Behavioral management programs (sometimes referred to as environmental enrichment programs or psychological well-being programs) are required by some regulatory agencies and are emphasized in professional standards of research animal care across the world. Multinational organizations such as the Council for International Organizations of Medical Sciences and the International Council for Laboratory Animal Science have set out principles of responsibility and oversight for countries with animal research and teaching programs, and these include the principle that the animals’ environment and management are species appropriate and contribute to their well-being (iclas.org/wp-content/uploads/2013/03/CIOMS-ICLAS-Principles-Final1.pdf). Some countries have established federal legislation that addresses these programs. For example, in the United States, the Animal Welfare Act (AWA) regulations direct that research institutions must “develop, document, and follow an appropriate plan for environment enhancement adequate to promote psychological well-being of nonhuman primates” (9 CFR 3.81; U.S. Department of Agriculture [USDA] 1991, www.nal.usda.gov/awic/final-rules-animal-welfare-9-cfr-part-3-0). This environmental enhancement plan should be an Institutional Animal Care and Use Committee (IACUC)–approved policy or standard operating procedure (SOP), and it must be made available to the Animal and Plant Health Inspection Service (APHIS) and any federal funding agency upon request. The AWA also requires exercise for dogs (Section 13(a)(2)(B) of the AWA [7 USC 2143]). Live vertebrate animal research being conducted with federal funding from the U.S. Public Health Service (notably including funding from the National Institutes of Health) must comply with the Guide. The Guide stipulates that enrichment should be provided for all laboratory animals. In addition, those research facilities that choose to become accredited by AAALAC International must also comply with the Guide or with the Guide for the Care and Use of Agricultural Animals in Research and Teaching (Federation of Animal Science Societies 2010), which also describes the provision of enrichment, and says most forms of enrichment should be provided. All relevant legal and professional standards should be followed when behavioral management programs are developed.

Constructs to Achieve with Behavioral Management

Behavioral management programs have general goals of increasing species-appropriate behavior, decreasing abnormal behavior, increasing resiliency, and reducing distress within the laboratory environment. In the Guide, there are also several other general tenets that can be met through behavioral management: offering novelty, providing opportunities for choice and control, habituating and preparing animals for procedures, and socially housing social species.

Offering animals novelty can be done through exposing them to novel objects, spaces, or activities that are stimulating to captive animals and give them practice in dealing with new challenges. This is helpful because if animals have been maintained in a completely consistent environment (i.e., lacking novelty), they may respond with fear or avoidance when novel stimuli are encountered. Novelty can be offered by rotating enrichment items, by offering new types of resources, by moving animals into larger activity caging, and by using PRT to teach animals new behaviors (i.e., the learning of new tasks is a stimulating experience). Social housing provides tremendous novelty with unpredictable and complex interactions with other animals. There is an important caveat to note with regard to novelty. Making changes in animal environments too often or too quickly may be stressful for some individuals. For example, individual animals who are rated as having highly inhibited temperaments are less likely to approach new objects; novel activities or objects may actually increase stress for such individuals without proper preparation (Roma et al. 2006; Coleman 2012).

Another principle is to give animals control and choice in their environments: “Well-conceived enrichment provides animals with choices and a degree of control over their environments, which allows them to better cope with environmental stressors” (Guide, p. 53). For example, different types of physical enrichment (e.g., visual barriers, elevated shelving, and protected contact panels) may allow animals to control their proximity to others, and this may reduce conflict and stress. Giving mice adequate nesting material also allows them to control their temperature and avoid stress associated with cooler temperatures. PRT relies on the animals’ voluntary cooperation, and allows them to exercise choice in whether to participate in training sessions (Laule et al. 2003).

Requiring animals to be habituated to and prepared for research procedures is another broad principle in modern standards for animal care. The Guide states that “dogs, nonhuman primates, and many other animals can be trained, through use of positive reinforcement techniques, to cooperate with research procedures.” Animals to be placed in restraint devices should be given training (with positive reinforcement) to adapt to the equipment and personnel ” [and] ” animals that do not adapt to necessary restraint systems should be removed from the study” (Guide, p. 29). Animal training programs based in positive methods are needed to meet these standards.

A final general tenet that behavioral management programs most directly address is that social species should be socially housed. “Single housing of social species should be the exception and justified based on experimental requirements or veterinary-related concerns about animal well-being. In these cases, it should be limited to the minimum period necessary” (Guide, p. 64), and social housing is the “default” method for social species. For some species there are few difficulties or dangers in social housing, but others require skilled staff members to form social groups and monitor animals in social settings.

Personnel Involved in Behavioral Management

Successful behavioral management programs vary widely in design and implementation, but all require the involvement of people with different backgrounds and roles in a research facility working together as a team. The complexity of a program and the part each person will play depend on many facility-specific factors, such as vivarium size and staffing, species being used, and the presence of dedicated behavior staff. In a small colony of mice, for instance, a successful behavioral management program may consist of a relatively static enrichment plan overseen and periodically updated by a single attending veterinarian in concert with the rest of the IACUC, which would review the program regularly, and may be implemented by animal care or research staff who would provide feedback to the veterinarian on predefined performance measures. In a larger and more complex facility, however, one can imagine that an ideal behavioral management program would include expanded roles for many layers of personnel.

Animal care staff members see the animals multiple times daily and are often the most familiar with individual animals or strain temperaments and traits. Thus, a member of the care staff trained to distinguish normal from abnormal behaviors may identify animals experiencing early or mild psychological distress or, in some cases, physiological disease (Gaskill et al. 2013). The recognition of abnormal behaviors (both the presence and absence of) is crucial because this is one of the primary performance measures available to gauge whether a program is successful, as outlined in the Guide. Having the care staff provide enrichment, such as novel foods, also offers an opportunity for daily positive human contact and the development of a positive relationship between animals and the humans they interact with most. In facilities where there is a dedicated behavior staff, having care staff be the primary providers of enrichment resources may preserve the ability of behavioral specialists to remain neutral observers and view animals in their most typical state. Care staff may also train animals for routine husbandry tasks, allowing for another positive human contact opportunity and also allowing the training of many animals (Adams et al. 2004).

In many ways, the role of research staff parallels that of care staff. Researchers are often in frequent contact with their animals and may notice subtle signs of (di)stress due to their familiarity with the individuals or changes in their experimental measures. Collaboration between research staff and the rest of the behavioral management team is critical because many behavioral management techniques have the potential to impact research outcomes, and many research procedures have the potential to impact animal behavior. Open communication regarding experimental procedures, socialization attempts, abnormal behaviors, and so forth, is key to striking a balance between animal well-being and successful research outcomes.

The broad training and expertise of laboratory animal veterinarians in matters of animal health and research model design gives them a valuable perspective in ensuring balance between behavioral management, animal safety, and research integrity. Especially in facilities with dedicated behavior staff, there are several areas of frequent interface between veterinarians and behavioral management. In facilities with a robust socialization program, veterinarians will necessarily be involved in treating wounds caused by social aggression. Veterinarians have an increasing role in treating abnormal behavior via psychoactive medications, sometimes in combination with behavioral techniques. The use of positive reinforcement to train animals for cooperation with common veterinary techniques, such as physical exams and blood collection, also requires the interaction of veterinarians and behavioral management staff.

As behavioral management programs have become more complex, the need for staff dedicated to these programs has become more apparent, and indeed, such an arrangement has become the norm in many large primate programs. While American veterinarians are given legal responsibility for environmental enhancement plans for nonhuman primates by the AWA (USDA 1991), 48% of primate facilities reported having a behavioral scientist (with a PhD or master’s degree) rather than a veterinarian providing primary oversight for behavioral management (Baker 2016). As discussed below, there are many necessary facets of successful behavior programs, and to expect care staff or veterinarians to manage these while keeping abreast of new developments in the large and evolving field of animal behavior, in addition to their normal duties, can be overwhelming to them.

Many other entities and individuals within a research organization may also contribute to behavioral management. The IACUC, notably, should include review of the behavioral management program during program reviews. Individual IACUC members should be trained to recognize abnormal behaviors or other signs of distress and note these when seen in animals during facility inspections, and the IACUC as a whole should work with operations staff and veterinarians to development optimal enrichment strategies for the species within a program. Facility managers and purchasing officers can provide valuable input into the cost–benefit analysis of new enrichment devices or procedures, while safety officials may have ideas for how to ensure personnel safety during implementation. Facility maintenance or a mechanical shop may be involved in the design and construction of enrichment devices or enhanced enclosures. Information technology staff may design ways to monitor the performance of a device. Regardless of which individuals in a facility have formal responsibility within the behavioral management program, all entities must work together toward the common goal of increased animal welfare and enrichment to achieve success.

Social Housing Program

Social housing serves a basic biological need for many laboratory animals. As indicated in the Guide, and by AAALAC International (http://www.aaalac.org/accreditation/positionstatements.cfm#social), social species should be housed in stable pairs or groups of compatible individuals unless precluded by experimental reasons, clinical issues, or behavioral incompatibility. Individually housed animals that are members of social species require scientific justification for single housing in the IACUC protocol to which they are assigned. Intermittent social or pair housing has been applied in some situations, typically to facilitate research needs. For most social species, group living is the most species-appropriate and desirable form of housing, although monogamous species (e.g., prairie vole and marmosets) are an obvious exception. If living in groups is not feasible, living with one other partner may be. For some species, particularly some domestic animals, interactions with humans is also an important means of supplying social stimulation.

Social housing programs should include an outline of the social introduction and monitoring processes to be used, the criteria used to select animals for introduction to one another (e.g., sex, age, and temperament), and the methods by which they are introduced. Some species, such as primates, may require a stepwise introduction process, which includes observations of interactions when animals are provided with first visual access, then protected contact via a divider of mesh or small holes, and finally full contact, while for other large animal species, such as livestock and dogs, introductions typically proceed from visual and olfactory contact directly to supervised full access in spaces large enough to allow escape in the case of an inappropriately aggressive interaction. For most rodents, typical management practices lead to the pair or group housing of littermates or young, sexually immature adults, which may reduce the necessity for closely observed introductions, or breeding pairs introduced via immediate full access contact.

Regardless of the species or method of introduction, socially housed animals should be regularly monitored for compatibility. Observations may be more intense in the days or weeks following introductions, but should continue at some level for all socially housed animals. Observations for compatibility should be conducted during routine cleaning, feeding, and research activities. Monitoring can be conducted by a trained observer in the room, via video recorder, or by remote viewing systems, such as Internet-secure Internet protocol (IP) cameras. Communication about the social introduction should be directed to all affected staff, if that information might impact their daily operations.

Environmental Enrichment Program

In an effort to address application of the term environmental enrichment to any change in an animal’s environment, regardless of measurable benefit for the animal, Newberry (1995) defined it as “an improvement in the biological functioning of captive animals resulting from modifications to their environment.” The scientific literature and regulatory documents have expanded on this definition, referring to environmental enrichment as features of a captive animal’s environment or husbandry that increase that animal’s number and range of normal behaviors, decrease abnormal behaviors, increase interaction with the environment, and enhance its ability to cope with behavioral and physiological challenges (Federation of Animal Science Societies 2010, p. 30). An environmental enrichment program consists of using a variety of techniques and providing a variety of resources to animals with the goal of modifying their behavior in these ways. Most of the nonsocial approaches used to improve the environments of research animals can be categorized into four general types: feeding, physical, sensory, and cognitive and occupational (Keeling et al. 1991). Food enrichment is consumable items that are either different in type from the animals’ standard diets or delivered in such a way as to encourage natural foraging behaviors. Physical enrichments are elements of an enclosure that allow animals to experience different microenvironmental conditions, such as shelters, perches, or bedding. Sensory resources are those that engage an animal’s senses without necessarily requiring interaction, such as television, music, or smells. Cognitive and occupational resources are those engaging animals in interaction with their environment in such a way as to be mentally stimulating, including the provision of puzzles, activities, or PRT. Of course, many techniques for improving animal environments could fall into more than one of these categories, such as puzzle feeders qualifying as both cognitive and food enrichment, and swimming pools qualifying as physical and sensory resources, but these general categories are useful for considering which aspects of an animal’s experience could be enhanced.

In general, the design and selection of resources for the enrichment program is made to encourage appropriate behaviors that mimic those seen for a species in their natural environment. In this way, enrichment resource design and management should rely heavily on the natural history of a species and not on what might look interesting or colorful to a human observer. Natural histories describe the environment and context in which species live naturally. These remain relevant to the welfare of laboratory animals despite sometimes thousands of generations of removal from the “wild” state, as laboratory strains released into the wild consistently revert to naturalistic patterns of behavior (Hutchinson et al. 2005). Some important elements of natural histories with particular relevance to enrichment resource design include diet and food gathering behaviors, including what animals eat, and whether they live near a readily available food source or spend many hours a day finding food; sleep habits, including when in the day an animal sleeps and whether it seeks or builds shelter; and social structure, such as whether animals form long-lasting dominance relationships or are territorial. For example, wild mice instinctively build elaborate nests in which they sleep during the day; this could be used to infer that mice might benefit from the provision of nesting material and minimizing disturbances during the day (Olsson and Dahlborn 2002; Hutchinson et al. 2005). Likewise, macaques spend a great deal of time covering wide ranges in the search of food, and techniques to increase foraging time have been shown to have some beneficial psychological effects in captive primates (Bennett et al. 2010; Gottlieb et al. 2011).

Implementing any new enrichment technique or resource requires a team approach with input from a variety of personnel. Any new enrichment should be approved prior to distribution to any research animals. This includes cases of “one-time” or limited enrichment resources that are often chosen as much for their effect on human morale as for animal benefit (i.e., seasonally themed novel foods) and those with the intent to be implemented broadly or on a repeat basis. A behavioral specialist should evaluate potential for efficacy or harmful effects with the help of peer-reviewed scientific literature. A veterinarian should assess the enrichment for any health concerns, safety risks, or potential confounding effects on the research. The animal care and facility management staffs should determine a method of sanitation and logistical aspects related to the provisioning of the enrichment. The goal should be to provide maximum benefit and minimum harm to animals, at a minimum cost in labor and money (Bennett et al. 2010). In facilities where a behavioral scientist heads the behavioral management program, she will likely conduct the initial review and design or selection. In facilities without such personnel, resource selection may fall to a designated individual or committee. It should be noted that information may be found outside the literature search databases typically used for biomedical research and may be found in information provided by a manufacturer or published in non-peer-reviewed trade journals. An example of the importance of enrichment resource preapproval is the known interaction between grapefruit and many pharmaceutical compounds commonly used in research facilities (Bailey et al. 2013). This interaction is likely to be known to veterinarians, but perhaps not to a well-intentioned enrichment committee seeking to implement new food resources.

The construction and purchase of enrichment resources will depend on the funds, supplies, and means available. Some facilities have dedicated mechanical shops that construct enrichment devices, while others rely on dedicated behavioral specialists or enlist volunteer care staff for their design, construction, and repair. Regardless, any new enrichment device should undergo pilot testing prior to widespread adoption. Considerations prior to and during this testing phase include the potential impact on the research project utilizing the “test subjects,” which will necessitate involvement of at least one willing primary investigator. During testing, devices should be monitored routinely to ensure they do not pose any safety risk to personnel or animals (e.g., certain plastics may be chewed and quickly develop sharp points). An assessment should be made of the efficacy of the enrichments, although the extent of this may depend on the resources and personnel available at the institution. Such a review would, at a minimum, determine whether the animals actually utilize the new device or resource, but optimally would include measuring effects on normal and abnormal behaviors or physiology in an objective manner. The ability to sanitize the enrichment device should also be reviewed as part of the testing phase. Whether this consists of visual inspection or more objective measures by such tools as ATPase testing or cultures will depend on the institution, existing SOPs, the vulnerability of the animals or personnel to potential fomite-transmitted pathogens, and the opinion of the design team and facility management.

Once an enrichment device has been tested, a team approach to program implementation should continue and determine whether the item is worth implementing more broadly. Again, this team should include the behavioral specialist (as available), veterinarian, and facility management and/or animal care staff. It may also include a purchasing or financial officer, to discuss the cost–benefit of implementation. All investigators whose animals will be impacted by the new enrichment device should be consulted, or at a minimum informed of the change, since enrichment devices and resource may impact important research variables. For enrichment resources that require manual distribution, such as novel foods and manipulanda, a system of documenting this provision should be developed to ensure complete implementation. After an enrichment device or resource is in use, there should also be a system by which concerns are reported by animal care staff or other personnel and where the device can be rereviewed for these reported concerns. Any injuries or negative health outcomes involving a device should be reported first to a veterinarian and, based on the severity and context of the incident, to relevant regulatory bodies as required by law. Such an incident should prompt a review of that device. If such a review is completed, it is important to consider the injury severity and rate against the total use and benefit when determining whether to remove or alter a device; a rarely used device with a high rate of injury would be a more obvious candidate for discontinuation than one used broadly with a low rate of minor injuries or mishaps. A periodic review of enrichment device efficacy should be conducted. As animals are exposed repeatedly to devices, some lose their novelty. This is especially true of puzzle-type devices provided to nonhuman primates (Meehan and Mench 2007). Literature regarding a device should also be monitored. An example of how consensus regarding enrichment programs evolves over time can be found in the consideration of mouse enrichment resources over the past few decades. By the late 1990s, a consensus had emerged that nesting material was a superior enrichment resource for rodents (Olsson and Dahlborn 2002). Since then, however, this consensus has developed significant nuance, with current literature suggesting the type of nesting material provided and subsequent form of the nest is a significant variable in determining how much benefit accrues to the animals (Hess et al. 2008; Gaskill et al. 2013).

Animal Training Program

Animal training is an integral component of behavioral management, and PRT is a powerful tool to gain cooperation and compliance by laboratory animals. Animal training occurs each time there is an interaction with an animal. When looking at the daily operations of a facility through the lens of animal training and operant conditioning, one can see animals responding to environmental cues all the time. For example, an animal caregiver approaches a group of animals with food, and the animals move toward the caregiver and are given the food. The animals are positively reinforced for moving toward the animal caregiver, and they are likely to do it again to gain food. An animal has learned and is now more likely to approach a person, as it previously received something it wanted (food) following that behavior. An animal caregiver spraying water with a hose approaches a group of animals who then move into an adjacent cage. Once they move, the spray from the hose ceases. These animals have been negatively reinforced for moving away from the animal caregiver and the next time will likely move quickly away from the caregiver spraying water. The behavior to move from one location to another is motived by avoiding something they find aversive (spraying water). These are examples of two different experiences for the animal, and some literature shows the use of negative reinforcement is more stressful for the animal than positive reinforcement (as measured by physiological and behavioral means, and response to humans). Personnel should be trained to recognize what types of negative reinforcement are used, to use it in the smallest amount possible to get the needed behavior, and to offer positive reinforcement following the animal’s cooperation.

Initiating a PRT program (sometimes called “clicker training”) is valuable and meets recommendations of the Guide (Perlman et al. 2012). Animal training techniques and some average required training times for a variety of behaviors are well documented in the literature (Schapiro et al. 2003; Coleman et al. 2008; Veeder et al. 2009; McMillan et al. 2014; Bloomsmith et al. 2015; Bliss-Moreau and Moadab 2016). These include conscious blood collection, urine collection, semen collection, restraint behaviors, presenting for injection, movement between enclosures, and managing aggressive behavior (see Schapiro et al. in Chapter 32 of this volume for a thorough review). When trainers talk to one another, they often describe individual differences in animals’ willingness to train. Coleman (2012) has described how temperament can impact training success in primates; in one study, animals with exploratory temperaments were more successful training candidates than those with inhibited temperaments.

As a manager of an animal program, it is critical to understand that animal training should be applied by people who have been educated in animal training techniques. It is also important to note that progress is measured in terms of the animal advancing through the training steps, not just in the time the trainer has devoted to training sessions. To that point, McMillan et al. (2014) described a refinement in training primates for chair restraint in which PRT techniques were applied for several months. For those animals not progressing through the training steps by a set time point prior to initiation of the study requiring the chair restraint, the lowest magnitude of negative reinforcement required was applied and then was followed immediately by a food reinforcer. Minimal stress was caused, and subjects were trained for the behavior in the needed time frame. Once an animal is fully trained, the behavior needs to be maintained if it is to remain useful. Managers should schedule maintenance training for their staff to employ as needed; the frequency will vary with behaviors and individual animals.

Behavioral Assessment Program

Behavioral assessment is a critical component of an effective behavioral management program. A solid understanding of the natural behavior of a species is necessary to identify species-appropriate behaviors, provide an effective enrichment program to promote a broad repertoire of species-appropriate behaviors, and identify abnormal behavior so that appropriate treatments can be applied. For example, ferrets and squirrel monkeys exhibit scent-marking behavior, so providing enrichment to promote this behavior is important. Most primates spend much of their day searching for, processing, and consuming food, so developing ways for them to express these behaviors in captivity is an essential part of the enrichment program for primates. Understanding behaviors that are fundamental to a species’ “lifestyle” and supplying the means for them to express them is an important consideration for their captive welfare. Per the Guide, “personnel responsible for animal care and husbandry should receive training in the behavioral biology of the species they work with to appropriately monitor the effects of enrichment as well as identify the development of adverse or abnormal behaviors” (p. 53). Education about the behavior of the species with which an individual works should begin at hire and be supplemented, reinforced, and updated throughout the career of a laboratory animal professional. This training should include the behavioral biology of the species, understanding behaviors that could be of concern, the mechanism by which to report behaviors of concern, and appropriate staff–animal interactions.

Since there are many different personnel (veterinary, animal care, and research staff) who work with any one animal, behavioral assessment programs should include a system of reporting and responding to behaviors of concern, such as stereotypic behaviors, fearful or aggressive behavior, hair plucking, barbering, hyperactivity, anxiety, and self-injurious behaviors. For example, animal caregivers may observe social aggression during routine feeding, veterinarians might observe an animal behaving fearfully when collecting biological samples, and research team members may observe an animal exhibiting self-directed abnormal behavior during testing. When such behaviors are observed, they should be reported to personnel responsible for behavioral care. This may be done verbally, especially if the animal is injured or in danger and immediate action is required, or in written form, such as on log sheets posted outside of each animal housing room. These log sheets should be reviewed regularly by personnel responsible for behavioral care who should assess the problem and provide viable treatments if appropriate. If treatments are applied, they should be documented and evaluated for efficacy.

A behavioral assessment program can be used to evaluate the presence, absence, rates, and durations of selected behaviors. These data can be recorded by using different observation and recording methodologies (Tables 5.1 and 5.2). As one example, the one-zero method will indicate whether individuals are expressing or not expressing particular behaviors during a time interval. Abnormal behaviors, fear-related behaviors, and other behaviors of concern are noted during brief observation periods using a check sheet–type format. Then if an individual meets predetermined thresholds for problematic behaviors, a more in-depth focal behavioral assessment can be completed. Based on this assessment, treatments are then provided and evaluated. Possible treatments may include social changes (such as a new social partner), animal training applications (such as desensitization to a stimulus causing fearful behavior), additional enrichment applications (such as additional foraging devices, destructibles, and visual barriers), and operational changes (such as cleaning the animal’s stall first, or reducing the amount of time an animal is separated from its social group for a procedure). If the behavioral problem is reduced or ameliorated, that treatment is typically maintained. Hair coverage scores are also sometimes completed as part of a behavioral assessment program for some species prone to self-induced alopecia. These scores are useful to identify individuals with pronounced or increasing hair loss, and objective evaluations of hair regrowth following treatment (see Figure 5.1 as an example of a hair scoring diagram and scoring system based on Luchins et al. 2011).

Table 5.1

Methods of Observation of Animal Behavior.

Table 5.2

Methods of Recording Animal Behavior.

Figure 5.1

Example of hair score template for nonhuman primates. (From Luchins, K.R. et al., J. Am. Assoc. Lab. Anim. Sci., 50(6), 926–938, 2011.)

Facility and Housing Design

The design of laboratory animal housing is a vital aspect of promoting animal well-being, as the physical environment can have a major influence on animal behavior. Animal housing should be designed to facilitate the expression of species-typical locomotor behavior, resting patterns, and activities. For example, arboreal species should have an adequate enclosure height and structures for climbing and resting off of the ground, and more terrestrial species should have more floor space available. Providing animals with areas for escape from others may reduce behavioral problems such as aggression. It is also important to keep in mind husbandry and care practices, policies, and requirements when designing animal rooms. Construction materials must be durable, sanitizable, and relatively easy to maintain. In addition, there are often regulatory requirements regarding room environmental parameters (e.g., airflow, temperature, and humidity) that can make providing the appropriate environment for a particular species challenging (e.g., nude, severe combined immunodeficiency [SCID], aged, or immunocompromised rodents many need to be housed in rooms with higher temperatures). Animal area and room doors should also be wide and tall enough to accommodate cage racks and equipment. With newer types of caging intended to accommodate social pairs or groups of animals, and with the growing use of larger “activity cages” to provide more space (sometimes on a rotating basis), rooms and doorways should be of sufficient size to allow their use. Room doors with viewing windows that have shutter-type options are preferred. Animal rooms with windows to the outside may be beneficial for some species. Another option is incorporating specialized lighting features and control mechanisms into the facility design that accommodates the natural behaviors of the animals, as well as allowing for husbandry and care procedures. For example, some nocturnal animals may be housed under reverse light cycle conditions such that husbandry and monitoring are done using red lights. Some other creative facility design ideas or concepts, such as a trickling water feature, may provide some background “white noise” (DeGenova and Abee 2006).

Sound abatement and use of materials that decrease sound transmission help reduce disruption and facilitate better behavioral management. Animal housing rooms and areas should be separated from high-traffic areas, as well as from cage wash or cage processing areas and areas where there is loud activity. Sound abatement measures should be considered, especially when housing sensitive species (e.g., rodent breeding colonies, gerbils, and rabbits) or particularly noisy species (e.g., dogs, swine, and nonhuman primates). It may also be important for animal housing areas and rooms to be in close proximity to testing and clinical procedure areas.

Constructing in-room pens or other enclosures instead of having caging in rooms has become more popular to maximize the space available to the animals, and to allow group housing of a variety of species (e.g., rabbits, cats, and farm animals). Such housing also allows the use of substrates (e.g., wood shavings, hay, and excelsior) on the floor of enclosures, which provides softness and a good opportunity to scatter food to promote foraging or rooting in the substrate. When caging is used, it should be flexible enough to allow introductions of unfamiliar animals (e.g., panels between cages that allow varying degrees of tactile contact between animals, and tunnels between cages). Features that add complexity and variety to the caging, such as “balconies,” “porches,” and “viewing ports,” have been reported to be well used by some species.

It is possible to appropriately house some laboratory animals outdoors (e.g., nonhuman primates and dogs); this should be done whenever possible, as the complexity of the outdoor environment is believed to be beneficial. Outdoor enclosures must be appropriately designed and constructed for the specific species to be housed so that the environment is safe and secure. Outdoor areas must include provisions for shade and protection from wind and other weather elements, as well as provide visual barriers from other animals in the group, and opportunities for species-typical behaviors and activities. Visual barriers and shade structures can also increase the complexity of the environment, and should be constructed to allow the research team and other personnel to clearly view the animals. Ground cover or other substrate may be needed to provide the animals with a comfortable living surface. Selection of materials will depend on the species as well as the population density. A suitable ground cover can assist with erosion control, but the ground cover needs to be a material that can be regularly maintained. Grass, sod, and small gravel, as well as wood chips, hay, and excelsior, are all possible choices that should be evaluated and considered by the veterinary, animal care, facility maintenance, and behavioral management staffs prior to use. The ability to incorporate enrichment items (e.g., small foods) in the substrates should be evaluated. Rotating these substrates or combining them may also be an option that would add variety to the environment. Outdoor areas may also include climbing and play structures. These outdoor areas and equipment should be regularly cleaned and sanitized. They should also be inspected for wear and tear or other potential hazards, and in such case, the damage should be immediately repaired or the equipment replaced. In some cases, indoor living animals can spend brief periods of time outside, and this can be beneficial.

When animals are housed in large indoor enclosures, in large groups, or in outdoor enclosures, animal training programs become more important to achieve reliable access to the animals. It is desirable to design enclosures in such a way that the animals move toward people to shift for cleaning or to enter a transport box, for example, rather than moving away from people, so that PRT can be used for the training. The design of the area into which the animal is moved should be considered carefully. For example, tall animals are unlikely to readily move into a transport box that requires an unnatural or uncomfortable body position. Thus, poor equipment design can thwart the benefits of PRT. A transport box or enclosure design that provides adequate space can make a tremendous difference on the training outcome (e.g., moving the animal) and the methods necessary to complete the task (positive or negative reinforcement).

To determine features of caging systems, considerations must be made for personnel and animals, including species-specific characteristics, socialization potential, research needs and applications, provisions for enrichment devices and distribution methods, husbandry routines, and animal accessing and training. These factors also play a sizable role in the preparation of facility budgets and allocating funds and resources, including personnel and materials costs. There may be financial implications to staffing and supply budgets as well, as new demands on infrastructure to accommodate additional space for preparation and storage of enrichment program materials arise. However, there are also some creative ways to minimize and reduce costs. For example, some facilities incorporate the use of recycled cardboard or paper materials for bedding. In some cases, modifications to husbandry or care practices are implemented (e.g., the interval between husbandry practices may be extended, thereby decreasing personnel time devoted to cleaning and disturbing animals less frequently), with appropriate approvals and while remaining within the relevant recommendations and requirements (e.g., Guide, Office of Laboratory Animal Welfare [OLAW], and AAALAC). In such situations, managers and supervisors will need to evaluate caregiver time for activities, such as preparing, distributing, collecting, and cleaning enrichment materials and devices, and SOPs will need to be reviewed, modified, and approved by the IACUC to expand the approved cleaning methods.

Coordination of Behavioral Management with Research

Behavioral management programs should be carefully coordinated with biomedical and behavioral research in which the animals are involved. Finding the best way to balance the needs of laboratory animals with the needs of the research project in which they are subjects is a complex task. With increasing attention being paid to the psychological well-being of animals, the process must also include this consideration. Behavioral management plans must be harmonized with the goals of the research so that the animals benefit from social housing, enrichment, and animal training, all applied in such a way that the research is not unnecessarily compromised.

The IACUC review process is one forum for this negotiation between investigators and those responsible for behavioral management. The review of research proposals by the IACUC should involve careful consideration of how the research might involve deviation from the standard animal care program, including any requested changes in enrichment or social housing. Preferably, there should be at least one individual serving on the IACUC who has expertise in behavioral management. IACUC protocol forms should include sections for describing plans for social housing, environmental enrichment, and animal training. If an IACUC proposal indicates that social species are to be housed alone, scientific justification must be provided to explain why the research cannot be accomplished with socially housed subjects. Any time that must be spent alone or in “protected contact” (i.e., housing with limited tactile interaction possible between two animals) must be minimized, and additional enrichment should be considered. Each protocol should include information on how animal training will be used within the study so that it is clear what procedures the research staff will train or habituate the animals to, and how that training will be accomplished. There should be a plan for what will be done if subjects do not habituate to research procedures during the expected time frames.

As IACUC protocols are reviewed, investigative staff members may be asked to make changes or accommodations to their studies that they have not made in the past. With new techniques available to improve well-being and with new expectations for standards of care, investigators are essentially being asked to recalibrate some of their studies, and this may take time. Clear communication is important, and instruction, including working examples from other facilities and reviewing published literature with investigators as they attempt to make accommodations, will be helpful. Investigators can be challenged if their funding is not adequate to support these changes, which may bring about increased time that animals are assigned to a study and time that staff is needed to work on the study. In the future, the researcher will be able to incorporate new techniques (e.g., time to train animals to cooperate with research procedures) into funding proposals.

Some routine behavioral management activities may need to be coordinated with ongoing research. For some studies, it is best to have the social environment consistent throughout the study duration, whereas other studies may accommodate social housing only during some phases, so social introductions and separations need to be coordinated with the research staff as the study progresses. Approaches such as intermittent social housing (e.g., animals are housed together during portions of each day or each week) may be useful. Providing enrichment resources, especially foods, may need to be coordinated with research staff, particularly if the research involves any restriction of access to foods or fluids. In some cases, food enrichment resources may need to be provided only after certain research procedures are completed, and scheduling may need to be determined. Low or no-calorie foods may be given to some animals that have restricted access to foods for research purposes. Animal training procedures to help animals habituate to research procedures are typically performed by the research staff members, but behaviors that are trained by others (e.g., animal care, behavioral management, or veterinary personnel) should be transferred to all who might be able to apply the same training methods. For example, if a monkey is trained to cooperate with an injection of a substance for research purposes, the veterinary staff should be taught the process so that they can use the same training methods when accessing the monkey for a physical examination.

Behavioral management can augment research goals by improving the quality of the research. Animal training can make research procedures less stressful for the animals and more efficient for the research team. Handling that reduces animal stress also reduces the potential confounding influence of distress on the study’s dependent measures. Human interactions, such as tickling rats, may help to reduce fear and avoidance of humans, and assist the rats in recovering more quickly from research procedures (Cloutier et al. 2015). Social housing can reduce the stressful influence of some research procedures, as the presence of a familiar companion can “buffer” the animal from these experiences (Gilbert and Baker 2011). Good science depends on animal models that are healthy both physically and psychologically, and good behavioral management programs can be an important means of maintaining healthy research animals.

Coordination of Behavioral Management with Veterinary and Animal Care Personnel

Teamwork, communication, and coordination of behavioral management activities with animal care and veterinary medicine are paramount to optimize the impact on animal welfare and to provide a holistic system of care. Setting up a system describing each group’s responsibility for communication and action is important for reducing confusion and ensuring that behavioral problems are addressed properly. As an example, when animals show excessive fearful behavior, the people who observe the behavior should communicate the incident to staff providing the behavioral care. Animal care staff may report an animal was expressing fearful behavior when they were passing out food, veterinary staff might see fearful behavior when they are restraining an animal, and research staff may report fearful behavior when they are exposing an animal to new research equipment. The staff responsible for the behavioral care should assess the behavior and its environmental triggers, implement treatments such as positive human interaction and animal training, and assess these treatments for effectiveness. If appropriate, treatments should be communicated and coordinated for implementation with other staff as needed. A report of excessive fear may be discussed with veterinary staff and result in evaluation as to whether psychoactive medications might assist in reducing the behavior. Any such treatment should be communicated with staff responsible for behavioral care and researchers, as they will be evaluating any increase or decrease in the behavior or there may be an impact on the study.

Record Keeping and Documentation

In general, the behavioral management program should be reviewed on a regular basis by behavioral management staff, the attending veterinarian, and the IACUC to ensure it is beneficial to animal welfare and that it reflects current scientific knowledge (Guide, p. 53). Record keeping is important for developing behavioral management programs and for monitoring and improving established programs. Records are useful to determine whether the program is running as designed, whether assigned responsibilities are completed, which interventions are effective, and to report on program progress. Development of meaningful documentation systems leads to objective evaluation systems that can be used for identifying programmatic strengths and weaknesses, internal reporting, regulatory reporting, and in some cases, scientific reporting in journals and professional conferences. All aspects of behavioral management (behavior, enrichment, socialization, and animal training) should be documented. This is consistent with recommendations in the Guide, which states, “Records of rearing and housing histories, mating histories, and behavioral profiles are useful for the management of many species, especially nonhuman primates” (p. 75).

Behavioral assessment records allow examining the frequency, duration, or severity of behaviors of concern, the impact of treatments on the problem, and determining whether a different course of action is needed. This information can also be used to evaluate the population’s behavioral health, such as the percentage of a colony expressing particular behaviors, and can depict behavioral responses to programmatic changes over time.

Record keeping should reflect that staff is following institutional SOPs for feeding, supplying enrichment devices, and treatments. Documentation should inform staff about what animals receive which enrichment resource, and should reflect enrichment device cleaning and sanitation outcomes. Records for social housing might include outcomes of each social introduction, reasons for separations, and the total number of socially and singly housed animals in the colony. If nonhuman primates are singly housed, the attending veterinarian is required to review the reasons for individual housing every 30 days. Maintaining such information allows programmatic evaluation and generation of progress reports. These are useful for assessments by outside groups (AAALAC International, U.S. Department of Agriculture [USDA], and Canadian Council on Animal Care [CCAC]) and IACUCs, as well as for advancing the program and comparing it with other programs and publications.

Animal training programs should have established communication and documentation systems, including clear communication of programmatic training goals, applications of training at the facility, and expectations for personnel implementation. These programs provide opportunities for consistency in the way in which animals are worked (i.e., to move the animals to where they are needed, all animals are called to the staff person, not sent away from a staff person), and communication among trainers and staff implementing or maintaining animal training is essential to its success. Records should be kept showing which animals have been trained and for what behaviors, the methods by which animals were trained (via positive or negative or a blend of the reinforcements), the cues the animals know, the expected animal response for each cue, a measurement of consistency in response, and the maintenance schedule (Perlman et al. 2012).

Selecting New Employees and Employee Training on Behavioral Management

In many programs, the animal caregivers are responsible for feeding and cleaning and also for preparing and distributing the environmental enrichment, moving animals from one location to another to facilitate social housing, and managing the feeding of animal groups. They should be trained on the importance of these daily responsibilities and that their interactions with animals can impact the animal’s welfare. With these daily human–animal interactions in mind, the institution should provide training on essential elements of behavioral management: behavior, enrichment, animal training, social group, and pair housing.

First and foremost, staff education is needed to identify appropriate social and nonsocial behaviors and behaviors of concern (e.g., self-injurious behaviors, hair plucking or barbering, and fearful behaviors) for each species, as well as how and to whom concerning behaviors should be reported. Behavioral education provides a caregiver with information on how the animal is responding to its environment and to the events taking place. As an example, being able to identify when animals are showing signs of social incompatibility during feeding times can alert the caregiver that tension is mounting and a different feeding technique may help and/or to contact a behavioral specialist so the problem can be evaluated.

Socialization programs can be complex and require significant time investment, hands-on training, and detailed documentation (Truelove et al. 2015). To complete their role, animal caregivers must be able to identify social behaviors such as aggression or play, apply feeding techniques involving PRT, and use training and reinforcement for social separation to facilitate research.

Caregivers should be trained on requirements for environmental enrichment, such as their role in distribution, documentation, sanitization, and monitoring for safety. This includes enrichment basics such as methods to load and clean enrichment devices; schedules for using different types of foraging devices and other forms of enrichment; how to identify when enrichment devices, structures, or items are damaged and in need of repair; and understanding that damaged devices can cause harm to animals and need to be removed, replaced, and repaired. Other instruction could include how to rotate devices or toys, learning where clean enrichment is stored, and knowing with whom to communicate if enrichment supplies are needed. In addition to these responsibilities, instruction should be given on the outcomes of providing enrichment, such as increasing species-typical behavior, such as nesting, enhanced social interaction, manipulation, and play, as well as the potential for the expression of fear and anxiety to novel objects, and what to do when this is observed.

Caregivers should be trained on how to positively reinforce animal behavior and how to recognize the beneficial impact that it has to their daily work, such as giving food reinforcement or praise to a pig that calmly walks down the hallway to a scale for routine weighing. It is important to discuss how human actions can impact animal responses, and how to appropriately and safely behave around a particular species. As an example, loud noises can startle and increase stress for the animals. Quietly placing items on metal tables or quietly closing a door can greatly reduce noise and disturbance for many research animals.

Upon hire, there should be some instruction on basic behavioral management, and then in the months and years following, continuing educational opportunities. Continuing education in aspects of behavioral management is essential for all staff within an organization as the program changes and is enhanced. Supervisors and managers need to provide leadership and support, as well as work together to create a culture that reflects the importance and significance of the behavioral management program. These opportunities may include further instruction in formalized staff meetings, specialized hands-on training sessions from behavioral management personnel or consultants, webinars, or attending workshops or conferences. In facilities with behavioral management staff on site, animal care and behavioral management cross-training is highly encouraged. These interactions promote the exchange of ideas, understanding of job responsibilities and challenges, and opportunities to teach behavioral management techniques relevant to assigned responsibilities, such as providing food reinforcement immediately following handling or movement from one location to another.

As with all jobs, there are particular personality traits that may lead to more successful personnel and program outcomes. For those working closely with animals in a research environment, managers should be looking for individuals with compassion for animals, willingness to cooperate and collaborate with others, thoroughness with attention to detail, and evidence of being accountable and responsible. Young and Cipreste (2004) describe characteristics of good animal trainers and say these factors are important in the success of the animal training program. These characteristics include patience, a calm demeanor, and the ability to be both consistent and analytical of their own behavior.

For those working in behavioral management programs, learning how to correctly and thoroughly implement behavioral management techniques requires training, time, and practice. Many of the skills needed for behavioral management staff can be acquired through hands-on experience, classroom instruction, workshops, reading published literature, or visiting behavioral management consultants. Especially when training opportunities are limited within a facility, there are many professional organizations, workshops, conferences, web-based resources, and other reading material that will be useful for staff training and continuing education in behavioral management (Tables 5.3 and 5.4).

Table 5.3

Examples of Professional Organizations Whose Scope Relates to the Behavioral Management of Captive Animals.

Table 5.4

Examples of Workshops, Conferences, and Other Learning Resources Related to Behavioral Management.

Structure of Behavioral Management Programs

Behavioral management programs typically fall into three categories: project based, section-wide, and facility-wide (Perlman et al. 2012). One institution may implement multiple approaches simultaneously, and programs may evolve from one structure to another. A project-based approach includes a few animals and a limited number of staff members. Often, this approach is used within a research laboratory or with a small group of animals, and relies on a motivated individual and may not persist when that individual is not present. The benefits include increased welfare of animals and a positive impact on job satisfaction of those implementing the program. Drawbacks may include limited resources and support, the efforts can be viewed as expendable when time is restricted, often there may be less emphasis on safety for animals and staff, and limited training of staff and supervision of activities. Lastly, inconsistent implementation of behavioral management programs across an institution may be problematic for oversight organizations such as USDA, IACUC, and AAALAC.

A section-wide approach includes a greater number of animals and sometimes more staff members than the project-based approach. This approach often has the support of a manager and is implemented within a unit or department. The benefits include improved safety and staff training, and improved animal management. With more animals and staff involved, there may be a greater chance that additional changes will follow. Drawbacks include limited support from other departments that may interface with the same animals, limited opportunities for the continuing education of staff (such as attending conferences or workshops), and the behavioral management activities may not persist beyond the manager’s tenure.

A facility-wide approach is implemented and supported by all departments throughout the entire facility and impacts the greatest number of animals. The benefits include support for continuing education and training of staff members, and allocation of resources toward the effort, such as dedicated staff and equipment. The program and goals are clearly defined, which includes both what is provided for the animals (e.g., all animals receive foraging opportunities daily) and who is responsible and accountable for providing those opportunities. Drawbacks include the cost of increased personnel and educational opportunities, but these are minimized through proper communication and education. Defining returns on investments should be part of the overall plan.

Characteristics of Successful Behavioral Management Programs

There are a number of hallmarks of research, teaching, and testing facilities that have superior behavioral management programs. When the psychological aspects of animal care programs are viewed as essential to daily work rather than as luxuries that will only be carried out when resources allow, then these programs flourish. Although upper-level management and administrative staff members may not engage directly in behavioral management programs, their support and interest are vital. Upper-level managers may determine the resources that will be devoted to behavioral management. Financial support is needed for personnel, supplies, equipment, storage space, and office space. Funds to send staff members to attend conferences and workshops on behavioral management are important for ensuring that they have the knowledge and skills to carry out the work. This is especially important in facilities that do not have individuals on staff that are trained in species-specific animal behavior. The most effective behavioral management programs also have forward-thinking individuals with a passion for improving animal welfare, and an organizational culture that embraces change and seeks improvement.

Behavioral management programs require constant evaluation and revision, especially as the animal population changes (e.g., new species are acquired), as needs of the animals change (e.g., new research procedures begin), and as new behavioral management techniques are employed (e.g., an animal training program is started). If behavioral problems are becoming more evident or more widespread (e.g., a certain abnormal behavior is observed more frequently or among a larger portion of the animal colony), then new plans should be devised to address and possibly prevent this problem behavior.

As with other elements of animal care programs, effective and standardized methods of communication with intentional redundancy are needed. Communication between those directing the behavioral management activities and animal care staff, veterinary staff, research staff, and shop or maintenance staff will be needed to carry out the program. For example, typically animal care staff members deliver enrichment items to the animals, but representatives of all these groups should be involved in determining the appropriateness of various types of enrichment for research animals.

Like other areas of laboratory animal care, behavioral management programs should be supported by SOPs and other written documents to describe central practices. Examples include SOPs for the enrichment program, for training animals for restraint procedures, and for social introduction procedures. Other written guidelines may include a schedule or calendar for delivering enrichment resources, detailed animal training plans for common procedures, descriptions of behaviors to look for among socially housed animals, and a written process for reporting behavioral problems. Written policies to promote the psychological well-being of nonhuman primates and to exercise dogs are required under the AWA.

Conclusions and Summary

Behavioral management is a critical part of a well-functioning animal research program, and is receiving increasing support and emphasis from the public, peer review and accreditation groups, and regulatory agencies. Behavior management programs are based on the goal of increasing animal well-being and species-appropriate behavior while decreasing abnormal behavior and distress. These goals are achieved by offering animals novelty, choice, and control within their environments (via environmental enrichment programs, good facility design, and animal training), habituating them to the procedures they will undergo (via collaboration with researchers, management, and veterinary staff), and allowing animals maximum social contact with conspecifics (via a species-appropriate socialization program). Each of these methods requires a team approach, with the investment of time, resources, and commitment from a variety of individuals within a facility, including behavior specialists, veterinarians, facility management, animal care staff, researchers, and the IACUC.

Successful behavioral management programs will necessarily evolve as new literature and technologies become available. With the increasing ease of use and decreasing cost of touchscreen devices, it is easy to anticipate these devices may be more commonly used to allow animals to interact with their environment in increasingly sophisticated ways, such as having switches to turn on or off sensory enrichment devices, such as television or music, or by completing simple mazes or puzzles to obtain a treat or other reward. With the advent of electronic record-keeping and analysis software built to handle “big data,” the review of a behavior management strategy’s efficacy may become much more routine, but may also introduce new context to conventional wisdom, such as with the increasing nuance regarding mouse nesting materials. Video and image analysis software are already used for automated behavior coding for mouse phenotyping purposes and to analyze nonhuman primate alopecia, and as these technologies become more reliable and cheaper, they could be used more routinely for behavioral assessment. Regardless of what changes in specific techniques may come, the characteristics of a well-functioning behavioral management team will remain constant: open communication with all relevant staff, adequate training in animal behavior according to each person’s role, the establishment and analysis of valid performance measures, and regular self-evaluation.

Acknowledgments

We greatly appreciate the collaboration of the entire Animal Resources Division at the Yerkes National Primate Research Center. Funding support was from the National Institutes of Health, Office of Research Infrastructure Programs (OD P51) OD011132. All aspects of management and research use at the Yerkes Center conformed to the Emory University IACUC and U.S. federal regulations and guidelines. We also appreciate the support of the National Institutes of Health Division of Veterinary Resources and its behavior unit. We are grateful for the assistance of Kristina Adams from the Animal Welfare Information Center for collecting literature resources. The Yerkes Center and the National Institutes of Health are fully accredited by the Association for Assessment and Accreditation of Laboratory Animal Care International.

Further Readings

• Bayne, K., and P.V.Turner. 2014. Laboratory Animal Welfare. New York: Elsevier.
• Young, R.J.2003. Environmental Enrichment for Captive Animals. Oxford: Wiley-Blackwell.

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