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Environmental Enrichment For Nonhuman Primates Resource Guide: Animal Behavior Research Findings Facilitate Comprehensive Captive Animal Care - The Birth of Behavioral Management

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Animal Behavior Research Findings Facilitate Comprehensive Captive Animal Care: The Birth of Behavioral Management

J. L. Weed1 and P. L. O’Neill-Wagner2
1Division of Veterinary Resources, Office of Research Services, National Institutes of Health, DHHS and 2Laboratory of Comparative Ethology, NIH Animal Center, Poolesville, Maryland, NICHD, DHHS.

Corresponding author:

J. L. Weed
9000 Rockville Pike
Bldg 14G, MSC 5590
Bethesda, MD 20892


During the past several decades there has been an explosive increase in animal behavior research in captive and wild animal populations. This growing body of scientific investigation expands the understanding of basic principles underlying animal behavior relative to biology, psychology, ecology, and natural history. As scientific research reveals increasing detail about the mechanisms influencing and driving animal behavior, the ability to appropriately manage and enhance the captive animal experience is opened to more possibilities and options including the area of animal well-being. In fact, this expanding informational resource is being applied today by a new breed of experts, Animal Behavior Managers, found working worldwide in facilities such as zoos, animal breeding colonies, and biomedical research institutions.

What prompted this shift from scientific discovery to applied principles of animal management? Some would consider the passage of welfare legislation (AWA, 1985) to be a defining moment for the regulatory acceptance and application of animal behavior research findings. While this legislation formally codified the idea of environmental enhancement and introduced the phrase 'psychological well-being', the concept had already been described in the 1972 and 1985 editions of The Guide for the Care and Use of Laboratory Animals (The Guide) and was likely the influence for later legislation. The Guide, published by the National Research Council through the Institute for Laboratory Animal Resources and the National Institutes of Health, is intended “to assist scientific institutes in providing professionally appropriate care for laboratory animals.” Proper management is defined in the 1972 Guide as “any system of housing and care that permits animals to grow, mature, reproduce, or behave normally, and to be maintained in physical comfort and good health.” Elsewhere in the 1972 edition, the term psychological well-being was utilized relative to physical activity and exercise. Revisions to the 1985 Guide include the recommendation that 'consideration be given to enriching the environment'. The term Behavioral Management also first appeared in the same edition and describes various ways to promote well being by providing social opportunities, structural complexities, and stimulating activities for captive animals. These regulations and guidelines responded to behavior goals for achieving psychological well-being using environmental enhancements in addition to the traditional clinical, husbandry, and design aspects of captive animal management.

From Environment Based to Behavior Based Terminology

Markowitz (1974; 1978) proposed a term Behavioral Engineering to describe changes in zoo collection management to expand the range and expression of natural behavior of the animals and thereby improve the animals' well-being. These changes included implementing naturalistic feeding, problem-solving, and locomotor challenges for the animals. As a result of Markowitz's innovations, animals began to engage in more species typical behavior. This allowed zoo animal managers to improve the visual, auditory, and learning experience of the zoo visitors, while stimulating and enriching the captive animals. Although it appeared to be a win-win situation his concept initially met with limited acceptance from the zoological community, likely due to the terminology. Zoo professionals were concerned that Behavioral Engineering terminology meant engineering the animal's behavior rather than engineering environments that improved the animal's well being (Markowitz, 1982; Markowitz, personal communication, 2006).

Similarly, the term Environmental Enrichment has experienced difficulties since its inception. Newberry (1995) describes some of the problems associated with this term. The difficulty with the 'EE' terminology is due to a limited number of scientifically guided assessments of enrichment techniques or procedures and hard evidence regarding effectiveness in actual use. The “EE” catch phrase came to include any implementation of changes in the captive animal's space regardless of the overall impact. Even though enrichment plans evolved out of the Animal Welfare Regulation mandate to “enhance the environment” those plans dedicated solely to enriching the animal's physical environment often fell short of desired behavioral outcomes due to individual animal social and housing needs, rearing history, biology, genetic makeup, developmental life stage, and experimental stressors.

A number of approaches focused more on structured activities such as individual animal training, socialization, and dietary diversity, to meet the needs of individual animals and researchers. Plans have been referred to as Behavioral Performance Plans (Swaisgood, & Sheperdson, 2005), Refined Husbandry and Management Plans, (Rice, 1994), Clinical Ethology Plans (Ladewig, 2005), Wildlife Management Plans for the Laboratory (Bayne, 1995), Interdisciplinary Approaches (Lund et al, 2006), Cooperative Approaches (Reinhardt & Cowley, 1990; Vertein & Reinhardt, 1989), and Time Management Plans (Schwammer, 1997), just to name a few.

Approaches differed in their attention toward individual animal needs. Treatment and prevention of individual behavior problems varied widely, as did performance training of animals relative to implementation of specific research protocols. While some environments allowed for expression of species normative behavior in captivity, others did not. Variation in terminology and focus very likely corresponded to variation in behavioral results. Animal responses to routine and standardized enrichment techniques have been wide-ranging, at times unanticipated, and even counter intuitive to popular belief (cf. Line et al., 1990; Markowitz & Timmel, 2005; Morgan et al., 1998).

Observing these diverse responses offered a much needed opportunity for reevaluating the systematic approach required to achieve well-being. Reviews by Bloomsmith & Else, 2005; Kulpa-Eddy et al., 2005; and Lutz & Novak, 2005, provide a historical perspective on the evolution of enrichment programs for animals with particular attention to programs for non-human primates. This lack of standardized enrichment implementation and diversity of outcomes most likely led to the widespread use of the more popular Behavioral Management terminology.

From Technically Based to Scientifically Based Enrichment

It is also likely that transitioning from the most prevalent term Environmental Enrichment to the less familiar Behavioral Management required a common purpose to gain acceptance. Use of the term Behavioral Management suggests a broader program scope regardless of whether it is implicitly or explicitly stated in any formal documentation (Rice et al., 2002). There also seems to be a general consensus from the literature that captive animal welfare programs are gradually evolving from technically based to scientifically based programs. This is a sensible transition since vast resources of scientific literature and clinically logged data continue to develop a strong foundation that allows for more comprehensive animal husbandry and clinical care programs. These advancements have taken generic environmentally based enrichment plans to a more scientific individualized animal enrichment technology based upon known relationships between the animal's environment, from birth to maturity, and its overall behavior profile.

Although scientifically based assessments of enrichment programs are in their infancy (Baker et al., 2006; Bloomsmith & Else, 2005; Crockett, 1998), current behavioral management plans at zoos and in primate laboratories have successfully advanced to a point where the behavioral and clinical needs of animals in socially and physically stimulating environments are currently an integral component of the overall animal program (Bloomsmith & Else, 2005; Maple & Archibald, 1991). Collaborative programs between clinical and behavioral specialists at these facilities are becoming the standard rather than the exception. Baker et al. (2006) surveyed several laboratory and university facilities which house non-human primates. The focus of the survey was enrichment and behavioral management. They found that nearly half of all enrichment program managers working at primate facilities had formal training in behavior methods. The day-to-day behavioral management of the animals is increasingly tasked to individuals trained specifically in animal behavior and assessment techniques. The impetus for this change may be due in part to the concerted efforts of a few individuals who began their careers working in the zoo community and in some cases managing primate research facilities.

Gail Laule and Tim Desmond were among the first to formally document methods for enhancing the captive experience for zoo and laboratory animals, (Desmond, 1994; Laule, 1993). One individual in particular, Dr. Michale Keeling, formerly at the M.D. Anderson Cancer Center in Texas, demonstrated great foresight by adopting these behavioral management techniques to the laboratory (Keeling et al., 1991). Dr. Keeling was a program director who realized the benefits of hiring individuals with behavioral backgrounds to work in the primate laboratory at Bastrop, Texas. Keeling and his colleagues (Keeling et al., 1991) proposed a strong bias for action regarding the management of primates and enrichment programs in laboratories. Many of those management tenets for working with non-human primates have become commonplace in the general laboratory and zoological community (Bloomsmith et al., 1991; Schapiro, 2000; Schapiro et al., 2003; Schapiro et al., 1994; Schapiro et al., 2005; Whittaker et al., 2001; NRC, 1998).

It is clear that the major focus of current environmental enhancement programs is more than just providing supplemental toys for animals to manipulate. This is true regardless of whether animals are housed in a research laboratory or zoological collection. The concept of behavioral management addresses questions about animal behavior as a critical and integral component of the overall health and well-being of these animals. Benefits from the efforts of dedicated animal behavior specialists working at all levels of laboratory and zoo collection management are being experienced by the animals as well as veterinarians, principal investigators, animal care staff, business office managers and the general public. Programs will continue to evolve and address well-being as more data are generated allowing improved captive animal management. The challenge for the future is to continue finding support for scientifically updating the principles and procedures of behavioral management. Markowitz and Timmel (2005) point out that there is continued reluctance from funding agencies to support needed basic research into issues relative to facility design, husbandry techniques or behavioral methods which potentially enhance animal well-being. Continued support from individuals responsible for laboratory and zoological review, accreditation, and oversight is critical to move these programs forward. This is especially true if the principles advocated by practitioners of behavioral management are to ultimately gain acceptance as the new standards of animal care.



J. L. Weed is supported by the Intramural Research Program of the NIH, Division of Veterinary Resources, Office of Research Services. Peggy O'Neill-Wagner is supported by the Intramural Research Program of the National Institute of Child Health and Human Development, Laboratory of Comparative Ethology.



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