By Amy Davis, JD, MPH

This post is a follow up to our May 27, 2014 post on the topic of environmental enrichment of animals in research settings. After that post was published, PRIM&R received a letter from Allyson J. Bennett, PhD, chair of the Committee on Animal Research and Ethics at the American Psychological Association (APA), and Sangeeta Panicker, PhD, director of research ethics at the APA, expressing their disapproval of our treatment of the topic (read the letter from Drs. Bennett and Panicker). In the spirit of transparency and respectful dialog, PRIM&R has written this second post, which we believe is a more considered treatment of an important and complex issue. We thank Drs. Bennett and Panicker for their feedback and for prompting us to take this second look.

There is no specific definition of “environmental enrichment.” (Mellen) It is a concept that has evolved and matured over the last 100 years at least, and is based on the idea that providing captive animals with more complex environments enhances their physical and mental health. (Adams, 2008)

It was in zoos where the earliest research occurred that spawned the evolution of environmental enrichment practices. The first zoos of the late 19th century were more like laboratories than places for public education and entertainment that we know today. Charles Darwin’s research spurred interest in studying animal species, which was most conveniently done in places where large collections of different animals could be enclosed, manipulated, and observed. (Young) The first steps toward environmental enrichment were taken to protect the physical health of these animals.

More sophisticated measures to advance animal welfare developed as scientists began to observe stereotypic behaviors in zoo animals. A psychobiologist named Robert Yerkes is credited for first observing, in research he conducted in the 1920s, that the well-being of captive primates improved with the introduction of apparatus with which the animals could interact. He later established the first primate research laboratory in the US (which later became the Yerkes National Primate Research Center). (USDA Perspective on Environmental Enrichment for Animals) Later, psychology research conducted in the 1940s and 50s expanded on this theme. Psychologist Donald Hebb, for example, explored the effects of early experience on problem-solving and behavior at maturity. In one of his experiments, he brought home a group of laboratory rats for his children to raise as pets. He simultaneously monitored a group of rats in the lab who were not exposed to the same social and environmental stimulation as the pet rats. He then tested the both sets of rats in the lab and found that the pet rats performed better at problem solving (such as moving through a maze) than the rats raised in the sterile or “impoverished” settings of the laboratory. Hebb concluded that “richer experience of the pet group during development made them better able to profit by new experiences at maturity.” (Adams, K.)
Studies that built on the work of Hebbs produced further evidence of the intellectual benefits of environmental stimuli on captive animals. Researchers ultimately concluded that animals raised in “richer environments” offering complex visual surroundings and opportunities for physical activity, were intellectually superior to animals raised in barren environments. It was at this time that researchers started to use the terminology of “enriched” (e.g., larger spaces, objects to play with and opportunities for social interaction) versus “restricted” environments. (Adams, K.)
Many studies of animal behavior conducted during the first half of the 20th century were based on interventions that could be directly observed and quantified. Researchers believed that animal behavior and training were conditioned responses to stimuli such as food and instinct. (Shepherdson) However, in the 1960s, psychologists Marian and Keller Breland, who studied under the behaviorist B.F. Skinner, conducted studies that revealed far more complex behaviors that could not be explained by “conditioned response” and came to be attributed to “complex mental states” and psychological needs. These studies showed, for example, that well fed, captive animals still had a need to forage, hunt or somehow “work” for their food, and that lacking these activities tended to stress the animals. (Shepherdson) Thus, scientists were learning that enriched environments should include more than physical and social stimuli, but also opportunities to meet subtler, innate behavioral needs.
Another astonishing discovery during this period of psychological research were findings showing that enriched housing not only reduced stress and increased the ability to learn, but actually led to physical changes to the brain and nervous systems. Mark Rosensweig and his colleagues, for example, compared the cerebral cortex of rodents raised in “enriched” environments with those raised in “impoverished” environments and found that the cerebral cortex of rats raised in enriched settings were heavier. (Rosenzweig)
The work of another renowned psychologist, Harry Harlow, advanced the concept of environmental enrichment through the study of environmental deprivation. His studies of rhesus monkeys reared in restricted environments revealed significant behavioral deficits including reduced exploratory, communicative, emotional, sexual, and maternal behaviors. (Jarred) He also found that primates raised in barren laboratories were more likely to develop aberrant behaviors such as “floating arm syndrome.” Modifications to the environment such as adding devices with which the animals could interact, reduced such aberrant behaviors. (Young)
The legislative history of animal welfare laws reflects the influence of the emerging scientific findings described above, politics, and cultural events. The first law to promote animal welfare, the Laboratory Animal Welfare Act, was promulgated in 1966 to prohibit the theft of pets for research. (Levin et al.) This act established “minimum standards for the handling, sale and transport of cats, dogs, nonhuman primates, rabbits, hamsters, and guinea pigs held by animal dealers or pre-research in laboratories.” (Adams) This act also limited the types of animals (animals transported across state lines) and institutions (facilities that received federal funding) to which it applied. As scientists and the public learned about the risks to and strategies for advancing welfare of captive animals the law was amended. The first amendment in 1970 removed the interstate transport condition and expanded coverage to all “warm-blooded” laboratory animals. In 1976, an amendment to the law outlawed the interstate transport of animals used for fighting events, and in 1985, the act was amended to explicitly cover research animals, an amendment that was intended to establish standards for minimizing pain and distress of research animals. Its requirements included: exercise for dogs, consideration of the psychological well-being of non-human primates, establishment of the institutional animal care and use committee (IACUC), consideration of alternatives to animal use, prevention of unintended duplication of experiments and tests, and training in the humane treatment of research animals. (Adams) These requirements form the regulatory foundation for environmental enrichment.
Over the years the concept of environmental enrichment became a scientific pursuit in and of itself. Although the reference to psychological well-being in the 1985 amendment referred only to non-human primates, the application of environmental enrichment practices gradually spread to all captive animals. (Adams) Eventually frameworks were developed for the more systematic application of these practices. Enrichment methods were categorized into five major types and goals, standardized as follows:
Categories of Enrichment:

• Social
• Occupational (puzzles, exercise machines)
• Physical (size of enclosure, fixtures, toys)
• Sensory (visual, auditory)
• Nutritional

Goals of Enrichment:

• Increase behavioral diversity
• Reduce the frequency of abnormal behavior
• Increase the range or number of normal (i.e., wild) behavior patterns (Young)

Two different approaches to the implementation of environmental enrichment emerged towards the end of the 20th century:

1. The “naturalistic” approach that relies on recreating natural habitats to stimulate natural behaviors within the captive environment.
2. The “behavioral engineering” approach, which Yerkes introduced, and which another researcher named Hal Markowitz built upon, relies on artificial devices and machines with which the animals interact to express natural behaviors. (Young, Mellen) 

Scientists debated the value of the alternative approaches, but over time began to recognize that both approaches provide benefit to the animals and could be implemented compatibly. A 21st century approach to environmental enrichment might be characterized as “holistic.” (Mellen) This strategy is based on the idea that enrichment practices should be tailored to the individual animal taking into consideration the animal’s species, natural history, individual history, physical environment, and access to social interaction with other animals and humans.
Although much research has been conducted over the last 100 years to discover optimal techniques for reducing stress and improving physical and mental health of captive animals, the search for the most effective kinds of enrichment for each species, and indeed each animal, is ongoing. (Swaisgood, et al.; Mellen)
Resources
Adams, Benjamin; Larson, Jean. “Legislative History of the Animal Welfare Act: Introduction” USDA. NAL. Animal Welfare Information Center.
Adams, Kristina M. “Refinement in the literature: Searching for environmental enrichment;” AATEX 14, Special Issue, 307-312; Proc. 6th World Congress on Alternatives & Animal Use in the Life Sciences. Tokyo, Japan: Japanese Society for Alternatives to Animal Experiments. 2008
Arras John D.; Fenton, Elizabeth; Kukla, Rebeca; eds. The Routledge Companion to Bioethics. New York: Routledge, 2015.
Jarrard, Leonard, ed. Cognitive Processes of Nonhuman Primates. “The Effect of Early Adverse and Enriched Environments on the Learning Ability of Rhesus Monkeys,” by H.F. Harlow, M.K. Harlow, K.A. Schiltz, and D.J. Mohr. New York: Elsevier, 1971 (Based on Sixth Annual Ssymposium on Cognition held at Carnegie-Mellon University 1970)
Kulpa-Eddy, Jodie A.; Taylor, Sylvia; Adams, Kristina M. “USDA Perspective on Environmental Enrichment for Animals.” ILAR Journal, Vol. 46, Issue 2. 2005: Pp. 83-94.
Levin, Lis H.; Reppy, William A. “Reforming the politics of animal research,” J Med Ethics, Article first published online: 25 February 2015. doi:10.1136/medethics-2012-101043.
Mellen, Jill; MacPhee, Marty Sevenich. “Philosophy of environmental enrichment: Past, present, and future.” Zoo Biology, Vol 20. 2001: Pp 211-226. Wiley-Liss, Inc. Article first published online: 10 August 2001. DOI: 10.1002/zoo.1021.
National Research Council Institute for Laboratory Animal Resources. Guide for the care and use of laboratory animals. Washington DC: The National Academies Press. 2011. 
PewResearchCenter. “Opinion Differences Between Public and Scientists.” 2015. 
Rosenzweig, M.R., Bennet, E.L., and Diamond, M.C. (1972). “Brain Changes in response to experience,” Scientific American, 226 (2), 22-29. 1972
Shepherdson, David J.; Mellen, Jill D.; Hutchins, Michael (eds). Second Nature: Environmental Enrichment for Captive Animals. (Based on papers from a conference held in Portland, OR) The Smithsonian Institution. 1998.
Swaisgood, Ronald R.; Shepherdson, David J. “Scientific approaches to enrichment and stereotypies in zoo animals: what’s been done and where should we go next?” Article first published online: 22 July 2005. DOI: 10.1002/zoo.2006
Young, Robert J. Environmental Enrichment for Captive Animals. Wiley-Blackwell, 2003.