Introduction to environmental enrichment for primates

Environmental enrichment refers to items or stimuli that are provided to captive animals to support their behavioral needs. All animals evolved distinct behavioral patterns, and difficulty in engaging in these behaviors can cause frustration or boredom, which, in turn, can lead to stress and the development of abnormal behaviors. Enrichment provides a way to increase opportunities for the expression of species-specific behaviors and decrease the occurrence of abnormal behaviors. As such, environmental enrichment is an integral part of caring for captive animals.

Two of the primary goals of enrichment are to reduce stress and improve the psychological well-being of captive animals. Animals living in captivity are exposed to a variety of stressors in their daily lives. Common husbandry practices, such as cage changes or cleaning, and environmental factors such as lighting, noise and temperature, may cause stress for some individuals. Environmental enrichment can help to ameliorate the effects of potential stressors associated with the captive environment and enhance the animals’ physical and mental health. Furthermore, enrichment can help promote resiliency to stress, which helps animals recover, behaviorally and physiologically, from aversive stimuli. This increased ability to respond appropriately to stress is widely considered an important aspect of well-being in captive animals. 

Enrichment is often classified into five broad and overlapping categories: social, physical, sensory, food, and cognitive/occupational. Ideally, animals should receive enrichment from all categories. Social enrichment typically consists of housing individuals with conspecifics, although it may also include interaction between a nonhuman primate and its caretaker. Positive human-primate interactions can promote psychological well-being for both species.  Social enrichment is described in more detail here. Physical enrichment is a common form of enrichment and includes items designed to provide physical structure (such as perches, floor substrate, or climbing areas) and items that provide opportunities to explore or manipulate (such as toys, mirrors, etc.). Sensory enrichment provides animals with visual, tactile, and olfactory opportunities and includes exposure to various sights (often through television or computer screens), sounds, and smells. Food enrichment provides opportunities for captive animals to increase the amount of time they spend searching for, processing, and eating, behaviors which occupy much of the activity budget of most species in the wild. It includes the use of foraging devices, many of which are commercially available. Finally, cognitive and occupational enrichment provide opportunities for nonhuman primates to obtain physical and/or mental stimulation, and includes both exercise and problem-solving tasks. Animal training can be considered a type of cognitive enrichment because the animals are learning. 

While specifics may change across species, there are general tenets of successful enrichment programs.

The Association of Zoos and Aquaria: https://www.aza.org/managing-animal-enrichment-and-training-programs

The Animal Welfare Institute: https://awionline.org/content/enrichment-and-refinement-databases

The Primate Info Net, maintained by the Library of the Wisconsin National Primate Research Center: http://pin.primate.wisc.edu/research/vet/

The Southwest National Primate Research Center: http://snprc.org/primates/primate-care/

The National Institutes of Health (NIH) and Office of Laboratory Animal Welfare (OLAW) have published a six-booklet series on enrichment for baboons, capuchins, chimpanzees, macaques, marmosets and tamarins, and squirrel monkeys:    http://grants.nih.gov/grants/olaw/Enrichment_for_Nonhuman_Primates.pdf

The Animal Welfare Information Center’s Environmental Enrichment for Nonhuman Primates Resource Guide; http://www.nal.usda.gov/awic/pubs/Primates2009/primates.shtml

European Primate Network: Advancing 3Rs and International Standards in Biological and Biomedical Research: EURPRIM-Net; http://www.euprim-net.eu/

The Shape of Enrichment: https://theshapeofenrichmentinc.wildapricot.org/

The Enrichment Record: http://enrichmentrecord.com/

The Animal Behavior Management Alliance: https://theabma.org/

Selected books on enrichment

Erwin, J, Maple. T.L., and Mitchell, G. (Eds.) (1979). “Captivity and Behavior: Primates in Breeding Colonies, Laboratories and Zoos. Van Nostrand Reinhold Company, New York.

Fortmen, J.D., Hewett, T.A., and Bennett, B.T. (2002). “The Laboratory Nonhuman Primate”. CRC Press, Boca Raton, London, New York, and Washington D.C.

Kleiman, D.G., Allen, M.E., Thompson, K.V., and Lumpkin, S. (Eds.) (1996). “Wild Mammals in Captivity”. The University of Chicago Press, Chicago.

Markowitz, H. (1982). “Behavioral Enrichment at the Zoo.” Van Nostrand Reinhold, New York.

National Research Council (1998). “The Psychological Well-Being of Nonhuman Primates”. National Academy Press, Washington, D.C. **This book is available online http://www.nap.edu/catalog/4909.html 

Novak, M. and Petto, A. (1991). “Through the Looking Glass: Issues of Psychological Well-being in Captive Nonhuman Primates”. American Psychological Association, Washington, D.C.

Reinhardt, V. (2008). “Taking Better Care of Monkeys and Apes”. Animal Welfare Institute, Washington, D.C.

Reinhardt, V. and Reinhardt, A. (2008). “Environmental Enrichment and Refinement for Nonhuman Primates Kept in Research Laboratories: A Photographic Documentation and Literature Review”. Animal Welfare Institute, Washington, D.C.

Segal, E.F. (1989). “Housing, care and psychological well-being of captive and laboratory primates. William Andrew Publishing, London.

Shepherdson, D.J., Mellen, J.D., and Hutchins, M. (Eds.) (1998). “Second Nature: Environmental Enrichment for Captive Animals”. Smithsonian Institution Press, Washington, D.C.

Vernes, M.K., and Louwerse, A.L. (Eds.) (2010). “BPRC’s Enrichment Manual for Macaques and Marmosets”. Biomedical Primate Research Centre, The Netherlands.

Winnicker, C., Honess, P., Schapiro, S.J., Bloomsmith, M.A., Lee, R., McCowan, B., Oettinger, and Simmons, J. H. (2013). “A Guide to the Behavior and Enrichment of Laboratory Macaques”. Charles River Laboratories.

Wolfe-Coote, S. (Ed.) (2005). “The Laboratory Primate”. Elsevier Academic Press, London.

Wolfensohn, S. and Honess, P. (2005) “Handbook of Primate Husbandry and Welfare”. Blackwell Publishing, Oxford, U.K.

Yerkes, R.M. (1925). “Almost Human.” Century, New York.

Young, R.J. (2003). “ Environmental Enrichment for Captive Animals”. Blackwell Publishing, Oxford, U.K.

Specific Categories

Safety

Baer, J.F. (1998). A veterinary perspective of potential risk factors in environmental enrichment. In “Second Nature: Environmental Enrichment for Captive Animals” (D.J. Shepherdson, J.D. Mellen and M. Hutchins, Eds.), pp. 277-301. Smithsonian Institution Press, Washington, D.C.

Bayne, K. (2005). Potential for unintended consequences of environmental enrichment for laboratory animals and research results. ILAR J 46, 129-139.

Bayne, K.A.L, Dexter, S.L., Hurst, J.K., Strange, G.M., and Hill, E.E. (1993). Kong toys for laboratory primates: are they really an enrichment of just fomites? Laboratory Animal Science 43, 78-85.

Hahn, N.E., Lau, D., Eckert, K. and Markowitz, H. (2000). Environmental enrichment-related injury in a macaque (Macaca fascicularis): intestinal linear foreign body. Comp Med 50, 556-558.

Honess, P.E. and Marin, C.M. (2006). Enrichment and aggression in primates. Neuroscience Biobehav Rev30, 413-436.

Physical enrichment

Anderson, M.R. (2014). Reaching new heights: The effect of an environmentally enhanced outdoor enclosure on gibbons in a zoo setting. J Appl Anim Welf Sci17, 216-227.

Baker, K.C. (1997). Straw and forage material ameliorate abnormal behaviors in adult chimpanzees. Zoo Biology 16, 225-236.

Beisner, B.A. and Isbell, L.A. (2008). Ground substrate affects activity budgets and hair loss in outdoor captive groups of rhesus macaques (Macaca mulatta). Am J Primatol 70, 1160-1168.

Bennett, A.J., Bailoo, J.D., Dutton, M.B., Michel, G.F., and Pierre, P.J. (2018). Psychological science applied to improve captive animal care: a model for development of a systematic, evidence-based assessment of environmental enrichment for nonhuman primates. Psyarxiv.com

Cannon, T.H., Heistermann, M., Hankison, S.J., Hockings, K.J., and McLennan, M.R. (2016). Tailored enrichment strategies and stereotypic behavior in captive individually housed macaques (Macaca spp.). J Appl Anim Welf Sci 19, 171-182.

Coleman, K. and Novak, M.A. (2017). Environmental enrichment in the 21st century. ILAR J 58, 295-307.

Costa, R., Sousa, C., and Llorente, M. (2018). Assessment of environmental enrichment for different primate species under low budget: A case study. J Appl Anim Welf Sci 21, 185-199.

Crast, J., Bloomsmith, M.A., and Jonesteller, T.J. (2016). Behavioral effects of an enhanced enrichment program for group-housed sooty mangabeys (Cercocebus atys). J Am Assoc Lab Anim Sci 55, 756-764.

De Groot, B. and Cheyne, S.M. (2016). Does mirror enrichment improve primate well-being. Anim. Welf 25, 163-170.

Doane, C.J., Andrews, K., Schaefer, L.J., Morelli,. N, McAllister, S., and Coleman, K. (2013). Dry bedding provides cost-effective enrichment for group-housed rhesus macaques (Macaca mulatta). J Am Assoc Lab Anim Sci52, 247-52.

Fernandez, E.J. and Timberlake, W. (2019). Selecting and testing environmental enrichment in lemurs. Front Psychol 10, 2119.

Gottlieb, D.H., O’Connor, J. R., and Coleman, K. (2014). Using porches to decrease feces painting in rhesus macaques (Macaca mulatta). J Am Assoc Lab Anim Sci53, 653-656.

Gray, A.E. and Nekaris, K.A.I. (2015). Trialling exudate-based enrichment efforts to improve the welfare of rescued slow lorises Nycticebusspp. Endanger Species Res 27, 21-29.

Kessel, A.L. and Brent, L. (1998). Cage toys reduce abnormal behavior in individually housed pigtail macaques. J Appl Anim Welf Sci 1, 227-234.

Line, S.W., Morgan, K.N., and Markowitz, H. (1991). Simple toys do not alter the behavior of aged rhesus monkeys. Zoo Biology 10, 473-484.

Luchins, K.R., Baker, K.C., Gilbert, M.H., Blanchard, J.L., and Bohm, R.P. (2011) Manzanita wood: a sanitizable enrichment option for nonhuman primates. J Am Assoc Lab Anim Sci50, 884-7.

Nakamichi, M. and Asanuma, K. (1998). Behavioral effects of perches on group-housed adult female Japanese monkeys. Percept Mot Skills 87, 707-714.

Nash, R., Johnston, H., Robbins, A., and Descovich, K. (2021). The effect of enrichment filling and engagement time on regurgitation and reingestion behaviour in three zoo-housed orangutans. J Zool Bot Gard 2, 10-20. 

Neal Webb, S.J., Hau, J., and Schapiro, S.J. (2018). Captive chimpanzee (Pan troglodytes) behavior as a function of space per animal and enclosure type. Am J Primatol 80, e22749.

Pierre, P.J., Torres, N., Rosga, M. and Sullivan, J. (2020). Calories delivered by nonhuman primate foraging enrichment: Data and methods to inform decisions concerning the dietary consequences of enrichment. bioRxiv.

Pruetz, J.D. and Bloomsmith, M. (1992). Comparing two manipulable objects as enrichment for captive chimpanzees. Animal Welfare 11, 127-137.

Renner, M. J., Feiner, A.J., Orr, M.G., and Delaney, B.A. (2000). Environmental enrichment for New World primates: Introducing food-irrelevant objects and direct and secondary effects. J Applied Anim Welf Sci 3, 23-32.

Robins, J.G.,and Waitt, C.D. (2011). Improving the welfare of captive macaques (Macaca sp.) through the use of water as enrichment. J Appl Anim Welf Sci 14, 75-84.

Schapiro, S.J., Bloomsmith, M.A., Porter, L.M., and Suarez, S.A. (1996). Enrichment effects on rhesus monkeys successively housed singly, in pairs, and in groups. Appl Anim Behav Sci 48, 159-171.

Schapiro, S.J., Bloomsmith, M.A., Suarez, S.A., and Porter, L.M. (1996). Effects of social and inanimate enrichment on the behavior of yearling rhesus monkeys. Am J Primatol 40, 247-260.

Sha, J.C.M., Ismail, R., Marlena, D., and Lee, J.L. (2016). Environmental complexity and feeding enrichment can mitigate effects of space constraints in captive callitrichids. Lab Anim 50, 137-144.

Wooddell, L.J., Beisner, B., Hannibal, D.L., Nathman, A.C., and McCowan, B. (2019). Increased produce enrichment reduces trauma in socially‐housed captive rhesus macaques (Macaca mulatta). Am J Primatol 81, e23073

Weed, J.L., Baker, S.C., Harbaugh, S.W., and Erwin, J. (1995). Innovative enclosures for laboratory primate: Evaluation of a “breeding condominium.” Lab Animal24, 28-32.

Whittaker, M., Laule, G., Perlman, J., Schapiro, S., and Keeling, M. (2001). A behavioral management approach to caring for great apes. In “The Apes: Challenges for the 21st Century Conference Proceedings”, Brookfield Zoo.

Williams, L.E., Abee, C.R., Barnes, S.R., and Ricker, R.B. (1988). Cage design and configuration for an arboreal species of primate. Lab Anim Sci. 38, 289-291.

Foraging enrichment

Baker, K.C. and Springer, D.A. (2006). Frequency of feeding enrichment and response of laboratory nonhuman primates to unfamiliar people. J Am Assoc Lab Anim Sci, 45, 69-73.

Bayne, K. (1991). The reduction of abnormal behaviors in individually housed rhesus monkeys with a foraging/grooming board. Am J Primatol 23, 23-35.

Bayne, K., Dexter, S.L., and Strange, G.M. (1993). The effects of food treat provisioning and human interaction on the behavioral well-being of rhesus monkeys. Contemp Top Lab Anim Sci 32, 6-9.

Brent, L. and Eichberg, J.W. (1991). Primate puzzleboard: A simple environmental enrichment device for captive chimpanzees. Zoo Biology 10.4, 353-360.

Crockett, C.M., Bellanca, R.U., Heffernan, K.S., Ronan, D.A., and Bonn, W.F. (2001). Puzzle ball foraging device for laboratory monkeys. Lab Primate Newsl 40, 4-7.

Holmes, S.N., Riley, J.M., Juneau, P., Pyne, D., and Hofing, G.L. (1995). Short-term evaluation of a foraging device for non-human primates. Lab Anim (London) 29, 364-69

Lam, K., Rupniak, N.M., and Iversen, S.D. (1991). Use of a grooming and foraging substrate to reduce cage stereotypies in macaques. J Med Primatol 20, 104-109.

Lutz, C.K. and Farrow, R.A. (1996). Foraging device for singly housed longtailed macaques does not reduce stereotypies. Contemp Top Lab Anim Sci 35, 75-78.

Maloney, M.A., Meiers, S.T., White, J., and Romano, M.A. (2006). Effects of three food enrichment items on the behavior of black lemurs (Eulemur macaco macaco) and ringtail lemurs (Lemur catta) at the Henson Robinson Zoo, Springfield, Illinois. J Appl Anim Welf Sci 9, 111-127.

Pyle, D.A., Bennett, A.L., Zarcone, T.J., Turkkan, J.S., Adams, R.J., and Hienz, R.D. (2002). Use of two food foraging devices by singly housed baboons. Laboratory Primate Newsletter 35, 15-21.

Runeson, E.P., Lee, G.H., Crockett, C.M., and Bellanca, R.U. (2011). Evaluating paint rollers as an intervention for alopecia in laboratory monkeys, Macaca nemestrina. J Appl Anim Welf Sci, 14, 138-149.

Sensory Enrichment

Ablard, K.M. and Nekaris, K.A.I. (2008). Naturalizing the captive environment of slender lorises (Loris lydekkerianus nordicus) via olfactory enrichment. Primate Eye 96, 281.

Andrews, G. and Iliff, S.A. (2005). The use of olfactory stimulation as a means of environmental enhancement. Contemp Top Lab Anim Sci 44, 98.

Bloomsmith, M.A. and Lambeth, S.P. (2000). Videotapes as enrichment for captive chimpanzees (Pan troglodytes). Zoo Biol 19, 541-551.

Claxton, A.M. (2011) The potential of the human–animal relationship as an environmental enrichment for the welfare of zoo-housed animals. Applied Animal Behaviour Science 133, 1-10.

Harris, L.D., Briand, E.J., Orth, R., and Galbicka, G. (1999). Assessing the value of television as environmental enrichment for individually housed rhesus monkeys: a behavioral economic approach. J Am Assoc Lab Anim Sci 38, 48-53.

Howell, S., Schwandt, M., Fritz, J., Roeder, E., and Nelson, C. (2003). A stereo music system as environmental enrichment for captive chimpanzees. Lab Anim (NY) 32, 31-36.

McDermott, J. and Hauser, M.D. (2007). Nonhuman primates prefer slow tempos but dislike music overall. Cognition  104, 654-68.

Meade, T.M., Hutchinson, E., Krall, C., and Watson, J. (2014). Use of an aquarium as a novel enrichment item for singly housed rhsus macaques (Macaca mulatta). J Am Assoc Lab Anim Sci53, 472-477.

Ogura T. and Matsuzawa T. (2012). Video preference assessment and behavioral management of single-caged japanese macaques (Macaca fuscata) by movie presentation. J Appl Anim Welf Sci 15, 101-12.

Platt, D.M. and Novak, M.A. (1997). Videostimulation as enrichment for captive rhesus monkeys (Macaca mulatta). Appl Anim Behav Sci 52, 39-155.

Richardson, A.S., Lambeth, S.P., and Schapiro, S.J. (2006). Control over the auditory environment: a study of music preference in captive chimpanzees (Pan troglodytes). Int J Primatol 27, 423.

Snowdon, C.T. and Teie, D. (2010). Affective responses in tamarins elicited by species-specific music. Biology Letters 6, 30-32.

Wells, D.L. (2009). Sensory stimulation as environmental enrichment for captive animals: A review. Appl Anim Behav Sci 118, 1-11.

Occupational enrichment (does not include PRT)

Celli, M.L., Tomanaga, M., Udono, T., Teramoto, M., and Nagano, K. (2003). Tool use task as environmental enrichment for captive chimpanzees. Appl Anim Behav Sci 81, 171-182.

Griffis, C.M., Martin, A.L., Perlman, J.E., and Bloomsmith, M.A. (2013). Play caging benefits the behavior of singly housed laboratory rhesus macaques (Macaca mulatta). J Am Assoc Lab Anim Sci52, 34-40.

Fontenot, M.B., Wilkes, M.N., and Lynch, C.S. (2006) Effects of outdoor housing on self-injurious and stereotypic behavior in adult male rhesus macaques (Macaca mulatta). J Am Assoc Lab Anim Sci 45, 35-43.

Kessel, A.L. and Brent, L. (1995). An activity cage for baboons, part II: long-term effects and management issues. Contemp Top Lab Anim Sci 34, 80-3.

Kurtycz, L.M., Wagner, K.E., and Ross, S.R. (2014). The choice to access outdoor areas affects the behavior of great apes. J Appl An Welf Sci. 1-13.

Lincoln, H., Andrews, M.W., and Rosenblum, L.A. (1995). Pigtail macaque performance on a challenging joystick task has important implications for enrichment and anxiety within a captive environment. Lab Anim Sci 45, 264-248.

Storey, P.L., Turner, P.V., and Tremblay, J.L. (2000). Environmental enrichment for rhesus macaques: a cost-effective exercise cage. Contemp Top Lab Anim Sci 39, 14-16.

Tarou, L.R., Kuhar, C.W., Adcock, D., Bloomsmith, M.A., and Maple, T. L. (2004). Computer-assisted enrichment for zoo-housed orangutans (Pongo pygmaeus). Anim Welf 13, 445-453.

Wolff, A. and Rupert, G. (1991). A practical assessment of a nonhuman primate exercise program. Lab Anim 20, 36-39.

General

Baker, K.C., Weed, J.L., Crockett, C.M., and Bloomsmith, M A. (2007). Survey of environmental enhancement programs for laboratory primates. Am J Primatol 69, 377-394.

Barbosa, M.N. and da Silva Mota, M.T. (2009). Behavioral and hormonal response of common marmosets, Callithrix jacchus, to two environmental conditions. Primates 50, 253-260.

Bayne, K.A.L., Hurst, J.K., and Dexter, S.L. (1992). Evaluation of the preference to and behavioral effects of an enriched environment on male rhesus monkeys. Lab Anim Sci, 42, 38-45.

Bayne, K. and Würbel, H. (2014). The impact of environmental enrichment on the outcome variability and scientific validity of laboratory animal studies. Rev Sci Tech 33, 273-80.

Bloomsmith, M.A., Brent, L.Y., and Schapiro, S.J. (1991). Guidelines for developing and managing an environmental enrichment program for nonhuman primates. Lab Anim Sci 41, 372-377.

Bloomsmith, M.A. and Else, J.G. (2005). Behavioral management of chimpanzees in biomedical research facilities: the state of the science. ILAR J 46, 192-201.

Boinski, S., Swing, S.P., Gross, T.S., and Davis, J.K (1999). Environmental enrichment of brown capuchins (Cebus apella): behavioral and plasma and fecal cortisol measures of effectiveness. Am J Primatol 48, 49-68.

Bourgeois, S.R. and Brent, L. (2005). Modifying the behaviour of singly caged baboons: Evaluating the effectiveness of four enrichment techniques. Anim Welf 14, 71-81.

Buchanan-Smith, H.M. (2011). Environmental enrichment for primates in laboratories. Adv Sci Res 5, 41-56.

Carlstead, K. and Shepherdson, D. (1994). Effects of environmental enrichment on reproduction. Zoo Biol 13, 447-458.

Coleman, K. (2012). Individual differences in temperament and behavioral management practices for nonhuman primates. Appl Anim Behav Sci 137, 106-13.

Coleman, K., Bloomsmith, M.A., Crockett, C.M., Weed, J.L., and Schapiro, S.J. (2012). Behavioral management, enrichment and psychological well-being of laboratory nonhuman primates. In: Abee C.R., Mansfield K., Tardif S., and Morris T. (Eds). Nonhuman Primates in Biomedical Research. London, UK: Academic Press; pp. 149-76.

Crockett, C.M. (1990). Psychological well-being and enrichment workshop held at Primate Centers’ Directors’ meeting. Lab Prim Newsl 29, 3-6.

Desmond, T. (1994). Behavioral management: an integrated approach to animal care. AZA Conference, 19-22.

Fox, C., Merali,Z., and Harrison C. (2006). Therapeutic and protective effect of environmental enrichment against psychogenic and neurogenic stress. Behav Brain Res 175, 1-8.

Gluck, J.P., Harlow, H.F., and Schiltz, K.A. (1973). Differential effect of early enrichment and deprivation on learning in the rhesus monkey (Macaca mulatta). J Comp Physiol Psych 84, 598-604.

Honess, P. and Wolfensohn, S. (2010). The extended welfare assessment grid: a matrix for the assessment of welfare and cumulative suffering in experimental animals. Alternatives to :aboratory Animals: ATLA 38, 205-12.

Hosey, G.R. (2005). How does the zoo environment affect the behaviour of captive primates? Appl Anim Behav Sci 105, 107-129.

Huber, H.F. and Lewis, K.P. (2011). An assessment of gum-based environmental enrichment for captive gummivorous primates. Zoo Biol 30 71-78.

Hubrecht, R.C. (2010). Enrichment: animal welfare and experimental outcomes. In The UFAW Handbook on the Care and Management of Laboratory and Other Research Animals (Hubrecht, R. and Kirkwood, J., Eds.). pp. 137-146. Wiley-Blackwell, London

Jennings, M., Prescott, M.J., Buchanan-Smith, H.M., Gamble, M.R., Gore, M., Hawkins, P., Hubrecht, R., Hudson, S., Keeley, J.R., Morris, K., Morton, D.B., Owen, S., Pearce, P.C., Robb, D., Rumble, R. ., Wolfensohn, S., and Buist, D. (2009). Refinements in husbandry, care and common procedures for non-human primates: Ninth report of the BVAAWF/FRAME/RSPCA/UFAW Joint Working Group on Refinement. Lab Anim 43 Suppl 1, 1-47.

Keeling, M.E., Alford, P.L., and Bloomsmith, M.A. (1991). Decision analysis for developing programs of psychological well-being: A bias-for-action approach. In Through the Looking Glass (Novak, M.A. and Petto, A.J, Eds.), pp. 57-65. American Psychological Association, Washington, D.C.

Laule, G. (1993). The use of behavioral management techniques to reduce or eliminate abnormal behavior. Anim Wel4, 1-2 and 8-11.

Lutz, C.K. and Novak, M.A. (2005). Environmental enrichment for nonhuman primates: theory and application. ILAR J 46, 178-191.

Lutz, C.K., Well, A., and Novak, M. (2003). Stereotypic and self-injurious behavior in rhesus macaques: a survey and retrospective analysis of environment and early experience. Am J Primatol 60, 1-15.

Markowitz, H. (1975). Analysis and control of behavior in the zoo. Research in Zoos and Aquariums: A Symposium, 77-90.

Márquez-Arias, A., Santillan-Doherty, A.M., Arenas-Rosas, R.V., Gasca-Matias, M.P., and Munoz-Delgado, J. (2010). Environmental enrichment for captive stumptail macaques (Macaca arctoides). J Med Primatol 39, 32-40.

Newberry, R.C. (1995). Environmental enrichment: Increasing the biological relevance of captive environments. Appl Anim Behav Sci 44, 229-243.

Novak, M.A. (2003). Self-injurious behavior in rhesus monkeys: new insights into its etiology, physiology, and treatment. Am J Primatol 59, 3-19.

Novak, M.A. and Meyer, J.S. (2009). Alopecia: possible causes and treatments, particularly in captive nonhuman primates. Comp Med 59, 18-26.

Rawlins, J.M., Johnson, J.G., and Coleman, K. (2004). The effect of novelty on device use in female rhesus macaques. Contemp Top Lab Anim Sci 43, 96.

Schapiro, S.J. and Lambeth, S.P. (2007). Control, choice, and assessments of the value of behavioral management to nonhuman primates in captivity. J Appl Anim Welf Sci 10,39-47.

Shepherdson, D.J. (1998). Introduction: Tracing the path of environmental enrichment in zoos. In Second Nature: Environmental Enrichment for Captive Animals (Shepherdson, D., Mellen, J., and Hutchins, M., Eds.), pp. 1-12. Smithsonian Institution Press, Washington, D.C.

Schneider, M.L., Moore, C.F., Suomi, S.J., and Champoux, M. (1991) Laboratory assessment of temperament and emvironmental enrichment in rhesus monkey infants (Macaca mulatta). Am J Primatol 25, 137-55.

Tarou, L.R. and Bashaw, M.J. (2007). Maximizing the effectiveness of environmental enrichment: suggestions from the experimental analysis of behavior. Appl Anim Behav Sci102, 189-204.

Thom, J.P. and Crockett, C.M. (2008). Managing environmental enhancement plans for individual research projects at a national primate research center. J Am Assoc Lab Anim Sci 47, 51-57.

Weed, J.L. and Raber, J.M. (2005). Balancing animal research with animal well-being: establishment of goals and harmonization of approaches. ILAR J 46, 118-128.

Weed, J.L. and O’Neill-Wagner, P.L. (2006). Animal behavior research findings facilitate comprehensive captive animal care: The birth of behavioral management. Environmental enrichment for nonhuman primates resource guide: Animal Welfare Information Center.

Wemelsfelder, F., et al. Assessing the ‘whole animal’: a free choice profiling approach. (2001). Anim Behav 62, 209-220.

Wolfensohn, S., Sharpe, S., Hall, I., Lawrence, S., Kitchen, S., and Dennis, M. (2015). Refinement of welfare through development of a quantitative system for assessment of lifetime experience. Anim Welf 24, 139-149.

Wood, W. (1998). Interactions among environmental enrichment, viewing crowds, and zoo chimpanzees (Pan troglodytes). Zoo Biol 17, 211-230.