At the request of the National Institutes of Health (NIH) and in response to congressional inquiry, the Institute of Medicine (IOM) recently conducted an analysis of the scientific necessity of chimpanzees for NIH-funded biomedical and behavioral research. This IOM committee issued its report, entitled “Chimpanzees in Biomedical and Behavioral Research: Assessing the Necessity” ( available at http://www.nap.edu/catalog.php?record_id=13257) on December 15, 2011. The report establishes criteria to guide current and future research use of chimpanzees and suggests that an independent oversight committee be established that uses the recommended criteria. Dr. Francis Collins, Director of NIH, has indicated that he is accepting the IOM committee recommendations and he has formed a Working Group within the NIH Council of Councils to advise on the implementation of the IOM committee recommendations. This Working Group has requested input from the public.
The American Society of Primatologists (ASP) is a non-profit educational and scientific organization whose purpose is to encourage the discovery, exchange and dissemination of information regarding nonhuman primates, including their biology, care, and conservation. The Society is an exceedingly diverse organization, comprised of approximately 700 scientists and educators from the disciplines of anthropology, psychology, the biological and biomedical sciences, veterinary medicine and other academic endeavors. The common theme that provides continuity and unity for ASP is a strong professional interest in nonhuman primates. Dr. Fragaszy, ASP President, has asked ASP’s Primate Care Committee to provide a statement related to implementing the recommendations of the IOM committee. This statement is below.
Since ASP is an organization based on the science of understanding nonhuman primates, our comments will focus on relevant scientific studies of behavior and the professional opinions of those who have worked with, studied, and cared for chimpanzees. We focus our comments on three areas of the IOM committee recommendations: defining an ethologically appropriate physical environment, defining an ethologically appropriate social environment, and defining acquiescent chimpanzees. Our comments address the Working Group’s request for “Factors to consider in reviewing currently active NIH-supported research using chimpanzees to advise on which studies currently meet the principles and criteria defined by the IOM report ….”
As far as we can discern, the term “ethologically appropriate” that is used in the IOM Committee recommendations has not been used in other regulations or guidelines for the care of captive chimpanzees. This term needs to be operationally defined to allow adherence to the new standards set out by the IOM Committee. Since “ethology” refers to the scientific study of animal behavior, an ethologically appropriate environment is one that is suitable to the behavior of a particular animal.
Defining an Ethologically Appropriate Physical Environment for Chimpanzees
For this section of our comments, we will rely heavily on information presented in: (a) two articles written by scientists who study chimpanzees in the wild (Pruetz & McGrew, 2001; Wrangham,1992) and who commented on the needs of captive chimpanzees by comparing them to wild chimpanzees; (b) the Chimpanzee Care Manual (AZA Ape TAG, 2010) which includes guidelines and recommendations by experts in the zoo community of the United States regarding the care of chimpanzees; and (3) two articles that describe the current status of behavioral management programs for laboratory-housed chimpanzees (Bloomsmith & Else, 2005; Brent, 2001).
Based on our review of the scientific literature related to chimpanzees, there seems to be a convergence of thinking from scientists working with chimpanzees in laboratories, zoos, and in the field, on several major features of the physical environment needed by captive chimpanzees. We propose that the environmental features that are repeatedly mentioned as important by scientists in these various settings, are the ones that should be incorporated into every ethologically appropriate environment for captive chimpanzees. These environmental characteristics are ones that allow and encourage some of the most prominent behaviors of wild chimpanzees, and behaviors that take up the largest portion of their time (Pruetz & McGrew, 2001). Even though the behavior of wild chimpanzees varies among different sites in Africa, they do also share many behavioral patterns (Wrangham, McGrew, deWaal & Heltne, 1994). The behaviors that we are focusing on are those that are characteristic of all populations of wild chimpanzees. Chimpanzees are adapted to display these behaviors, so an ethologically appropriate environment is one that facilitates the expression of these natural behaviors. These major categories of behavior are foraging behavior, nesting behavior, traveling/climbing/brachiating, and problem-solving behavior.
1) Foraging behavior. Wild chimpanzees spend the largest portion of their waking hours feeding and foraging, so captive environments should allow for multiple opportunities each day to search for, process and acquire a wide variety of foods (Pruetz & McGrew, 2001; Bloomsmith & Else, 2005). In the wild, the proportion of time devoted to foraging varies from site to site, with a range of about 30% to 60% of their waking hours (Wrangham, 1977; Boesch & Boesch, 2000; Matsumoto-Oda et al., 1998). Wild chimpanzees eat a huge variety of food types and eat many times throughout the day (Badrian & Malenky, 1984; Kano & Mulavwa, 1984; Wrangham, 1977). The presentation of food in a variety of ways is an important form of environmental enrichment for captive chimpanzees. There is a good deal of evidence that these techniques increase foraging time, increase the diversity of natural behaviors expressed, and decrease aggression and abnormal behavior in captive chimpanzees (Bloomsmith et al,. 1988; Maki et al., 1989; Nash, 1982). For these reasons, a physical environment that allows effective feeding enrichment is recommended for laboratory-housed (Bloomsmith & Else, 2005) and for zoo-housed chimpanzees (AZA Ape TAG, 2010), and should be a part of any ethologically appropriate environment.
2) Nesting behavior. Wild chimpanzees build nests made from branches and leaves, and spend about 12 of every 24 hours in those nests, including sleeping in the nests at night, and resting in them during the day (Furth & McGrew, 1998; Hiraiwa-Hasegawa, 1989). These nests are normally occupied for a single night, but occasionally are reused by the animals. Nests are usually constructed well off the ground at a height of 30-40 feet. Since wild chimpanzees spend half of their time in nests, this should be viewed as an important component of chimpanzee environments (Pruetz & McGrew, 2001). Captive environments should include elevated platforms or other comfortable, stable spaces for nesting (Coe et al., 2001). In addition, appropriate soft, flexible and safe materials (e.g., browse, hay, excelsior, blankets, branches) should be provided daily for chimpanzees to build nests.
3) Traveling, climbing and brachiating. Wild chimpanzees spend about 10-20% of their waking time traveling (Boesch & Boesch, 2000; Ghiglieri, 1985; Wrangham, 1977). They walk or run for about 1.5 hours daily, and climb five to ten trees per day, and this is the case across all studied chimpanzee populations (Wrangham, 1992). Most of this time is traveling is on the ground, with some time climbing and brachiating (van Lawick-Goodall, 1968). Therefore, ethologically appropriate environments for chimpanzees should allow traveling, climbing, and brachiating. Captive chimpanzees preferentially spend time in high spaces available to them (Goff et al., 1994; Ross & Lukas, 2006; Ross et al., 2011; Traylor-Holtzer & Fritz, 1985). We recommend that chimpanzees have the opportunity to climb to a height of at least 20 feet, consistent with the recommendation in the Chimpanzee Care Manual (AZA Ape TAG, 2010).
Studies have shown that the complexity and quality of space in which primates live is a more important predictor of activity than the amount of space available to them (Wilson, 1982; Joint Working Group on Refinement for Nonhuman Primates, 2009). In other words, providing larger enclosures that do not function well to facilitate species-typical use of the space do not necessarily improve behavioral indicators of welfare. It is important that the physical environments for chimpanzees provide areas for refuge with visual barriers from conspecifics, escape routes to avoid other chimpanzees, climbing structures for travel and movement, variety in substrates (e.g., dirt, grass, sand, deep mulch, straw) and other features that function to increase species-typical behavior and reduce abnormal behaviors (Baker, 1997; Brent, 1992; Caws, Wehnelt & Aureli, 2008; Pruetz & McGrew, 2001; Ross et al., 2009). In addition, although it has not been well-studied, access to the outdoors is probably a very effective form of enrichment (Baker & Ross, 1998), and should be provided to captive chimpanzees at least the majority of the year (AZA Ape TAG, 2010). It is important to recognize that chimpanzees show an ability to adjust to reduced available space by making compensatory changes in social behavior (e.g., increased grooming), and do not show evidence of distress in more socially crowded conditions (Nieuwenjuijsen & de Waal, 1982; Videan and Fritz, 2007). If physical environments are smaller, it is possible to compensate for this lack of space by increasing the functionality and complexity of the environment through such features.
4) Problem-solving behaviors. Chimpanzees are well-known for their intelligence and cognitive flexibility, and captive environments should allow them to use these abilities. One of the best-studied ways in which chimpanzees solve problems is through using tools. Chimpanzee tool traditions include using many objects such as moss, leaves, twigs, sticks, logs and rocks in various ways to serve as sponges, wipes, containers, lures, whisks, hooks, hole enlargers, missiles, clubs, and hammers (Wrangham, 1992). Chimpanzees commonly use tools to acquire food, such as the well-known use of sticks to “fish” for termites, or using rocks to open nuts with sturdy outer coverings (Biro, Sousa & Matsuzawa, 2006). All populations of wild chimpanzees studied use tools in some form or fashion (Wrangham, 1992), so ethologically appropriate environments for captive chimpanzees should encourage the use of tools and other means of solving problems. Offering such challenges to the chimpanzees which they can volunteer to solve can also involve the use of technology such as computers (Parr et al., 2009; Bloomsmith et al., 2001), exchange tasks with humans (Brosnan & deWaal, 2005), or teaching chimpanzees through positive reinforcement training methods (Perlman et al., 2010).
Defining an Ethologically Appropriate Social Environment for Chimpanzees
1) Experts in chimpanzee behavior who study chimpanzees in the field, zoo and laboratory environments agree that social housing is the foundation for captive chimpanzee welfare (Pruetz & McGrew, 2001; Wrangham, 1992; AZA Ape TAG, 2010; Bloomsmith & Else, 2005; Brent, 2001). An ethologically appropriate environment must support the social needs of captive chimpanzees and include conspecific social partners. Social behavior is also a time-consuming part of wild chimpanzees’ activity, with about 10% of their waking time spent interacting socially (Pruetz & McGrew, 2001). Chimpanzees housed without contact with companions show high levels of anxiety and aggression (Baker, 1996). A few weeks of single housing may result in increases in abnormal behavior, detectable in the first week after removal from social groups (Brent et al., 1989). Chimpanzees should not be housed alone for any extended period of time unless it is deemed to be necessary for their physical or psychological well-being, following the recommendation for chimpanzees AZA-accredited zoos (AZA Ape TAG, 2010).
2) Since chimpanzees are well-known for the complexity of their social interactions and for multi-animal interactions (e.g., alliances, consolation), we propose a minimum group size of three chimpanzees, to allow such interactions. Chimpanzees in the wild often travel in small “parties” of three to eight individuals (AZA Ape TAG, 2010, Boesch, 1996), so this proposed minimum group size is similar to a small chimpanzee traveling party. A minimum group size of three has the added benefit that if a group member dies or must be removed from the group, no chimpanzee is left living alone as a result. Plans for managing small groups of chimpanzees should be in place to minimize any periods of living in undersized groups.
3) We recommend group sizes larger than three, as larger groups more closely approximate the size of wild chimpanzee communities. It is also preferable for groups to contain multiple adult members of both sexes. Relatively large groups housed in appropriately complex environments can model the fission/fusion nature of wild chimpanzee groups in which there are fluid and shifting associations of individuals within a large community (Goodall, 1986), and fulfill the Pruetz & McGrew (2001) recommendation that captive chimpanzees have the opportunity to interact with a wide range of social partners. Multiple adult male group members are particularly desirable, given the intense relationships among adult males both in the wild and in captivity (AZA Ape TAG, 2010; Boesch & Boesch, 2000; Fitch et al., 1989; Kawanaka, 1990; Wrangham, 1992). Multi-male, mixed-sex groups stimulate a wider variety of species-appropriate behaviors than what is observed in groups containing only one adult male. It is also preferable for chimpanzee groups to contain immature members of varying ages. However, with the current status of the laboratory chimpanzee population in which little reproduction is allowed, it will not be possible for most chimpanzees to live in species-typical groups that contain immature members. These recommendations for larger group sizes, multiple adult male membership, and age-graded groups are consistent with the recommended group compositions in AZA-accredited zoos (AZA Ape TAG, 2010).
4) Any research that requires extensive periods of single housing cannot be deemed acceptable under the criteria of ethologically appropriate social environments. A more difficult question is whether brief periods of single housing might be allowable. For example, the IOM Committee report endorsed the value of neuroimaging studies with chimpanzees, but some of these studies (e.g., PET imaging) involve a period of approximately 18- 24 hours of single housing following the administration of a radioactive ligand to the subject of the imaging (this protects other chimpanzees from being exposed to the radioactivity in the subject’s feces or urine). Since social interactions are the foundation of chimpanzee welfare, research that requires single housing must be extremely well-justified, and the periods of single housing must be minimized. We propose that occasional periods of single housing of up to 24-hours each in duration, no more than four times per year, may be deemed acceptable for research purposes if the single housing is extremely well justified. This proposal is based on practical experience in managing chimpanzees and a review of the literature concerning responses to brief separation from peers (Hennessy, 1997). Chimpanzees are occasionally removed from their social groups for health care purposes (e.g., treatment of a wound or illness), and they are typically separated from their group members for hours following routine physical examinations that require anesthesia. While chimpanzees certainly do respond to these separations, and are likely experiencing some stress, they do not appear to suffer prolonged distress due to these social separations, and generally can be successfully reintroduced to their social groups without incident. Since management of chimpanzees occasionally requires this same procedure, we feel it can reasonably be done for research purposes, if four times or less per year.
5) Requiring housing with conspecifics during research periods has implications for studies of infectious diseases using chimpanzees (e.g., hepatitis). Additional chimpanzees will be exposed to infectious agents through their social partners and could become infected themselves. This could impact the health of those chimpanzees, as well as their future research value. The use of social housing in infectious disease research leads to the quandary of balancing the needs for animal welfare, with adhering to the principles of the 3Rs (e.g., to reduce the number of animals used in research). With a relatively small population of laboratory chimpanzees available for research, these issues are especially pronounced.
Defining “Acquiescent Chimpanzees”
Chimpanzees can be trained using positive reinforcement techniques to cooperate with a variety of husbandry, veterinary and research procedures (Bloomsmith et al., 1998; Bloomsmith et al., 2006; Coleman et al., 2008; Laule et al., 1996; Laule et al., 2003). This type of training has become increasingly common with captive chimpanzees in laboratory, sanctuary and zoo settings over the last 20 years. Positive reinforcement training relies on the voluntary participation of the chimpanzees—there is no consequence to them if they decide to not participate, other than the failure to earn additional rewards. During positive reinforcement training, the animal receives a reward such as food for offering a particular behavior. For example, if the desired behavior is for the animal to move to the front of the cage, when he moves to this location, he receives a food reward (Perlman et al., 2010). We propose that positive reinforcement training is the optimal methodology to achieve acquiescence with research procedures.
1) This type of training is already being integrated into the care of captive chimpanzees. In the laboratory environment, the Office of Laboratory Animal Welfare reported on their review of chimpanzee facilities (OLAW Report, 2010), and concluded that, “In situations where it is safe and feasible, chimpanzees and other nonhuman primates should be given positive reinforcement training to perform desired cooperative activities. This type of training may also aid in reducing stress from capture and restraint and the need for chemical darts.” In AZA-accredited zoos, staff working with chimpanzees are expected to use conditioning techniques to facilitate husbandry procedures and behavioral research investigations (AZA Ape TAG, 2010), and many zoos have successful positive reinforcement training programs.
2) Both practical experience and some published studies indicate that positive reinforcement training reduces distress experienced by chimpanzees (Lambeth et al., 2006; Pomerantz & Terkel, 2009), so this approach is consistent with the intention of the IOM Committee recommendations. Additional support for the value of positive reinforcement training in reducing indicators of stress has been demonstrated for numerous other species, including hamadryas baboons (O’Brien et al., 2008), rhesus macaques (Clay et al., 2009) and horses (Innes & McBride, 2008; Warren-Smith & McGreevy, 2007). Positive reinforcement can increase motivation for animals to participate in training procedures (Innes & McBride, 2008). Practical experience with training chimpanzees at multiple research facilities indicates that they can be trained on a wide variety of research procedures (Perlman et al., 2010). Female chimpanzees have been trained for urine collection to allow hormonal assessments of their reproductive cycle (Herndon et al., in press) which is important for some studies of cognition. Chimpanzees have been trained for voluntary blood collection (Coleman et al., 2008) and used for studies involving pharmacokinetics. Many chimpanzees have been trained to voluntarily present for injections, including sedatives. This training supports a wide range of research studies, including neuroimaging studies which the IOM Committee recommends continuing under appropriate circumstances. Positive reinforcement training so that chimpanzees will readily move to testing areas, or to voluntarily separate from social partners for brief testing periods, has been important in supporting studies of cognition and emotion, as well as neuroimaging studies (Russell et al., 2006; Taglialatela et al., 2009; 2011).
3) To train chimpanzees who are acquiescent, we propose that the training methods should follow these criteria:
4) It will be important for research staff and others working with chimpanzees to be competent in training terminology and methods so that they can effectively follow these guidelines. They will also need to be competent in identifying chimpanzee behaviors so that they can discern when chimpanzees are exhibiting fearful, abnormal, stress-related or avoidance behaviors (all evidence of a lack of acquiescence) during training and research sessions. There are many resources available for staff members to learn this information such as books, published articles, workshops and websites (see Perlman et al., 2012).
5) Requiring research procedures to be conducted with acquiescent chimpanzees may place practical limits on the frequency of certain research procedures, and will increase the cost of conducting chimpanzee research. For example, the onset of a project could be delayed in order to successfully train potential subjects for cooperation with research procedures. If a research project includes the collection of blood samples, there will be some limit on how frequently chimpanzees will cooperate with this procedure. These limits will vary among individual chimpanzees, so it may be difficult for investigators to predict how frequently they will be able to collect samples or conduct procedures in a similar fashion across many subjects. In addition, chimpanzees will need to be assigned to studies for longer periods of time, to allow the training to be accomplished. Additional training will be required during the course of research studies when chimpanzees “regress” in their performance of tasks (e.g., following injection and sedation, they may fail to cooperate with a subsequent injection procedure). Additionally, the cost of trainers and training supplies will need to be included in research grant budgets, further increasing the cost of conducting chimpanzee research.
AZA Ape TAG 2010. Chimpanzee (Pan troglodytes) Care Manual. Association of Zoos and Aquariums, Silver Spring, MD.
Badrian, N. & Malenky, R.K. (1984). Feeding ecology of Pan paniscus in the Lomako Forest, Zaire. The Pygmy Chimpanzee. Evolutionary Biology and behavior. R. L. Susman, Editors. New York: Plenum Press. 275-299.
Baker, K.C. (1996). Chimpanzees in single cages and small social groups: Effects of housing on behavior. Contemporary Topics in Laboratory Animal Science. 35(3), 71-74.
Baker, K.C. (1997). Human interaction as enrichment for captive chimpanzees. A preliminary report. [Abstract] American Journal of Primatology. 42(2), 92.
Baker, K.C. & Ross, S.K. (1998). Outdoor access: The behavioral benefits to chimpanzees. [Abstract] American Journal of Primatology. 45(2), 166.
Biro, D., Sousa, C., & Matsuzawa, T. (2006). Ontogeny and cultural propagation of tool use by wild chimpanzees at Bossou, Guinea: case studies in nut cracking and leaf folding. Cognitive Development in Chimpanzees. Matsuzawa T. Tomonaga M. Tanaka M. Editors. New York: Springer. 476-508.
Bloomsmith, M.A., Alford, P.L ., & Maple, T.L. (1988). Successful feeding enrichment for captive chimpanzees. American Journal of Primatology. 16(2), 155-164.
Bloomsmith, M.A., Baker, K.C., Lambeth, S.P., Ross, S.K., & Schapiro, S.J. (2001). Is giving chimpanzees control over environmental enrichment a good idea? The Apes: Challenges for the 21st Century. Conference Proceedings. Brookfield: Brookfield Zoo. 88-89.
Bloomsmith, M.A. & Else, J.G. (2005). Behavioral management of chimpanzees in biomedical research facilities: the state of the science. ILAR Journal. 46(2), 192-201.
Bloomsmith, M.A., Schapiro, S.J., & Strobert, E.A. (2006). Preparing chimpanzees for laboratory research. ILAR Journal. 47(4), 316-325.
Bloomsmith, M.A., Stone, A.M., & Laule, G.E. (1998). Positive reinforcement training to enhance the voluntary movement of group-housed chimpanzees within their enclosures. Zoo Biology. 17, 333-341.
Boesch, C. (1996). Social grouping in Tai chimpanzees. Great Ape Societies. W.C. McGrew L.F. Marchant T. Nishida, Editors. Cambridge: Cambridge University Press. 101-113.
Boesch, C. & Boesch-Achermann, H. (2000). The chimpanzees of the Tai forest: Behavioral Ecology and Evolution. New York: Oxford University Press. viii, 316.
Brent, L. (1992). Woodchip bedding as enrichment for captive chimpanzees in an outdoor enclosure. Animal Welfare. 1,161-170.Brent, L. (2001). The influence of rearing condition on chimpanzee introductions. The Apes: Challenges for the 21st Century. Conference Proceedings. Brookfield: Brookfield Zoo. 103-104.
Brent, L., Lee, D.R., & Eichberg, J.W. (1989). The effects of single caging on chimpanzee behavior. Laboratory Animal Science. 39(4), 345-346.
Brosnan, S.F. & de Waal, F.B.M. (2005). Responses to a simple barter task in chimpanzees, (Pan troglodytes). Primates. 46(3) 173-182.
Caws, C.E., Wehnelt, S., & Aureli, F. (2008). The effect of a new vertical structure in mitigating aggressive behaviour in a large group of chimpanzees (Pan troglodytes). Animal Welfare. 17(2), 149-154.
Clay, A.W., Bloomsmith, M.A ., Marr, M.J., & Maple, T.L. (2009). Habituation and desensitization as methods for reducing fearful behavior in singly housed rhesus macaques. American Journal of Primatology. 71(1), 30-39.
Coe, J.C., Fulk, R., & Brent, L. (2001). Chimpanzee facility design. Care and Management of Captive Chimpanzees. Brent L, Editors. San Antonio: American Society of Primatologists. 39-81.
Coleman, K., Pranger, L., Maier, A., Lambeth, S.P., Perlman, J.P, Thiele, E., & Schapiro, S.J. (2008). Training rhesus macaques for venipuncture using positive reinforcement techniques: A comparison with chimpanzees. Journal of the American Association for Laboratory Animal Science. 47(1), 37-41.
Fitch, A.L., Merhalski, J.J., & Bloomsmith, M.A. (1989). Social housing for captive adult male chimpanzees: Comparing single-male and multi-male social groups. American Journal of Primatology. Supplement, 1, 87-91.
Fruth, B. & McGrew, W.C. (1998). Resting and nesting in primates: Behavioral ecology of inactivity. American Journal of Primatology. 46(1), 3-5.
Ghiglieri, M.P. (1985). The social ecology of chimpanzees. Scientific American. 252(6), 102-104, 109-113.
Goff, C., Howell, S.M., Fritz, J., & Nankivell, B. (1994). Space use and proximity of captive chimpanzee mother/offspring pairs. Zoo Biology. 13, 61-68.
Goodall, J. (1986). The Chimpanzees of Gombe Patterns of Behavior. Cambridge: Harvard University Press. xii, 673.
Hennessy, M.B. (1997). Hypothalamic-pituitary-adrenal responses to brief social separation. Neuroscience and Biobehavioral Reviews 21: 11-29.
Herndon, J.G., Paredes, J., Wilson, M.E., Bloomsmith, M.A., Chennareddi, L.C., & Walker, M. (in press). Endocrine confirmation of cyclic ovulation in the aged chimpanzee (Pan troglodytes). Age.
Hiraiwa-Hasegawa, M. (1989). Sex differences in the behavioral development of chimpanzees at Mahale. Understanding Chimpanzees. P.G. Heltne L.A. Marquardt, Editors. Cambridge, Massachusetts: Harvard University Press. 104-115.
Innes, L., & McBride, S. (2008). Negative versus positive reinforcement: An evaluation of training strategies for rehabilitated horses. Applied Animal Behaviour Science, 112, 357 – 368.
Joint Working Group on Refinement. (2009). Refinements in husbandry, care and common procedures for non-human primates: ninth report of the BVAAWF/FRAME/RSPCS/UFAW Joint Working Group on Refinement. Lab Animal 43:S1:1-S1:47.
Kano, T. & Mulavwa, M. (1984). Feeding ecology of the pygmy chimpanzees (Pan paniscus) of Wamba. The Pygmy Chimpanzee. Evolutionary Biology and Behavior. R. L. Susman, Editors. New York: Plenum Press. 233-274.
Kawanaka, K. (1990). Age differences in ant-eating by adult and adolescent males. The Chimpanzees of the Mahale Mountains. Sexual and Life History Strategies. T. Nishida, Editors. Tokyo: University of Tokyo Press. 207-222.
Lambeth, S.P., Hau, J., Perlman, J.E., Martino, M., & Schapiro, S.J. (2006). Positive reinforcement training affects hematologic and serum chemistry values in captive chimpanzees (Pan troglodytes). American Journal of Primatology. 68(3), 245-256.
Laule, G.E., Bloomsmith, M.A., & Schapiro, S.J. (2003). The use of positive reinforcement training techniques to enhance the care, management, and welfare of primates in the laboratory. Journal of Applied Animal Welfare Science, 6(3), 163-174.
Laule, G.E., Thurston, R.H., Alford, P.L., & Bloomsmith, M.A. (1996). Training to reliably obtain blood and urine samples from a young diabetic chimpanzee (Pan troglodytes). Zoo Biology. 15, 587-591.
Maki, S., Alford, P.L., Bloomsmith, M.A., & Franklin, J. (1989). Food puzzle device simulating termite fishing for captive chimpanzees (Pan troglodytes). American Journal of Primatology. (Suppl. 1), 71-78.
Matsumoto-Oda, A., Hosaka, K., Huffman, M.A., & Kawanaka, K. (1998). Factors affecting party size in chimpanzees of the Mahale mountains. International Journal of Primatology. 19(6), 999-1011.
Nash, V.J. (1982). Tool use by captive chimpanzees at an artificial termite mound. Zoo Biology. 1(3), 211-221.
O’Brien, J.K., Heffernan, S., Thomson, P.C., & McGreevy, P.D. (2008). Effect of positive reinforcement training on physiological and behavioural stress responses in the hamadryas baboon (Papio hamadryas). Animal Welfare. 17(2), 125-138.
Parr, L.A., Hecht, E., Barks, S.K., Preuss, T.M., & Votaw, J.R. (2009). Face processing in the chimpanzee brain. Current Biology. 19(1), 50-53.
Perlman, J.E., Bloomsmith, M.A., Whittaker, M.A., McMillan, J.L., Minier, D.E., & McCowan, B. (in press). Implementing positive reinforcement animal training programs at primate laboratories. Applied Animal Behaviour Science.
Perlman, J., Horner, V., Bloomsmith, M., Lambeth, S., & Schapiro, S. (2010). Positive reinforcement training: Social learning, and chimpanzee welfare. The chimpanzee mind (pp. 320-331). Chicago, IL: The University of Chicago Press.
Pomerantz, O. & Terkel, J. (2009). Effects of positive reinforcement training techniques on the psychological welfare of zoo-housed chimpanzees (Pan troglodytes). American Journal of Primatology. 71(8), 687-695.
Pruetz, J.D.E. & McGrew, W.C. (2001). What does a chimpanzee need? Using natural behavior to guide the care and management of captive populations. Care and Management of Captive Chimpanzees. Brent, L., Editor. San Antonio: American Society of Primatologists. 17-37.
Report to Office of Extramural Research Acting Director on Office of Laboratory Animal Welfare (OLAW) Site Visits to Chimpanzee Facilities (2010). Report available at: http://grants.nih.gov/grants/olaw/Report_on_OLAW_Visits_to_Chimpanzee_Facilities.pdf
Ross, S.R., Calcutt, S., Schapiro, S.J. & Hau, J. (2011b). Space use selectivity by great apes in an indoor-outdoor enclosure. American Journal of Primatology. 73, 197-208.Ross, S.R. & Lukas, K.E. (2006). Use of space in a non-naturalistic environment by chimpanzees (Pan troglodytes) and lowland gorillas (Gorilla gorilla gorilla). Applied Animal Behaviour Science. 96, 143-152.
Ross, S.R., Schapiro, S.J., Hau, J., & Lukas, K.E. (2009). Space use as an indicator of enclosure appropriateness: a novel measure of captive animal welfare. Applied Animal Behaviour Science. 121(1), 42-50.
Russell, J.L., Taglialatela, J.P., & Hopkins, W.D. (2006). The use of positive reinforcement training in chimpanzees (Pan troglodytes) for voluntary presentation for IM injections. American Journal of Primatology, 68(1), 122.
Taglialatela, J.P., Russell, J.L., Schaeffer, J.A., & Hopkins, W.D. (2009). Visualizing vocal perception in the chimpanzee brain. Cerebral Cortex. 19, 1151-1157.
Taglialatela, J.P., Russell, J.L., Schaeffer, J.A., & Hopkins, W.D. (2011). Chimpanzee vocal signaling points to a multimodal origin of human language. Plos One. 6(4) e18852.
Traylor-Holzer, K . & Fritz, P. (1985). Utilization of space by adult and juvenile groups of captive chimpanzees (Pan troglodytes). Zoo Biology. 4(2), 115-127.
van Lawick-Goodall, J. (1968). The behaviour of free-living chimpanzees in the Gombe Stream Reserve. Animal Behaviour Monographs. 1, 165-311.
Videan, E.N. & Fritz, J. (2007). Effects of short- and long-term changes in spatial density on the social behavior of captive chimpanzees. Applied Animal Behaviour Science. 102, 95-105.
Warren-Smith, A.K. & McGreevy, P.D. (2007). The use of blended positive and negative reinforcement in shaping the halt response of horses (Equus caballus) Animal Welfare. 16(4), 481-488.
Wrangham, R.W. (1977). Feeding behaviour of chimpanzees in Gombe National Park, Tanzania. Primate Ecology: Studies of feeding and ranging behavior in Lemurs, Monkeys, and Apes. T. H. Clutton-Brock, Editors. New York: Academic Press. 503-538.
Wrangham, R.W. (1992). Living naturally: Aspects of wild environments relevant to captive chimpanzee management. Chimpanzee Conservation and Public Healthy: Environments for the Future. J. Erwin J.C. Landon, Editors. Rockville: Diagnon/Bioqual. 71-81
Wrangham, R.W., McGrew, W.C., de Waal, F.B.M., & Heltne, P.G. eds (1994). Chimpanzee Cultures. Cambridge, MA: Harvard University Press. xxiii, 424.