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Refinements to captive chimpanzee (Pan troglodytes) care: a selfmedication paradigm

Published online by Cambridge University Press:  01 January 2023

SJ Neal Webb ,
J Hau  and
SJ Schapiro
SJ Neal Webb*
Affiliation:
The University of Texas MD Anderson Cancer Center, Michale E Keeling Center for Comparative Medicine and Research, 650 Cool Water Drive, Bastrop, TX 78602, USA Department of Experimental Medicine, University of Copenhagen, Faculty of Health Sciences and University Hospital, 3B Blegdamsvej, DK-2200 Copenhagen, Denmark
J Hau
Affiliation:
Department of Experimental Medicine, University of Copenhagen, Faculty of Health Sciences and University Hospital, 3B Blegdamsvej, DK-2200 Copenhagen, Denmark
SJ Schapiro
Affiliation:
The University of Texas MD Anderson Cancer Center, Michale E Keeling Center for Comparative Medicine and Research, 650 Cool Water Drive, Bastrop, TX 78602, USA Department of Experimental Medicine, University of Copenhagen, Faculty of Health Sciences and University Hospital, 3B Blegdamsvej, DK-2200 Copenhagen, Denmark
*
∗ Contact for correspondence and requests for reprints: sjneal@mdanderson.org
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Abstract

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In an effort to enhance welfare, behavioural management continually refines methods of non-human primate (NHP) care. Chimpanzees (Pan troglodytes) are one of the most cognitively complex captive NHPs and they have been observed to self-medicate in the wild. The population of captive chimpanzees in the US is aged (due to a breeding moratorium instituted in 1998) and will progressively require more medical care as they get older. To functionally simulate natural self-medication behaviour, provide chimpanzees with the opportunity to voluntarily participate in their own healthcare, and open new avenues of communication between caregivers and chimpanzees, we used a medication choice paradigm that allowed chimpanzees to choose their daily arthritis medication. We provided four arthritic, mobility-impaired chimpanzees with meloxicam or ibuprofen in blue or green Gatorade® to establish associations between the coloured drinks and the effects of the medications. We subsequently gave each chimpanzee a choice between the two medications. Behaviour was recorded using 15-min focal animal observations. Mobility was assessed using interactive mobility tests and a caregiver-rating system. One chimpanzee showed a medication preference (ibuprofen over meloxicam). The chimpanzees exhibited no significant behavioural or mobility differences over time, suggesting that ibuprofen and meloxicam may not differ significantly in their ability to alleviate arthritic symptoms. Whether or not the chimpanzees show a medication preference, the opportunity to make meaningful choices and the functional simulation of a complex behaviour, self-medication, is present when using this medication choice technique. Furthermore, the paradigm itself could have potential applications for additional medication options and treatment regimens.

Keywords

animal welfarebehavioural managementcaptivitychimpanzeeschoicevoluntary participation
Type
Articles
Information
Animal Welfare , Volume 27 , Issue 4 , November 2018 , pp. 327 - 341
Copyright
© 2018 Universities Federation for Animal Welfare

References

Albert, KS and Gernaat, CM 1984 Pharmacokinetics of ibupro-fen. American Journal of Medicine 77: 40–46. https://doi.org/10.1016/S0002-9343(84)80017-0Google Scholar
Altmann, J 1974 Observational study of behavior: Sampling methods. Behaviour 49: 227–267. https://doi.org/10.1163/156853974X00534CrossRefGoogle ScholarPubMed
Association of Zoos and Aquariums (AZA) Ape TAG 2010 Chimpanzee (Pan troglodytes) Care Manual. Association of Zoos and Aquariums: Silver Spring, Maryland, USAGoogle Scholar
Bae, JW, Kim, MJ, Jang, CG and Lee, SY 2007 Determination of meloxicam in human plasma using a HPLC method with UV detection and its application to a pharmacokinetic study. Journal of Chromatography, B, Analytical Technologies in the Biomedical and Life Sciences 859: 69–73. https://doi.org/10.1016/j.jchromb.2007.09.004CrossRefGoogle ScholarPubMed
Baker, KC 2004 Benefits of positive human interaction for social-ly-housed chimpanzees. Animal Welfare 13: 239–245.Google ScholarPubMed
Baker, KC 2016 Survey of 2014 behavioral management programs for laboratory primates in the United States. American Journal of Primatology 78: 780–796. https://doi.org/10.1002/ajp.22543CrossRefGoogle ScholarPubMed
Baker, KC and Aureli, F 1997 Behavioural indicators of anxiety: An empirical test in chimpanzees. Behaviour 134: 1031–1050. https://doi.org/10.1163/156853997X00386CrossRefGoogle Scholar
Baker, KC, Bloomsmith, MA, Coleman, K, Crockett, CM, Worlein, J, Lutz, CK, McCowan, B, Pierre, P and Weed, J 2017 The behavioral management consortium: A partnership for promoting consensus and best practices. In: Schapiro, SJ (ed) Handbook of Primate Behavioral Management pp 9–23. CRC Press: Boca Raton, Florida, USA. https://doi.org/10.1201/9781315120652-3CrossRefGoogle Scholar
Baker, KC, Weed, JL, Crockett, CM and Bloomsmith, MA 2007 Survey of environmental enhancement programs for labora-tory primates. American Journal of Primatology 69: 377–394. https://doi.org/10.1002/ajp.20347CrossRefGoogle Scholar
Behringer, V, Stevens, JMG, Hohmann, G, Möstl, E, Selzer, D and Deschner, T 2014 Testing the effect of medical positive rein-forcement training on salivary cortisol levels in bonobos and orang-utans. PLoS ONE 9: 1–9. https://doi.org/10.1371/journal.pone.0108664Google Scholar
Bloomsmith, MA, Laule, GE, Alford, PL and Thurston, RH 1994 Using training to moderate chimpanzee aggression during feeding. Zoo Biology 13: 557–566. https://doi.org/10.1002/zoo.1430130605Google Scholar
Bloomsmith, MA, Stone, AM and Laule, GE 1998 Positive rein-forcement training to enhance the voluntary movement of group-housed chimpanzees within their enclosures. Zoo Biology 17: 333–341. https://doi.org/10.1002/(SICI)1098-2361(1998)17:4<333::AID-ZOO6>3.0.CO;2-A3.0.CO;2-A>CrossRefGoogle Scholar
Boelsterli, UA, Redinbo, MR and Saitta, KS 2013 Multiple NSAID-induced hits injure the small intestine: underlying mecha-nisms and novel strategies. Toxicological Sciences 131: 654–667. https://doi.org/10.1093/toxsci/kfs310Google Scholar
Bridges, JP, Haller, RL, Buchl, SJ, Magden, ER, Lambeth, SP and Schapiro, SJ 2015 Establishing a behavioral manage-ment program for geriatric chimpanzees. American Journal of Primatology 77: 111Google Scholar
Capitanio, JP 2017 Variation in biobehavioral organization. In: Schapiro, SJ (ed) Handbook of Primate Behavioral Management pp 55–73. CRC Press: Boca Raton, Florida, USA. https://doi.org/10.1201/9781315120652-6CrossRefGoogle Scholar
Coleman, K, Pranger, L, Maier, A, Lambeth, SP, Perlman, JE, Thiele, E and Schapiro, SJ 2008 Training rhesus macaques for venipuncture using positive reinforcement techniques: A com-parison with chimpanzees. Journal of the American Association for Laboratory Animal Science 47: 37–41Google Scholar
de Roode, JC, Lefèvre, T and Hunter, MD 2013 Self-medication in animals. Science 340: 150–151. https://doi.org/10.1126/sci-ence.1235824CrossRefGoogle ScholarPubMed
Desmond, T and Laule, G 1994 Use of positive reinforcement training in the management of species. Zoo Biology 13: 471–477. https://doi.org/10.1002/zoo.1430130509CrossRefGoogle Scholar
Fowler, A, Koutsioni, Y and Sommer, V 2007 Leaf-swallowing in Nigerian chimpanzees: Evidence for assumed self-medication. Primates 48: 73–76. https://doi.org/10.1007/s10329-006-0001-6CrossRefGoogle ScholarPubMed
Friend, TH 1991 Symposium: Response of animals to stress. Journal of Dairy Science 74: 292–303. https://doi.org/10.3168/jds.S0022-0302(91)78173-3CrossRefGoogle Scholar
Fruth, B, Ikombe, NB, Matshimba, GK, Metzger, S, Muganza, DM, Mundry, R and Fowler, A 2014 New evidence for self-medication in bonobos: Manniophyton fulvum leaf- and stemstrip-swallowing from LuiKotale, Salonga National Park, DR Congo. American Journal of Primatology 76: 146–158. https://doi.org/10.1002/ajp.22217CrossRefGoogle ScholarPubMed
Graham, ML 2017 Positive reinforcement training and research. In: Schapiro, SJ (ed) Handbook of Primate Behavioral Management pp 187–200. CRC Press: Boca Raton, Florida, USA. https://doi.org/10.1201/9781315120652-13Google Scholar
Hanson, JD, Larson, ME and Snowdon, CT 1976 The effects of control over high intensity noise on plasma cortisol levels in rhesus monkeys. Behavioral Biology 16: 333–340. https://doi.org/10.1016/S0091-6773(76)91460-7CrossRefGoogle ScholarPubMed
Heilbronner, SR, Rosati, AG, Stevens, JR, Hare, B and Hauser, MD 2008 A fruit in the hand or two in the bush? Divergent risk preferences in chimpanzees and bonobos. Biology Letters 4: 246–249. https://doi.org/10.1098/rsbl.2008.0081Google ScholarPubMed
Hopkins, WD and Latzman, RD 2017 Future research with captive chimpanzees in the United States: Integrating scientific programs with behavioral management. In: Schapiro, SJ (ed) Handbook of Primate Behavioral Management pp 139–155. CRC Press: Boca Raton, Florida, USA. https://doi.org/10.1201/9781315120652-11CrossRefGoogle Scholar
Hopper, LM, Freeman, HD and Ross, SR 2016 Reconsidering coprophagy as an indicator of negative welfare for captive chim-panzees. Applied Animal Behaviour Science 176: 112–119. https://doi.org/10.1016/j.applanim.2016.01.002CrossRefGoogle Scholar
Huffman, MA 1997 Current evidence for self-medication in pri-mates: A multidisciplinary perspective. American Journal of Physical Anthropology 104: 171–200. https://doi.org/10.1002/(SICI)1096-8644(1997)25+<171::AID-AJPA7>3.0.CO;2-7Google Scholar
Huffman, MA, Spiezio, C, Sgaravatti, A and Leca, JB 2010 Leaf swallowing behavior in chimpanzees (Pan troglodytes): Biased learning and the emergence of group level cultural differences. Animal Cognition 13: 871–880. https://doi.org/10.1007/s10071-010-0335-8CrossRefGoogle Scholar
Lambeth, S, Bloomsmith, M, Baker, K, Perlman, JE, Hook, M and Schapiro, SJ 2001 Control over videotape enrichment for socially housed chimpanzees: Subsequent challenge tests. American Journal of Primatology 54: 62–63Google Scholar
Lambeth, SP, Hau, J, Perlman, JE, Martino, M and Schapiro, SJ 2006 Positive reinforcement training affects hematologic and serum chemistry values in captive chimpanzees (Pan troglodytes). American Journal of Primatology 68: 245–256. https://doi.org/10.1002/ajp.20148CrossRefGoogle Scholar
Laule, G, Thurston, RH, Alford, PL and Bloomsmith, MA 1996 Training to reliably obtain blood and urine samples from a diabetic chimpanzee (Pan troglodytes). Zoo Biology 15: 587–591. https://doi.org/10.1002/(SICI)1098-2361(1996)15:6<587::AID-ZOO4>3.0.CO;2-73.0.CO;2-7>CrossRefGoogle Scholar
Laule, G and Whittaker, M 2002 The use of positive reinforce-ment techniques with chimpanzees for enhanced care and wel-fare. In: Brent, L (ed) Special Topics in Primatology, Volume 2: Care and Management of Captive Chimpanzees pp 242–265. American Society of Primatologists: San Antonio, Texas, USAGoogle Scholar
Laule, G and Whittaker, M 2007 Enhancing nonhuman primate care and welfare through the use of positive reinforcement training. Journal of Applied Animal Welfare Science 10: 31–38. https://doi.org/10.1080/10888700701277311CrossRefGoogle ScholarPubMed
Leotti, LA, Iyengar, SS and Ochsner, KN 2010 Born to choose: The origins and value of the need for control. Trends in Cognitive Sciences 14: 457–463. https://doi.org/10.1016/j.tics.2010.08.001Google ScholarPubMed
Magden, ER 2017 Positive reinforcement training and health care. In: Schapiro, SJ (ed) Handbook of Primate Behavioral Management pp 201–215. CRC Press: Boca Raton, Florida, USA. https://doi.org/10.1201/9781315120652-14CrossRefGoogle Scholar
Magden, ER, Haller, RL, Thiele, EJ, Buchl, SJ, Lambeth, SP and Schapiro, SJ 2013 Acupuncture as an adjunct therapy for osteoarthritis in chimpanzees (Pan troglodytes). Journal of the American Association for Laboratory Animal Science 52: 475–480Google Scholar
Magden, ER, Sleeper, MM, Buchl, SJ, Jones, RA, Thiele, EJ and Wilkerson, GK 2016 Use of an implantable loop recorder in a chimpanzee (Pan troglodytes) to monitor cardiac arrhythmias and assess the effects of acupuncture and laser therapy. Comparative Medicine 66: 52–58Google Scholar
Masi, S, Gustafsson, E, Saint Jalme, M, Narat, V, Todd, A, Bomsel, MC and Krief, S 2012 Unusual feeding behavior in wild great apes, a window to understand origins of self-medication in humans: Role of sociality and physiology on learning process. Physiology and Behavior 105: 337–349. https://doi.org/10.1016/j.physbeh.2011.08.012Google ScholarPubMed
McDonald, JH 2014 Handbook of Biological Statistics, Third Edition pp 29–39. Sparky House Publishing: Baltimore, Maryland, USAGoogle Scholar
McKinley, J, Buchanan-Smith, H, Bassett, L and Morris, K 2003 Training common marmosets (Callithrix jacchus) to cooper-ate during routine laboratory procedures: Ease of training and time investment. Journal of Applied Animal Welfare Science 6: 209–220. https://doi.org/10.1207/S15327604JAWS0603_06CrossRefGoogle ScholarPubMed
Mellor, D 2016 Moving beyond the ‘Five Freedoms’ by updating the ‘Five Provisions’ and introducing aligned ‘Animal Welfare Aims’. Animals 6: 59–79. https://doi.org/10.3390/ani6100059Google Scholar
Mineka, S, Gunnar, M and Champoux, M 1986 Control and early socioemotional development: Infant rhesus monkeys reared in controllable versus uncontrollable environments. Child Development 57: 1241–1256. https://doi.org/10.2307/1130447Google Scholar
Morgan, KN and Tromborg, CT 2007 Sources of stress in cap-tivity. Applied Animal Behaviour Science 102: 262–302. https://doi.org/10.1016/j.applanim.2006.05.032Google Scholar
National Institutes of Health 2013 Council of councils working group on the use of chimpanzees in NIH-supported research report. https://dpcpsi.nih.gov/council/chimpanzee_researchGoogle Scholar
Neal Webb, SJ, Hau, J and Schapiro, SJ 2018 Captive chim-panzee (Pan troglodytes) behavior as a function of space per animal and enclosure type. American Journal of Primatology 80: e22749. https://doi.org/10.1002/ajp.22749CrossRefGoogle ScholarPubMed
Neal Webb, SJ, Hau, J and Schapiro, SJ Does (group) size mat-ter? Captive chimpanzee (Pan troglodytes) behavior as a function of group size and composition, in prepGoogle Scholar
Nunamaker, EA, Rick Lee, D and Lammey, ML 2012 Chronic diseases in captive geriatric female chimpanzees (Pan troglodytes). Comparative Medicine 62: 131–136Google Scholar
Obbo, CJD, Makanga, B, Mulholland, DA, Coombes, PH and Brun, R 2013 Antiprotozoal activity of Khaya anthotheca, (Welv) CDC a plant used by chimpanzees for self-medication. Journal of Ethnopharmacology 147: 220–223. https://doi.org/10.1016/j.jep.2013.03.007CrossRefGoogle Scholar
Owen, MA, Swaisgood, RR, Czekala, NM and Lindburg, DG 2005 Enclosure choice and well-being in giant pandas: Is it all about control? Zoo Biology 24: 475–481. https://doi.org/10.1002/zoo.20064CrossRefGoogle Scholar
Perlmuter, LC and Monty, RA 1977 The importance of per-ceived control: Fact or fantasy? Experiments with both humans and animals indicate that the mere illusion of control significantly improves performance in a variety of situations. American Scientist 65: 759–765Google Scholar
Pomerantz, O and Terkel, J 2009 Effects of positive reinforce-ment training techniques on the psychological welfare of zoo-housed chimpanzees (Pan troglodytes). American Journal of Primatology 71: 687–695. https://doi.org/10.1002/ajp.20703Google Scholar
Popilskis, SJ, Lee, DR and Elmore, DB 2008 Anesthesia and analgesia in nonhuman primates. In: Anesthesia and Analgesia in Laboratory Animals, Second Edition pp 335–363. Elsevier: Amsterdam, The Netherlands. https://doi.org/10.1016/B978-012373898-1.50016-4CrossRefGoogle Scholar
Reamer, LA, Haller, RL, Thiele, EJ, Freeman, HD, Lambeth, SP and Schapiro, SJ 2014 Factors affecting initial training suc-cess of blood glucose testing in captive chimpanzees (Pan troglodytes): Chimpanzee diabetic treatment training. Zoo Biology 33: 212–220. https://doi.org/10.1002/zoo.21123CrossRefGoogle Scholar
Reinhardt, V 1997 Training nonhuman primates to cooper-ate during handling procedures: A review. Animal Technology 48: 55–74Google Scholar
Reinhardt, V 2003 Working with rather than against macaques during blood collection. Journal of Applied Animal Welfare Science 6:189–197. https://doi.org/10.1207/S15327604JAWS0603_04CrossRefGoogle ScholarPubMed
Ross, SR 2006 Issues of choice and control in the behaviour of a pair of captive polar bears (Ursus maritimus). Behavioural Processes 73: 117–120. https://doi.org/10.1016/j.beproc.2006.04.003Google Scholar
Sambrook, TD and Buchanan-Smith, HM 1997 Control and complexity in novel object enrichment. Animal Welfare 6: 207–216Google Scholar
Schapiro, SJ 2017 Handbook of Primate Behavioral Management. CRC Press: Boca Raton, Florida, USA. https://doi.org/10.1201/9781315120652CrossRefGoogle Scholar
Schapiro, SJ, Brosnan, SF, Hopkins, WD, Whiten, A, Kendal, R, Sherwood, CC and Lambeth, SP 2017 Collaborative research and behavioral management. In: Schapiro, SJ (ed) Handbook of Primate Behavioral Management pp 243–254. CRC Press: Boca Raton, Florida, USA. https://doi.org/10.1201/9781315120652-17Google Scholar
Schapiro, SJ, Perlman, JE and Boudreau, BA 2001 Manipulating the affiliative interactions of group-housed rhesus macaques using positive reinforcement training techniques. American Journal of Primatology 55: 137–149. https://doi.org/10.1002/ajp.1047CrossRefGoogle ScholarPubMed
Schapiro, SJ, Reamer, LA, Mareno, MC and Lambeth, SP 2014 Providing chimpanzees with opportunities to voluntarily participate in their own care: Choice of medications. American Journal of Primatology 76: 73 (Abstract)Google Scholar
Tasker, L and Buchanan-Smith, HM 2016 Linking welfare and quality of scientific output through refinement of enhanced socialization with carestaff in cynomolgus macaques (Macaca fascicularis) used for regulatory toxicology. Joint Meeting of the International Primatological Society and the American Society of Primatologists. 21-26 August 2016, Chicago, Illinois, USACrossRefGoogle Scholar
Tennessen, T 1989 Coping with confinement: features of the environment that influence animals’ ability to adapt. Applied Animal Behaviour Science 22: 139–149. https://doi.org/10.1016/0168-1591(89)90050-6CrossRefGoogle Scholar
Videan, EN, Fritz, J, Schwandt, ML, Smith, HF and Howell, S 2005 Controllability in environmental enrichment for captive chimpanzees (Pan troglodytes). Journal of Applied Animal Welfare Science 8: 117–130. https://doi.org/10.1207/s15327604jaws0802_4CrossRefGoogle Scholar