Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-31T16:26:57.820Z Has data issue: false hasContentIssue false
  • English
  • Français

Does mirror enrichment improve primate well-being?

Published online by Cambridge University Press:  01 January 2023

B de Groot  and
SM Cheyne
B de Groot*
Affiliation:
Lange Brugstraat 44C2, 4811 WS, Breda, The Netherlands
SM Cheyne
Affiliation:
Department of Social Sciences, Oxford Brookes University, Gibbs Building, Gipsy Lane, Headington, Oxford OX3 0BP, UK
*
* Contact for correspondence and requests for reprints: [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Primates are highly social animals and appropriate enrichment is required to ensure their psychological well-being. Mirrors are sometimes used as social or sensory environmental enrichment. In this paper we investigate the suitability of mirrors as enrichment for captive primates, by reviewing the literature on mirror implementation in captive primate environments. Mirror-directed responses are mainly social as the mirror self-image is often seen as a conspecific. Although positive exploration and affiliative behaviours are observed, negative aggressive behaviours towards the mirror are most frequently recorded, and abnormal behaviours in primates do not decrease in mirror-enriched environments. There appear to be differences in habituation rates to mirrors amongst primates. While habituation to enrichment is generally perceived to be undesirable, this criterion should not apply when mirrors elicit negative behaviours. Primates that show mirror self-recognition, which are mostly great apes, may be best suitable for mirror enrichment, as they do not perceive the mirror self-image as a threatening conspecific. Increasing the understanding of the reflective properties of a mirror might help primates to understand that the image in the mirror is not real. This could be attained by using small, mobile mirrors. We suggest that mirrors can make decent primate enrichment if the primate understands its reflective properties, which should be evaluated on an individual level. Appropriate use of mirrors as sensory enrichment can improve primate well-being and prevent suffering.

Keywords

abnormal behaviouranimal welfarecaptivityself-recognitionsolitarystress
Type
Research Article
Information
Animal Welfare , Volume 25 , Issue 2 , May 2016 , pp. 163 - 170
Copyright
© 2016 Universities Federation for Animal Welfare

References

Anderson, JR 1983 Responses to mirror image stimulation and assessment of self-recognition in mirror- and peer-reared stump-tail macaques. The Quarterly Journal of Experimental Psychology Section B: Comparative and Physiological Psychology 35(3): 201–212. http://dx.doi.org/10.1080/14640748308400905CrossRefGoogle Scholar
Anderson, JR and Chamove, AS 1986 Infant stumptailed macaques reared with mirrors or peers: Social responsiveness, attachment, and adjustment. Primates 27(1): 63–82. http://dx.doi.org/10.1007/BF02382523CrossRefGoogle Scholar
Anderson, JR and Gallup, GG 2011 Do rhesus monkeys recognize themselves in mirrors? American Journal of Primatology 73(7): 603–606. http://dx.doi.org/10.1002/ajp.20950CrossRefGoogle ScholarPubMed
Anderson, JR and Roeder, JJ 1989 Responses of capuchin mon-keys (Cebus apella) to different conditions of mirror-image stimu-lation. Primates 30(4): 581–587. http://dx.doi.org/10.1007/BF02380884CrossRefGoogle Scholar
Arnold, K and Barton, RA 2001 Postconflict behaviour of spec-tacled leaf monkeys (Trachypithecus obscurus): I. Reconciliation. International Journal of Primatology 22(2): 243–266. http://dx.doi.org/10.1023/A:1005623631652CrossRefGoogle Scholar
Averill, JR 1983 Studies on anger and aggression: Implications for theories of emotion. American Psychologist 38(11): 1145–1160. http://dx.doi.org/10.1037/0003-066X.38.11.1145CrossRefGoogle ScholarPubMed
Bayne, KAL 1989 Environmental enrichment alternatives for lab-oratory nonhuman primates. In: Driscoll, JW (ed) Animal Care and Use in Behavioral Research: Regulations, Issues and Applications pp 91–102. Animal Welfare Information Centre: Beltsville, MD, USAGoogle Scholar
Bayne, KAL, Hurst, JK and Dexter, SL 1992 Evaluation of the preference to and behavioral effects of an enriched environment on male rhesus monkeys. Laboratory Animal Science 42(1): 38–45Google ScholarPubMed
Bezerra, BM, Barnett, AA, Souto, A and Jones, G 2011 Ethogram and natural history of golden-backed uakaris (Cacajao melanocephalus). International Journal of Primatology 32(1): 46–68. http://dx.doi.org/10.1007/s10764-010-9435-1CrossRefGoogle Scholar
Birkett, LP and Newton-Fisher, NE 2011 How abnormal is the behaviour of captive, zoo-living chimpanzees? PloS One 6(6): e20101. http://dx.doi.org/10.1371/journal.pone.0020101CrossRefGoogle ScholarPubMed
Boissy, A, Manteuffel, G, Jensen, MB, Moe, RO, Spruijt, B, Keeling, LJ, Winckler, C, Forkman, B, Dimitrov, I, Langbein, J, Bakken, M, Veissier, I and Aubert, A 2007 Assessment of positive emotions in animals to improve their welfare. Physiology & Behavior 92(3): 375–397. http://dx.doi.org/10.1016/j.phys-beh.2007.02.003CrossRefGoogle ScholarPubMed
Brent, L and Stone, AM 1996 Long-term use of televisions, balls, and mirrors as enrichment for paired and singly caged chim-panzees. American Journal of Primatology 39(2): 139–145. http://dx.doi.org/10.1002/(SICI)1098-2345(1996)39:2<139::AID-AJP5>3.0.CO;2-#3.0.CO;2-#>CrossRefGoogle Scholar
BIAZA (British and Irish Association of Zoos and Aquariums) 2014 Animal Welfare: Environmental Enrichment. http://www.biaza.org.uk/animal-management/animal-welfare/Google Scholar
Broom, DM 1991 Animal welfare: Concepts and measurement. Journal of Animal Science 69(10): 4167–4175CrossRefGoogle ScholarPubMed
Carlstead, K and Shepherdson, D 1994 Effects of environmen-tal enrichment on reproduction. Zoo Biology 13(5): 447–458. http://dx.doi.org/10.1002/zoo.1430130507CrossRefGoogle Scholar
Chang, L, Fang, Q, Zhang, S, Poo, MM and Gong, N 2015 Mirror-induced self-directed behaviors in rhesus monkeys after visual-somatosensory training. Current Biology 25(2): 212–217. http://dx.doi.org/10.1016/j.cub.2014.11.016CrossRefGoogle ScholarPubMed
Clark, JD, Rager, DR and Calpin, JP 1997 Animal well-being I. General considerations. Comparative Medicine 47(6): 564–570Google ScholarPubMed
Clarke, AS, Czekala, NM and Lindburg, DG 1995 Behavioral and adrenocortical responses of male cynomolgus and lion-tailed macaques to social stimulation and group formation. Primates 36(1): 41–56. http://dx.doi.org/10.1007/BF02381914CrossRefGoogle Scholar
Dalle Zotte, A, Princz, Z, Matics, Z, Gerencsér, Z, Metzger, S and Szendrő, Z 2009 Rabbit preference for cages and pens with or without mirrors. Applied Animal Behaviour Science 116(2): 273–278. http://dx.doi.org/10.1016/j.applanim.2008.08.011CrossRefGoogle Scholar
Davidson, RJ, Putnam, KM and Larson, CL 2000 Dysfunction in the neural circuitry of emotion regulation: a possible prelude to violence. Science 289(5479): 591–594. http://dx.doi.org/10.1126/science.289.5479.591CrossRefGoogle ScholarPubMed
Dawkins, MS 2004 Using behaviour to assess animal welfare. Animal Welfare 13(S1): S3–S7Google Scholar
Dettmer, E and Fragaszy, D 2000 Determining the value of social companionship to captive tufted capuchin monkeys (Cebus apella). Journal of Applied Animal Welfare Science 3(4): 293–304. http://dx.doi.org/10.1207/S15327604JAWS0304_2CrossRefGoogle Scholar
De Veer, MW and Van den Bos, R 1999 A critical review of methodology and interpretation of mirror self-recognition research in nonhuman primates. Animal Behaviour 58(3): 459–468. http://dx.doi.org/10.1006/anbe.1999.1166CrossRefGoogle Scholar
De Waal, FB, Dindo, M, Freeman, CA and Hall, MJ 2005 The monkey in the mirror: hardly a stranger. Proceedings of the National Academy of Sciences of the United States of America 102(32): 11140–11147. http://dx.doi.org/10.1073/pnas.0503935102CrossRefGoogle ScholarPubMed
Dolhinow, P 1978 A behaviour repertoire for the Indian langur monkey (Presbytis entellus). Primates 19(3): 449–472. http://dx.doi.org/10.1007/BF02373308CrossRefGoogle Scholar
Edgar, JL and Seaman, SC 2010 The effect of mirrors on the behaviour of singly housed male and female laboratory rabbits. Animal Welfare 19(4): 461–471Google Scholar
Eglash, AR and Snowdon, CT 1983 Mirror-image responses in pygmy marmosets (Cebuella pygmaea). American Journal of Primatology 5(3): 211–219. http://dx.doi.org/10.1002/ajp.1350050305CrossRefGoogle ScholarPubMed
Fraser, D, Weary, DM, Pajor, EA and Milligan, BN 1997 A scientific conception of animal welfare that reflects ethical con-cerns. Animal welfare 6(3): 187–205Google Scholar
Gallup, GG, McClure, MK, Hill, SD and Bundy, RA 1971 Capacity for self-recognition in differentially reared chim-panzees. The Psychological Record 21(1): 69–74CrossRefGoogle Scholar
Gallup, GG Jr 1970 Chimpanzees: Self-recognition. Science 167:86–87. http://dx.doi.org/10.1126/science.167.3914.86CrossRefGoogle Scholar
Gilbert, P and Allan, S 1994 Assertiveness, submissive behaviour and social comparison. British Journal of Clinical Psychology 33(3): 295–306. http://dx.doi.org/10.1111/j.2044-8260.1994.tb01125.xCrossRefGoogle ScholarPubMed
Grewal, BS 1981 Self-wrist biting in Arashiyama-B troop of Japanese monkeys (Macaca fuscata fuscata). Primates 22(2): 277–280. http://dx.doi.org/10.1007/BF02382617CrossRefGoogle Scholar
Harris, HG and Edwards, AJ 2004 Mirrors as environmental enrichment for African green monkeys. American Journal of Primatology 64(4): 459–467. http://dx.doi.org/10.1002/ajp.20092CrossRefGoogle ScholarPubMed
Heschl, A and Burkart, J 2006 A new mark test for mirror self-recognition in non-human primates. Primates 47(3): 187–198. http://dx.doi.org/10.1007/s10329-005-0170-8CrossRefGoogle Scholar
Honess, PE and Marin, CM 2006a Behavioural and physiological aspects of stress and aggression in non-human primates. Neuroscience & Biobehavioral Reviews 30(3): 390–412. http://dx.doi.org/10.1016/j.neubiorev.2005.04.003CrossRefGoogle Scholar
Honess, PE and Marin, CM 2006b Enrichment and aggression in primates. Neuroscience & Biobehavioral Reviews 30(3): 413–436. http://dx.doi.org/10.1016/j.neubiorev.2005.05.002CrossRefGoogle ScholarPubMed
Hosey, GR 2005 How does the zoo environment affect the behav-iour of captive primates? Applied Animal Behaviour Science 90(2): 107–129. http://dx.doi.org/10.1016/j.applanim.2004.08.015CrossRefGoogle Scholar
Hosey, GR, Melfi, V and Pankhurst, S 2009 Animal welfare. In: Hosey, GR, Melfi, V and Pankhurst, S (eds) Zoo Animals: Behaviour, Management and Welfare pp 219–258. Oxford University Press: Oxford, UKGoogle Scholar
Hyatt, CW 1998 Responses of gibbons (Hylobates lar) to their mirror images. American Journal of Primatology 45(3): 307–311. http://dx.doi.org/10.1002/(SICI)1098-2345(1998)45:3<307::AID-AJP7>3.0.CO;2-#3.0.CO;2-#>CrossRefGoogle ScholarPubMed
Inoue-Nakamura, N 1997 Mirror self-recognition in nonhuman primates: A phylogenetic approach. Japanese Psychological Research 39(3): 266–275. http://dx.doi.org/10.1111/1468-5884.00059CrossRefGoogle Scholar
Lambeth, SP and Bloomsmith, MA 1992 Mirrors as enrich-ment for captive chimpanzees (Pan troglodytes). Journal of the American Association for Laboratory Animal Science 42(3): 261–266Google Scholar
Ledbetter, D and Basen, J 1982 Failure to demonstrate self-recognition in gorillas. American Journal of Primatology 2(3): 301–310. http://dx.doi.org/10.1002/ajp.1350020309CrossRefGoogle ScholarPubMed
Lutz, CK and Novak, MA 2005 Environmental enrichment for non-human primates: Theory and application. ILAR journal 46(2): 178–191. http://dx.doi.org/10.1093/ilar.46.2.178CrossRefGoogle Scholar
Lutz, CK, Well, A and Novak, M 2003 Stereotypic and self-inju-rious behavior in rhesus macaques: A survey and retrospective analysis of environment and early experience. American Journal of Primatology 60(1): 1–15. http://dx.doi.org/10.1002/ajp.10075CrossRefGoogle ScholarPubMed
Marchal, P and Anderson, JR 1993 Mirror-image responses in capuchin monkeys (Cebus capucinus): Social responses and use of reflected environmental information. Folia Primatologica 61(3): 165–173. http://dx.doi.org/10.1159/000156745CrossRefGoogle ScholarPubMed
Mason, GJ 1991a Stereotypies: A critical review. Animal behaviour 41(6): 1015–1037. http://dx.doi.org/10.1016/S0003-3472(05)80640-2CrossRefGoogle Scholar
Mason, GJ 1991b Stereotypies and suffering. Behavioural Processes, 25(2): 103–115. http://dx.doi.org/10.1016/0376-6357(91)90013-PCrossRefGoogle ScholarPubMed
McAfee, LM, Mills, DS and Cooper, JJ 2002 The use of mirrors for the control of stereotypic weaving behaviour in the stabled horse. Applied Animal Behaviour Science 78(2): 159–173. http://dx.doi.org/10.1016/S0168-1591(02)00086-2CrossRefGoogle Scholar
Meehan, CL and Mench, JA 2007 The challenge of challenge: Can problem solving opportunities enhance animal welfare? Applied Animal Behaviour Science, 102(3): 246-261. http://dx.doi.org/10.1016/j.applanim.2006.05.031CrossRefGoogle Scholar
Mills, DS and Davenport, K 2002 Evidence for the importance of visual stimuli in the control of equine weaving behaviour. Animal Science 74: 95–101CrossRefGoogle Scholar
Moberg, GP 2000 Biological response to stress: Implications for animal welfare. In: Moberg, GP and Mench, JA (eds) The Biology of Animal Stress: Basic Principles and Implications for Animal Welfare pp 1–21. CABI Publishing: Oxon, UK. http://dx.doi.org/10.1079/9780851993591.0001CrossRefGoogle Scholar
Morgan, KN and Tromborg, CT 2007 Sources of stress in cap-tivity. Applied Animal Behaviour Science 102(3): 262–302. http://dx.doi.org/10.1016/j.applanim.2006.05.032CrossRefGoogle Scholar
National Research Council 2008 Recognition and alleviation of distress in laboratory animals. The National Academies Press: Washington, DC, USAGoogle Scholar
Novak, MA and Suomi, SJ 1988 Psychological well-being of pri-mates in captivity. American Psychologist 43(10): 765–773. http://dx.doi.org/10.1037/0003-066X.43.10.765CrossRefGoogle Scholar
O’Connor, LE, Berry, JW, Weiss, J and Gilbert, P 2002 Guilt, fear, submission, and empathy in depression. Journal of Affective Disorders 71(1): 19–27. http://dx.doi.org/10.1016/S0165-0327(01)00408-6CrossRefGoogle ScholarPubMed
Olsson, IAS and Westlund, K 2007 More than numbers matter: The effect of social factors on behaviour and welfare of laborato-ry rodents and non-human primates. Applied Animal Behaviour Science 103(3): 229–254. http://dx.doi.org/10.1016/j.applan-im.2006.05.022CrossRefGoogle Scholar
Patterson, FG and Cohn, RH 2006 Self-recognition and self-awareness in lowland gorillas. In: Parker, ST, Mitchell, RW and Boccia, ML (eds) Self-Awareness in Animals and Humans: Developmental Perspectives pp 273–290. Cambridge University Press: Cambridge, UKGoogle Scholar
Piller, CA, Stookey, JM and Watts, JM 1999 Effects of mirror-image exposure on heart rate and movement of isolated heifers. Applied Animal Behaviour Science 63(2): 93–102. http://dx.doi.org/10.1016/S0168-1591(99)00010-6CrossRefGoogle Scholar
Posada, S and Colell, M 2007 Another gorilla (Gorilla gorilla goril-la) recognizes himself in a mirror. American Journal of Primatology 69(5): 576–583. http://dx.doi.org/10.1002/ajp.20355CrossRefGoogle Scholar
Potter-Effron, RT and Potter-Effron, PS 2006 Letting go of anger: The eleven most common anger styles and what to do about them. New Harbinger Publications: Oakland, CA, USAGoogle Scholar
Povinelli, DJ, Gallup, GG, Eddy, TJ, Biershwale, DT, Engstrom, MC, Perilloux, HK and Toxopeus, ID 1997 Chimpanzees recognize themselves in mirrors. Animal Behaviour 53(5): 1083–1088. http://dx.doi.org/10.1006/anbe.1996.0303CrossRefGoogle Scholar
Price, EE and Stoinski, TS 2007 Group size: Determinants in the wild and implications for the captive housing of wild mammals in zoos. Applied Animal Behaviour Science 103(3): 255–264. http://dx.doi.org/10.1016/j.applanim.2006.05.021CrossRefGoogle Scholar
Rabin, LA 2003 Maintaining behavioural diversity in captivity for conservation: Natural behaviour management. Animal Welfare 12(1): 85–94Google Scholar
Rajala, AZ, Reininger, KR, Lancaster, KM and Populin, LC 2010 Rhesus monkeys (Macaca mulatta) do recognize themselves in the mirror: implications for the evolution of self-recognition. PLoS One 5(9): e12865. http://dx.doi.org/10.1371/journal.pone.0012865CrossRefGoogle ScholarPubMed
Ridley, RM and Baker, HF 1982 Stereotypy in monkeys and humans. Psychological medicine 12(1): 61–72. http://dx.doi.org/10.1017/S0033291700043294CrossRefGoogle ScholarPubMed
Seltzer, LJ and Ziegler, TE 2007 Non-invasive measurement of small peptides in the common marmoset (Callithrix jacchus): A radio-labeled clearance study and endogenous excretion under varying social conditions. Hormones and Behavior 51(3): 436–442. http://dx.doi.org/10.1016/j.yhbeh.2006.12.012CrossRefGoogle Scholar
Sherwin, CM 2004 Mirrors as potential environmental enrich-ment for individually housed laboratory mice. Applied Animal Behaviour Science 87(1): 95–103. http://dx.doi.org/10.1016/j.applanim.2003.12.014CrossRefGoogle Scholar
Shillito, DJ, Gallup, GG Jr and Beck, BB 1999 Factors affecting mirror behaviour in western lowland gorillas, Gorilla gorilla. Animal Behaviour 57(5): 999–1004. http://dx.doi.org/10.1006/anbe.1998.1062CrossRefGoogle ScholarPubMed
Skibiel, AL, Trevino, HS and Naugher, K 2007 Comparison of several types of enrichment for captive felids. Zoo biology 26(5): 371–381. http://dx.doi.org/10.1002/zoo.20147CrossRefGoogle ScholarPubMed
Slater, KY, Schaffner, CM and Aureli, F 2009 Sex differences in the social behavior of wild spider monkeys (Ateles geoffroyi yucatanensis). American Journal of Primatology 71(1): 21–29. http://dx.doi.org/10.1002/ajp.20618CrossRefGoogle ScholarPubMed
Stevenson, MF and Poole, TB 1976 An ethogram of the com-mon marmoset (Calithrix jacchus jacchus): General behavioural repertoire. Animal Behaviour 24(2): 428–451. http://dx.doi.org/10.1016/S0003-3472(76)80053-XCrossRefGoogle Scholar
Straumann, C and Anderson, JR 1991 Mirror-induced social facilitation in stumptailed macaques (Macaca arctoides). American Journal of Primatology 25(2): 125–132. http://dx.doi.org/10.1002/ajp.1350250206CrossRefGoogle ScholarPubMed
Suarez, SD and Gallup, GG Jr 1981 Self-recognition in chim-panzees and orangutans, but not gorillas. Journal of Human Evolution 10(2): 175–188. http://dx.doi.org/10.1016/S0047-2484(81)80016-4CrossRefGoogle Scholar
Suddendorf, T and Collier-Baker, E 2009 The evolution of pri-mate visual self-recognition: Evidence of absence in lesser apes. Proceedings of the Royal Society B: Biological Sciences 276(1662): 1671–1677. http://dx.doi.org/10.1098/rspb.2008.1754CrossRefGoogle ScholarPubMed
Swartz, KB and Evans, S 1991 Not all chimpanzees (Pan troglodytes) show self-recognition. Primates 32(4): 483–496. http://dx.doi.org/10.1007/BF02381939CrossRefGoogle Scholar
Tamashiro, KL, Nguyen, M and Sakai, RR 2005 Social stress: From rodents to primates. Frontiers in Neuroendocrinology 26(1): 27–40. http://dx.doi.org/10.1016/j.yfrne.2005.03.001CrossRefGoogle ScholarPubMed
Tarou, LR and Bashaw, MJ 2007 Maximizing the effectiveness of environmental enrichment: Suggestions from the experimental analysis of behavior. Applied Animal Behaviour Science 102(3): 189–204. http://dx.doi.org/10.1016/j.applanim.2006.05.026CrossRefGoogle Scholar
Troisi, A 2002 Displacement activities as a behavioral measure of stress in nonhuman primates and human subjects. Stress 5(1): 47–54. http://dx.doi.org/10.1080/102538902900012378CrossRefGoogle ScholarPubMed
Ujhelyi, M, Merker, B, Buk, P and Geissmann, T 2000 Observations on the behavior of gibbons (Hylobates leucogenys, H. gabriellae, and H. lar) in the presence of mirrors. Journal of Comparative Psychology 114(3): 253–262. http://dx.doi.org/10.1037/0735-7036.114.3.253CrossRefGoogle Scholar
Walraven, V, Van Elsacker, L and Verheyen, R 1995 Reactions of a group of pygmy chimpanzees (Pan paniscus) to their mirror-images: Evidence of self-recognition. Primates 36(1): 145–150. http://dx.doi.org/10.1007/BF02381922CrossRefGoogle Scholar
Watanabe, S 2002 Preference for mirror images and video image in Java sparrows (Padda oryzivora). Behavioural Processes 60(1): 35–39. http://dx.doi.org/10.1016/S0376-6357(02)00094-3CrossRefGoogle ScholarPubMed
Wells, DL 2009 Sensory stimulation as environmental enrich-ment for captive animals: A review. Applied Animal Behaviour Science 118(1): 1–11. http://dx.doi.org/10.1016/j.applan-im.2009.01.002CrossRefGoogle Scholar
Westergaard, GC and Hyatt, CW 1994 The responses of bonobos (Pan paniscus) to their mirror images: Evidence of self-recognition. Human Evolution 9(4): 273–279. http://dx.doi.org/10.1007/BF02435514CrossRefGoogle Scholar
Würbel, H and Garner, JP 2007 Refinement of rodent research through environmental enrichment and systematic randomisation. NC3Rs 9: 1–9Google Scholar
Zaragoza, F, Ibáñez, M, Mas, B, Laiglesia, S and Anzola, B 2011 Influence of environmental enrichment in captive chim-panzees (Pan troglodytes spp) and gorillas (Gorilla gorilla gorilla): Behavior and faecal cortisol levels. Revista Científica 21(5): 447–456Google Scholar