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A Comparison of the Effects of Simple Versus Complex Environmental Enrichment on the Behaviour of Group-Housed, Subadult Rhesus Macaques

Published online by Cambridge University Press:  11 January 2023

S J Schapiro ,
M A Bloomsmith ,
S A Suarez  and
L M Porter
S J Schapiro*
Affiliation:
Department of Veterinary Sciences, The University of Texas MD Anderson Cancer Center, Science Park, Bastrop, TX 78602, USA
M A Bloomsmith
Affiliation:
Department of Veterinary Sciences, The University of Texas MD Anderson Cancer Center, Science Park, Bastrop, TX 78602, USA
S A Suarez
Affiliation:
Department of Veterinary Sciences, The University of Texas MD Anderson Cancer Center, Science Park, Bastrop, TX 78602, USA
L M Porter
Affiliation:
Department of Veterinary Sciences, The University of Texas MD Anderson Cancer Center, Science Park, Bastrop, TX 78602, USA
*
† Contact for correspondence and requests for reprints
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Abstract

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Enrichment of the environments of captive primates is currently of interest as both a basic and an applied research question, particularly when social and inanimate enhancements are used simultaneously. We measured the behavioural effects of two intensities of inanimate enrichment on 12 unimale-multifemale groups and 12 all-male groups from three cohorts of three to four-year-old rhesus macaques (Macaca mulatta). Half of the groups received a simple, inexpensive enrichment programme while the other groups received a more complex and costly combination of physical andfeeding enhancements. Observations were conducted on 93 subadults of both sexes during their initial year of group housing. Intensity of enrichment did not differentially affect the amount of time subjects spent in any of the activities analysed. Subjects that received the more complex programme spent only 8.3 per cent of their time using the extra enhancements. Therefore, there was little demonstrated benefit of the more costly enrichment programme. The three cohorts differed in the amount of time that they spent inactive, behaving agonistically, playing and located near a group mate. A planned comparison of one cohort that had been single-housed without visual access to social groups, to the two cohorts that had visual access to social groups during single caging, revealed differences in play and socially-located behaviour, which may have been due to differences in extra-cage conditions two years prior to the present study. When primates are housed socially with conspecifics as ‘social enhancements ‘, the relatively simple inanimate enrichment programme we used was as effective as the more costly programme. When enrichment resources are limited, inanimate enrichment efforts should be focused on monkeys that are not socially enriched.

Keywords

animal welfareenvironmental enrichmentgroup housinginanimate enrichmentrhesus macaquesocial enrichment
Type
Research Article
Information
Animal Welfare , Volume 6 , Issue 1 , February 1997 , pp. 17 - 28
Copyright
© 1997 Universities Federation for Animal Welfare

References

Altmann, J 1974 Observational study of behavior: sampling methods. Behaviour 49: 227–267CrossRefGoogle ScholarPubMed
Anderson, J R, Rortais, A and Guillemein, S 1994 Diving and underwater swimming as enrichment activities for captive rhesus macaques (Macaca mulatta). Animal Welfare 3: 275–283CrossRefGoogle Scholar
Bayne, K and Dexter, S 1992 Removing an environmental enrichment device can result in a rebound of abnormal behavior in rhesus monkeys (Macaca mulatta). American Journal of Primatology 27: 15Google Scholar
Bayne, K A L, Dexter, S L, Hurst, J D, Strange, G M and Hill, E E 1993 Kong toys for laboratory primates: are they really an enrichment or just fomites? Laboratory Animal Science 43: 78–85Google ScholarPubMed
Bayne, K, Dexter, S, Mainzer, H, McCully, C, Campbell, G and Yamada, F 1992 The use of artificial turf as a foraging substrate for individually housed rhesus monkeys (Macaca mulatta). Animal Welfare 1: 39–53CrossRefGoogle Scholar
Bayne, K, Mainzer, H, Dexter, S, Campbell, G, Yamada, F and Suomi, S 1991 The reduction of abnormal behaviors in individually housed rhesus monkeys (Macaca mulatta) with a foraging/grooming board. American Journal of Primatology 23: 23–35CrossRefGoogle ScholarPubMed
Beckley, S and Novak, M 1989 Examination of various foraging components and their suitability as enrichment tools for captively housed primates. American Journal of Primatology Supplement 1: 37–43Google Scholar
Bloomsmith, M A, Alford, P L and Maple, T L 1988 Successful feeding enrichment for captive chimpanzees. American Journal of Primatology 16: 155–164CrossRefGoogle ScholarPubMed
Bloomsmith, M A, Brent, L Y and Schapiro, S J 1991 Guidelines for developing and managing an environmental enrichment program for nonhuman primates. Laboratory Animal Science 41: 372–377Google ScholarPubMed
Bloomsmith, M A, Finlay, T W, Merhalski, J J and Maple, T L 1990 Rigid plastic balls as enrichment devices for captive chimpanzees. Laboratory Animal Science 40: 319–322Google ScholarPubMed
Bramblett, C 1989 Mental well-being in anthropoids. In: Segal, E F (ed) Housing, Care and Psychological Wellbeing of Captive and Laboratory Primates pp 1–11. Noyes Publications: New Jersey, USAGoogle Scholar
Bramblett, R D and Bramblett, C A 1988 A liquid dispenser for caged primates. Laboratory Primate Newsletter 27: 16Google Scholar
Brent, L and Eichberg, J W 1991 Primate puzzleboard: a simple environmental enrichment device for captive chimpanzees. Zoo Biology 10: 353–360CrossRefGoogle Scholar
Brent, L, Fisher, S and Eichberg, J W 1993 Social factors influencing performance of a foraging task for captive chimpanzees. Folia Primatologica 61: 177–185CrossRefGoogle ScholarPubMed
Byrne, G D and Suomi, S 1991 Effects of woodchips and buried food on behavior patterns and psychological well-being of captive rhesus monkeys. American Journal of Primatology 23: 141–151CrossRefGoogle ScholarPubMed
Chamove, A S, Anderson, J R, Morgan-Jones, S C and Jones, S P 1982 Deep woodchip litter: hygiene, feeding and behavioral enhancement in eight primate species. International Journal for the Study of Animal Problems 3: 308–318Google Scholar
Champoux, M, DiGregorio, G, Schneider, M L and Suomi, S J 1990 Inanimate environmental enrichment for group-housed rhesus macaque infants. American Journal of Primatology 22: 61–67CrossRefGoogle ScholarPubMed
Clarke, A S, Czekala, N M and Lindburg, D G 1995 Behavioral and adrenocortical responses of male cynomolgus and lion-tailed macaques to social stimulation and group formation. Primates 36: 41–56CrossRefGoogle Scholar
Coe, C L 1991 Is social housing of primates always the optimal choice? In: Novak M A and Petto A J (eds) Through the Looking Glass: Issues of Psychological Well-being in Captive Nonhuman Primates pp 78–92. American Psychological Association: Washington DC, USACrossRefGoogle Scholar
Crockett, C M, Bowers, C L, Bowden, D M and Sackett, G P 1994 Sex differences in compatibility of pair-housed adult longtailed macaques. American Journal of Primatology 32: 73–94CrossRefGoogle ScholarPubMed
Dienske, H, van Vreeswijk, W and Koning, H 1980 Adequate mothering by partially isolated rhesus monkeys after observation of maternal care. Journal of Abnormal Psychology 89: 489–492CrossRefGoogle ScholarPubMed
Gilbert, S G and Wrenshall, E 1989 Environmental enrichment for monkeys used in behavioral toxicology studies. In: Segal, E F (ed) Housing, Care and Psychological Wellbeing of Captive and Laboratory Primates pp 244–254. Noyes Publications: New Jersey, USAGoogle Scholar
Goo, G P and Sassenrath, E N 1980 Persistent adrenocortical activation in female rhesus monkeys after new breeding group formation. Journal of Medical Primatology 9: 325–334CrossRefGoogle Scholar
Gullekson, R, Bench, L, Harrigan, K and Pyle, K 1991 Seed-feeder as a foraging device for singly housed cynomolgus monkeys (Macaca fascicularis). Lab Animal 20: 44–46Google Scholar
Hayes, S L 1990 Increasing foraging opportunities for a group of captive capuchin monkeys (Cebus capucinus). Laboratory Animal Science 40: 515–519Google ScholarPubMed
Kessel, A L and Brent, L 1996 Space utilization by captive-born baboons (Papio sp.) before and after provision of structural enrichment. Animal Welfare 5: 37–44CrossRefGoogle Scholar
Lindburg, D G 1971 The rhesus monkey in North India. In: Rosenblum, L A (ed) Primate Behavior: Developments in Field and Laboratory Research Volume 2 pp 1–106. Academic Press: New York, USAGoogle Scholar
Line, S W 1987 Environmental enrichment for laboratory primates. Journal of the American Veterinary Medical Association 190: 854–859Google ScholarPubMed
Line, S W and Morgan, K N 1991 The effects of two novel objects on the behavior of singly caged adult rhesus macaques. Laboratory Animal Science 41: 365–369Google ScholarPubMed
Line, S W, Morgan, K N and Markowitz, H 1991 Simple toys do not alter the behavior of aged rhesus monkeys. Zoo Biology 10: 473–484CrossRefGoogle Scholar
Line, S W, Morgan, K N, Markowitz, H, Roberts, J A and Riddell, M 1990 Behavioral responses of long-tailed macaques (Macaca fascicularis) to pair formation. Laboratory Primate Newsletter 29(4): 1–5Google Scholar
Maki, S and Bloomsmith, M A 1989 Uprooted trees facilitate the psychological well-being of captive chimpanzees. Zoo Biology 8: 79–87CrossRefGoogle Scholar
Mason, W A 1991 Effects of social interaction on well-being: development aspects. Laboratory Animal Science 41: 323–328Google ScholarPubMed
Noldus, L P J J 1991 The observer: a software system for collection and analysis of observational data. Behavior Research Methods, Instruments, and Computers 23: 415–429CrossRefGoogle Scholar
Novak, M A and Drewsen, K H 1989 Enriching the lives of captive primates: issues and problems. In: Segal, E F (ed) Housing, Care and Psychological Wellbeing of Captive and Laboratory Primates pp 161–182. Noyes Publications: New Jersey, USAGoogle Scholar
Novak, M A, Musante, A, Munroe, H, O’Neill, P L, Price, C and Suomi, S J 1993 Old, socially housed rhesus monkeys manipulate objects. Zoo Biology 12: 285–298CrossRefGoogle Scholar
Novak, M A, O’Neill, P and Suomi, S J 1992 Adjustments and adaptations to indoor and outdoor environments: continuity and change in young adult rhesus monkeys. American Journal of Primatology 28: 125–138CrossRefGoogle ScholarPubMed
Novak, M A and Suomi, S J 1988 Psychological well-being of primates in captivity. American Psychologist 43: 765–773CrossRefGoogle ScholarPubMed
Novak, M A and Suomi, S J 1991 Social interaction in nonhuman primates: an underlying theme for primate research. Laboratory Animal Science 41: 308–314Google ScholarPubMed
O’Neill, P L, Novak, M A and Suomi, S J 1991 Normalizing laboratory-reared rhesus macaque (Macaca mulatta) behavior with exposure to complex outdoor enclosures. Zoo Biology 10: 237–245CrossRefGoogle Scholar
Parks, K A and Novak, M A 1993 Observations of increased activity and tool use in captive rhesus monkeys exposed to troughs of water. American Journal of Primatology 29: 13–25CrossRefGoogle ScholarPubMed
Reinhardt, V 1989 Behavioral response of unrelated adult male rhesus monkeys familiarized and paired for the purpose of environmental enrichment. American Journal of Primatology 17: 243–248CrossRefGoogle ScholarPubMed
Reinhardt, V 1993 Promoting increased foraging behavior in caged stump-tailed macaques. Folia Primatologica 61: 47–51CrossRefGoogle ScholarPubMed
Reinhardt, V 1994 Pair-housing rather than single-housing for laboratory rhesus macaques. Journal of Medical Primatology 23: 426–431CrossRefGoogle ScholarPubMed
Reinhardt, V, Houser, D, Eisele, S, Cowley, D and Vertein, R 1988 Behavioral responses of unrelated rhesus monkey females paired for the purpose of environmental enrichment. American Journal of Primatology 14: 135–140CrossRefGoogle ScholarPubMed
Reinhardt, V, Liss, C and Stevens, C 1995 Social housing of previously single-caged macaques: what are the options and the risks? Animal Welfare 4: 307–328CrossRefGoogle Scholar
Rutnbaugh, D M, Washburn, D and Savage-Rumbaugh, E S 1989 On the care of captive chimpanzees: methods of enrichment. In: Segal, E F (ed) Housing, Care and Psychological Wellbeing of Captive and Laboratory Primates pp 357–375. Noyes Publications: New Jersey, USAGoogle Scholar
Ruppenthal, G C, Walker, C G and Sackett, G P 1991 Rearing infant monkeys (Macaca nemestrina) in pairs produces deficient social development compared with rearing in single cages. American Journal of Primatology 25: 103–113CrossRefGoogle ScholarPubMed
Schapiro, S J and Bloomsmith, M A 1994 Behavioral effects of enrichment on pair-housed juvenile rhesus monkeys. American Journal of Primatology 32: 159–170CrossRefGoogle ScholarPubMed
Schapiro, S J and Bloomsmith, M A 1995 Behavioral effects of enrichment on singly-housed, yearling rhesus monkeys: an analysis including three enrichment conditions and a control group. American Journal of Primatology 35: 89–101CrossRefGoogle ScholarPubMed
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. Applied Animal Behaviour Science 48: 159–171CrossRefGoogle Scholar
Schapiro, S J, Bloomsmith, M A, Suarez, S A and Porter, L M 1995a Maternal behavior of primiparous rhesus monkeys: effects of limited social restriction and inanimate environmental enrichment. Applied Animal Behaviour Science 45: 139–149CrossRefGoogle Scholar
Schapiro, S J, Lee-Parritz, D E, Taylor, L L, Watson, L, Bloomsmith, M A and Petto, A 1994 Behavioral management of specific pathogen-free (SPF) rhesus macaques: group formation, reproduction, and parental competence. Laboratory Animal Science 44: 229–234Google ScholarPubMed
Schapiro, S J, Porter, L M, Suarez, S A and Bloomsmith, M A 1995b The behavior of singly-caged, yearling rhesus monkeys is affected by the environment outside of the cage. Applied Animal Behaviour Science 45: 151–163CrossRefGoogle Scholar
Schapiro, S J, Porter, L M, Suarez, S A and Bloomsmith, M A 1995c Age and social experience affect the breeding performance of subadult male rhesus monkeys (Macaca mulatta). Contemporary Topics in Laboratory Animal Science 34: 93–95Google ScholarPubMed
Smuts, B B, Cheney, D L, Seyfarth, R M, Wrangham, R W and Struhsaker, T T (eds) 1987 Primate Societies. University of Chicago Press: Chicago, USAGoogle Scholar
Teas, J, Richie, T, Taylor, H and Southwick, C 1980 Population patterns and behavioral ecology of rhesus monkeys (Macaca mulatta) in Nepal. In: Lindburg, D (ed) The Macaques: Studies in Ecology, Behavior, and Evolution pp 247–262. Van Nostrand Reinhold Co: New York, USAGoogle Scholar
Voss, W R, Buchl, S J, Keeling, M E, Hilliard, J, Lerche, N, Schapiro, S J and Bloomsmith, MA 1991 Derivation strategy for establishing a Macaca mulatta (rhesus) colony specifically pathogen-free of Herpes B virus and simian retrovirus. AALAS Bulletin 30: 18–19Google Scholar