Effects of environmental enrichment on reproduction
Abstract
Although there have been few demonstrations of a direct empirical relationship between environmental enrichment and reproductive success in captive animals, indirect and anecdotal evidence indicates the importance of physical and temporal complexity for reproduction. We discuss three major mechanisms through which environmental enrichment that specifically increases the complexity of an animal's surroundings may influence reproductive physiology and behavior: developmental processes, modulation of stress and arousal, and modification of social interactions. In complex environments developing animals learn that performing active behavior produces appropriate functional outcomes. Learning to control their environment influences their ability to adapt to novel situations, which may profoundly influence their reproductive behavior as adults in breeding situations. Chronic stress may compromise reproductive physiology and behavior; enrichment reduces stress by providing increased opportunity for behavioral coping responses. However, some degree of acute stress may be beneficial for reproduction by maintaining an animal's level of responsiveness to socio‐sexual stimuli necessary for sexual arousal and reproductive activation. Finally, environmental enrichment may influence reproductive success by stabilizing social groups, reducing aggression and increasing affiliative and play behaviors. It is concluded that multi‐variate multi‐institutional behavioral research in zoos will play a…
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The quantity and quality of substrates and effective environmental enrichment are areas where improving the wellbeing of animals can be interconnected with improving the outcomes of breeding programs.
“The quantity and quality of substrates and effective environmental enrichment have been highlighted as areas where improving the wellbeing of animals can be interconnected with improving the outcomes of breeding programs [76].”
From The Concept of Agency, Animal Wellbeing, and the Practical Realities of Ex Situ Breeding Programs in Zoos and Aquariums (2024) · cites this paper as [76]
Cites
Conflict, arousal, and curiosity.
Berlyne, D. E. (1960) · McGraw-Hill Book Company · doi:10.1037/11164-000 · Cited by 6,018 · see citing works
The Physiology of Reproduction
Blandau, R. J. (1988) · JAMA · doi:10.1001/jama.1988.03410200127050 · Cited by 3,000 · see citing works
SMITH, G. M. (1979) · British Journal of Anaesthesia · doi:10.1093/bja/51.4.388-a · Cited by 849 · see citing works
Stress, Health, and the Social Environment
Henry, J. P., & STEPHENS, P. M. (1977) · Topics in environmental physiology and medicine · doi:10.1007/978-1-4612-6363-0 · Cited by 608 · see citing works
Prenatal Stress Feminizes and Demasculinizes the Behavior of Males
Ward, I. L. (1972) · Science · doi:10.1126/science.175.4017.82 · Cited by 545 · see citing works
Stress in Farm Animals: A Need for Reevaluation
Dantzer, R., & Mormède, P. (1983) · Journal of Animal Science · doi:10.2527/jas1983.5716 · Cited by 491 · see citing works
Wiepkema, P. R., & Koolhaas, J. M. (1993) · Animal Welfare · doi:10.1017/s0962728600015876 · Cited by 461 · see citing works
Hediger, H., & Sircom, G. (1950) · Cited by 457 · see citing works
Stress, Health, and the Social Environment: A Sociobiologic Approach to Medicine
Henry, J. P., & STEPHENS, P. M. (1977) · Medical Entomology and Zoology · Cited by 417 · see citing works
Creative Conservation: Interactive Management of Wild and Captive Animals
Thorne, E. T., Olney, P., Mace, G. M., & Feistner, A. T. C. (1996) · Journal of Wildlife Management · doi:10.2307/3802403 · Cited by 348 · see citing works
Behavioral and physiological correlates of stress in laboratory cats
Carlstead, K., Brown, J. L., & Strawn, W. (1993) · Applied Animal Behaviour Science · doi:10.1016/0168-1591(93)90062-t · Cited by 347 · see citing works
Self-citationStress and brain noradrenaline: a review.
Glavin, G. (1985) · Neuroscience and Biobehavioral Reviews · doi:10.1016/0149-7634(85)90048-x · Cited by 322 · see citing works
Housing, Care and Psychological Well-Being of Captive and Laboratory Primates
Segal, E. F. (1990) · Cited by 321 · see citing works
The influence of food presentation on the behavior of small cats in confined environments
Shepherdson, D. J., Carlstead, K., Mellen, J. D., & Seidensticker, J. C., IV (1993) · Zoo Biology · doi:10.1002/zoo.1430120206 · Cited by 321 · see citing works
Self-citationPrimates: the road to self-sustaining populations
Benirschke, K. (1986) · Cited by 295 · see citing works
Psychobiology of reproductive behavior: An evolutionary perspective
(1988) · General and Comparative Endocrinology · doi:10.1016/0016-6480(88)90221-3 · Cited by 266 · see citing works
Neuroimmune networks: physiology and diseases
(1990) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(90)90073-s · Cited by 239 · see citing works
STRESS, AROUSAL, AND THE PITUITARY-ADRENAL SYSTEM: A PSYCHOENDOCRINE HYPOTHESIS
Hennessy, J. W., & Levine, S. (1979) · Cited by 238 · see citing works
Controllability and predictability in acquired motivation
Mineka, S., & Hendersen, R. W. (1985) · Annual Review of Psychology · doi:10.1146/annurev.ps.36.020185.002431 · Cited by 234 · see citing works
Gentsch, C., Lichtsteiner, M., & Feer, H. (1981) · Physiology & Behavior · doi:10.1016/0031-9384(81)90320-6 · Cited by 233 · see citing works
Behavioral Enrichment in the Zoo
Markowitz, H. (1981) · Cited by 232 · see citing works
Behavioral and adrenocortical responses to environmental changes in leopard cats (Felis bengalensis)
Carlstead, K., Brown, J. L., & Seidensticker, J. C., IV (1993) · Zoo Biology · doi:10.1002/zoo.1430120403 · Cited by 211 · see citing works
Self-citationMellen, J. D. (1991) · Zoo Biology · doi:10.1002/zoo.1430100202 · Cited by 194 · see citing works
Thorpe, W. H. (1964) · Nature · doi:10.1038/202058c0 · Cited by 188 · see citing works
The Interrelations of Emotions as Suggested by Recent Physiological Researches
Cannon, W. B. (1914) · The American Journal of Psychology · doi:10.2307/1413414 · Cited by 188 · see citing works
Stress, social status, and reproductive physiology in free-living baboons.
Sapolsky, R. M. (1987) · Cited by 167 · see citing works
Influence of Stress on Reproduction: Measure of Well-being
Moberg, G. P. (1985) · Springer eBooks · doi:10.1007/978-1-4614-7544-6_14 · Cited by 166 · see citing works
Choosing between predictable and unpredictable shock conditions: Data and theory.
Badia, P., Harsh, J., & Abbott, B. B. (1979) · Psychological Bulletin · doi:10.1037/0033-2909.86.5.1107 · Cited by 153 · see citing works
Mineka, S., Gunnar, M. R., & Champoux, M. (1986) · Child Development · doi:10.2307/1130447 · Cited by 147 · see citing works
Sapolsky, R. M. (1986) · Endocrinology · doi:10.1210/endo-118-4-1630 · Cited by 140 · see citing works
Suomi, S. J. (1987) · Cited by 138 · see citing works
Relationships between Social Organization and Behavioral Endocrinology in a Monogamous Mammal
Carter, C. S., Getz, L. L., & Cohen-Parsons, M. (1986) · Advances in the study of behavior · doi:10.1016/s0065-3454(08)60189-8 · Cited by 125 · see citing works
Adrenal hormonal indices of stress in laboratory rats
Natelson, B. H., Creighton, D., McCarty, R. C., Tapp, W. N., Pitman, D. L., & Ottenweller, J. E. (1987) · Physiology & Behavior · doi:10.1016/0031-9384(87)90408-2 · Cited by 121 · see citing works
Successful feeding enrichment for captive chimpanzees
Bloomsmith, M. A., Alford, P. L., & Maple, T. L. (1988) · American Journal of Primatology · doi:10.1002/ajp.1350160206 · Cited by 120 · see citing works
Renner, M., & Rosenzweig, M. R. (1986) · Journal of comparative psychology · doi:10.1037/0735-7036.100.3.229 · Cited by 115 · see citing works
A Psychological Setting of Somatic Disease: The ‘Giving up — Given Up’ Complex
Engel, G. L. (1967) · Proceedings of the Royal Society of Medicine · doi:10.1177/003591576706000618 · Cited by 112 · see citing works
Abbott, B. B., Schoen, L. S., & Badia, P. (1984) · Psychological Bulletin · doi:10.1037/0033-2909.96.1.45 · Cited by 102 · see citing works
The effect of deprivation of visual incentives on visual exploration motivation in monkeys.
Butler, R. A. (1957) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0048106 · Cited by 94 · see citing works
Hansen, S., Stanfield, E. J., & Everitt, B. J. (1980) · Nature · doi:10.1038/286152a0 · Cited by 92 · see citing works
Psychobiology of Coping in Animals: The Effects of Predictability
Weinberg, J., & Levine, S. D. (1980) · Springer eBooks · doi:10.1007/978-1-4684-1042-6_2 · Cited by 90 · see citing works
Pituitary-adrenal consequences of adjunctive activities in pigs
Dantzer, R., & Mormède, P. (1981) · Hormones and Behavior · doi:10.1016/0018-506x(81)90003-9 · Cited by 68 · see citing works
Predictability, control, and the pituitary-adrenal response in rats.
Davis, H., & Levine, S. (1982) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0077892 · Cited by 68 · see citing works
Control of Their Environment Reduces Emotionality in Rats
Joffe, J. M., Rawson, R. A., & Mulick, J. A. (1973) · Science · doi:10.1126/science.180.4093.1383 · Cited by 66 · see citing works
Correlates of sexual and maternal competence in captive gorillas
Beck, B., & Power, M. L. (1988) · Zoo Biology · doi:10.1002/zoo.1430070405 · Cited by 64 · see citing works
Mormède, P., Dantzer, R., Bluthé, R.-M., & Caritez, J. C. (1984) · Genetics Selection Evolution · doi:10.1186/1297-9686-16-1-85 · Cited by 61 · see citing works
Environmental Contingencies as Sources of Stress in Animals
Overmier, J. B., Patterson, J., & Wielkiewicz, R. M. (1980) · Springer eBooks · doi:10.1007/978-1-4684-1042-6_1 · Cited by 60 · see citing works
Gorilla adaptations to naturalistic environments
Ogden, J. J., Finlay, T. W., & Maple, T. L. (1990) · Zoo Biology · doi:10.1002/zoo.1430090205 · Cited by 60 · see citing works
Konarska, M., Stewart, R. E., & McCarty, R. C. (1989) · Physiology & Behavior · doi:10.1016/0031-9384(89)90245-x · Cited by 58 · see citing works
Line, S. W., Markowitz, H., Morgan, K. N., & Strong, S. E. (1991) · American Psychological Association eBooks · doi:10.1037/10080-016 · Cited by 57 · see citing works
(2020) · Indiana University Press eBooks · doi:10.2307/j.ctvxw3p70.29 · Cited by 56 · see citing works
Effect of transportation stress on ovarian function in superovulated Hereford heifers
Edwards, L. M., Rahe, C. H., Griffin, J. L., Wolfe, D. F., Marple, D. N., Cummins, K. A., & Pitchett, J. F. (1987) · Theriogenology · doi:10.1016/0093-691x(87)90016-1 · Cited by 47 · see citing works
Epple, G. (1978) · Hormones and Behavior · doi:10.1016/0018-506x(78)90043-0 · Cited by 46 · see citing works
Renner, M. J. (2012) · International Journal of Comparative Psychology · doi:10.46867/c45303 · Cited by 45 · see citing works
Potentiative action of α- and β-adrenergic receptor stimulation in inducing lordosis behavior
Fernández‐Guasti, A., Larsson, K., & Beyer, C. (1985) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(85)90283-7 · Cited by 40 · see citing works
Reevaluation of mechanisms that mediate brain differences between enriched and impoverished animals.
Uphouse, L. L. (1980) · Psychological Bulletin · doi:10.1037//0033-2909.88.1.215 · Cited by 40 · see citing works
Inhibition of the Pituitary-Adrenal Response to Stress during Deprivation-Induced Feeding
Heybach, J. P., & Vernikos-Danellis, J. (1979) · Endocrinology · doi:10.1210/endo-104-4-967 · Cited by 38 · see citing works
Space or novelty?: Effects of altered cage size on Galago behavior
Nash, L. T., & Chilton, S. (1986) · American Journal of Primatology · doi:10.1002/ajp.1350100105 · Cited by 37 · see citing works
Effects of housing differences upon activity budgets in captive sifakas (Propithecus verreauxi)
Macedonia, J. M. (1987) · Zoo Biology · doi:10.1002/zoo.1430060107 · Cited by 32 · see citing works
Stress-Induced Behavior: Chemotherapy without Drugs
Antelman, S. M., & Caggiula, A. R. (1980) · Springer eBooks · doi:10.1007/978-1-4684-3456-9_4 · Cited by 31 · see citing works
Aggression in Captive Pigtail Monkey Groups: Effects of Provision of Cover
Erwin, J. M., Anderson, B., Erwin, N. A., Lewis, L., & Flynn, D. (1976) · Perceptual and Motor Skills · doi:10.2466/pms.1976.42.1.319 · Cited by 31 · see citing works
Differences in adaptive abilities of three breeds of Chinese pigs
Bluthé, R.-M., Mormède, P., Dantzer, R., & Caritez, J. C. (1984) · Applied Animal Behaviour Science · doi:10.1016/0168-1591(84)90069-8 · Cited by 25 · see citing works
Estep, D. Q., & Baker, S. C. (1991) · Zoo Biology · doi:10.1002/zoo.1430100605 · Cited by 22 · see citing works
Alpha-1- and Alpha-2-Noradrenergic Receptors Modulate Lordosis Behavior in Female Guinea Pigs
Vincent, P. A., & Feder, H. H. (2008) · Neuroendocrinology · doi:10.1159/000125052 · Cited by 17 · see citing works
Enriched sensory experience in adulthood increases subsequent exploratory behaviour in the rat
Inglis, I. (1975) · Animal Behaviour · doi:10.1016/0003-3472(75)90117-7 · Cited by 14 · see citing works
Environmental Psychology and Great Ape Reproduction
Maple, T. L. (1983) · WBI Studies Repository · Cited by 13 · see citing works
Harrangue, R. (1980) · Educational Horizons · Cited by 12 · see citing works
Breeding cheetahs: at Whipsnade Park
MANTON, V. J. A. (1970) · International Zoo Yearbook · doi:10.1111/j.1748-1090.1970.tb01289.x · Cited by 10 · see citing works
Fertility and artificial insemination in pigs.
Paredis, F. (1962) · PubMed · Cited by 9 · see citing works
Effect of transportation on sexual behavior of cats.
De, W. (1980) · PubMed · Cited by 6 · see citing works
Male dominance hierarchies and their possible effects upon breeding in cheetahs: Acinonyx jubatus
Benzon, T. A., & Smith, R. (1974) · International Zoo Yearbook · doi:10.1111/j.1748-1090.1974.tb00813.x · Cited by 5 · see citing works
O'Donoghue, E. R. (1982) · Zoo Biology · doi:10.1002/zoo.1430010210 · Cited by 5 · see citing works
Davis, D. G. (1963) · International Zoo Yearbook · doi:10.1111/j.1748-1090.1963.tb03621.x · Cited by 2 · see citing works
A survey and analysis of management practices in the North American Red Panda SSP
Roberts, M. (1989) · Smithsonian Digital Repository (Smithsonian Institution) · Cited by 1 · see citing works
Davis, D. G. (1962) · International Zoo Yearbook · doi:10.1111/j.1748-1090.1962.tb00046.x · Cited by 1 · see citing works
Flagged first, then by citations
2 of the 77 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Why and how should we use environmental enrichment to tackle stereotypic behaviour?
Mason, G. J., Clubb, R., Latham, N., & Vickery, S. S. (2006) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2006.05.041 · Cited by 607 · see citing works
Philosophy of environmental enrichment: Past, present, and future
Mellen, J. D., & Sevenich, M. (2001) · Zoo Biology · doi:10.1002/zoo.1021 · Cited by 367 · see citing works
Swaisgood, R. R., & Shepherdson, D. J. (2005) · Zoo Biology · doi:10.1002/zoo.20066 · Cited by 349 · see citing works
Self-citationAnimal domestication and behavior
(2002) · doi:10.1079/9780851995977.0000 · Cited by 288 · see citing works
Swaisgood, R. R. (2007) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2006.05.027 · Cited by 184 · see citing works
Carlstead, K., & Brown, J. L. (2005) · Zoo Biology · doi:10.1002/zoo.20050 · Cited by 176 · see citing works
Self-citationThe Value of Enrichment to Reintroduction Success
Reading, R. P., Miller, B. J., & Shepherdson, D. J. (2013) · Zoo Biology · doi:10.1002/zoo.21054 · Cited by 163 · see citing works
Self-citationExternal and internal influences on disease risk in cats
Buffington, C. A. T. (2002) · Journal of the American Veterinary Medical Association · doi:10.2460/javma.2002.220.994 · Cited by 162 · see citing works
Mallapur, A., Sinha, A., & Waran, N. (2005) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2005.02.012 · Cited by 152 · see citing works
To hunt or not to hunt? A feeding enrichment experiment with captive large felids
Bashaw, M. J., Bloomsmith, M. A., Marr, M., & Maple, T. L. (2003) · Zoo Biology · doi:10.1002/zoo.10065 · Cited by 138 · see citing works
Martin‐Wintle, M. S., Shepherdson, D. J., Zhang, G., Huang, Y., Luo, B., & Swaisgood, R. R. (2017) · Biological Conservation · doi:10.1016/j.biocon.2017.01.010 · Cited by 135 · see citing works
Self-citationEnrichment and aggression in primates
Honess, P. E., & Marin, C. M. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.05.002 · Cited by 128 · see citing works
Searching for behavioral indicators of welfare in zoos: Uncovering anticipatory behavior
Watters, J. V. (2014) · Zoo Biology · doi:10.1002/zoo.21144 · Cited by 120 · see citing works
Bassler, A., Arnould, C., Butterworth, A., Colin, L., de Jong, I. C., Ferrante, V., Ferrari, P., Haslam, S. M., Wemelsfelder, F., & Blokhuis, H. J. (2013) · Poultry Science · doi:10.3382/ps.2013-03208 · Cited by 120 · see citing works
A quantitative assessment of the efficacy of an environmental enrichment programme for giant pandas
Swaisgood, R. R., White, A. M., Zhou, X., Zhang, H., Zhang, G., Wei, R., Hare, V. J., Tepper, E. M., & Lindburg, D. G. (2001) · Animal Behaviour · doi:10.1006/anbe.2000.1610 · Cited by 119 · see citing works
Free mate choice enhances conservation breeding in the endangered giant panda
Martin-Wintle, M. S., Shepherdson, D., Zhang, G., Zhang, H., Li, D., Zhou, X., Li, R., & Swaisgood, R. R. (2015) · Nature Communications · doi:10.1038/ncomms10125 · Cited by 118 · see citing works
Self-citationThe Effects of Visitor Density and Intensity on the Behavior of Two Captive Jaguars (Panthera onca)
Sellinger, R. L., & Ha, J. C. (2005) · Journal of Applied Animal Welfare Science · doi:10.1207/s15327604jaws0804_1 · Cited by 108 · see citing works
Comparison of several types of enrichment for captive felids
Skibiel, A. L., Trevino, H. S., & Naugher, K. (2007) · Zoo Biology · doi:10.1002/zoo.20147 · Cited by 106 · see citing works
Mallapur, A., & Chellam, R. (2002) · Zoo Biology · doi:10.1002/zoo.10063 · Cited by 105 · see citing works
Enclosure choice and well-being in giant pandas: is it all about control?
Owen, M. A., Swaisgood, R. R., Czekala, N. M., & Lindburg, D. G. (2005) · Zoo Biology · doi:10.1002/zoo.20064 · Cited by 100 · see citing works
Fecal corticoid metabolite measurement in the cheetah (Acinonyx jubatus)
Jurke, M. H., Czekala, N. M., Lindburg, D. G., & Millard, S. E. (1997) · Zoo Biology · doi:10.1002/(sici)1098-2361(1997)16:2 · Cited by 94 · see citing works
Moreira, N., Brown, J. L., Moraes, W., Swanson, W. F., & Monteiro‐Filho, E. L. A. (2007) · Zoo Biology · doi:10.1002/zoo.20139 · Cited by 87 · see citing works
Brown, J. L., Paris, S., Prado-Oviedo, N. A., Meehan, C. L., Hogan, J. N., Morfeld, K. A., & Carlstead, K. (2016) · PLoS ONE · doi:10.1371/journal.pone.0145673 · Cited by 83 · see citing works
Self-citationAnimal Activity and Visitor Learning at the Zoo
Altman, J. D. (1998) · Anthrozoös · doi:10.1080/08927936.1998.11425083 · Cited by 80 · see citing works
Alligood, C. A., & Leighty, K. A. (2015) · Animal Behavior and Cognition · doi:10.12966/abc.08.01.2015 · Cited by 78 · see citing works
Use of behavior to evaluate reproductive problems in captive mammals
Lindburg, D. G., & Fitch‐Snyder, H. (1994) · Zoo Biology · doi:10.1002/zoo.1430130506 · Cited by 78 · see citing works
Piñeiro, A., Barja, I., Silván, G., & Illera, J. C. (2012) · Wildlife Research · doi:10.1071/wr10218 · Cited by 76 · see citing works
Cortisol analysis of hair of captive chimpanzees (Pan troglodytes)
Yamanashi, Y., Morimura, N., Mori, Y., Hayashi, M., & Suzuki, J. (2013) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2013.08.013 · Cited by 75 · see citing works
Behavioral Abnormalities in Captive Nonhuman Primates
Mallapur, A., & Choudhury, B. C. (2003) · Journal of Applied Animal Welfare Science · doi:10.1207/s15327604jaws0604_2 · Cited by 73 · see citing works
Is training zoo animals enriching?
Melfi, V. A. (2013) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2013.04.011 · Cited by 72 · see citing works
Keen, H. A., Nelson, O. L., Robbins, C. T., Evans, M. A., Shepherdson, D. J., & Newberry, R. C. (2013) · Animal Cognition · doi:10.1007/s10071-013-0684-1 · Cited by 69 · see citing works
Self-citationEnvironmentally Enriched Male Mink Gain More Copulations than Stereotypic, Barren-Reared Competitors
Díez‐León, M., Bowman, J., Bursian, S. J., Filion, H., Galicia, D., Kanefsky, J., Napolitano, A. C., Palme, R., Schulte‐Hostedde, A. I., Scribner, K. T., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0080494 · Cited by 65 · see citing works
The importance of chemical communication studies to mammalian conservation biology: A review
Campbell‐Palmer, R., & Rosell, F. (2011) · Biological Conservation · doi:10.1016/j.biocon.2011.04.028 · Cited by 64 · see citing works
Liu, J., Chen, Y., Guo, L., Gu, B., Liu, H., Hou, A., Liu, X., Sun, L., & Liu, D. (2006) · Zoo Biology · doi:10.1002/zoo.20106 · Cited by 64 · see citing works
Preliminary Evaluation of Environmental Enrichment Techniques for African Lions (Panthera leo)
Powell, D. (1995) · Animal Welfare · doi:10.1017/s0962728600018054 · Cited by 63 · see citing works
Effects of Foraging Enrichment on the Behaviour of Parrots
Coulton, L., Waran, N. K., & Young, R. J. (1997) · Animal Welfare · doi:10.1017/s0962728600020066 · Cited by 61 · see citing works
Behaviour-based husbandry—a holistic approach to the management of abnormal repetitive behaviors
Bacon, H. (2018) · Animals · doi:10.3390/ani8070103 · Cited by 57 · see citing works
Public Attitudes to Housing Systems for Pregnant Pigs
Ryan, E. B., Fraser, D., & Weary, D. M. (2015) · PLoS ONE · doi:10.1371/journal.pone.0141878 · Cited by 56 · see citing works
Preferences for toy types and presentations in kennel housed dogs
Pullen, A., Merrill, R. J. N., & Bradshaw, J. W. S. (2010) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2010.04.004 · Cited by 54 · see citing works
Yamanashi, Y., Teramoto, M., Morimura, N., Hirata, S., Suzuki, J., Hayashi, M., Kinoshita, K., Murayama, M., & Idani, G. (2016) · MethodsX · doi:10.1016/j.mex.2016.01.004 · Cited by 48 · see citing works
Yamanashi, Y., Teramoto, M., Morimura, N., Hirata, S., Inoue‐Murayama, M., & Idani, G. (2016) · PLoS ONE · doi:10.1371/journal.pone.0160029 · Cited by 47 · see citing works
Melfi, V. A., & Feistner, A. T. C. (2002) · Animal Welfare · doi:10.1017/s0962728600028165 · Cited by 46 · see citing works
Menargues, A., Uríos, V., & Mauri, M. F. (2008) · Animal Welfare · doi:10.1017/s096272860003222x · Cited by 46 · see citing works
Environmental enrichment for felids: an integrated approach
Mellen, J. D., & Shepherdson, D. J. (1997) · International Zoo Yearbook · doi:10.1111/j.1748-1090.1997.tb01209.x · Cited by 46 · see citing works
Self-citationCummings, D., Brown, J. L., Rodden, M. D., & Songsasen, N. (2007) · Zoo Biology · doi:10.1002/zoo.20138 · Cited by 46 · see citing works
Melfi, V. A., & Thomas, S. (2005) · Anthrozoös · doi:10.2752/089279305785594063 · Cited by 44 · see citing works
Swaisgood, R. R., Zhang, G., Zhou, X., & Zhang, H. (2006) · Cambridge University Press eBooks · doi:10.1017/cbo9780511542244.012 · Cited by 43 · see citing works
Role of familiarity and preference in reproductive success in ex situ breeding programs
MARTIN, M. S., & SHEPHERDSON, D. J. (2012) · Conservation Biology · doi:10.1111/j.1523-1739.2012.01880.x · Cited by 42 · see citing works
Self-citationStress, Well-Being and Reproductive Success
Edwards, K. L., Edes, A. N., & Brown, J. L. (2019) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-23633-5_5 · Cited by 43 · see citing works
The veterinary, behavioural and welfare implications of bear farming in Asia
Maas, B. (2000) · doi:10.13140/rg.2.2.29240.34561 · Cited by 41 · see citing works
Barja, I., Silván, G., Martínez-Fernández, L., & Illera, J. C. (2011) · Journal of Chemical Ecology · doi:10.1007/s10886-011-9928-1 · Cited by 39 · see citing works
Does simple feeding enrichment raise activity levels of captive ring-tailed lemurs (Lemur catta)?
Dishman, D. L., Thomson, D. M., & Karnovsky, N. J. (2008) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2008.06.012 · Cited by 38 · see citing works
Study on activity pattern and incidence of stereotypic behavior in captive tigers
Mohapatra, R. K., Panda, S., & Acharya, U. R. (2014) · Journal of Veterinary Behavior · doi:10.1016/j.jveb.2014.04.003 · Cited by 37 · see citing works
Commentary: Improving well‐being for captive giant pandas: Theoretical and practical issues
Swaisgood, R. R., Ellis, S., Forthman, D. L., & Shepherdson, D. J. (2003) · Zoo Biology · doi:10.1002/zoo.10111 · Cited by 36 · see citing works
Self-citationZhang, Z., Lin, W., Li, Y., Yuan, X., He, X., Zhao, H., Mo, J., Lin, J., Yang, L., Liang, B., et al. (2023) · Aquaculture · doi:10.1016/j.aquaculture.2023.739651 · Cited by 36 · see citing works
Food hiding and enrichment in captive Asian elephants
Wiedenmayer, C. P. (1998) · Applied Animal Behaviour Science · doi:10.1016/s0168-1591(97)00091-9 · Cited by 35 · see citing works
Meagher, R. K., Dallaire, J. A., Campbell, D. L. M., Ross, M., Møller, S. H., Hansen, S. W., Díez‐León, M., Palme, R., & Mason, G. J. (2014) · PLoS ONE · doi:10.1371/journal.pone.0110589 · Cited by 34 · see citing works
Burgener, N., Gusset, M., & Schmid, H. (2008) · Journal of Applied Animal Welfare Science · doi:10.1080/10888700701729254 · Cited by 32 · see citing works
Noninvasive reproductive monitoring in the okapi (Okapia johnstoni).
Schwarzenberger, F., Rietschel, W., Matern, B., Schaftenaar, W., Bircher, P., van Puijenbroeck, B., & Leus, K. (1999) · PubMed · Cited by 32 · see citing works
Delfour, F., Vaicekauskaite, R., García‐Párraga, D., Pilenga, C., Serres, A., Brasseur, I., Pascaud, A., Perlado-Campos, E., Contreras, G. J. S., Baumgartner, K., et al. (2021) · Animals · doi:10.3390/ani11061715 · Cited by 30 · see citing works
der Weyde, L. K. V., Martin, G. B., & Paris, M. C. J. (2015) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2015.12.022 · Cited by 29 · see citing works
Williams, E., Carter, A., Hall, C., & Bremner-Harrison, S. (2019) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2019.104876 · Cited by 26 · see citing works
Stereotypic behaviour predicts reproductive performance and litter sex ratio in giant pandas
Martin‐Wintle, M. S., Owen, M. A., Wintle, N. J. P., Zhang, G., Zhang, H., & Swaisgood, R. R. (2020) · Scientific Reports · doi:10.1038/s41598-020-63763-5 · Cited by 27 · see citing works
The effects of intrinsic enrichment on captive felids
Damasceno, J., Genaro, G., Quirke, T., McCarthy, S., McKeown, S., & O’Riordan, R. M. (2017) · Zoo Biology · doi:10.1002/zoo.21361 · Cited by 27 · see citing works
Analysis of factors that affect maternal behaviour and breeding success in great apes in captivity
ABELLO, M. T., & COLELL, M. (2006) · International Zoo Yearbook · doi:10.1111/j.1748-1090.2006.00323.x · Cited by 26 · see citing works
Hampson, M. C., & Schwitzer, C. (2016) · PLoS ONE · doi:10.1371/journal.pone.0155992 · Cited by 26 · see citing works
Assessment of stress in non-human primates: application of the neutrophil activation test
Honess, P. E., Marin, C., Brown, A., & Wolfensohn, S. (2005) · Animal Welfare · doi:10.1017/s0962728600029614 · Cited by 26 · see citing works
SULSER, C. E., Steck, B. L., & Baur, B. (2008) · International Zoo Yearbook · doi:10.1111/j.1748-1090.2007.00040.x · Cited by 25 · see citing works
Young Belugas Diversify Adult Beluga (Delphinapterus leucas) Behavior
Hill, H. M. M., Guarino, S., Crandall, S., Lenhart, E., & Dietrich, S. (2015) · Animal Behavior and Cognition · doi:10.12966/abc.08.06.2015 · Cited by 26 · see citing works
Capacity building for better animal welfare
Melfi, V. A., & Hosey, G. (2011) · International Zoo Yearbook · doi:10.1111/j.1748-1090.2011.00136.x · Cited by 25 · see citing works
Glaeser, S. S., Shepherdson, D., Lewis, K., Prado, N., Brown, J. L., Lee, B., & Wielebnowski, N. (2021) · Animals · doi:10.3390/ani11092566 · Cited by 24 · see citing works
Self-citationDíez‐León, M., & Mason, G. J. (2015) · Zoo Biology · doi:10.1002/zoo.21249 · Cited by 24 · see citing works
Hill, H. M. M., Campbell, C., Dalton, L., & Osborn, S. D. (2013) · Zoo Biology · doi:10.1002/zoo.21093 · Cited by 24 · see citing works
Are wild animals suited to a travelling circus life?
Iossa, G., Soulsbury, C. D., & Harris, S. (2009) · Animal Welfare · doi:10.1017/s0962728600000270 · Cited by 23 · see citing works
The role of animal‐based attractions in ecological sustainability
Shani, A., & Pizam, A. (2010) · Worldwide Hospitality and Tourism Themes · doi:10.1108/17554211011052212 · Cited by 23 · see citing works
Frumkin, N. B., Wey, T. W., Exnicios, M., Benham, C. K., Hinton, M. G., Lantz, S. M., Atherton, C., Forde, D., & Karubian, J. O. (2016) · Zoo Biology · doi:10.1002/zoo.21274 · Cited by 22 · see citing works
Effects of scent enrichment on behavioral and physiological indicators of stress in zoo primates
Vaglio, S., Kaburu, S., Pearce, R., Bryant, L., McAuley, A., Lott, A., Sheppard, D. J., Smith, S. B., Tompkins, B. E., Elwell, E. J., et al. (2021) · American Journal of Primatology · doi:10.1002/ajp.23247 · Cited by 23 · see citing works
Khonmee, J., Brown, J. L., Rojanasthien, S., Aunsusin, A., Thumasanukul, D., Kongphoemphun, A., Siriaroonrat, B., Tipkantha, W., Punyapornwithaya, V., & Thitaram, C. (2014) · PLoS ONE · doi:10.1371/journal.pone.0091633 · Cited by 22 · see citing works
Glass Panels and Peepholes: Nonhuman Animals and the Right to Privacy
Pepper, A. (2020) · Pacific philosophical quarterly · doi:10.1111/papq.12329 · Cited by 21 · see citing works
Scarlata, C. D., Elias, B. A., Godwin, J., Powell, R. A., Shepherdson, D. J., Shipley, L. A., & Brown, J. L. (2012) · Journal of Mammalogy · doi:10.1644/11-mamm-a-223.1 · Cited by 21 · see citing works
Self-citationSkovlund, C. R., Kirchner, M. K., Moos, L. W., Alsted, N., Manteca, X., Talló-Parra, O., Stelvig, M., & Forkman, B. (2021) · Animal Welfare · doi:10.7120/09627286.30.1.001 · Cited by 24 · see citing works
Swaisgood, R. R., White, A. M., Zhou, X., Zhang, G., & Lindburg, D. G. (2005) · Journal of comparative psychology · doi:10.1037/0735-7036.119.3.325 · Cited by 20 · see citing works
Effect of Wood-Pile Feeders on the Behaviour of Captive Bush Dogs (Speothos Venaticos)
Ings, R., Waran, N. K., & Young, R. J. (1997) · Animal Welfare · doi:10.1017/s0962728600019618 · Cited by 20 · see citing works
Eguizábal, G. V., Palme, R., Villarreal, D., Borgo, C. D., Rienzo, J. A. D., & Busso, J. M. (2013) · Zoo Biology · doi:10.1002/zoo.21100 · Cited by 17 · see citing works
Environmental enrichment for captive stumptail macaques (Macaca arctoides)
Márquez-Arias, A., Santillán‐Doherty, A. M., Arenas-Rosas, R. V., Gasca-Matías, M. P., & Muñóz-Delgado, J. (2009) · Journal of Medical Primatology · doi:10.1111/j.1600-0684.2009.00392.x · Cited by 17 · see citing works
An investigation of the auditory perception of western lowland gorillas in an enrichment study
Brooker, J. S. (2016) · Zoo Biology · doi:10.1002/zoo.21312 · Cited by 17 · see citing works
Ratite Conservation: Linking Captive-Release and Welfare
Navarro, J. L., & Martella, M. B. (2011) · Animal welfare · doi:10.1007/978-3-642-19297-5_11 · Cited by 17 · see citing works
Scarlata, C., Elias, B., Godwin, Jr., Powell, R., Shepherdson, D., Shipley, L., & Brown, J. (2013) · Animal Welfare · doi:10.7120/09627286.22.3.357 · Cited by 16 · see citing works
Self-citationChadwick, C. L. (2014) · University of Salford Institutional Repository (University of Salford) · Cited by 16 · see citing works
Damasceno, J. (2018) · Revista Brasileira de Zoociências · doi:10.34019/2596-3325.2018.v19.24748 · Cited by 15 · see citing works
A brief note on the effects of novel enrichment on an unwanted behaviour of captive bonobos
Csatádi, K., Leus, K., & Pereboom, Z. (2007) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2007.09.001 · Cited by 15 · see citing works
Bobcat (Lynx rufus) Breeding in Captivity: The Importance of Environmental Enrichment
Mollá, M. I., Quevedo, M. Á., & Castro, F. (2011) · Journal of Applied Animal Welfare Science · doi:10.1080/10888705.2011.551619 · Cited by 13 · see citing works
The effects of visitor density on sika deer<i>(Cervus nippon)</i>behaviour in Zhu-Yu-Wan Park, China
Shen-Jin, L., Todd, P., Yan, Y., Lin, Y., Hongmei, F., & Wan-Hong, W. (2010) · Animal Welfare · doi:10.1017/s0962728600001172 · Cited by 13 · see citing works
Duarte, A. C., Trujillo, F., & Superina, M. (2016) · Zoo Biology · doi:10.1002/zoo.21305 · Cited by 13 · see citing works
Chadwick, C. L., Rees, P. A., & Stevens‐Wood, B. (2013) · Zoo Biology · doi:10.1002/zoo.21085 · Cited by 12 · see citing works
Effects of Nearby Construction Work on the Behavior of Asiatic Lions (Panthera leo persica)
Williams, L. J., Finch, K., Agnew, R., & Holmes, L. (2021) · Journal of Zoological and Botanical Gardens · doi:10.3390/jzbg2010005 · Cited by 12 · see citing works
Reactions of nomadic and resident parrot species
Mettke‐Hofmann, C. (2000) · International Zoo Yearbook · doi:10.1111/j.1748-1090.2000.tb00730.x · Cited by 12 · see citing works
Hacker, C., Miller, L., & Schulte, B. (2018) · Animal Welfare · doi:10.7120/09627286.27.1.055 · Cited by 14 · see citing works
Evaluating stress and well-being in the giant panda: a system for monitoring
Swaisgood, R. R., Owen, M. A., Czekala, N. M., Mauroo, N. F., Hawk, K., & Tang, J. C. L. (2006) · Cambridge University Press eBooks · doi:10.1017/cbo9780511542244.013 · Cited by 11 · see citing works
Ncube, S. F., & Ndagurwa, H. G. T. (2010) · Current Zoology · doi:10.1093/czoolo/56.4.389 · Cited by 11 · see citing works
- Authors
- Carlstead, K., & Shepherdson, D.
- Affiliations
- Smithsonian Institution (US)
- Oregon Zoo (US)
- Corresponding author
- Carlstead, Kathy
- Venue
- Zoo Biology
- Publisher
- Wiley
- Published
- 1994-01
- Volume
- 13
- Issue
- 5
- Pages
- 447-458
- ISSN
- 0733-3188 (ISSN-L)
- 1098-2361
- OpenAlex
- W1991949166
- Cited by
- 202
- References
- 77
- Citations by year
- 2026: 5 · 2025: 5 · 2024: 10 · 2023: 10 · 2022: 5 · 2021: 14 · 2020: 8 · 2019: 2 · 2018: 7 · 2017: 4 · 2016: 11 · 2015: 11 · 2014: 10 · 2013: 12 · 2012: 10
- FWCI
- 7.00
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Zoo Biology (publishedVersion)
- Smithsonian Digital Repository (Smithsonian Institution) (submittedVersion)
- Topics
- Health Sciences › Veterinary › Small Animals › Animal Behavior and Welfare Studies
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
- Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
- Keywords
- environmental enrichment, reproductive success, captive animals, zoo animals, stress, arousal, social interaction, aggression, affiliative behavior, play behavior, reproductive physiology, reproductive behavior, captive breeding
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review