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Pacing polar bears and stoical sheep: testing ecological and evolutionary hypotheses about animal welfare

Published online by Cambridge University Press:  11 January 2023

R Clubb  and
G Mason
R Clubb
Affiliation:
Department of Zoology, University of Oxford, South Parks Road, Oxford OXI 3PS, UK
G Mason*
Affiliation:
Department of Zoology, University of Oxford, South Parks Road, Oxford OXI 3PS, UK
*
* Contact for correspondence and requests for reprints: Georgia.Mason@zoo.ox.ac.uk
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Abstract

Responses to potential threats to welfare vary greatly between species. Even closely related animals often differ in their fear of humans and/or novelty; their behavioural responses to pain; and when captive, their overall welfare and the form and frequency of their stereotypies. Such species differences stimulate hypotheses about I) the way that responses to challenge co-vary with other biological traits; 2) the adaptive value of particular responses; and 3) the factors predicting responses to evolutionarily new scenarios, such as captivity. We illustrate how these ideas can be statistically tested with multi-species comparisons, and show how techniques such as the Comparative Analysis of Independent Contrasts can be used to control for any non-independence of data points caused by species’ relatedness. For each of the three types of hypothesis, we then provide several welfare-relevant examples including one that has been fully tested (respectively, the relationships between sociality and anti-predator behaviour in antelopes; predation pressure, foraging niche and neophobia in parrots; and home range size and stereotypy in carnivores). Ultimate explanations such as these, based on species’ ecology and evolutionary history, have great explanatory appeal. Species comparisons can also have great practical value, allowing the test of hypotheses that would be almost impossible to investigate experimentally, and generating principles that allow predictions about the welfare of similar unstudied species. Multi-species data, for example from the many taxa held in zoos, thus hold enormous potential for increasing the fundamental understanding of animal welfare.

Keywords

animal welfarecomparative methodsecological nicheevolutionspecies differencesstereotypy
Type
Research Article
Information
Animal Welfare , Volume 13 , Issue S1: Science in the Service of Animal Welfare: Proceedings of the UFAW International Symposium, Edinburgh, 2-4 April 2003 , February 2004 , pp. S33 - S40
Copyright
© 2004 Universities Federation for Animal Welfare

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References

Barnes, R, Greene, K, Holland, J and Lamm, M 2002 Management and husbandry of duikers at the Los Angeles Zoo. Zoo Biology 21: 107–121CrossRefGoogle Scholar
Bateson, P 1991 Assessment of pain in animals. Animal Behaviour 42: 827–839CrossRefGoogle Scholar
Beauchamp, G 2002 Higher-level evolution of intraspecific flock-feeding in birds. Behavioral Ecology and Sociobiology 51: 480487CrossRefGoogle Scholar
Bininda-Emonds, O R P, Gittleman, J L and Purvis, A 1999 Building large phylogenies by combining phylogenetic information: a complete phylogeny of the extant Carnivora (Mammalia). Biological Sciences 74: 143–175Google ScholarPubMed
Björklund, M 1997 Are ‘comparative methods’ always necessary? Oikos 80: 607–612CrossRefGoogle Scholar
Blomberg, S P, Garland, T and Ives, A R 2003 Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57: 717–745Google ScholarPubMed
Brashares, J S, Garland, T and Arcese, P 2000 Phylogenetic analysis of coadaptation in behavior, diet, and body size in the African antelope. Behavioral Ecology 11: 452–463CrossRefGoogle Scholar
Broom, D M 1998 Welfare, stress, and the evolution of feelings. Advances in the Study of Behavior 27: 371–403CrossRefGoogle Scholar
Broom, D M 2001 Evolution of pain. In: Lord, Souls by and Morton, D (eds) International Congress and Symposium Series 246 pp 17–25. Royal Society of Medicine Press: London, UKGoogle Scholar
Cheverud, J M, Dow, M M and Leutenegger, W 1985 The quantitative assessment of phylogenetic constraints in comparative analyses: sexual dimorphism in body weight among primates. Evolution 39: 1335–1351CrossRefGoogle ScholarPubMed
Clarke, A S and Lindburg, D G 1993 Behavioral contrasts between male cynamolgus and lion-tailed macaques. American Journal of Primatology 29: 49–59CrossRefGoogle Scholar
Clarke, A S and Mason, W A 1988 Differences among three macaque species in responsiveness to an observer. International Journal of Primatology 9: 347–364CrossRefGoogle Scholar
Clarke, A S, Czekala, N M and Lindburg, DG 1995 Behavioural and adrenocortical responses of male cynomolgus and lion-tailed macaques to social stimulation and group formation. Primates 36: 41–56CrossRefGoogle Scholar
Clarke, A S, Mason, W A and Mendoza, S P 1994 Heart rate patterns under stress in three species of macaques. American Journal of Primatology 33: 133–148CrossRefGoogle ScholarPubMed
Clubb, R E 2001 The roles of foraging niche, rearing conditions and current husbandry on the development of stereotypies in carnivores. PhD Thesis, University of Oxford, UK.Google Scholar
Clubb, R and Mason, G 2003 Captivity effects on wide-ranging carnivores. Nature 425: 473–474CrossRefGoogle ScholarPubMed
Clutton-Brock, J 1999 A Natural History of Domesticated Mammals. Cambridge University Press: Cambridge, UKGoogle Scholar
Day, R L, Coe, R L, Kendal, J R and Laland, K N 2003 Neophilia, innovation and social learning: a study of intergeneric differences in callitrichid monkeys. Animal Behaviour 65: 559–571CrossRefGoogle Scholar
Degen, A A, Kam, M, Khokhlova, I S, Krasnov, B R and Barraclough T, G 1998 Average daily metabolic rate of rodents: habitat and dietary comparisons. Functional Ecology 12: 63–73CrossRefGoogle Scholar
Diamond, J 1997 Guns, Germs, and Steel: the Fates of Human Societies. W W Norton and Company: London, UKGoogle Scholar
Dittrich, L 1976 Food presentation in relation to behaviour in ungulates. International Zoo Yearbook 66: 48–54CrossRefGoogle Scholar
Ebensperger, L A and Cofré, H 2001 On the evolution of group-living in the New World cursorial hystricognath rodents. Behavioral Ecology 12: 227–236CrossRefGoogle Scholar
Felsenstein, J 1985 Phylogenies and the comparative method. American Naturalist 125: 1–15CrossRefGoogle Scholar
Forbis T, A, Floyd, S K and de Queiroz, A 2002 The evolution of embryo size in angiosperms and other seed plants: implications for the evolution of seed dormancy. Evolution 56: 2112–2125Google ScholarPubMed
Forthman-Quick, D L 1984 An integrative approach to environmental enrichment. Zoo Biology 3: 65–77CrossRefGoogle Scholar
Freckleton, R P, Harvey, P H and Pagel, M 2002 Phylogenetic analysis and comparative data: a test and review of evidence. American Naturalist 160: 712–726CrossRefGoogle Scholar
Gage, M J G and Freckleton, R P 2003 Relative testis size and sperm morphometry across mammals: no evidence for an association between sperm competition and sperm length. Proceedings of the Royal Society of London, Series B, Biological Sciences 270: 625–632CrossRefGoogle ScholarPubMed
Garland, T and Diaz-Uriarte, R 1999 Polytomies and phylogenetically independent contrasts: examination of the bounded degrees of freedom approach. Systematic Biology 48: 547–558CrossRefGoogle ScholarPubMed
Garner, J P, Mason, G J and Smith, R 2003 Stereotypic route-tracing in experimentally caged songbirds correlates with general behaviour disinhibition. Animal Behaviour 66: 711–727CrossRefGoogle Scholar
Ginsberg, J R and Macdonald, D W 1990 Foxes, Wolves, Jackals and Dogs: an Action Plan for the Conservation of Canids. International Union for the Conservation of Nature and Natural Resources (IUCN): Gland, SwitzerlandGoogle Scholar
Gittleman, J L 1989 The comparative approach in ethology: aims and limitations. In: Bateson, P P G and Klopfer, P H (eds) Perspectives in Ethology 8 pp 55–76. Plenum Press: New York, USAGoogle Scholar
Gittleman, J L and Luh, H-K 1992 On comparing comparative methods. Annual Review of Ecology and Systematics 23: 383–404CrossRefGoogle Scholar
Gittleman, J L and Purvis, A 1998 Body size and species-richness in carnivores and primates. Proceedings of the Royal Society of London, Series B, Biological Sciences 265: 113–119CrossRefGoogle ScholarPubMed
Glickman, S E and Hartz, K E 1964 Exploratory behavior in several species of rodents. Journal of Comparative and Physiological Psychology 58: 101–104CrossRefGoogle ScholarPubMed
Glickman, S E and Sroges, R W 1966 Curiosity in zoo animals. Behaviour 26: 151–188CrossRefGoogle ScholarPubMed
Grafen, A 1989 The phylogenetic regression. Philosophical Transactions of the Royal Society of London 326: 119–156Google ScholarPubMed
Grafen, A and Ridley, M 1996 Statistical tests for discrete cross-species data. Journal of Theoretical Biology 183: 255–267CrossRefGoogle Scholar
Greenberg, R 1990 Novelty responses: the bridge between psychology, behavioral ecology and community ecology. Trends in Ecology and Evolution 10: 165–166CrossRefGoogle Scholar
Harvey, P H and Clutton-Brock T, H 1985 Life history variation in primates. Evolution 39: 559–581CrossRefGoogle ScholarPubMed
Harvey, P H and Pagel, M D 1991 The Comparative Method in Evolutionary Biology. Oxford University Press: Oxford, UKGoogle Scholar
Hedenstrom, A and Rosen, M 2001 Predator versus prey: on aerial hunting and escape strategies in birds. Behavioral Ecology 12: 150–156CrossRefGoogle Scholar
Hediger, H 1950 Wild Animals in Captivity. Butterworths: London, UKGoogle Scholar
Leal, M 2000 Avoiding versus confronting the predator: endurance capacity influences escape tactics in Anolis lizards. Proceedings of the 37th Annual Meeting of the Animal Behaviour Society, August 5-9, Morehouse College and Zoo Atlanta, Atlanta, Georgia, USA. Abstract available at: http://www.animalbehavior.org/ABS/Program/Past/Morehouse_00/absAL.html.Google Scholar
Martins, E P and Hansen T, F 1996 The statistical analysis of interspecific data: a review and evaluation of phylogenetic comparative methods. In: Martins, E P (ed) Phylogenies and the Comparative Method in Animal Behavior pp 22–75. Oxford University Press: Oxford, UKGoogle Scholar
Mason, G, Cooper, J and Clarebrough, C 2001 Frustrations of fur-farmed mink. Nature 410: 35–36CrossRefGoogle ScholarPubMed
Mason, G J 1993a Age and context affect the stereotypies of caged mink. Behaviour 127: 191–229CrossRefGoogle Scholar
Mason, G J 1993b Forms of stereotypic behaviour. In: Lawrence, A B and Rushen, J (eds) Stereotypic Animal Behaviour: Fundamentals and Applications to Welfare pp 7–40. CAB International: Wallingford, UKGoogle Scholar
Mason, G J and Mendl, M 1997 Do the stereotypies of pigs, chickens and mink reflect adaptive species differences in the control of foraging? Applied Animal Behaviour Science 53: 45–58CrossRefGoogle Scholar
Mellen, J D, Wildt, D E and Shoemaker, A 2000 AAZPA Felid Taxon Advisory Group Regional Collection Plan 2000-2002. Disney's Animal Kingdom: Lake Buena Vista, Florida, USAGoogle Scholar
Mendoza, S P and Mason, W A 1997 Autonomic balance in Saimiri sciureus and Callicebus moloch: relation to life-style. Folia Primatology 68: 307–318CrossRefGoogle ScholarPubMed
Mettke-Hofmann, C, Winkler, H and Leisler, B 2002 The significance of ecological factors for exploration and neophobia in parrots. Ethology 108: 249–272CrossRefGoogle Scholar
Meyer-Holzapfel, M 1968 Abnormal behaviour in zoo animals. In: Fox, M W (ed) Abnormal Behaviour in Animals pp 476–503. W B Saunders: London, UKGoogle Scholar
Mooney, J C and Lee, P C 1999 Reproductive parameters in captive woolly monkeys (Lagothrix lagotricha). Zoo Biology 18: 421–4273.0.CO;2-6>CrossRefGoogle Scholar
Morris, D 1964 The response of animals to a restricted environment. In: Edholm, O G (ed) The Biology of Survival: Symposia of the Zoological Society of London No. 13 pp 99–120. Zoological Society of London: London, UKGoogle Scholar
Morrow, E H, Pitcher T, E and Arnqvist, G 2003 No evidence that sexual selection is an ‘engine of speciation’ in birds. Ecology Letters 6: 228–234CrossRefGoogle Scholar
Nowell, K and Jackson, P 1996 Wild Cats: Status Survey and Conservation Action Plan. International Union for the Conservation of Nature and Natural Resources (IUCN): Cambridge, UKGoogle Scholar
Nunn, C L, Gittleman, J L and Antonovics, J 2000 Promiscuity and the primate immune system. Science 290: 1168–1170CrossRefGoogle ScholarPubMed
O'Reilly, K M and Wingfield, J C 2001 Ecological factors underlying the adrenocortical response to capture stress in Arctic-breeding shorebirds. General and Comparative Endocrinology 124: 1–11CrossRefGoogle ScholarPubMed
Ormrod, S A 1987 The welfare of animals in captivity. In: Gibson, T E (ed) Proceedings of the Animal Welfare Foundation's 4th Symposium pp 22–27. British Veterinary Association Animal Welfare Foundation: London, UKGoogle Scholar
Pagel, M 1994 Detecting correlated evolution on phylogenies — a general method for the comparative analysis of discrete characters. Proceedings of the Royal Society of London, Series B, Biological Sciences 255: 37–45Google Scholar
Pagel, M 1997 Inferring evolutionary processes from phylogenies. Zoologica Scripta 26: 331–348CrossRefGoogle Scholar
Pagel, M 1999 Inferring the historical pattern of biological evolution. Nature 401: 877–884CrossRefGoogle ScholarPubMed
Pagel, M D 1992 A method for the analysis of comparative data. Journal of Theoretical Biology 156: 431–442CrossRefGoogle Scholar
Pedersen, V and Jeppesen, L L 1998 Different cage sizes and effects of behaviour and physiology in farmed and blue foxes. Scientifur 22: 13–21Google Scholar
Pérez-Barbéria, F J, Gordon, I J and Illius, A W 2001 Phylogenetic analysis of stomach adaptation in digestive strategies in African ruminants. Oecologia 129: 498–508CrossRefGoogle ScholarPubMed
Petter, J J 1975 Breeding of Malagasy lemurs in captivity. In: Martin, R D (ed) Breeding Endangered Species in Captivity pp 187–202. Academic Press: London, UKGoogle Scholar
Portugal, M M and Asa, C S 1995 Effects of chronic melengestrol acetate contraceptive treatment on perineal tumescence, body weight, and sociosexual behavior on hamadryas baboons (Papio hamadryas). Zoo Biology 14: 251–259CrossRefGoogle Scholar
Prescott, M J and Buchanan-Smith, H M 2004 Cage sizes for tamarins in the laboratory. Animal Welfare 13: in pressGoogle Scholar
Price, T 1997 Correlated evolution and independent contrasts. Philosophical Transactions of the Royal Society of London 352: 519–529CrossRefGoogle ScholarPubMed
Primack, R B 1998 Essentials of Conservation Biology. Sinauer Associates: Sunderland, Massachusetts, USAGoogle Scholar
Purvis, A 1995 A composite estimate of primate phylogeny. Philosophical Transactions of the Royal Society of London 348: 405–421Google ScholarPubMed
Purvis, A and Rambaut, A 1995 Comparative analysis of independent contrasts (CAIC): an Apple MacIntosh application for analysing comparative data. Computer Applications in the Biosciences 11: 247–251Google ScholarPubMed
Purvis, A and Webster, A J 1999 Phylogenetically independent comparisons and primate phylogeny. In: Lee, P (ed) Comparative Primate Socioecology pp 44–68. Cambridge University Press: Cambridge, UKCrossRefGoogle Scholar
Purvis, A, Gittleman, J L, Cowlishaw, G and Mace, G M 2000 Predicting extinction risk in declining species. Proceedings of the Royal Society of London, Series B, Biological Sciences 267: 1947–1952CrossRefGoogle ScholarPubMed
Rohlf, F J 2001 Comparative methods for the analysis of continuous variables: geometric interpretations. Evolution 55: 2143–2160Google ScholarPubMed
Ruggiero, A and Lawton, J H 1998 Are there latitudinal and altitudinal Rapoport effects in the geographic ranges of Andean passerine birds. Biological Journal of the Linnean Society 63: 283304CrossRefGoogle Scholar
Rushen, J and Congdon, P 1987 Electro-immobilization of sheep may not reduce aversiveness of a painful treatment. Veterinary Record 120: 37–38CrossRefGoogle Scholar
Sambraus, H H 1985 Mouth-based anomalous syndromes. In: Fraser, A F (ed) Ethology in Farm Animals pp 391–422. Elsevier: Amsterdam, The NetherlandsGoogle Scholar
Savage, A, Zirofsky, D S, Shideler, S E, Smith T, E and Lasley, B L 2002 Use of levonorgestrel as an effective means of contraception in the white-faced saki (Pithecia pithecia). Zoo Biology 21: 49–57CrossRefGoogle Scholar
Shepherdson, D J, Mellen, J D and Hutchins, M 1998 Second Nature: Environmental Enrichment for Captive Animals. Zoo and Aquarium Biology and Conservation Series. Smithsonian Institution Press: Washington, USAGoogle Scholar
Sol, D, Timmermans, S and Lefebvre, L 2002 Behavioural flexibility and invasion success in birds. Animal Behaviour 63: 495–502CrossRefGoogle Scholar
Stearns, S C 1983 The influence of size and phylogeny on patterns of covariation among life-history traits in mammals. Oikos 41: 173–187CrossRefGoogle Scholar
Terlouw EM, C, Lawrence, A B and Illius, A W 1991 Influences of feeding level and physical restriction on development of stereotypies in sows. Animal Behaviour 42: 981–991CrossRefGoogle Scholar
van Hoek, C S and ten Cate, C 1998 Abnormal behavior in caged birds kept as pets. Journal of Applied Animal Welfare Science 1: 51–64CrossRefGoogle ScholarPubMed
Vitale, A F, Visaberghi, E and De Lilli, C 1991 Responses to a snake model in captive crab-eating macaques (Macaca fascicularis) and captive tufted capuchins (Cenus apella). International Journal of Primatology 12: 277–286CrossRefGoogle Scholar
Wingfield, J C, O'Reilly, K M and Astheimer, A B 1995 Modulation of the adrenocortical response to acute stress in Arctic birds — a possible ecological basis. American Zoologist 35: 285–294CrossRefGoogle Scholar
Wingfield, J C, Vleck, C M and Moore, M C 1992 Seasonal changes of the adrenocortical response to stress in birds of the Sonoran desert. The Journal of Experimental Zoology 264: 419–428CrossRefGoogle ScholarPubMed
Wolf, M C, Garland, T and Griffith, B 1998 Predictors of avian and mammalian translocation success: reanalysis with phylogenetic independent contrasts. Biological Conservation 86: 243–255CrossRefGoogle Scholar
Woodroffe, R and Ginsberg, J R 1998 Edge effects and the extinction of populations inside protected areas. Science 280: 2126–2128CrossRefGoogle ScholarPubMed