Hostname: page-component-78c5997874-fbnjt Total loading time: 0 Render date: 2024-11-20T00:46:51.698Z Has data issue: false hasContentIssue false

A critical review of animal-based welfare indicators for polar bears (Ursus maritimus) in zoos: Identification and evidence of validity

Published online by Cambridge University Press:  01 January 2023

CR Skovlund*
Affiliation:
Research and Conservation, Copenhagen Zoo, Roskildevej 38, 2000 Frederiksberg, Denmark Section of Animal Welfare and Disease Control, Department of Veterinary and Animal Sciences, University of Copenhagen, Groennegaardsvej 8, 1870 Frederiksberg C, Denmark
MK Kirchner
Affiliation:
Section of Animal Welfare and Disease Control, Department of Veterinary and Animal Sciences, University of Copenhagen, Groennegaardsvej 8, 1870 Frederiksberg C, Denmark
LW Moos
Affiliation:
Section of Animal Welfare and Disease Control, Department of Veterinary and Animal Sciences, University of Copenhagen, Groennegaardsvej 8, 1870 Frederiksberg C, Denmark
N Alsted
Affiliation:
Section of Animal Welfare and Disease Control, Department of Veterinary and Animal Sciences, University of Copenhagen, Groennegaardsvej 8, 1870 Frederiksberg C, Denmark
X Manteca
Affiliation:
Zoo Animal Welfare Education Centre (ZAWEC), Veterinary Faculty, Universitat Autònoma de Barcelona, 08193 Bellaterra (Barcelona), Spain
O Tallo-Parra
Affiliation:
Zoo Animal Welfare Education Centre (ZAWEC), Veterinary Faculty, Universitat Autònoma de Barcelona, 08193 Bellaterra (Barcelona), Spain
M Stelvig
Affiliation:
Research and Conservation, Copenhagen Zoo, Roskildevej 38, 2000 Frederiksberg, Denmark
B Forkman
Affiliation:
Section of Animal Welfare and Disease Control, Department of Veterinary and Animal Sciences, University of Copenhagen, Groennegaardsvej 8, 1870 Frederiksberg C, Denmark
*
* Contact for correspondence: [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.

Captive polar bears (Ursus maritimus) are well-documented as being prone to behavioural disorders and, as a result, their welfare is the cause of increasing concern. There is therefore a need for an evidence-based approach to the assessment of the welfare of this species and identification of valid welfare indicators is the first step towards achieving this. To this end, a critical evaluation of peer-reviewed literature was undertaken. Searches of Web of Science and Scopus took place in May 2020 for publications relevant to the welfare of captive polar bears which met inclusion criteria. Further, validity of extracted indicators was assessed via investigation of evidence of content, construct and criterion validity along with strength of evidence at publication-level. Database searches and snowballing unearthed 46 publications included for review. Identified indicators were sorted into nine behavioural, four physiological (based on physiological or biological sampling) and five physical (based on visual inspection) categories. Among behavioural indicators, the strongest evidence of validity was found for abnormal behaviour. For the physiological indicators, validity was only established for faecal glucocorticoid metabolite concentration. Content validity was assumed for all physical indicators. Generalisability and strength of evidence was generally compromised by low sample sizes and experimental limitations, and only a small number of papers investigated welfare indicators directly, resulting in a paucity of validated indicators. Potential welfare indicators that warrant further validation are highlighted. Overall, this review provides an overview of current valid and promising welfare indicators along with identified gaps in knowledge, relevant for the provision of a methodology for assessing and monitoring welfare of captive polar bears.

Type
Research Article
Creative Commons
Creative Common License - CCCreative Common License - BY
This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited.
Copyright
© The Author(s), 2023. Published by Cambridge University Press on behalf of The Universities Federation for Animal Welfare

References

Alroy, J, Baldwin, D and Maschgan, ER 1980 Multiple beta cell neoplasms in a polar bear: An immunohistochemical study. Veterinary Pathology 17: 331337. https://doi.org/10.1177/030098588001700307CrossRefGoogle Scholar
Altman, JD 1999 Effects of inedible, manipulable objects on captive bears. Journal of Applied Animal Welfare Science 2: 123132. https://doi.org/10.1207/s15327604jaws0202_4CrossRefGoogle ScholarPubMed
Ames, A 1993 The behaviour of captive polar bears. UFAW Animal Welfare Research Report No 5 pp 67. UFAW: Wheathampstead, UKGoogle Scholar
AZA Bear, TAG 2009 Polar Bear (Ursus maritimus) Care Manual. Association of Zoos and Aquariums, Silver Spring, MD, USAGoogle Scholar
Bechsh⊘ft, T, Rigét, FF, Sonne, C, Letcher, RJ, Muir, DCG, Novak, MA, Henchey, E, Meyer, JS, Eulaers, I, Jaspers, VLB, Eens, M, Covaci, A and Dietz, R 2012 Measuring environmen-tal stress in East Greenland polar bears, 1892-1927 and 1988-2009: What does hair cortisol tell us? Environment International 45:1521. https://doi.org/10.1016/j.envint.2012.04.005CrossRefGoogle Scholar
Bechsh⊘ft, T, Sonne, C, Dietz, R, Born, EW, Novak, MA, Henchey, E and Meyer, JS 2011 Cortisol levels in hair of East Greenland polar bears. Science of the Total Environment 409: 831834. https://doi.org/10.1016/j.scitotenv.2010.10.047CrossRefGoogle Scholar
Belshaw, Z, Asher, L, Harvey, ND and Dean, RS 2015 Quality of life assessment in domestic dogs: An evidence-based rapid review. Veterinary Journal206: 203-212. https://doi.org/10.1016/j.tvjl.2015.07.016CrossRefGoogle Scholar
Benn, AL, McLelland, DJ and Whittaker, AL 2019 A review of welfare assessment methods in reptiles, and preliminary appli-cation of the Welfare Quality® protocol to the pygmy blue-tongue skink, Tiliqua adelaidensis, using animal-based measures. Animals 9: 122. https://doi.org/10.3390/ani9010027CrossRefGoogle Scholar
Bourne, DC, Cracknell, JM and Bacon, HJ 2010 Veterinary issues related to bears (Ursidae). International Zoo Yearbook 44: 1632. https://doi.org/10.1111/j.1748-1090.2009.00097.xCrossRefGoogle Scholar
Bowen, L, Keith Miles, A, Stott, J, Waters, S and Atwood, T 2015 Enhanced biological processes associated with alopecia in polar bears (Ursus maritimus). Science of the Total Environment 529:114120. https://doi.org/10.1016/j.scitotenv.2015.05.039CrossRefGoogle ScholarPubMed
Brando, S, Broom, DM, Acasuso-Rivero, C and Clark, F 2018 Optimal marine mammal welfare under human care: Current efforts and future directions. Behavioural Processes 156:1636. https://doi.org/10.1016/j.beproc.2017.09.011CrossRefGoogle ScholarPubMed
Broom, DM 1986 Indicators of poor welfare. British Veterinary Journal 142: 524526. https://doi.org/10.1016/0007-1935(86)90109-0CrossRefGoogle ScholarPubMed
Bryant, JL and Roth, TL 2018 Annual faecal glucocorticoid metabolite concentrations in pregnant and pseudopregnant polar bears (Ursus maritimus) in North American zoos. Journal of Zoo and Aquarium Research 6: 611Google Scholar
Byrne, G and Suomi, SJ 2002 Cortisol reactivity and its relation to home-cage behavior and personality ratings in tufted capuchin (Cebus apella) juveniles from birth to six years of age. Psychoneuroendocrinology 27: 139154. https://doi.org/10.1016/S0306-4530(01)00041-5CrossRefGoogle ScholarPubMed
Cabib, S 2006 The neurobiology of stereotypy II: The role of stress. In: Mason, G and Rushen, J (eds) Stereotypic Animal Behaviour: Fundamentals and Applications to Welfare Welfare, Second Edition pp 227255. CABI: Wallingford, Oxford, UK. https://doi.org/10.1079/9780851990040.0227CrossRefGoogle Scholar
Cameron, EZ and Ryan, SJ 2016 Welfare at multiple scales: Importance of zoo elephant population welfare in a world of declining wild populations. PLoS One 11: e0158701. https://doi.org/10.1371/journal.pone.0158701CrossRefGoogle Scholar
Canino, W and Powell, D 2010 Formal behavioral evaluation of enrichment programs on a zookeeper's schedule: A case study with a polar bear (Ursus maritimus) at the Bronx Zoo. Zoo Biology 29: 503508. https://doi.org/10.1002/zoo.20247Google ScholarPubMed
Carlstead, K, Fraser, J, Bennett, C and Kleiman, DG 1999 Black rhinoceros (Diceros bicornis) in US zoos: II. Behavior, breeding success, and mortality in relation to housing facilities. Zoo Biology 18: 3552. https://doi.org/10.1002/(SICI)1098-2361(1999)18:1<35::AID-ZOO5>3.0.CO;2-L3.0.CO;2-L>CrossRefGoogle Scholar
Carlstead, K, Seidensticker, J and Baldwin, R 1991 Environmental enrichment for zoo bears. Zoo Biology 10: 316. https://doi.org/10.1002/zoo.1430100103CrossRefGoogle Scholar
Carlstead, K and Shepherdson, D 1994 Effects of environmen-tal enrichment on reproduction. Zoo Biology 13: 447458. https://doi.org/10.1002/zoo.1430130507CrossRefGoogle Scholar
Catapani, ML, Pires, JSR and Vasconcellos, AS 2019 Single-or pair-housed: Which is better for captive southern tamanduas? Journal of Applied Animal Welfare Science 22: 289297. https://doi.org/10.1080/10888705.2018.1508352CrossRefGoogle ScholarPubMed
Clegg, ILK, Borger-Turner, JL and Eskelinen, HC 2015 C-Well: The development of a welfare assessment index for captive bottlenose dolphins (Tursiops truncatus). Animal Welfare 24: 267282. https://doi.org/10.7120/09627286.24.3.267CrossRefGoogle Scholar
Cless, IT and Lukas, KE 2017 Variables affecting the manifestation of and intensity of pacing behavior: A preliminary case study in zoo-housed polar bears. Zoo Biology 36: 307315. https://doi.org/10.1002/zoo.21379CrossRefGoogle ScholarPubMed
Cless, IT, Voss-Hoynes, HA, Ritzmann, RE and Lukas, KE 2015 Defining pacing quantitatively: A comparison of gait charac-teristics between pacing and non-repetitive locomotion in zoo-housed polar bears. Applied Animal Behaviour Science 169: 7885. https://doi.org/10.1016/j.applanim.2015.04.002CrossRefGoogle Scholar
Cohen, E and Fennell, D 2016 The elimination of Marius, the giraffe: Humanitarian act or callous management decision? Tourism Recreation Research 41: 168176. https://doi.org/10.1080/02508281.2016.1147211CrossRefGoogle Scholar
Cremers, PW and Geutjes, SL 2012 The cause of stereotypic behaviour in a male polar bear (Ursus maritimus). In: Spink, AJ, Grieco, F, Krips, OE, Loijens, LWS and Noldus, PHZ (eds) Proceedings of Measuring Behavior pp 338340. 28-31 August 2012, Utrecht, The NetherlandsGoogle Scholar
Curry, E, Safayi, S, Meyerson, R and Roth, TL 2015 Reproductive trends of captive polar bears in North American zoos: A historical analysis. Journal of Zoo and Aquarium Research 3: 99106Google Scholar
Dawkins, MS 1998 Evolution and animal welfare. The Quarterly Review of Biology 73: 305328. https://doi.org/10.1086/420307CrossRefGoogle ScholarPubMed
Dawkins, MS 2007 Observing Animal Behaviour: Design and Analysis of Quantitative Data. Oxford University Press: Oxford, UK10.1093/acprof:oso/9780198569350.001.0001CrossRefGoogle Scholar
Demaster, BDP and Stirling, I 1981 Ursus maritimus. Mammalian Species 145: 17. https://doi.org/10.2307/3503828CrossRefGoogle Scholar
Derocher, AE and Stirling, I 1990 Observations of aggregating behaviour in adult male polar bears (Ursus maritimus). Canadian Journal of Zoology 68: 13901394. https://doi.org/10.1139/z90-207CrossRefGoogle Scholar
Duncan, IJ and Petherick, JC 1991 The implications of cognitive processes for animal welfare. Journal of Animal Science 69: 50175022. https://doi.org/10.2527/1991.69125017xCrossRefGoogle ScholarPubMed
Eo, KY and Kwon, OD 2014 Dermatitis caused by Dermatophilus congolensis in a zoo polar bear (Ursus maritimus). Pakistan Veterinary Journal 34: 560562Google Scholar
Folk, GE, Berberich, JJ and Sanders, DK 1973 Bradycardia of the polar bear. Arctic 26: 7879. https://doi.org/10.14430/arctic2900Google Scholar
Forthman, DL, Elder, SD, Bakeman, R, Kurkowski, TW, Noble, CC and Winslow, SW 1992 Effects of feeding enrich-ment on behavior of three species of captive bears. Zoo Biology 11:187195. https://doi.org/10.1002/zoo.1430110307CrossRefGoogle Scholar
Fureix, C and Meagher, RK 2015 What can inactivity (in its var-ious forms) reveal about affective states in non-human animals? A review. Applied Animal Behaviour Science 171: 824. https://doi.org/10.1016/j.applanim.2015.08.036CrossRefGoogle Scholar
Garner, JP 2005 Stereotypies and other abnormal repetitive behaviors: Potential impact on validity, reliability, and replicability of scientific outcomes. ILAR Journal 46: 106117. https://doi.org/10.1093/ilar.46.2.106CrossRefGoogle ScholarPubMed
Hamilton, SG and Derocher, AE 2019 Assessment of global polar bear abundance and vulnerability. Animal Conservation 22:8395. https://doi.org/10.1111/acv.12439CrossRefGoogle Scholar
Harvey, ND, Moesta, A, Kappel, S, Wongsaengchan, C, Harris, H, Craigon, PJ and Fureix, C 2019 Could greater time spent displaying waking inactivity in the home environment be a marker for a depression-like state in the domestic dog? Animals 9:119. https://doi.org/10.3390/ani9070420CrossRefGoogle Scholar
Hein, A, Palme, R, Baumgartner, K, von Fersen, L, Woelfing, B, Greenwood, AD, Bechshoft, T and Siebert, U 2020 Faecal glucocorticoid metabolites as a measure of adreno-cortical activity in polar bears (Ursus maritimus). Conservation Physiology 8: 116. https://doi.org/10.1093/conphys/coaa012CrossRefGoogle Scholar
Hill, SP and Broom, DM 2009 Measuring zoo animal welfare: Theory and practice. Zoo Biology 28: 531544. https://doi.org/10.1002/zoo.20276Google ScholarPubMed
Holdgate, MR, Meehan, CL, Hogan, JN, Miller, LJ, Soltis, J, Andrews, J and Shepherdson, DJ 2016 Walking behavior of zoo elephants: Associations between GPS-measured daily walking distances and environmental factors, social factors, and welfare indicators. PLoS One 11: 117. https://doi.org/10.1371/journal.pone.0150331CrossRefGoogle ScholarPubMed
Joyce-Zuniga, NM, Newberry, RC, Robbins, CT, Ware, JV, Jansen, HT and Nelson, OL 2016 Positive reinforcement training for blood collection in grizzly bears (Ursus arctos horribilis) results in undetectable elevations in serum cortisol levels: A pre-liminary investigation. Journal of Applied Animal Welfare Science 19:210215. https://doi.org/10.1080/10888705.2015.1126523CrossRefGoogle Scholar
Kelly, KR, Harrison, ML, Size, DD and MacDonald, SE 2014 Individual effects of seasonal changes, visitor density, and concur-rent bear behavior on stereotypical behaviors in captive polar bears (Ursus maritimus). Journal of Applied Animal Welfare Science 18: 115. https://doi.org/10.1080/10888705.2014.924832Google Scholar
Kenny, DE, Irlbeck, NA, Chen, TC, Lu, Z and Holick, MF 1998 Determination of vitamins D, A, and E in sera and vitamin D in milk from captive and free-ranging polar bears (Ursus maritimus), and 7-dehydrocholesterol levels in skin from captive polar bears. Zoo Biology 17: 285293. https://doi.org/10.1002/(SICI)1098-2361(1998)17:4<285::AID-ZOO3>3.0.CO;2-53.0.CO;2-5>CrossRefGoogle Scholar
Kikusui, T, Winslow, JT and Mori, Y 2006 Social buffering: Relief from stress and anxiety. Philosophical Transactions of the Royal Society B: Biological Sciences 361: 22152228. https://doi.org/10.1098/rstb.2006.1941CrossRefGoogle ScholarPubMed
Kitchener, AC 2004 The problems of old bears in zoos. International Zoo News 51: 282293Google Scholar
Knierim, U and Winckler, C 2009 On-farm welfare assessment in cattle: Validity, reliability and feasibility issues and future per-spectives with special regard to the Welfare Quality® approach. Animal Welfare 18: 45145810.1017/S0962728600000865CrossRefGoogle Scholar
Koene, P 1998 Adaptation of blind brown bears to a new envi-ronment and its residents: Stereotypy and play as welfare indica-tors. Ursus 10: 579587Google Scholar
Krebs, BL, Marrin, D, Phelps, A, Krol, L and Watters, JV 2018 Managing aged animals in zoos to promote positive welfare: A review and future directions. Animals 8: 122. https://doi.org/10.3390/ani8070116CrossRefGoogle ScholarPubMed
Kuczaj, S, Thad Lacinak, OF and Trone, M 2002 Keeping envi-ronmental enrichment enriching. International Journal of Comparative Psychology 15: 12713710.46867/C4XK5NCrossRefGoogle Scholar
Kutska, D 2009 Variation in visitor perceptions of a polar bear enclosure based on the presence of natural vs unnatural enrich-ment items. Zoo Biology 28: 292306. https://doi.org/10.1002/zoo.20226CrossRefGoogle Scholar
Lacasse, C and Gamble, KC 2006 Tracheitis associated with Bordetella bronchiseptica in a polar bear (Ursus maritimus). Journal of Zoo and Wildlife Medicine 37: 190192. https://doi.org/10.1638/05-055.1CrossRefGoogle Scholar
LaDouceur, EEB, Garner, MM, Davis, B and Tseng, F 2014 A Retrospective study of end-stage renal disease in captive polar bears (Ursus maritimus). Journal of Zoo and Wildlife Medicine 45: 6977. https://doi.org/10.1638/2013-0071R.1CrossRefGoogle ScholarPubMed
Lehner, PN 1979 Handbook of Ethological Methods. Garland STPM Press: New York, USAGoogle Scholar
Lin, RC, Engeli, E, Prowten, AW, Erb, HN, Ducharme, NG and Goodrich, LR 2005 Antebrachial fractures in four captive polar bears (Ursus maritimus). Veterinary Surgery 34: 358365. https://doi.org/10.1111/j.1532-950X.2005.00055.xCrossRefGoogle ScholarPubMed
Linder, AC, Gottschalk, A, Lyhne, H, Langbak, MG, Jensen, TH and Pertoldi, C 2020 Using behavioral instability to investi-gate behavioral reaction norms in captive animals: Theoretical implications and future perspectives. Symmetry 12: 603. https://doi.org/10.3390/sym12040603CrossRefGoogle Scholar
Lintzenich, BA, Ward, AM, Edwards, MS, Griffin, ME and Robbins, CT 2006 Polar bear nutrition guidelines. Polar Bears International, AZA Bear TAG pp 65. https://nagonline.net/wp-con-tent/uploads/2018/11/Lintzenich-et-al.-2006-Polar-Bear-Nutrition-Guidelines.pdfGoogle Scholar
Macbeth, BJ, Cattet, MRL, Obbard, ME, Middel, K and Janz, DM 2012 Evaluation of hair cortisol concentration as a biomark-er of long-term stress in free-ranging polar bears. Wildlife Society Bulletin 36: 747758. https://doi.org/10.1002/wsb.219CrossRefGoogle Scholar
Malcolm, KD, McShea, WJ, Van Deelen, TR, Bacon, HJ, Liu, F, Putman, S, Zhu, X and Brown, JL 2013 Analyses of fecal and hair glucocorticoids to evaluate short- and long-term stress and recovery of Asiatic black bears (Ursus thibetanus) removed from bile farms in China. General and Comparative Endocrinology 185: 97106. https://doi.org/10.1016/j.ygcen.2013.01.014CrossRefGoogle Scholar
Manteca, X, Amat, M, Salas, M and Temple, D 2016 Animal-based indicators to assess welfare in zoo animals. CAB Reviews 11:1-10. https://doi.org/10.1079/PAVSNNR201611010CrossRefGoogle Scholar
Maślak R, Sergiel A, Bowles D and Paśko Ł 2016 The wel-fare of bears in zoos: A case study of Poland. Journal of Applied Animal Welfare Science 19: 2436. https://doi.org/10.1080/10888705.2015.1071671CrossRefGoogle Scholar
Maślak, R, Sergiel, A and Hill, SP 2013 Some aspects of loco-motory stereotypies in spectacled bears (Tremarctos ornatus) and changes in behavior after relocation and dental treatment. Journal of Veterinary Behavior: Clinical Applications and Research 8: 335341. https://doi.org/10.1016/j.jveb.2013.05.004CrossRefGoogle Scholar
Mason, G, Clubb, R, Latham, N and Vickery, S 2007 Why and how should we use environmental enrichment to tackle stereo-typic behaviour? Applied Animal Behaviour Science 102: 163188. https://doi.org/10.1016/j.applanim.2006.05.041CrossRefGoogle Scholar
Mason, GJ and Latham, NR 2004 Can't stop, won't stop: Is stereo-typy a reliable animal welfare indicator? Animal Welfare 13: 576910.1017/S096272860001438XCrossRefGoogle Scholar
McGowan, RTS, Robbins, CT, Alldredge, JR and Newberry, RC 2010 Contra-freeloading in grizzly bears: Implications for captive foraging enrichment. Zoo Biology 29: 484502. https://doi.org/10.1002/zoo.20282Google Scholar
Meagher, RK 2009 Observer ratings: Validity and value as a tool for animal welfare research. Applied Animal Behaviour Science 119:114. https://doi.org/10.1016/j.applanim.2009.02.026CrossRefGoogle Scholar
Mellor, DJ 2015 Positive animal welfare states and encouraging environment-focused and animal-to-animal interactive behaviours. New Zealand Veterinary Journal 63: 916. https://doi.org/10.1080/00480169.2014.926800CrossRefGoogle ScholarPubMed
Mellor, DJ 2016 Updating animal welfare thinking: Moving beyond the ‘Five Freedoms’ towards ‘A life worth living.’ Animals 6: 21. https://doi.org/10.3390/ani6030021CrossRefGoogle ScholarPubMed
Messier, F, Taylor, MK and Ramsay, MA 1992 Seasonal activ-ity patterns of female polar bears (Ursus maritimus) in the Canadian Arctic as revealed by satellite telemetry. Journal of Zoology 226: 219229. https://doi.org/10.1111/j.1469-7998.1992.tb03835.xCrossRefGoogle Scholar
Miller, LJ, Pisacane, CB and Vicino, GA 2016 Relationship between behavioural diversity and faecal glucocorticoid metabo-lites: A case study with cheetahs (Acinonyx jubatus). Animal Welfare 25: 325329. https://doi.org/10.7120/09627286.25.3.325CrossRefGoogle Scholar
Mislan, P, Derocher, AE, St Louis, VL, Richardson, E, Lunn, NJ and Janz, DM 2016 Assessing stress in Western Hudson Bay polar bears using hair cortisol concentration as a biomarker. Ecological Indicators 71: 4754. https://doi.org/10.1016/j.eco-lind.2016.06.034CrossRefGoogle 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 112. CAB International: Wallingford, UK. https://doi.org/10.1079/9780851993591.0000CrossRefGoogle Scholar
Montaudouin, S and Le Pape, G 2004 Comparison of the behav-iour of European brown bears (Ursus arctos arctos) in six different parks, with particular attention to stereotypies. Behavioural Processes 67: 235244. https://doi.org/10.1016/j.beproc.2004.02.008CrossRefGoogle ScholarPubMed
Montaudouin, S and Le Pape, G 2005 Comparison between 28 zoological parks: Stereotypic and social behaviours of captive brown bears (Ursus arctos). Applied Animal Behaviour Science 92:129141. https://doi.org/10.1016/j.applanim.2004.10.015CrossRefGoogle Scholar
Morgan, KN and Tromborg, CT 2007 Sources of stress in cap-tivity. Applied Animal Behaviour Science 102: 262302. https://doi.org/10.1016/j.applanim.2006.05.032CrossRefGoogle Scholar
Mormède, P, Andanson, S, Aupérin, B, Beerda, B, Guémené, D, Malmkvist, J, Manteca, X, Manteuffel, G, Prunet, P, van Reenen, CG, Richard, S and Veissier, I 2007 Exploration of the hypothalamic-pituitary-adrenal function as a tool to evaluate animal welfare. Physiology and Behavior 92: 317339. https://doi.org/10.1016/j.physbeh.2006.12.003CrossRefGoogle ScholarPubMed
Morris, PJ, Legendre, AM, Bowersock, TL, Brooks, DE, Krahwinkel, DJ, Shires, GMH and Walker, MA 1989 Diagnosis and treatment of systemic blastomycosis in a polar bear (Ursus maritimus) with itraconazole. Journal of Zoo and Wildlife Medicine 20: 336345Google Scholar
Morrison, JF, Vakharia, K and Moreland, DB 2017 Lumbar laminectomy in a captive, adult polar bear (Ursus maritimus). Surgical Neurology International 8: 17. https://doi.org/10.4103/sni.sni_133_17Google Scholar
Möstl, E and Palme, R 2002 Hormones as indicators of stress. Domestic Animal Endocrinology 23: 6774. https://doi.org/10.1016/S0739-7240(02)00146-7CrossRefGoogle ScholarPubMed
Normando, S, Pollastri, I, Florio, D, Ferrante, L, Macchi, E, Isaja, V and de Mori, B 2018 Assessing animal welfare in animal-visitor interactions in zoos and other facilities. A pilot study involving giraffes. Animals 8: 153. https://doi.org/10.3390/ani8090153CrossRefGoogle ScholarPubMed
O’Connor, AM and Sargeant, JM 2014 Critical appraisal of studies using laboratory animal models. ILAR Journal 55: 405417. https://doi.org/10.1093/ilar/ilu038CrossRefGoogle ScholarPubMed
Øritsland, NA, Lentfer, JW and Ronald, K 1974 Radiative sur-face temperatures of the polar bear. Journal of Mammalogy 55:459461. https://doi.org/10.2307/1379018CrossRefGoogle Scholar
Palme, R 2012 Monitoring stress hormone metabolites as a use-ful, non-invasive tool for welfare assessment in farm animals. Animal Welfare 21: 331337. https://doi.org/10.7120/09627286.21.3.331CrossRefGoogle Scholar
Palme, R 2019 Non-invasive measurement of glucocorticoids: Advances and problems. Physiology and Behavior 199: 229243. https://doi.org/10.1016/j.physbeh.2018.11.021CrossRefGoogle ScholarPubMed
Park, KA, Duncan, C, Noi, P, Sonne, C, Laidre, K, Obbard, M, Wiig, Ø, Aars, J, Regehr, E, Gustafson, LL and Atwood, T 2015 Establishing a definition of polar bear (Ursus maritimus) health: A guide to research and management activities. Science of the Total Environment Journal 514: 371378. https://doi.org/10.1016/j.scitotenv.2015.02.007Google Scholar
Pawluski, J, Jego, P, Henry, S, Bruchet, A, Palme, R, Coste, C and Hausberger, M 2017 Low plasma cortisol and fecal cortisol metabolite measures as indicators of compromised welfare in domestic horses (Equus caballus). PLoS One 12: 118. https://doi.org/10.1371/journal.pone.0182257CrossRefGoogle ScholarPubMed
Poulsen, EM, Honeyman, V, Valentine, PA and Teskey, GC 1996 Use of fluoxetine for the treatment of stereotypical pacing behavior in a captive polar bear. Journal of the American Veterinary Medical Association 209: 14701474Google Scholar
Rees, PA 2015 Studying Captive Animals: A Workbook of Methods in Behaviour, Welfare and Ecology. Wiley-Blackwell: New York, USAGoogle Scholar
Renner, MJ and Kelly, AL 2006 Behavioral decisions for managing social distance and aggression in captive polar bears (Ursus maritimus). Journal of Applied Animal Welfare Science 9: 233239. https://doi.org/10.1207/s15327604jaws0903_5CrossRefGoogle ScholarPubMed
Richter, SH and Hintze, S 2019 From the individual to the pop-ulation – and back again? Emphasising the role of the individual in animal welfare science. Applied Animal Behaviour Science 212: 18. https://doi.org/10.1016/j.applanim.2018.12.012CrossRefGoogle Scholar
Rose, PE, Nash, SM and Riley, LM 2017 To pace or not to pace? A review of what abnormal repetitive behavior tells us about zoo animal management. Journal of Veterinary Behavior: Clinical Applications and Research 20: 1121. https://doi.org/10.1016/j.jveb.2017.02.007CrossRefGoogle Scholar
Ross, SR 2006 Issues of choice and control in the behaviour of a pair of captive polar bears (Ursus maritimus). Behavioural Processes 73: 117120. https://doi.org/10.1016/j.beproc.2006.04.003CrossRefGoogle ScholarPubMed
Salas, M, Manteca, X, Abáigar, T, Delclaux, M, Enseñat, C, Martínez-Nevado, E, Quevedo, and Fernández-Bellon, H 2018 Using farm animal welfare protocols as a base to assess the welfare of wild animals in captivity — case study: Dorcas gazelles (Gazella dorcas). Animals 8: 114. https://doi.org/10.3390/ani8070111CrossRefGoogle ScholarPubMed
Salas, M, Temple, D, Abáigar, T, Cuadrado, M, Delclaux, M, Enseñat, C, Almagro, V, Martínez-Nevado, E, Quevedo, , Carbajal, A, Tallo-Parra, O, Sabés-Alsina, M, Amat, M, Lopez-Bejar, M, Fernández-Bellon, H and Manteca, X 2016 Aggressive behavior and hair cortisol levels in captive Dorcas gazelles (Gazella dorcas) as animal-based welfare indicators. Zoo Biology 35: 467473. https://doi.org/10.1002/zoo.21323CrossRefGoogle ScholarPubMed
Saudargas, RA and Drummer, LC 1996 Single subject (small N) research designs and zoo research. Zoo Biology 15: 173181. https://doi.org/10.1002/(SICI)1098-2361(1996)15:2<173::AID-ZOO7>3.0.CO;2-83.0.CO;2-8>CrossRefGoogle Scholar
Shepherdson, D, Carlstead, K and Wielebnowski, N 2004 Cross-institutional assessment of stress responses in zoo animals using longitudinal monitoring of faecal corticoids and behaviour. Animal Welfare 13: 10511310.1017/S0962728600014445CrossRefGoogle Scholar
Shepherdson, D, Lewis, KD, Carlstead, K, Bauman, J and Perrin, N 2013 Individual and environmental factors associated with stereotypic behavior and fecal glucocorticoid metabolite lev-els in zoo housed polar bears. Applied Animal Behaviour Science 147: 268277. https://doi.org/10.1016/j.applanim.2013.01.001CrossRefGoogle Scholar
Smith, CF and Cordes, DO 1972 Dermatitis caused by Dermatophilus congolensis infection in polar bears (Thalactos mar-itimus). The British Veterinary Journal 128: 366371. https://doi.org/10.1016/S0007-1935(17)36887-2CrossRefGoogle Scholar
Smith, TS, Amstrup, SC, Kirschhoffer, BJ and York, G 2020 Efficacy of aerial forward-looking infrared surveys for detecting polar bear maternal dens. PLoS One 15: 110. https://doi.org/10.1371/journal.pone.0222744Google ScholarPubMed
Špinka, M 2019 Animal agency, animal awareness and animal wel-fare. Animal Welfare 28: 1120. https://doi.org/10.7120/09627286.28.1.011CrossRefGoogle Scholar
Stirling, I 1974 Midsummer observations on behavior of wild polar bears (Ursus maritimus). Canadian Journal of Zoology 52: 11911198. https://doi.org/10.1139/z74-157CrossRefGoogle Scholar
Stirling, I 1998 Polar Bears. University of Michigan Press: Ann Arbor, MI, USAGoogle Scholar
Stirling, I, Thiemann, GW and Richardson, E 2008 Quantitative support for a subjective fatness index for immobi-lized polar bears. Journal of Wildlife Management 72: 568574. https://doi.org/10.2193/2007-123CrossRefGoogle Scholar
Swaisgood, RR and Shepherdson, DJ 2005 Scientific approach-es to enrichment and stereotypies in zoo animals: What's been done and where should we go next? Zoo Biology 24: 449518. https://doi.org/10.1002/zoo.20066CrossRefGoogle Scholar
Swaisgood, RR, White, AM, Zhou, X, Zhang, H, Zhang, G, Wei, R, Hare, VJ, Tepper, EM and Lindburg, DG 2001 A quantitative assessment of the efficacy of an environmental enrichment programme for giant pandas. Animal Behaviour 61:447457. https://doi.org/10.1006/anbe.2000.1610CrossRefGoogle Scholar
Tetley, CL and O’Hara, SJ 2012 Ratings of animal personality as a tool for improving the breeding, management and welfare of zoo mammals. Animal Welfare 21: 463476. https://doi.org/10.7120/09627286.21.4.463CrossRefGoogle Scholar
Todman, JB and Dugard, P 2001 Single-Case and Small-N Experimental Designs: A Practical Guide to Randomization Tests, First Edition. Routledge: New York, USA. https://doi.org/10.4324/9781410600943CrossRefGoogle Scholar
Tuyttens, FAM, Stadig, L, Heerkens, JLT, van Laer, E, Buijs, S and Ampe, B 2016 Opinion of applied ethologists on expectation bias, blinding observers and other debiasing techniques. Applied Animal Behaviour Science 181: 2733. https://doi.org/10.1016/j.applanim.2016.04.019CrossRefGoogle Scholar
Vickery, S and Mason, G 2003a Understanding stereotypies in captive bears: The first step towards treatment. In: Gilbert, TC (ed) Proceedings of The Fifth Annual Symposium on Zoo Research pp 3851. Federation of Zoological Gardens of Great Britain and Ireland: Winchester, UKGoogle Scholar
Vickery, SS and Mason, GJ 2003b Behavioral persistence in captive bears: Implications for reintroduction. Ursus 14: 3543Google Scholar
Wagman, JD, Lukas, KE, Dennis, PM, Willis, MA, Carroscia, J, Gindlesperger, C and Schook, MW 2018 A work-for-food enrichment program increases exploration and decreases stereo-typies in four species of bears. Zoo Biology 37: 315. https://doi.org/10.1002/zoo.21391CrossRefGoogle ScholarPubMed
Waroff, AJ, Fanucchi, L, Robbins, CT and Nelson, OL 2017 Tool use, problem-solving, and the display of stereotypic behav-iors in the brown bear (Ursus arctos). Journal of Veterinary Behavior 17: 6268. https://doi.org/10.1016/j.jveb.2016.11.003CrossRefGoogle Scholar
Watters, JV 2014 Searching for behavioral indicators of welfare in zoos: Uncovering anticipatory behavior. Zoo Biology 33: 251256. https://doi.org/10.1002/zoo.21144CrossRefGoogle ScholarPubMed
Watters, JV, Krebs, B and Pacheco, E 2019 Measuring welfare through behavioral observation and adjusting it with dynamic envi-ronments. In: Kaufman, A, Bashaw, M and Maple, T (eds) Scientific Foundations of Zoos and Aquariums: Their Role in Conservation and Research pp 212240. Cambridge University Press: Cambridge, UK. https://doi.org/10.1017/9781108183147.009CrossRefGoogle Scholar
Wechsler, B 1991 Stereotypies in polar bears. Zoo Biology 10:177188. https://doi.org/10.1002/zoo.1430100209CrossRefGoogle Scholar
Wechsler, B 1992 Stereotypies and attentiveness to novel stim-uli: A test in polar bears. Applied Animal Behaviour Science 33: 381388. https://doi.org/10.1016/S0168-1591(05)80074-7CrossRefGoogle Scholar
Wemelsfelder, F and Mullan, S 2014 Applying ethological and health indicators to practical animal welfare assessment. Revue Scientifique et Technique (International Office of Epizootics) 33: 111120. https://doi.org/10.20506/rst.33.1.2259Google ScholarPubMed
Wenker, CJ, Stich, H, Müller, M and Lussi, A 1999 A retro-spective study of dental conditions of captive brown bears (Ursus arctos spp) compared with free-ranging Alaskan grizzlies (Ursus arctos horribilis). Journal of Zoo and Wildlife Medicine 30: 208221Google Scholar
Whitham, JC and Wielebnowski, N 2009 Animal-based wel-fare monitoring: Using keeper ratings as an assessment tool. Zoo Biology 28: 545560. https://doi.org/10.1002/zoo.20281Google Scholar
Wielebnowski, NC, Fletchall, N, Carlstead, K, Busso, JM and Brown, JL 2002 Non-invasive assessment of adrenal activity associated with husbandry and behavioral factors in the North American clouded leopard population. Zoo Biology 21: 7798. https://doi.org/10.1002/zoo.10005CrossRefGoogle Scholar
Wiig, Ø, Amstrup, S, Atwood, T, Laidre, K, Lunn, N, Obbard, M, Regehr, E and Thiemann, G 2015 Ursus maritimus. The IUCN Red List of Threatened Species: e.T22823A14871490. https://doi.org/10.2305/IUCN.UK.2015-4.RLTS.T22823A14871490.enCrossRefGoogle Scholar
Williams, E, Chadwick, CL, Yon, L and Asher, L 2018 A review of current indicators of welfare in captive elephants (Loxodonta africana and Elephas maximus). Animal Welfare 27: 235249. https://doi.org/10.7120/09627286.27.3.235CrossRefGoogle Scholar
Wooddell, LJ, Hamel, AF, Murphy, AM, Byers, KL, Kaburu, SSK, Meyer, JS, Suomi, SJ and Dettmer, AM 2017 Relationships between affiliative social behavior and hair cortisol concentrations in semi-free ranging rhesus monkeys. Psychoneuroendocrinology 84: 109115. https://doi.org/10.1016/j.psyneuen.2017.06.018CrossRefGoogle ScholarPubMed
Yamanashi, Y, Teramoto, M, Morimura, N, Nogami, E and Hirata, S 2018 Social relationship and hair cortisol level in captive male chimpanzees (Pan troglodytes). Primates 59: 145152. https://doi.org/10.1007/s10329-017-0641-8CrossRefGoogle ScholarPubMed
Yon, L, Williams, E, Harvey, ND and Asher, L 2019 Development of a behavioural welfare assessment tool for rou-tine use with captive elephants. PLoS One 14: 120. https://doi.org/10.1371/journal.pone.0210783CrossRefGoogle Scholar
Supplementary material: File

Skovlund et al. supplementary material
Download undefined(File)
File 237.3 KB