Hostname: page-component-586b7cd67f-dsjbd Total loading time: 0 Render date: 2024-11-23T21:02:58.079Z Has data issue: false hasContentIssue false

Linking the roles of personality and stress physiology for managing the welfare of captive big cats

Published online by Cambridge University Press:  01 January 2023

J Vaz*
Affiliation:
School of Science, Western Sydney University, Locked Bag 1797, Penrith 2751, NSW, Australia
AG McElligott
Affiliation:
Department of Infectious Diseases and Public Health, Jockey Club College of Veterinary Medicine and Life Sciences, City University of Hong Kong, Hong Kong, China Centre for Animal Health and Welfare, Jockey Club College of Veterinary Medicine and Life Sciences, City University of Hong Kong, Hong Kong, China
E Narayan
Affiliation:
School of Agriculture and Food Sciences, Faculty of Science, The University of Queensland, St Lucia, QLD 4072, Australia
*
* 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.

Animal welfare is important for the humane treatment of animals under our care. Zoos and rescue centres manage various charismatic animals, such as big cats, with limited resources. It is therefore essential for caretakers to understand the needs of an individual big cat to ensure its welfare. However, these needs may differ due to a big cat's personality, which may be identified by its coping style in a stressful situation. In addition, stress is one of the major factors affecting animal welfare. There is limited evidence showing strong associations between personality and stress physiology in big cats. This review focuses on the integration of personality and stress physiology of captive big cats, to highlight possible improvements in their husbandry. Our review identifies key factors that may influence big cat responses to stressors. These influencing factors include: i) social interactions; ii) environment; iii) life history and evolutionary traits; iv) genetics; and v) health. The first two factors are relatively well covered in the literature; however, the final three are potentially very promising avenues for future research to better understand how we can improve big cat welfare.

Type
Research Article
Copyright
© 2022 Universities Federation for Animal Welfare

References

Allendorf, FW, Hohenlohe, PA and Luikart, G 2010 Genomics and the future of conservation genetics. Nature Reviews Genetics 11: 697. https://doi.org/10.1038/nrg2844CrossRefGoogle ScholarPubMed
Andersson, L, Haley, CS, Ellegren, H, Knott, SA, Johansson, M, Andersson, K, Andersson-Eklund, L, Edfors-Lilja, I, Fredholm, M and Hansson, I 1994 Genetic mapping of quanti-tative trait loci for growth and fatness in pigs. Science 263: 1771. https://doi.org/10.1126/science.8134840CrossRefGoogle Scholar
Antonevich, AL, Rödel, HG, Hudson, R, Alekseeva, GS, Erofeeva, MN and Naidenko, SV 2020 Predictors of individual differences in play behavior in Eurasian lynx cubs. Journal of Zoology 311: 5665. https://doi.org/10.1111/jzo.12761CrossRefGoogle Scholar
Azevedo, A, Wauters, J, Kirschbaum, C, Serra, R, Rivas, A and Jewgenow, K 2020 Sex steroids and glucocorticoid ratios in Iberian lynx hair. Conservation Physiology 8. https://doi.org/10.1093/conphys/coaa075CrossRefGoogle Scholar
Baker, KA and Pullen, PK 2013 The impact of housing and hus-bandry on the personality of cheetah (Acinonyx jubatus). Journal of Zoo and Aquarium Research 1: 3540Google Scholar
Bednekoff, PA 2010 Life histories and predation risk. In: Breed, MD and Moore, J (eds) Encyclopedia of Animal Behavior pp 283287. Academic Press: Oxford, UK. https://doi.org/10.1016/B978-0-08-045337-8.00332-6CrossRefGoogle Scholar
Bertocchi, M, Spiezio, C, Di Ianni, F, Macchi, E, Parmigiani, E, Sandri, C, Ponzio, P and Quintavalla, F 2015 Welfare of a pair of captive tigers - a hand-reared female and a parent-reared male. Journal of Advances in Agriculture 5: 545556. https://doi.org/10.24297/jaa.v5i1.4508CrossRefGoogle Scholar
Bertram, BCR 1975 Social factors influencing reproduction in wild lions. Journal of Zoology 177: 463482. https://doi.org/10.1111/j.1469-7998.1975.tb02246.xCrossRefGoogle Scholar
Bhattacharjee, S, Kumar, V, Chandrasekhar, M, Malviya, M, Ganswindt, A, Ramesh, K, Sankar, K and Umapathy, G 2015 Glucocorticoid stress responses of reintroduced tigers in relation to anthropogenic disturbance in Sariska Tiger Reserve in India. PLoS One 10: e0127626. https://doi.org/10.1371/journal.pone.0127626CrossRefGoogle ScholarPubMed
Boccacino, D, Maia, CM, Santos, EF and Santori, RT 2018 Effects of environmental enrichments on the behaviors of four captive jaguars: Individuality matters. Oecologia Australis 22(1): 6373. https://doi.org/10.4257/oeco.2018.2201.06CrossRefGoogle Scholar
Bolger, N 1990 Coping as a personality process: A prospective study. Journal of Personality and Social Psychology 59: 525537. https://doi.org/10.1037/0022-3514.59.3.525CrossRefGoogle ScholarPubMed
Braastad, BO 1998 Effects of prenatal stress on behaviour of off-spring of laboratory and farmed mammals. Applied Animal Behaviour Science 61: 159180. https://doi.org/10.1016/S0168-1591(98)00188-9CrossRefGoogle Scholar
Brambell, R 1965 Report of the technical committee to enquire into the welfare of animals kept under intensive livestock husbandry sys-tems. Her Majesty's Stationary Office: London, UKGoogle Scholar
Brown, EW, Olmsted, RA, Martenson, JS and O’Brien, SJ 1993 Exposure to FIV and FIPV in wild and captive cheetahs. Zoo Biology 12: 135142. https://doi.org/10.1002/zoo.1430120112CrossRefGoogle Scholar
Brown, JL, Goodrowe, KL, Simmons, LG, Armstrong, DL and Wildt, DE 1988 Evaluation of the pituitary-gonadal response to GnRH, and adrenal status, in the leopard (Panthera pardus japo-nensis) and tiger (Panthera tigris). Journal of Reproduction and Fertility 82: 227236. https://doi.org/10.1530/jrf.0.0820227CrossRefGoogle ScholarPubMed
Burgener, N, Gusset, M and Schmid, H 2008 Frustrated appet-itive foraging behavior, stereotypic pacing, and fecal glucocorticoid levels in snow leopards (Uncia uncia) in the Zurich Zoo. Journal of Applied Animal Welfare Science 11: 7483. https://doi.org/10.1080/10888700701729254CrossRefGoogle ScholarPubMed
Burstahler, CM, Terwissen, CV and Roth, JD 2019 Latitudinal gradient in cortisol concentrations in Canada lynx (Lynx canaden-sis) is not explained by diet. Canadian Journal of Zoology 97: 748753. https://doi.org/10.1139/cjz-2018-0204CrossRefGoogle Scholar
Cannon, WB 1914 The emergency function of the adrenal medul-la in pain and the major emotions. American Journal of Physiology 33: 356393. https://doi.org/10.1152/ajplegacy.1914.33.2.356CrossRefGoogle Scholar
Capitanio, JP 2011 Nonhuman primate personality and immuni-ty: Mechanisms of health and disease. Personality and Temperament in Nonhuman Primates: 233-255. https://doi.org/10.1007/978-1-4614-0176-6_9CrossRefGoogle Scholar
Caramaschi, D, Carere, C, Sgoifo, A and Koolhaas, JM 2013 Neuroendocrine and autonomic correlates of animal personali-ties. In: Carere, C and Maestripieri, D (eds) Animal Personalities – Behavior, Physiology, and Evolution pp 353380. The University of Chicago Press: Chicago, IL, USA. https://doi.org/10.7208/chicago/9780226922065.003.0013CrossRefGoogle Scholar
Carere, C, Caramaschi, D and Fawcett, TW 2010 Covariation between personalities and individual differences in coping with stress: converging evidence and hypotheses. Current Zoology 56: 728740. https://doi.org/10.1093/czoolo/56.6.728CrossRefGoogle Scholar
Carere, C, Drent, PJ, Privitera, L, Koolhaas, JM and Groothuis, TGG 2005 Personalities in great tits, Parus major: sta-bility and consistency. Animal Behaviour 70: 795805. https://doi.org/10.1016/j.anbehav.2005.01.003CrossRefGoogle Scholar
Carlstead, K and Shepherdson, D 2000 Alleviating stress in zoo animals with environmental enrichment. In: Moberg, GP and Mench, JA (eds) The Biology of Animal Stress: Basic Principles and Implications for Animal Welfare pp 337354. CAB International: Wallingford, UK. https://doi.org/10.1079/9780851993591.0337CrossRefGoogle Scholar
Cavigelli, SA 2005 Animal personality and health. Behaviour 142: 12231244. https://doi.org/10.1163/156853905774539355CrossRefGoogle Scholar
Chadwick, C 2014 Social behaviour and personality assessment as a tool for improving the management of cheetahs ( Acinonyx jubatus) in captivity. Doctor of Philosophy, University of Salford, UKGoogle Scholar
Cho, YS, Hu, L, Hou, H, Lee, H, Xu, J, Kwon, S, Oh, S, Kim, H-M, Jho, S, Kim, S, Shin, Y-A, Kim, BC, Kim, H, Kim, C-U, Luo, S-J, Johnson, WE, Koepfli, K-P, Schmidt-Küntzel, A, Turner, JA, Marker, L, Harper, C, Miller, SM, Jacobs, W, Bertola, LD, Kim, TH, Lee, S, Zhou, Q, Jung, H-J, Xu, X, Gadhvi, P, Xu, P, Xiong, Y, Luo, Y, Pan, S, Gou, C, Chu, X, Zhang, J, Liu, S, He, J, Chen, Y, Yang, L, Yang, Y, He, J, Liu, S, Wang, J, Kim, CH, Kwak, H, Kim, J-S, Hwang, S, Ko, J, Kim, C-B, Kim, S, Bayarlkhagva, D, Paek, WK, Kim, S-J, O’Brien, SJ, Wang, J and Bhak, J 2013 The tiger genome and comparative analysis with lion and snow leopard genomes. Nature Communications 4: 17. https://doi.org/10.1038/ncomms3433CrossRefGoogle ScholarPubMed
Clark, AB and Ehlinger, TJ 1987 Pattern and adaptation in individ-ual behavioral differences. In: Bateson, PPG and Klopfer, PH (eds) Perspectives in Ethology, Volume 7 Alternatives pp 147. Springer US: Boston, MA, USA. https://doi.org/10.1007/978-1-4613-1815-6_1CrossRefGoogle Scholar
Clary, D, Skyner, LJ, Ryan, CP, Gardiner, LE, Anderson, WG and Hare, JF 2014 Shyness-Boldness, but not exploration, pre-dicts glucocorticoid stress response in Richardson's ground squir-rels (Urocitellus richardsonii). Ethology 120: 11011109. https://doi.org/10.1111/eth.12283CrossRefGoogle Scholar
Clubb, R and Mason, G 2003 Captivity effects on wide-ranging carnivores. Nature 425: 473474. https://doi.org/10.1038/425473aCrossRefGoogle ScholarPubMed
Clutton-Brock, T and Sheldon, BC 2010 Individuals and popu-lations: the role of long-term, individual-based studies of animals in ecology and evolutionary biology. Trends in Ecology & Evolution 25: 562573. https://doi.org/10.1016/j.tree.2010.08.002CrossRefGoogle Scholar
Cociu, M, Wagner, G, Micu, NE and Mihaescu, G 1974 Adaptational gastro-enteritis in Siberian tigers: Panthcra tigris altaica: at Bucharest Zoo. International Zoo Yearbook 14: 171174. https://doi.org/10.1111/j.1748-1090.1974.tb00812.xCrossRefGoogle Scholar
Cockrem, J 2013 Corticosterone responses and personality in birds: Individual variation and the ability to cope with environmen-tal changes due to climate change. General and Comparative Endocrinology 190: 156163. https://doi.org/10.1016/j.ygcen.2013.02.021CrossRefGoogle Scholar
Conforti, VA, Morato, RG, Augusto, AM, de Oliveira e Sousa, L, de Avila, DM, Brown, JL and Reeves, JJ 2012 Noninvasive monitoring of adrenocortical function in captive jaguars (Panthera onca). Zoo Biology 31: 426441. https://doi.org/10.1002/zoo.20409CrossRefGoogle ScholarPubMed
Coppens, CM, de Boer, SF and Koolhaas, JM 2010 Coping styles and behavioural flexibility: towards underlying mechanisms. Philosophical Transactions of the Royal Society B: Biological Sciences 365: 4021. https://doi.org/10.1098/rstb.2010.0217CrossRefGoogle ScholarPubMed
Creel, S, Christianson, D and Schuette, P 2013 Glucocorticoid stress responses of lions in relationship to group composition, human land use, and proximity to people. Conservation Physiology 1: 19. https://doi.org/10.1093/conphys/cot021CrossRefGoogle ScholarPubMed
Deary, IJ, Weiss, A and Batty, GD 2010 Intelligence and person-ality as predictors of illness and death: How researchers in differ-ential psychology and chronic disease epidemiology are collabo-rating to understand and address health inequalities. Psychological Science in the Public Interest 11: 5379. https://doi.org/10.1177/1529100610387081CrossRefGoogle Scholar
DeCaluwe, HB, Wielebnowski, NC, Howard, J, Pelican, KM and Ottinger, MA 2013 Behavioral reactions relate to adrenal activity and temperament in male clouded leopards Neofelis nebu-losa. Applied Animal Behaviour Science 149: 6371. https://doi.org/10.1016/j.applanim.2013.09.008CrossRefGoogle Scholar
Dembiec, DP, Snider, RJ and Zanella, AJ 2004 The effects of transport stress on tiger physiology and behavior. Zoo Biology 23: 335346. https://doi.org/10.1002/zoo.20012CrossRefGoogle Scholar
Dunston, EJ, Abell, J, Doyle, RE, Evershed, M and Freire, R 2016 Exploring African lion (Panthera leo) behavioural phenotypes: individual differences and correlations between sociality, boldness and behaviour. Journal of Ethology 34: 277290. https://doi.org/10.1007/s10164-016-0473-9CrossRefGoogle Scholar
Ellis, BJ, Jackson, JJ and Boyce, WT 2006 The stress response systems: Universality and adaptive individual differences. Developmental Review 26: 175212. https://doi.org/10.1016/j.dr.2006.02.004CrossRefGoogle Scholar
Fanson, KV and Wielebnowski, NC 2013 Effect of housing and husbandry practices on adrenocortical activity in captive Canada lynx (Lynx canadensis). Animal Welfare 22: 159165. https://doi.org/10.7120/09627286.22.2.159CrossRefGoogle Scholar
Feaver, J, Mendl, M and Bateson, P 1986 A method for rating the individual distinctiveness of domestic cats. Animal Behaviour 34: 10161025. https://doi.org/10.1016/S0003-3472(86)80160-9CrossRefGoogle Scholar
Finkemeier, M-A, Langbein, J and Puppe, B 2018 Personality research in mammalian farm animals: Concepts, measures, and relationship to welfare. Frontiers in Veterinary Science 5: 131. https://doi.org/10.3389/fvets.2018.00131CrossRefGoogle ScholarPubMed
Freeman, HD and Gosling, SD 2010 Personality in nonhuman primates: a review and evaluation of past research. American Journal of Primatology 72: 653671. https://doi.org/10.1002/ajp.20833CrossRefGoogle ScholarPubMed
Friedman, HS 1990 Where is the disease-prone personality? Conclusion and future directions. In: Friedman, HS (ed) Personality and Disease pp xvi, 315-xvi, 315. John Wiley & Sons: Oxford, UKGoogle Scholar
Friedman, HS 2008 The multiple linkages of personality and dis-ease. Brain, Behavior, and Immunity 22: 668675. https://doi.org/10.1016/j.bbi.2007.09.004CrossRefGoogle Scholar
Gartner, MC 2017 Felid personality and its implications. In: Vonk, J, Weiss, A and Kuczaj, SA (eds) Personality in Nonhuman Animals pp 225236. Springer International Publishing: Cham, Switzerland. https://doi.org/10.1007/978-3-319-59300-5_11CrossRefGoogle Scholar
Gartner, MC and Powell, DM 2012 Personality assessment in snow leopards (Uncia uncia). Zoo Biology 31: 151165. https://doi.org/10.1002/zoo.20385Google ScholarPubMed
Gartner, MC, Powell, DM and Weiss, A 2014 Personality structure in the domestic cat (Felis silvestris catus), Scottish wildcat (Felis silvestris grampia), clouded leopard (Neofelis nebulosa), snow leop-ard (Panthera uncia), and African lion (Panthera leo): a comparative study. Journal of Comparative Psychology 128: 414426. https://doi.org/10.1037/a0037104CrossRefGoogle ScholarPubMed
Gartner, MC, Powell, DM and Weiss, A 2016 Comparison of subjective well-being and personality assessments in the clouded leopard (Neofelis nebulosa), snow leopard (Panthera uncia), and African Lion (Panthera leo). Journal of Applied Animal Welfare Science 19: 294302. https://doi.org/10.1080/10888705.2016.1141057CrossRefGoogle ScholarPubMed
Gartner, MC and Weiss, A 2013 Scottish wildcat (Felis silvestris grampia) personality and subjective well-being: Implications for captive management. Applied Animal Behaviour Science 147: 261267. https://doi.org/10.1016/j.applanim.2012.11.002CrossRefGoogle Scholar
Gershenfeld, HK, Neumann, PE, Mathis, C, Crawley, JN, Li, X and Paul, SM 1997 Mapping Quantitative Trait Loci for open-field behavior in mice. Behavior Genetics 27: 201210. https://doi.org/10.1023/A:1025653812535CrossRefGoogle ScholarPubMed
Gosling, SD and John, OP 1999 Personality dimensions in non-human animals: A cross-species review. Current Directions in Psychological Science 8: 6975. https://doi.org/10.1111/1467-8721.00017CrossRefGoogle Scholar
Gosling, SD and Mehta, PH 2013 Personalities in a comparative perspective: what do human psychologists glean from animal per-sonality studies? In: Carere, C and Maestripieri, D (eds) Animal Personalities – Behavior, Physiology, and Evolution pp 124145. The University of Chicago Press: Chicago, IL, USA. https://doi.org/10.7208/chicago/9780226922065.003.0006CrossRefGoogle Scholar
Goswami, S, Tyagi, P, Malik, P, Pandit, S, Kadivar, R, Fitzpatrick, M and Mondol, S 2020 Effects of personality and rearing-history on the welfare of captive Asiatic lions (Panthera leo persica). PeerJ 8. https://doi.org/10.7717/peerj.8425CrossRefGoogle Scholar
Groothuis, TGG and Carere, C 2005 Avian personalities: char-acterization and epigenesis. Neuroscience & Biobehavioral Reviews 29: 137150. https://doi.org/10.1016/j.neubiorev.2004.06.010CrossRefGoogle Scholar
Harrison, R 1964 Animal Machines: The New Factory Farming Industry. Vincent Stuart: London, UKGoogle Scholar
Ivanov, EA, Rozhnov, VV and Naidenko, SV 2017 The effect of ambient temperature on glucocorticoid level in the Amur tiger (Panthera tigris altaica). Russian Journal of Ecology 48: 294297. https://doi.org/10.1134/S1067413617030079CrossRefGoogle Scholar
Johnson, RA and Wichern, DW 2007 Applied Multivariate Statistical Analysis, Sixth Edition. Pearson Education, Inc: USA. https://doi.org/10.1002/0471667196.ess6094CrossRefGoogle Scholar
Jurke, MH, Czekala, NM, Lindburg, DG and Millard, SE 1997 Fecal corticoid metabolite measurement in the cheetah (Acinonyx jubatus). Zoo Biology 16: 133147. https://doi.org/10.1002/(SICI)1098-2361(1997)16:2<133::AID-ZOO4>3.0.CO;2-B3.0.CO;2-B>CrossRefGoogle Scholar
Kaiser, S, Hennessy, MB and Sachser, N 2015 Domestication affects the structure, development and stability of biobehavioural profiles. Frontiers in Zoology 12: S19. https://doi.org/10.1186/1742-9994-12-S1-S19CrossRefGoogle ScholarPubMed
Kamyk, CM 2017 Boldness and natural behaviors in the African lion ( Panthera leo): How are they related? Honors theses and capstones, University of New Hampshire, Durham, USAGoogle Scholar
Koolhaas, JM, de Boer, SF, Coppens, CM and Buwalda, B 2010 Neuroendocrinology of coping styles: Towards understanding the biology of individual variation. Frontiers in Neuroendocrinology 31: 307321. https://doi.org/10.1016/j.yfrne.2010.04.001CrossRefGoogle ScholarPubMed
Koolhaas, JM, Korte, SM, De Boer, SF, Van Der Vegt, BJ, Van Reenen, CG, Hopster, H, De Jong, IC, Ruis, MAW and Blokhuis, HJ 1999 Coping styles in animals: current status in behavior and stress-physiology. Neuroscience & Biobehavioral Reviews 23: 925935. https://doi.org/10.1016/S0149-7634(99)00026-3CrossRefGoogle ScholarPubMed
Koolhaas, JM and Van Reenen, CG 2016 Animal behavior and well-being symposium: Interaction between coping style/personal-ity, stress, and welfare: Relevance for domestic farm animals. Journal of Animal Science 94: 22842296. https://doi.org/10.2527/jas.2015-0125CrossRefGoogle Scholar
Korte, SM, Olivier, B and Koolhaas, JM 2007 A new animal wel-fare concept based on allostasis. Physiology & Behavior 92: 422428. https://doi.org/10.1016/j.physbeh.2006.10.018CrossRefGoogle Scholar
Ludwig, C, Wachter, B, Silinski-Mehr, S, Ganswindt, A, Bertschinger, H, Hofer, H and Dehnhard, M 2013 Characterisation and validation of an enzyme-immunoassay for the non-invasive assessment of faecal glucocorticoid metabolites in cheetahs (Acinonyx jubatus). General and Comparative Endocrinology 180: 1523. https://doi.org/10.1016/j.ygcen.2012.10.005CrossRefGoogle ScholarPubMed
Malviya, M, Kumar, V, Mandal, D, Sarkar, MS, Nigam, P, Gopal, R, Sankar, K, Umapathy, G and Ramesh, K 2018 Correlates of physiological stress and habitat factors in reintroduction-based recovery of tiger (Panthera tigris) populations. Hystrix, the Italian Journal of Mammalogy 29: 195201Google Scholar
Maniam, J, Antoniadis, C and Morris, MJ 2014 Early-life stress, HPA axis adaptation, and mechanisms contributing to later health outcomes. Frontiers in Endocrinology 5: 73. https://doi.org/10.3389/fendo.2014.00073CrossRefGoogle ScholarPubMed
Marinath, L, Vaz, J, Kumar, D, Thiyagesan, K and Baskaran, N 2019 Drivers of stereotypic behaviour and physiological stress among captive jungle cat (Felis chaus Schreber, 1777) in India. Physiology & Behavior 210: 112651. https://doi.org/10.1016/j.phys-beh.2019.112651CrossRefGoogle ScholarPubMed
Mason, G and Mendl, M 1993 Why is there no simple way of measuring animal welfare? Animal Welfare 2: 301319Google Scholar
Matteri, RL, Carroll, JA and Dyer, CJ 2000 Neuroendocrine responses to stress. In: Moberg, G and Mench, JA (eds) Biology of Animal Stress pp 4376: CABI: Wallingford, UK. https://doi.org/10.1079/9780851993591.0043CrossRefGoogle Scholar
Mellor, DJ 2017 Operational details of the Five Domains Model and its key applications to the assessment and management of ani-mal welfare. Animals 7: 60. https://doi.org/10.3390/ani7080060CrossRefGoogle Scholar
Mesa-Cruz, JB, Brown, JL and Kelly, MJ 2014 Effects of natural environmental conditions on faecal glucocorticoid metabolite concentrations in jaguars (Panthera onca) in Belize. Conservation Physiology 2: cou039. https://doi.org/10.1093/conphys/cou039CrossRefGoogle ScholarPubMed
Mesa-Cruz, JB, Brown, JL, Waits, LP and Kelly, MJ 2016 Non-invasive genetic sampling reveals diet shifts, but little difference in endoparasite richness and faecal glucocorticoids, in Belizean felids inside and outside protected areas. Journal of Tropical Ecology 32: 226239. https://doi.org/10.1017/S0266467416000213CrossRefGoogle 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
Moberg, G 1985 Biological response to stress: Key to assessment of animal well-being? In: Moberg, G (ed) Animal Stress pp 2749. Springer: Amsterdam, The Netherlands. https://doi.org/10.1007/978-1-4614-7544-6_3CrossRefGoogle Scholar
Moberg, G 2000 Biological response to stress: Implications for animal welfare. In: Moberg, G (ed) The Biology of Animal Stress: Basic Principles and Implications for Animal Welfare pp 121. CABI: Wallingford, UK. https://doi.org/10.1079/9780851993591.0001CrossRefGoogle Scholar
Monaghan, P and Haussmann, MF 2015 The positive and negative consequences of stressors during early life. Early Human Development 91: 643647. https://doi.org/10.1016/j.earlhumdev.2015.08.008CrossRefGoogle ScholarPubMed
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
Narayan, E, Baskaran, N and Vaz, J 2017 Conservation physiol-ogy of tigers in zoos: Integrating stress physiology and behaviour to monitor their health and welfare. In: Singh, KP (ed) Big Cats. IntechOpen: London, UK. https://doi.org/10.5772/intechopen.69780CrossRefGoogle Scholar
Narayan, E, Parnell, T, Clark, G, Martin-Vegue, P, Mucci, A and Hero, J 2013 Faecal cortisol metabolites in Bengal (Panthera tigris tigris) and Sumatran tigers (Panthera tigris sumatrae). General and Comparative Endocrinology 194: 318325. https://doi.org/10.1016/j.ygcen.2013.10.002CrossRefGoogle ScholarPubMed
Nogueira, GP and Silva, JC 1997 Plasma cortisol levels in captive wild felines after chemical restraint. Brazilian Journal of Medical Biological Research 30: 13591361. https://doi.org/10.1590/S0100-879X1997001100016CrossRefGoogle ScholarPubMed
Oakley, RH and Cidlowski, JA 2013 The biology of the gluco-corticoid receptor: New signaling mechanisms in health and dis-ease. The Journal of Allergy and Clinical Immunology 132: 10331044. https://doi.org/10.1016/j.jaci.2013.09.007CrossRefGoogle Scholar
Palme, R, Rettenbacher, S, Touma, C, El-Bahr, SM and Möstl, E 2005 Stress hormones in mammals and birds: Comparative aspects regarding metabolism, excretion, and non-invasive mea-surement in fecal Samples. Annals of the New York Academy of Sciences 1040: 162171. https://doi.org/10.1196/annals.1327.021CrossRefGoogle Scholar
Parnell, T, Narayan, EJ, Magrath, MJL, Roe, S, Clark, G, Nicolson, V, Martin-Vegue, P, Mucci, A and Hero, J-M 2014 Evaluating physiological stress in Sumatran tigers (Panthera tigris) managed in Australian zoos. Conservation Physiology 2: cou038. https://doi.org/10.1093/conphys/cou038CrossRefGoogle ScholarPubMed
Pastorino, GQ, Paini, F, Williams, CL, Faustini, M and Mazzola, SM 2017a Personality and sociality in captive tigers (Panthera tigris). Annual Research & Review in Biology 21: 117. https://doi.org/10.9734/ARRB/2017/38122CrossRefGoogle Scholar
Pastorino, GQ, Viau, A, Curone, G, Pearce-Kelly, P, Faustini, M, Vigo, D, Mazzola, SM and Preziosi, R 2017b Role of person-ality in behavioral responses to new environments in captive Asiatic lions (Panthera leo persica). Veterinary Medicine International 2017: 17. https://doi.org/10.1155/2017/6585380Google Scholar
Pavlova, E, Ivanov, E, Kirluk, V, Rozhnov, V and Naidenko, S 2015 Assessment of physiological status of felids as an indicator of their welfare in the wild. Studia Ecologiae et Bioethicae 13: 107122. https://doi.org/10.21697/seb.2015.13.1.06CrossRefGoogle Scholar
Phillips, C and Peck, D 2007 The effects of personality of keep-ers and tigers (Panthera tigris tigris) on their behaviour in an inter-active zoo exhibit. Applied Animal Behaviour Science 106: 244258. https://doi.org/10.1016/j.applanim.2007.01.007CrossRefGoogle Scholar
Phillips, C, Tribe, A, Lisle, A, Galloway, TK and Hansen, K 2017 Keepers’ rating of emotions in captive big cats, and their use in determining responses to different types of enrichment. Journal of Veterinary Behavior 20: 2230. https://doi.org/10.1016/j.jveb.2017.03.006CrossRefGoogle Scholar
Pribbenow, S, Jewgenow, K, Vargas, A, Serra, R, Naidenko, S and Dehnhard, M 2014 Validation of an enzyme immunoassay for the measurement of faecal glucocorticoid metabolites in Eurasian (Lynx lynx) and Iberian lynx (Lynx pardinus). General and Comparative Endocrinology 206: 166177. https://doi.org/10.1016/j.ygcen.2014.07.015CrossRefGoogle ScholarPubMed
Razal, C, Pisacane, C and Miller, L 2016 Multifaceted approach to personality assessment in cheetahs (Acinonyx jubatus). Animal Behavior and Cognition 3: 2231. https://doi.org/10.12966/abc.02.02.2016CrossRefGoogle Scholar
Réale, D and Dingemanse, NJ 2012 Encyclopedia of Life Science. John Wiley and Sons Ltd: Chichester, UKGoogle Scholar
Sachser, N, Kaiser, S and Hennessy, MB 2013 Behavioural pro-files are shaped by social experience: when, how and why. Philosophical Transactions of the Royal Society B: Biological Sciences 368: 20120344. https://doi.org/10.1098/rstb.2012.0344CrossRefGoogle Scholar
Sapolsky, R, Romero, LM and Munck, AU 2000 How do glu-cocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Reviews 21: 5589. https://doi.org/10.1210/edrv.21.1.0389Google ScholarPubMed
Sapolsky, RM 2005 The influence of social hierarchy on primate health. Science 308: 648. https://doi.org/10.1126/science.1106477CrossRefGoogle ScholarPubMed
Schildkraut, R 2016 Characteristation of positive welfare indices in captive African lions ( Panthera leo), University of Sydney, NSW, AustraliaGoogle Scholar
Schneiderman, N, Ironson, G and Siegel, SD 2005 Stress and health: psychological, behavioral, and biological determinants. Annual Review of Clinical Psychology 1: 607628. https://doi.org/10.1146/annurev.clinpsy.1.102803.144141CrossRefGoogle ScholarPubMed
Selye, H 1973 The evolution of the stress concept. American Scientist 61: 692699Google ScholarPubMed
Sgambelluri, E 2018 Noninvasive collection of saliva in Panthera leo: Creation and validation of a novel technique for health assessment in captive African lions ( Panthera leo). Masters, Antioch University, New England, USAGoogle Scholar
Sheriff, MJ, Dantzer, B, Delehanty, B, Palme, R and Boonstra, R 2011 Measuring stress in wildlife: techniques for quantifying glu-cocorticoids. Oecologia 166: 869887. https://doi.org/10.1007/s00442-011-1943-yCrossRefGoogle Scholar
Shrout, PE and Fleiss, JL 1979 Intraclass correlations: Uses in assessing rater reliability. Psychological Bulletin 86: 420428. https://doi.org/10.1037/0033-2909.86.2.420CrossRefGoogle ScholarPubMed
Stamps, JA 2007 Growth-mortality tradeoffs and ‘personality traits’ in animals. Ecology Letters 10: 355363. https://doi.org/10.1111/j.1461-0248.2007.01034.xCrossRefGoogle ScholarPubMed
Stearns, SC 1976 Life-history tactics: A review of the ideas. The Quarterly Review of Biology 51: 347. https://doi.org/10.1086/409052CrossRefGoogle ScholarPubMed
Terio, KA, Marker, L and Munson, L 2004 Evidence for chronic stress in captive but not free-ranging cheetahs (Acinonyx jubatus) based on adrenal morphology and function. Journal of Wildlife Diseases 40: 259266. https://doi.org/10.7589/0090-3558-40.2.259CrossRefGoogle Scholar
Terio, KA and Munson, L 2000 Gastritis in cheetahs and relat-edness to adrenal function. In: Pukazhenthi, B, Wildt, D and Mellen, J (eds) Felid Taxon Advisory Group Action Plan. Riverbanks Zoological Park & Botanical Garden, American Zoo and Aquarium Association: Columbia, SC, USAGoogle Scholar
Terwissen, CV, Mastromonaco, GF and Murray, DL 2013 Influence of adrenocorticotrophin hormone challenge and exter-nal factors (age, sex, and body region) on hair cortisol concentration in Canada lynx (Lynx canadensis). General and Comparative Endocrinology 194: 162167. https://doi.org/10.1016/j.ygcen.2013.09.010CrossRefGoogle 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
Torgerson-White, L and Bennett, C 2014 Rating methodolo-gy, personality axes, and behavioral plasticity: A case study in African Lions. Animal Behavior and Cognition 1: 230248. https://doi.org/10.12966/abc.08.02.2014CrossRefGoogle Scholar
Touma, C, Sachser, N, Möstl, E and Palme, R 2003 Effects of sex and time of day on metabolism and excretion of corticos-terone in urine and feces of mice. General and Comparative Endocrinology 130: 267278. https://doi.org/10.1016/S0016-6480(02)00620-2CrossRefGoogle ScholarPubMed
Van Buskirk, J 2012 Behavioural plasticity and environmental change. In: Candolin, UW and Wong, BBM (eds) Behavioural Responses to a Changing World. Mechanisms and Consequences pp 145158. Oxford University Press: Oxford, UK. https://doi.org/10.1093/acprof:osobl/9780199602568.003.0011CrossRefGoogle Scholar
van Oers, K, de Jong, G, van Noordwijk, AJ, Kempenaers, B and Drent, PJ 2005 Contribution of genetics to the study of ani-mal personalities: A review of case studies. Behaviour 142: 11851206. https://doi.org/10.1163/156853905774539364Google Scholar
van Oers, K and Mueller, JC 2010 Evolutionary genomics of ani-mal personality. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 365: 39914000. https://doi.org/10.1098/rstb.2010.0178CrossRefGoogle Scholar
Vaz, J, Narayan, EJ, Dileep Kumar, R, Thenmozhi, K, Thiyagesan, K and Baskaran, N 2017 Prevalence and determi-nants of stereotypic behaviours and physiological stress among tigers and leopards in Indian zoos. PLoS One 12: e0174711. https://doi.org/10.1371/journal.pone.0174711CrossRefGoogle Scholar
Wang, Q, Liu, D, Holyoak, M, Jia, T, Yang, S, Liu, X, Kong, X and Jiang, G 2019 Innate preference for native prey and personality implications in captive amur tigers. Applied Animal Behaviour Science 210: 95102. https://doi.org/10.1016/j.applanim.2018.10.006CrossRefGoogle Scholar
Ward, SJ and Melfi, V 2015 Keeper-animal interactions: Differences between the behaviour of zoo animals affect stock-manship. PLoS One 10: e0140237. https://doi.org/10.1371/journal.pone.0140237CrossRefGoogle Scholar
Watson, R, Munro, C, Edwards, KL, Norton, V, Brown, JL and Walker, SL 2013 Development of a versatile enzyme immunoas-say for non-invasive assessment of glucocorticoid metabolites in a diversity of taxonomic species. General and Comparative Endocrinology 186: 1624. https://doi.org/10.1016/j.ygcen.2013.02.001CrossRefGoogle Scholar
Webster, AB, Burroughs, REJ, Laver, P and Ganswindt, A 2018 Non-invasive assessment of adrenocortical activity as a measure of stress in leopards Panthera pardus. African Zoology: 1-8. https://doi.org/10.1080/15627020.2018.1467280CrossRefGoogle Scholar
Wielebnowski, NC 1999 Behavioral differences as predictors of breeding status in captive cheetahs. Zoo Biology 18: 335349. https://doi.org/10.1002/(SICI)1098-2361(1999)18:4<335::AID-ZOO8>3.0.CO;2-X3.0.CO;2-X>CrossRefGoogle Scholar
Wielebnowski, NC, Fletchall, N, Carlstead, K, Busso, JM and Brown, JL 2002 Noninvasive assessment of adrenal activity asso-ciated with husbandry and behavioral factors in the North American clouded leopard population. Zoo Biology 21: 7798. https://doi.org/10.1002/zoo.10005CrossRefGoogle Scholar
Wielebnowski, NC and Watters, J 2007 Applying fecal endocrine monitoring to conservation and behavior studies of wild mammals: important considerations and preliminary tests. Israel Journal of Ecology & Evolution 53: 439460. https://doi.org/10.1560/IJEE.53.3.439CrossRefGoogle Scholar
Wildt, DE, Howard, JG, Bush, M, Phillips, LG, Teare, A, Simmons, LG, Brown, JL and Chakraborty, PK 1988 A com-parative analysis of ejaculate and hormonal characteristics of the captive male cheetah, tiger, leopard, and puma. Biology of Reproduction 38: 245255. https://doi.org/10.1095/biolreprod38.2.245CrossRefGoogle Scholar
Wildt, DE, O’Brien, SJ, Howard, JG, Caro, TM, Roelke, ME, Brown, JL and Bush, M 1987 Similarity in ejaculate-endocrine characteristics in captive versus free-ranging cheetahs of two sub-species. Biology of Reproduction 36: 351360. https://doi.org/10.1095/biolreprod36.2.351CrossRefGoogle Scholar
Williams, TD 2008 Individual variation in endocrine systems: moving beyond the ‘tyranny of the Golden Mean’. Philosophical Transactions of the Royal Society B: Biological Sciences 363: 1687. https://doi.org/10.1098/rstb.2007.0003CrossRefGoogle ScholarPubMed
Wingfield, JC, Maney, DL, Breuner, CW, Jacobs, JD, Lynn, S, Ramenofsky, M and Richardson, RD 2015 Ecological bases of hormone-behavior interactions: The ‘emergency life history stage.’ Integrative and Comparative Biology 38: 191206. https://doi.org/10.1093/icb/38.1.191Google Scholar
Wolf, M, van Doorn, GS, Leimar, O and Weissing, FJ 2007 Life-history trade-offs favour the evolution of animal personalities. Nature 447: 581. https://doi.org/10.1038/nature05835CrossRefGoogle ScholarPubMed
Wolfensohn, S, Shotton, J, Bowley, H, Davies, S, Thompson, S and Justice, WSM 2018 Assessment of welfare in zoo animals: Towards optimum quality of life. Animals 8: 110. https://doi.org/10.3390/ani8070110CrossRefGoogle ScholarPubMed
Young, KM, Walker, SL, Lanthier, C, Waddell, WT, Monfort, SL and Brown, JL 2004 Noninvasive monitoring of adrenocorti-cal activity in carnivores by fecal glucocorticoid analyses. General and Comparative Endocrinology 137: 148165. https://doi.org/10.1016/j.ygcen.2004.02.016CrossRefGoogle ScholarPubMed
Zayan, R 1991 The specificity of social stress. Behavioural Processes 25: 8193. https://doi.org/10.1016/0376-6357(91)90011-NCrossRefGoogle ScholarPubMed
Zoological Information Management System (ZIMS) https://www.species360.org/Google Scholar
Supplementary material: File

Vaz et al. supplementary material
Download undefined(File)
File 161 KB