Close and frightening: predator presence affects cortisol levels in captive felines Volobueva K.A., Naidenko S.V. P. 187-195 Exhibitions, where animals of various species are kept close to each other, are increasingly used in zoos and live collections. Such co-housing may not be suitable for some species: the presence of a large predator may cause stress to smaller heterospecifics (for example, potential prey) and even when the enclosures have no direct intersections and are merely close together. We evaluated the effects of a potentially dangerous predator on the welfare of typical potential prey/competitors kept in close proximity to this predator. Amur wildcats and caracals were kept one at a time in enclosures next to lynx. Stress level was assessed by analysing the dynamics of glucocorticoids (cortisol’s metabolites) using non-invasive methods. The results showed that the presence of a predator in a neighbouring enclosure with an Amur wildcat did not change their cortisol concentrations significantly. However, hormone levels in animals kept at some distance from the lynx were twice as high as when they were in close proximity to the predator. Unlike Amur wildcats, caracals were more sensitive to the presence of a heterospecific. For Amur wildcats the presence of shelters in enclosures and the absence of direct lynxes’ pursuit may have been sufficient to reduce the negative impact of a large predator.
DOI: 10.15298/rusjtheriol.23.2.08References- Alekseeva G.S., Loshchagina J.A., Erofeeva M.N. & Naidenko S.V. 2020. Stressed by maternity: changes of cortisol level in lactating domestic cats // Animals. Vol.10. No.5. P.903.
- Anderson U.S., Benne M., Bloomsmith M.A. & Maple T.L. 2002. Retreat space and human visitor density moderate undesirable behavior in petting zoo animals // Journal of Applied Animal Welfare Science. Vol.5. No.2. P.125–137.
- Anisman H., Hayley S., Kelly O., Borowski T. & Merali Z. 2001. Psychogenic, neurogenic, and systemic stressor effects on plasma corticosterone and behavior: mouse strain-dependent outcomes // Behavioral Neuroscience. Vol.115. No.2. P.443.
- Apfelbach R., Blanchard C.D., Blanchard R.J., Hayes R.A. & McGregor I.S. 2005. The effects of predator odors in mammalian prey species: a review of field and laboratory studies // Neuroscience and Biobehavioral Reviews. Vol.29. No.8. P.1123–1144.
- Bayazit V. 2009. Evaluation of Cortisol and Stress in Captive Animals // Australian Journal of Basic and Applied Sciences. Vol.3. No.2. P.1022–1031.
- Blanchard R.J., Nikulina J.N., Sakai R.R., McKittrick C., McEwen B. & Blanchard D.C. 1998. Behavioral and endocrine change following predatory stress // Physiology & Behavior. Vol.63. No.4. P.561–569.
- Blaney E.C. & Walls D.L. 2004. The influence of a camouflage net barrier on the behavior, welfare, and public perceptions of zoo-housed gorillas // Animal Welfare. Vol.13. No.2. P.111–118.
- Brown J.L. & Comizzoli P. 2018. Female cat reproduction // Skinner M.K. (ed.). Encyclopedia of Reproduction. 2nd ed. Academic Press: Elsevier. Vol.2. P.692–701. http://dx.doi.org/10.1016/B978-0-12-809633-8.20638-9.
- Carlstead K., Brown J.L. & Seidensticker J. 1993. Behavioral and adrenocortical responses to environmental changes in leopard cats (Felis bengalensis) // Zoo Biology. Vol.12. No.4. P.321–331.
- Chaby L.E., Cavigelli S.A., Hirrlinger A.M., Caruso M.J. & Braithwaite V.A. 2015. Chronic unpredictable stress during adolescence causes long-term anxiety // Behavioral Brain Research. Vol.278. P.492–495.
- Coe J.C. 2001. Mixed-species exhibits // Bell C.E. (ed.). Encyclopedia of the World’s Zoos. Vol.2. Chicago: IL Fitzroy Dearborn Publishers. P.817–821.
- Creel S., Dantzer B., Goymann W. & Rubenstein D.R. 2013. The ecology of stress: effects of the social environment // Functional Ecology. Vol.27. No.1. P.66–80.
- Crossey B., Chimimba C., du Plessis C., Hall G. & Ganswindt A. 2020. Using faecal glucocorticoid metabolite analyses to elucidate stressors of African wild dogs Lycaon pictus from South Africa // Wildlife Biology. Vol.2020. No.1. P.1–10.
- File S.E., Zangrossi H., Sanders F.L. & Mabbutt P.S. 1995. Dissociation between behavioral and corticosterone responses to repeated exposures to cat odor // Physiology & Behavior. Vol.54. No.6. P.1109–1111.
- Gerlinskaya L.A., Moshkin M.P. & Evsikov V.I. 1993. [Methodological approaches to the assessment of stressed wild mammals] // Ecologiya. Vol.6. P.97–100 [in Russian, with English summary].
- Ghimirey Y., Petersen W., Jahed N., Akash M., Lynam A.J., Kun S., Din J., Nawaz M.A., Singh P., Dhendup T., Marcus C., Gray T.N.E. & Phyoe Kyaw P. 2022. Prionailurus bengalensis. The IUCN Red List of Threatened Species: e.T18146A212958253. https://dx.doi.org/10.2305/IUCN.UK.2022-1.RLTS.T18146A212958253.en
- Hardie S.M., Prescott M.J. & Buchannan-Smith H.M. 2003. Ten years of mixed-species troops at Belfast Zoological Gardens // Primate Report. Vol.65. P.21–38.
- Hediger H. 2013. Wild Animals in Captivity. Oxford: Butterworth-Heinemann. 240 p.
- Hemsworth P.H. & Barnett J.L. 2000. Human-animal interactions and animal stress // Moberg G.P. & Mench J.A. (eds.). The Biology of Animal Stress: Basic Principles and Implications for Animal Welfare. Wallingford, UK: CABI Publishing. P.309–335.
- Hillman E., Mayer C. & Schroder L. 2004. Lying behaviour and adrenocortical response as indicators of the thermal tolerance of pigs of different weights // Animal Welfare. Vol.13. No.3. P.329–335.
- Hulsman A., Dalerum F., Ganswindt A., Muenscher S., Bertschinger H. & Paris M. 2011. Non-invasive monitoring of glucocorticoid metabolites in brown hyaena (Hyaena brunnea) faeces // Zoo Biology. Vol.30. No.4. P.451–458.
- Husak J.F. & Moore I.T. 2008. Stress hormones and mate choice // Trends in Ecology & Evolution. Vol.23. No.10. P.532–534.
- İlemin Y., Kaynaş B.Y. & Yılmaz T. 2020. Evidence on sympatric occurrence of Caracal caracal and Lynx lynx in Anatolia // Biology Bulletin. Vol.47. P.633–639.
- Ivanov E.A., Rozhnov V.V. & Naidenko S.V. 2017. The effect of ambient temperature on glucocorticoid level in the Amur tiger (Panthera tigris altaica) // Russian Journal of Ecology. Vol.48. No.3. P.294.
- Ivanov E.A., Sidorchuk N.V., Rozhnov V.V. & Naidenko S.V. 2014. Noninvasive estimation of the hypothalamic-pituitary-adrenal system activity in the Far East leopard // Doklady Biological Sciences. Vol.456. No.1. P.165. DOI: 10.1134/S0012496614030120
- Jansen C., Leslie A.J., Cristescu B., Teichman K.J. & Martins Q. 2019. Determining the diet of an African mesocarnivore, the caracal: scat or GPS cluster analysis? // Wildlife Biology. Vol.2019. No.1. P.1–8.
- Jewgenow K., Naidenko S.V., Goeritz F., Vargas A. & Dehnhard M. 2006. Monitoring testicular activity of male Eurasian (Lynx lynx) and Iberian (Lynx pardinus) lynx by fecal testosterone metabolite measurement // General and Comparative Endocrinology. Vol.149. No.2. P.151–158.
- Khorozyan I. & Heurich M. 2023. Patterns of predation by the Eurasian lynx Lynx lynx throughout its range: ecological and conservation implications // Mammal Review. Vol.53. No.3. P.177–188. DOI: 10.1111/mam.12317
- Keay J.M., Singh J., Gaunt M.C. & Kaur T. 2006. Fecal glucocorticoids and their metabolites as indicators of stress in various mammalian species: a literature review // Journal of Zoo and Wildlife Medicine. Vol.37. No.3. P.234–244.
- Koolhaas J.M., Bartolomucci A., Buwalda B., de Boer S.F., Flügge G., Korte M.S., Meerlo P., Murison R., Olivier B. & Palanza P. 2011. Stress revisited: a critical evaluation of the stress concept // Neuroscience & Biobehavioral Reviews. Vol.35. No.5. P.1291–1301.
- Koordinierte K.O.R.A. 2004. Status and Conservation of the Eurasian lynx (Lynx lynx) in Europe in 2001. 19th ed. Switzerland: Kora. 319 p.
- Larm M., Hovland A.L., Palme R., Thierry A.-M., Miller A.L., Landa A., Angerbjörn A. & Eide N.E. 2021. Fecal glucocorticoid metabolites as an indicator of adrenocortical activity in Arctic foxes (Vulpes lagopus) and recommendations for future studies // Polar Biology. Vol.44. P.1925–1937.
- Law S., Prankel S., Schwitzer C. & Dutton J. 2021. Inter-specific interactions involving Lemur catta housed in mixed-species exhibits in UK zoos // Journal of Zoo and Aquarium Research. Vol.9. No.4. P.247–258.
- Leonardi R., Buchanan-Smith H.M., Dufour V., MacDonald C. & Whiten A. 2010. Living together: behavior and welfare in single and mixed species groups of capuchin (Cebus apella) and squirrel monkeys (Saimiri sciureus) // American Journal of Primatology. Vol.72. No.1. P.33–47.
- Liu J., Chen Y., Guo L., Gu Bo & Liu H. 2006. Stereotypic behavior and fecal cortisol level in captive giant pandas in relation to environmental enrichment // Zoo Biology. Vol.25. No.6. P.445–459.
- Malinow M.R., Hill J.D. & Ochsner 3rd A.J. 1974. Heart rate in caged rhesus monkeys (Macaca mulatta) // Laboratory Animal Science. Vol.24. No.3. P.537–540.
- Marai I.F.M. & Rashwan A.A. 2004. Rabbits’ behavioural response to climatic and managerial conditions: a review // Archives Animal Breeding. Vol.47. No.5. P.469–482.
- McGlone J.J. & Curtis S.E. 1985. Behavior and performance of weanling pigs in pens equipped with hide areas // Journal of Animal Science. Vol.60. No.1. P.20–24.
- Millspaugh J.J. & Washburn B.E. 2004. Use of fecal glucocorticoid metabolite measures in conservation biology research: considerations for application and interpretation // General and Comparative Endocrinology. Vol.13. No.3. P.189–199.
- Moqanaki E.M., Farhadinia M.S., Tourani M. & Akbari H. 2016. The caracal in Iran: current state of knowledge and priorities for conservation // Cat News Special. Vol.10. P.27–32.
- Morgan K.N. & Tromborg C.T. 2007. Sources of stress in captivity // Applied Animal Behaviour Science. Vol.102. No.3–4. P.262–302.
- Mousavi M., Moqanaki E.M., Farhadinia M.S., Adibi M.A., Rabiee K. & Khosravi S. 2016. The largest lesser cat in Iran — current status of the Eurasian lynx // Cat News Special. Vol.10. P.33–37.
- Naidenko S.V. 1997. [Social Behaviour of the Lynx (Lynx lynx L., Felidae, Carnivora) and Some Features of its Formation in Ontogeny]. Diss. PhD Biol. Sci. Moscow: IPEE RAN. 251 p. [in Russian].
- Naidenko S.V., Berezhnoi M.A., Kumar V. & Umapathy G. 2019. Comparison of tigers’ fecal glucocorticoids level in two extreme habitats // PLoS ONE. Vol.14. No.4. P.e0214447. DOI: 10.1371/journal.pone.0214447
- Naidenko S.V., Ivanov E.A., Lukarevskii V.S., Hernandez-Blanco J.A., Sorokin P.A., Litvinov M.N., Kotlyar A.K. & Rozhnov V.V. 2011. Activity of the hypothalamo–pituitary–adrenals axis in the Siberian tiger (Panthera tigris altaica) in captivity and in the wild, and its dynamics throughout the year // Biology Bulletin. Vol.38. P.301–305.
- Nájera F., Sánchez-Cuerda S., López G., Del Rey-Wamba T., Rueda C., Vallverdú-Coll N., Panadero J., Palacios M.J., López-Bao J.V. & Jiménez J. 2019. Lynx eats cat: disease risk assessment during an Iberian lynx intraguild predation // European journal of Wildlife Research. Vol.65. P.1–5.
- Palme R. 2019. Non-invasive measurement of glucocorticoids: advances and problems // Physiology & Behavior. Vol.199. P.229–243.
- Pavlova E.V. & Naidenko S.V. 2012. [Characteristics of the basal adrenal activity and its relation to the behavior of far-east cat (Prionailurus bengalensis euptilura)] // Zoologicheskii Zhurnal. Vol.91. P.1261–1272 [in Russian, with English summary].
- Pavlova E.V. & Naidenko S.V. 2008. [Noninvasive monitoring of glucocorticoids in the feces of the Amur leopard cat (Prionailurus bengalensis euptilura)] // Zoologicheskii Zhurnal. Vol.87. No.11. P.1375–1381 [in Russian, with English summary].
- Pearce G.P. & Patterson A.M. 1993. The effect of space restriction and provision of toys during rearing on the behaviour productivity, and physiology of male pigs // Applied Animal Behaviour Science. Vol.36. No.1. P.11–28.
- Popov S.V. 2010. [Environmental uncertainty and arousal/stress as the direct determinants of animal behaviour] // Zhurnal Obshchei Biologii. Vol.71. No.4. P.287–297 [in Russian, with English summary].
- Probst C. & Matschei C. 2008. Mixed-species exhibits with mammals in central European zoos // International Zoo News. Vol.55. No.6. P.324–347
- Romero L.M. & Butler L.K. 2007. Endocrinology of Stress // International Journal of Comparative Psychology. Vol.20. No.2. P.89–95. DOI:10.46867/ijcp.2007.20.02.15
- Ross S.R., Holmes A.N. & Lonsdorf E.V. 2009. Interactions between zoo-housed great apes and local wildlife //American Journal of Primatology. Vol.71. No.6. P.458–465.
- Sheriff M.J., Dantzer B., Delehanty B., Palme R. & Boonstra R. 2011. Measuring stress in wildlife: Techniques for quantifying glucocorticoids // Oecologia. Vol.166. No.4. P.869–887.
- Slos S. & Stoks R. 2008. Predation risk induces stress proteins and reduces antioxidant defense // Functional Ecology. Vol.22. No.4. P.637–642.
- Sunde P., Overskaug K. & Kvam, T. 1999. Intraguild predation of lynxes on foxes: evidence of interference competition? // Ecography. Vol.22. No.5. P.521–523.
- Timmer M. & Sandi C. 2010. A role for glucocorticoids in the long-term establishment of a social hierarchy // Psychoneuroendocrinology. Vol.35. No.10. P.1543–1552.
- Wielebnowski N.C., Fletchall N., Carlstead K., Busso J.M. & Brown J.L. 2002. Noninvasive assessment of adrenal activity associated with husbandry and behavioral factors in the North American clouded leopard population // Zoo Biology. Vol.21. No.1. P.77–98.
- Yudin V.G. 2015. [Amur Wildcat]. Vladivostok: Dal’nauka. 443 p. [in Russian].
- Ziegler T. 2002. Selected mixed species exhibits in zoological gardens (Part 1) // Primate Report. Vol.64. P.1–89.
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