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Can eye surface temperature be used to indicate a stress response in harbour seals (Phoca vitulina)?

Published online by Cambridge University Press:  01 January 2023

AM MacRae*
Affiliation:
Animal Welfare Program, University of British Columbia, 2357 Main Mall, Vancouver BC, V6T IZ4, Canada
P McGreevy
Affiliation:
Sydney School of Veterinary Science, Faculty of Science, University of Sydney, Sydney, NSW 2006, Australia
RR Daros
Affiliation:
Animal Welfare Program, University of British Columbia, 2357 Main Mall, Vancouver BC, V6T IZ4, Canada Graduate Program in Animal Science, School of Life Sciences, Pontifícia Universidade Católica do Paraná, Curitiba, PR, 80215-901, Brazil
D Fraser
Affiliation:
Animal Welfare Program, University of British Columbia, 2357 Main Mall, Vancouver BC, V6T IZ4, Canada
*
* Contact for correspondence: amelia.macrae@ubc.ca
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Abstract

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Infra-red thermography (IRT) is increasingly being used to estimate physiological stress responses in animals via changes in eye surface temperature. The aim of this study was to determine whether eye temperature of harbour seals (Phoca vitulina) changes in response to routine handling and the potentially painful procedure of flipper-tagging, and if responses to tagging can be mitigated by subcutaneous injection of lidocaine. Orphaned pups (n = 52) at a rehabilitation facility were assigned to one of four treatments: Lidocaine (handled twice, once for injection and once for tagging); Saline (also handled twice); Tag Only (handled once); Sham Tag (handled once). Eye temperature increased more when pups were first handled compared to pups that were not handled and increased further in pups that underwent a second handling. Eye temperature of pups that were tagged without any previous treatment (Tag Only) increased compared to pups that were sham-tagged. Eye temperature also tended to increase after pups were injected with lidocaine but not saline. These results suggest that: (i) handling causes a physiological stress response; (ii) increased eye temperature arising from the second handling suggests the first handling was likely aversive, resulting in sensitisation to further handling; (iii) the rise in eye temperature after tagging, but not sham-tagging, may reflect pain from tagging; and (iv) lidocaine, at the dosage tested, did not appear to reduce the physiological response to tagging. These results show promise for the use of eye temperature to monitor stress responses and for evaluating the potential aversiveness of routine procedures in seals.

Type
Research Article
Copyright
© 2021 Universities Federation for Animal Welfare

References

Alam, MGS and Dobson, H 1986 The effect of various veteri-nary procedures on plasma concentrations of cortisol, luteinising hormone and prostaglandin F2 alpha metabolite in the cow. The Veterinary Journal 118: 710. https://doi.org/10.1136/vr.118.1.7Google Scholar
Bates, D, Mächler, M, Bolker, B and Walker, S 2015 Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67: 148. https://doi.org/10.18637/jss.v067.i01CrossRefGoogle Scholar
Buynitsky, T and Mostofsky, DI 2009 Restraint stress in biobe-havioral research: Recent developments. Neuroscience and Biobehavioral Reviews 33: 10891098. https://doi.org/10.1016/j.neu-biorev.2009.05.004CrossRefGoogle ScholarPubMed
Cepeda, MS, Tzortzopoulou, A, Thackrey, M, Hudcova, J, Arora Gandhi, P and Schumann, R 2012 Adjusting the pH of lidocaine for reducing pain on injection. Evidence-Based Child Health 7: 149215. https://doi.org/10.1002/ebch.1811CrossRefGoogle Scholar
Cook, NJ, Church, JS, Schaefer, AL, Webster, JR, Matthews, LR and Suttie, JM 2005 Stress and pain assessment of velvet antler removal from Elk (Cervus elaphus canadensis) and Reindeer (Rangifer tarandus). Online Journal of Veterinary Research 9: 2436Google Scholar
Cook, NJ, Schaefer, AL, Warren, L, Burwash, L, Anderson, M and Baron, V 2001 Adrenocortical and metabolic responses to ACTH injection in horses: An assessment by salivary cortisol and infrared ther-mography of the eye. Canadian Journal of Animal Science 81: 621Google Scholar
Dahlborn, K, Bugnon, P, Nevalainen, T, Raspa, M, Verbost, P and Spangenberg, E 2013 Report of the Federation of European Laboratory Animal Science Associations Working Group on Animal Identification. Laboratory Animals 47: 211. https://doi.org/10.1177/002367712473290CrossRefGoogle Scholar
Dai, F, Cogi, NH, Heinzl, EUL, Dalla Costa, E, Canali, E and Minero, M 2015 Validation of a fear test in sport horses using infrared thermography. Journal of Veterinary Behavior: Clinical Applications and Research 10: 128136. https://doi.org/10.1016/j.jveb.2014.12.001CrossRefGoogle Scholar
Fenner, K, Yoon, S, White, P, Starling, M and McGreevy, P 2016 The effect of noseband tightening on horses’ behavior, eye temperature, and cardiac responses. PLoS One 11: 120. https://doi.org/10.1371/journal.pone.0154179CrossRefGoogle ScholarPubMed
Flecknell, PA 2000 Animal pain: an introduction. In: Flecknell, PA and Waterman-Pearson, A (eds) Pain Management in Animals pp 17. WB Saunders: London, UK. https://doi.org/10.1016/B978-0-7020-1767-4.50004-7CrossRefGoogle Scholar
Gulland, FMD, Haulena, M and Dierauf, LA 2001 Seals and sea lions. In: Dierauf, LA and Gulland, FMD (eds) CRC Handbook of Marine Mammal Medicine: Health, Disease, and Rehabilitation, Second Edition pp 907915. Taylor & Francis: Boca Raton, USA. https://doi.org/10.1201/9781420041637.ch41CrossRefGoogle Scholar
Gutiérrez, J, Simeone, C, Gulland, F and Johnson, S 2016 Development of retrobulbar and auriculopalpebral nerve blocks in California sea lions (Zalophus californianus). Journal of Zoo and Wildlife Medicine 47: 236243. https://doi.org/10.1638/2015-0035.1CrossRefGoogle ScholarPubMed
Hemmer, H 1990 Domestication: The Decline in Environmental Appreciation. Cambridge University Press: Cambridge, UKGoogle Scholar
Kim, EJ, Kim, ES, Covey, E and Kim, JJ 2010 Social transmission of fear in rats: the role of 22-kHz ultrasonic distress vocalization. PLoS One 5: e15077. https://doi.org/10.1371/journal.pone.0015077CrossRefGoogle ScholarPubMed
Künzl, C and Sachser, N 1999 The behavioural endocrinology of domestication: A comparison between the domestic guinea pig (Cavia aperea f porcellus) and its wild ancestor, the cavy (Cavia aperea). Hormones and Behavior 35: 2837. https://doi.org/10.1006/hbeh.1998.1493CrossRefGoogle ScholarPubMed
Kuznetsova, A, Brockhoff, PB and Christensen, RHB 2017 LmerTest: tests in linear mixed effects models. Journal of Statistical Software 82: 126. https://doi.org/10.18637/jss.v082.i13CrossRefGoogle Scholar
Lapierre, JL, Schreer, JF, Burns, JM and Hammill, MO 2007 Effect of diazepam on heart and respiratory rates of harbor seal pups following intravenous injection. Marine Mammal Science 23:209217. https://doi.org/10.1111/j.1748-7692.2006.00097.xCrossRefGoogle Scholar
Leslie, E, Hernández-Jover, M, Newman, R and Holyoake, P 2010 Assessment of acute pain experienced by piglets from ear tagging, ear notching and intraperitoneal injectable transponders. Applied Animal Behaviour Science 127: 8695. https://doi.org/10.1016/j.applanim.2010.09.006CrossRefGoogle Scholar
MacRae, AM, Haulena, M and Fraser, D 2010 The effect of diet and feeding level on survival and weight gain of hand-raised harbor seal pups (Phoca vitulina). Zoo Biology 29: 110. https://doi.org/10.1002/zoo.20356Google Scholar
MacRae, AM, Makowska, IJ and Fraser, D 2018 Initial evaluation of facial expressions and behaviours of harbour seal pups (Phoca vitulina) in response to tagging and microchipping. Applied Animal Behaviour Science 205: 167174. https://doi.org/10.1016/j.applanim.2018.05.001CrossRefGoogle Scholar
McCafferty, DJ 2007 The value of infrared thermography for research on mammals: previous applications and future directions. Mammal Review 37: 207223. https://doi.org/10.1111/j.1365-2907.2007.00111.xCrossRefGoogle Scholar
McGreevy, P, Warren-Smith, A and Guisard, Y 2012 The effect of double bridles and jaw-clamping crank nosebands on temperature of eyes and facial skin of horses. Journal of Veterinary Behavior: Clinical Applications and Research 7: 142148. https://doi.org/10.1016/j.jveb.2011.08.001CrossRefGoogle Scholar
Moberg, GP 2000 Biological responses 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 121. CABI Publishing: Wallingford, UK. https://doi.org/10.1079/9780851993591.0001CrossRefGoogle Scholar
National Research Council 2009 Recognition and Alleviation of Pain in Laboratory Animals. The National Academies Press: Washington, DC, USAGoogle Scholar
Olsson, A and Phelps, EA 2007 Social learning of fear. Nature Neuroscience 10: 10951102. https://doi.org/10.1038/nn1968CrossRefGoogle ScholarPubMed
Pavlidis, I and Levine, JA 2002 Thermal image analysis for poly-graph testing. IEEE Engineering in Medicine and Biology 21: 5664. https://doi.org/10.1109/MEMB.2002.1175139CrossRefGoogle ScholarPubMed
Price, EO 1998 Behavioural genetics and the process of domes-tication. In: Grandin, T (ed) Genetics and the Behaviour of Domestic Animals pp 3165. Academic Press: New York, USAGoogle Scholar
R Core Team 2015 R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing: Vienna, AustriaGoogle Scholar
Rutherford, KMD 2002 Assessing pain in animals. Animal Welfare 11: 3153CrossRefGoogle Scholar
Stewart, M, Schaefer, AL, Haley, DB, Colyn, J, Cook, NJ, Stafford, KJ and Webster, JR 2008a Infrared thermography as a non-invasive method for detecting fear-related responses of cat-tle to handling procedures. Animal Welfare 17: 387393CrossRefGoogle Scholar
Stewart, M, Stafford, KJ, Dowling, SK, Schaefer, AL and Webster, JR 2008b Eye temperature and heart rate variability of calves disbudded with or without local anaesthetic. Physiology & Behavior 93: 789797. https://doi.org/10.1016/j.phys-beh.2007.11.044CrossRefGoogle ScholarPubMed
Stewart, M, Stookey, JM, Stafford, KJ, Tucker, CB, Rogers, AR, Dowling, SK, Verkerk, GA, Schaefer, AL and Webster, JR 2009 Effects of local anesthetic and a nonsteroidal antiinflam-matory drug on pain responses of dairy calves to hot-iron dehorning. Journal of Dairy Science 92: 15121519. https://doi.org/10.3168/jds.2008-1578CrossRefGoogle Scholar
Stewart, M, Verkerk, GA, Stafford, KJ, Schaefer, AL and Webster, JR 2010 Noninvasive assessment of autonomic activity for evaluation of pain in calves, using surgical castration as a model. Journal of Dairy Science 93: 36023609. https://doi.org/10.3168/jds.2010-3114CrossRefGoogle ScholarPubMed
Stewart, M, Webster, JR, Schaefer, AL, Cook, NJ and Scott, SL 2005 Infrared thermography as a non-invasive tool to study animal welfare. Animal Welfare 14: 319325CrossRefGoogle Scholar
Stewart, M, Webster, JR, Verkerk, GA, Schaefer, AL, Colyn, JJ and Stafford, KJ 2007 Non-invasive measurement of stress in dairy cows using infrared thermography. Physiology & Behavior 92: 520525. https://doi.org/10.1016/j.phys-beh.2007.04.034CrossRefGoogle ScholarPubMed
Torrey, S, Devillers, N, Lessard, M, Farmer, C and Widowski, T 2009 Effect of age on the behavioral and physiological responses of piglets to tail docking and ear notching. Journal of Animal Science 87: 17781786. https://doi.org/10.2527/jas.2008-1354CrossRefGoogle ScholarPubMed
Travain, T, Colombo, ES, Heinzl, E, Bellucci, D, Prato Previde, E and Valsecchi, P 2015 Hot dogs: Thermography in the assessment of stress in dogs (Canis familiaris): A pilot study. Journal of Veterinary Behavior: Clinical Applications and Research 10:1723. https://doi.org/10.1016/j.jveb.2014.11.003CrossRefGoogle Scholar
Valverde, A and Gunkel, CI 2005 Pain management in hors-es and farm animals. Journal of Veterinary Emergency and Critical Care 15: 295307. https://doi.org/10.1111/j.1476-4431.2005.00168.xCrossRefGoogle Scholar
Yarnell, K, Hall, C and Billett, E 2013 An assessment of the aversive nature of an animal management procedure (clipping) using behavioral and physiological measures. Physiology & Behavior 118: 3239. https://doi.org/10.1016/j.phys-beh.2013.05.013CrossRefGoogle ScholarPubMed