Hostname: page-component-77c89778f8-m8s7h Total loading time: 0 Render date: 2024-07-17T07:43:32.575Z Has data issue: false hasContentIssue false
  • English
  • Français

A review of behavioural and physiological responses of sheep to stressors to identify potential behavioural signs of distress

Published online by Cambridge University Press:  11 January 2023

MS Cockram
MS Cockram*
Affiliation:
Animal Welfare Research Group, Division of Animal Health and Welfare, Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush Veterinary Centre, Easter Bush, Roslin, Midlothian EH25 9RG, UK
*
M.S.Cockram@ed.ac.uk
Get access Rights & Permissions [Opens in a new window]

Abstract

This paper discusses the potential for using observations of behaviour to recognise distress in sheep. The term distress is used to describe situations in which an animal is likely to be suffering, and is indicating this by overt behavioural signs. Literature on the behavioural responses of sheep to procedures that induce a physiological stress response is reviewed. This approach is based on human analogy and the assumption that physiological changes can be used to differentiate between stimuli that induce an emotional response in sheep and those that do not. The degree to which the behaviour of sheep in certain situations represents, at least in part, an expression of emotional behaviour, or whether it can be fully explained as a functional response to a specific situation, is a fundamental and unresolved question in ethological and psychological studies. Therefore, the validity of compiling a list of objective common behavioural indicators of distress in sheep will be contentious. However, it is important to be able to recognise and deal with suffering, and the use of behavioural methods for the identification of distress in sheep is a practical welfare issue. There is a need for further research to identify indicators of distress in sheep, but in the meantime it would be reasonable to make the judgement that, in some circumstances, sheep that are found to be vocalising, panting, and/or showing markedly increased locomotory activity could be experiencing distress.

Keywords

animal welfarebehaviourbehavioural indicatorsdistresssheepstress
Type
Research Article
Information
Animal Welfare , Volume 13 , Issue 3 , August 2004 , pp. 283 - 291
Copyright
© 2004 Universities Federation for Animal Welfare

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Archer, J 1973 Tests for emotionality in rats and mice: a review. Animal Behaviour 21: 205–235CrossRefGoogle ScholarPubMed
Baldock, NM and Sibly, RM 1990 Effects of handling and transportation on the heart rate and behaviour of sheep. Applied Animal Behaviour Science 28: 15–39CrossRefGoogle Scholar
Black, H, Matthews, LR and Bremner, KJ 1994 The behaviour of male lambs transported by sea from New Zealand to Saudi Arabia. New Zealand Veterinary Journal 42: 16–23CrossRefGoogle ScholarPubMed
Blaxter, KL, Graham, NM, Wainman, FW and Armstrong, DG 1959 Environmental temperature, energy metabolism and heat regulation in sheep. II. The partition of heat losses in closely clipped sheep. Journal of Agricultural Science 52: 25–40CrossRefGoogle Scholar
Bobek, S, Niezgoda, J, Pierzchala, K, Litynski, P and Sechman, A 1986 Changes in circulating levels of iodothyronines, cortisol and endogenous thiocyanate in sheep during emotional stress caused by isolation of the animals from the flock. Zentralblatt Fur Veterinarmedizin Reihe A (Journal of Veterinary Medicine, Series A, Animal Physiology, Pathology and Clinical Veterinary Medicine) 33: 698–705Google ScholarPubMed
Boivin, X, Nowak, R, Despres, G, Tournadre, H and Le Neindre, P 1997 Discrimination between shepherds by lambs reared under artificial conditions. Journal of Animal Science 75: 2892–2898CrossRefGoogle ScholarPubMed
Bowers, CL, Friend, TH, Grissom, KK and Lay, DC 1993 Confinement of lambs (Ovis aries) in metabolism stalls increased adrenal function, thyroxine and motivation for movement. Applied Animal Behaviour Science 36: 149–158CrossRefGoogle Scholar
Cannon, WB 1939 Bodily Changes in Pain, Hunger, Fear and Rage: An Account of Recent Research into the Function of Emotional Excitement. Appleton-Century Company: New York, USAGoogle Scholar
Cockram, MS, Imlah, P, Goddard, PJ, Harkiss, GD and Waran, NK 1993 The behavioural, endocrine and leukocyte response of ewes to repeated removal of lambs before the age of natural weaning. Applied Animal Behaviour Science 38: 127–142CrossRefGoogle Scholar
Cockram, MS, Kent, JE, Goddard, PJ, Waran, NK, McGilp, IM, Jackson, RE, Muwanga, GM and Prytherch, S 1996 Effect of space allowance during transport on the behavioural and physiological responses of lambs during and after transport. Animal Science 62: 461–477CrossRefGoogle Scholar
Cockram, MS, Ranson, M, Imlah, P, Goddard, PJ, Burrells, C and Harkiss, GD 1994 The behavioural, endocrine and immune response of sheep to isolation. Animal Production 58: 389–399Google Scholar
Connolly, GE, Timm, RM, Howard, WE and Longhurst, WM 1976 Sheep killing behavior of captive coyotes. Journal of Wildlife Management 40: 400–407CrossRefGoogle Scholar
Cook, CJ, Mellor, DJ, Harris, PJ, Ingram, JR and Matthews, LR 2000 Hands-on and hands-off measurement of stress. In: Moberg, GP and Mench, JA (eds) The Biology of Animal Stress: Basic Principles and Implications for Animal Welfare pp 123–146. CAB International: Wallingford, UKCrossRefGoogle Scholar
Desire, L, Boissy, A and Veissier, I 2002 Emotions in farm animals: a new approach to animal welfare in applied ethology. Behavioural Processes 60: 165–180Google ScholarPubMed
Done-Currie, JR, Hecker, JF and Wodzicka-Tomaszewska, M 1984 Behaviour of sheep transferred from pasture to an animal house. Applied Animal Behaviour Science 12: 121–130CrossRefGoogle Scholar
Dwyer, CM 2004 How has the risk of predation shaped the behavioural responses of sheep to fear and distress? Animal Welfare 13(3): 269–281Google Scholar
Ewbank, R 1985 Behavioral responses to stress in farm animals. In: Moberg, GP (ed) Animal Stress pp 71–79. American Physiological Society: Bethesda, USACrossRefGoogle Scholar
Fraser, AF 1960 Spontaneously occurring forms of ‘tonic immobility’ in farm animals. Canadian Journal of Comparative Medicine and Veterinary Science 24: 330–333Google ScholarPubMed
Frid, A 1997 Vigilance by female Dall's sheep: interactions between predation risk factors. Animal Behaviour 53: 799–808CrossRefGoogle Scholar
Gay, CC 2000 Clinical examination of sheep and goats. In: Radostitis, OM, Mayhew, IG and Houston, DM (eds) Veterinary Clinical Examination and Diagnosis, 9th Edition pp 179–190. WB Saunders: London, UKGoogle Scholar
Graham, AD, Christopherson, RJ and Thompson, JR 1981 Endocrine and metabolic changes in sheep associated with acclimation to constant and intermittent cold exposure. Canadian Journal of Animal Science 61: 81–90CrossRefGoogle Scholar
Guerrini, VH and Bertchinger, H 1982 Effect of ambient temperature and humidity on plasma cortisol in sheep. British Veterinary Journal 138: 175–182CrossRefGoogle ScholarPubMed
Guerrini, VH, Koster, N and Bertchinger, H 1980 Effect of ambient temperature and humidity on urine output in sheep. American Journal of Veterinary Research 41: 1851–1853Google ScholarPubMed
Hales, JRS 1973 Effects of exposure to hot environments on the regional distribution of blood flow and on cardiorespiratory function in sheep. Pflugers Archiv 344: 133–148CrossRefGoogle ScholarPubMed
Hales, JRS and Brown, GD 1974 Net energetic and thermoregulatory efficiency during panting in sheep. Comparative Biochemistry and Physiology 49A: 413-422CrossRefGoogle Scholar
Henry, JP 1976 Mechanism of psychosomatic disease in animals. Advances in Veterinary Science and Comparative Medicine 20: 115–145Google ScholarPubMed
Houpt, KA 1998 Domestic Animal Behaviour for Veterinarians and Animal Scientists. Manson: London, UKGoogle Scholar
Johnson, EO, Kamilaris, TC, Chrousos, GP and Gold, PW 1992 Mechanisms of stress — a dynamic overview of hormonal and behavioral homeostasis. Neuroscience and Biobehavioral Reviews 16: 115–130CrossRefGoogle Scholar
Johnson, RW, Von Borell, E, Anderson, LL, Kojic, LD and Cunnick, JE 1994 Intracerebroventricular injection of corticotropin-releasing hormone in the pig: acute effects on behaviour, adrenocorticotropin secretion, and immune suppression. Endocrinology 135: 642–648CrossRefGoogle ScholarPubMed
Knowles, TG 1998 A review of the road transport of slaughter sheep. Veterinary Record 143: 212–219CrossRefGoogle ScholarPubMed
Koolhaas, JM, Korte, SM, De Boer, SF, Van Der Vegt, BJ, Hopster, H, De Jong, IC, Ruis, MAW and Blokhuis, HJ 1999 Coping styles in animals: current status in behavior and stress physiology. Neuroscience and Biobehavioral Reviews 23: 925–935CrossRefGoogle ScholarPubMed
Le Neindre, P, Poindron, P, Trillat, G and Orgeur, P 1993 Influence of breed on reactivity of sheep to humans. Genetics, Selection, Evolution 25: 447–458CrossRefGoogle Scholar
Lundberg, U and Frankenhaeuser, M 1980 Pituitary–adrenal and sympathetic–adrenal correlates of distress and effort. Journal of Psychosomatic Research 24: 125–130CrossRefGoogle ScholarPubMed
Lynch, JJ, Hinch, GN and Adams, DB 1992 The Behaviour of Sheep: Biological Principles and Implications for Production. Commonwealth Agricultural Bureaux International: Oxon, UKGoogle Scholar
Lyons, DM, Price, EO and Moberg, GP 1993 Social grouping tendencies and separation-induced distress in juvenile sheep and goats. Developmental Psychobiology 26: 251–259CrossRefGoogle ScholarPubMed
MacArthur, RA, Geist, V and Johnston, RH 1982 Cardiac and behavioural responses of mountain sheep to human disturbance. Journal of Wildlife Management 46: 351–358Google Scholar
Mason, JW 1971 A re-evaluation of the concept of “non-specificity” in stress theory. Journal of Psychiatric Research 8: 323–333CrossRefGoogle Scholar
Mellor, DJ, Cook, CJ and Stafford, KJ 2000 Quantifying some responses to pain as a stressor. In: Moberg, GP and Mench, JA (eds) The Biology of Animal Stress: Basic Principles and Implications for Animal Welfare pp 171–198. CAB International: Wallingford, UKCrossRefGoogle Scholar
Moberg, GP 1985 Biological response to stress: key to assessment of animal well-being? In: Moberg GP (ed) Animal Stress pp 27–49. American Physiological Society: Bethesda, USACrossRefGoogle 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 1–21. CAB International: Wallingford, UKCrossRefGoogle Scholar
Moberg, GP, Anderson, CO and Underwood, TR 1980 Ontogeny of the adrenal and behavioral responses of lambs to emotional stress. Journal of Animal Science 51: 138–142CrossRefGoogle ScholarPubMed
Moberg, GP and Wood, VA 1982 Effect of differential rearing on the behavioral and adrenocortical response of lambs to a novel environment. Applied Animal Ethology 8: 269–279CrossRefGoogle Scholar
Morgan CA, III, Rasmusson, AM, Wang, S, Hoyt, G, Hauger, RL and Hazlett, G 2002 Neuropeptide-Y, cortisol, and subjective distress in humans exposed to acute stress: replication and extension of previous report. Biological Psychiatry 52: 136–142CrossRefGoogle ScholarPubMed
Morton, DB and Griffiths, PHM 1985 Guidelines on the recognition of pain, distress and discomfort in experimental animals and an hypothesis for assessment. Veterinary Record 116: 431–436CrossRefGoogle Scholar
Nag, PK, Ashtekar, SP, Nag, A, Kothari, D, Bandyopadhyay, P and Desai, H 1997 Human heat tolerance in a simulated environment. Indian Journal of Medical Research 105: 226–234Google Scholar
Orgeur, P, Mavric, N, Yvore, P, Bernard, S, Nowak, R, Schaal, B and Levy, F 1998 Artificial weaning in sheep: consequences on behavioural, hormonal and immuno-pathological indicators of welfare. Applied Animal Behaviour Science 58: 87–103CrossRefGoogle Scholar
Paranhos da Costa MR, Silva RG da and Souza RC da 1992 Effect of air temperature and humidity on ingestive behaviour of sheep. Biometeorology 36: 218–222CrossRefGoogle Scholar
Parrott, RF, Lloyd, DM and Goode, JA 1996 Stress hormone responses of sheep to food and water deprivation at high and low ambient temperatures. Animal Welfare 5: 45–56Google Scholar
Parrott, RF, Thornton, SN, Forsling, ML and Delaney, CE 1987 Endocrine and behavioural factors affecting water balance in sheep subjected to isolation stress. Journal of Endocrinology 112: 305–310CrossRefGoogle ScholarPubMed
Poindron, P, Soto, R and Romeyer, A 1997 Decrease of response to social separation in preparturient ewes. Behavioural Processes 40: 45–51CrossRefGoogle ScholarPubMed
Ramos, A and Mormede, P 1998 Stress and emotionality: a multidimensional and genetic approach. Neuroscience and Biobehavioral Reviews 22: 33–57CrossRefGoogle ScholarPubMed
Rhind, SM, Reid, HW, McMillen, SR and Palmarini, G 1998 The role of cortisol and β-endorphin in the response of the immune system to weaning in lambs. Animal Science 66: 397–402CrossRefGoogle Scholar
Riesenfeld, T, Hammarlund, K, Norsted, T and Sedin, G 1996 Irregular breathing in young lambs and newborn infants during heat stress. Acta Paediatrica 85: 467–470CrossRefGoogle ScholarPubMed
Romeyer, A and Bouissou, MF 1992 Assessment of fear reactions in domestic sheep, and influence of breed and rearing conditions. Applied Animal Behaviour Science 34: 93–119CrossRefGoogle Scholar
Ruckebusch, Y and Malbert, CH 1986 Stimulation and inhibition of food intake in sheep by centrally administered hypothalamic releasing factors. Life Sciences 38: 929–936CrossRefGoogle ScholarPubMed
Rushen, J 1986 Some problems with the physiological concept of stress. Australian Veterinary Journal 63: 359–361CrossRefGoogle ScholarPubMed
Rushen, J 1990 Use of aversion learning techniques to measure distress in sheep. Applied Animal Behaviour Science 28: 3–14CrossRefGoogle Scholar
Rushen, J 2000 Some issues in the interpretation of behavioural responses to stress. In: Moberg, GP and Mench, JA (eds) The Biology of Animal Stress: Basic Principles and Implications for Animal Welfare pp 23–42. CAB International: Wallingford, UKCrossRefGoogle Scholar
Sanford, J, Ewbank, R, Molony, V, Tavernor, WD and Uvarov, O 1986 Guidelines for the recognition and assessment of pain in animals. Veterinary Record 118: 334–338Google Scholar
Schaefer, AL, Young, BA and Turner, BV 1982 The effects of cold exposure on blood flow distribution in sheep. Journal of Thermal Biology 7: 15–21CrossRefGoogle Scholar
Selye, H 1936 A syndrome produced by diverse nocuous agents. Nature 138: 32CrossRefGoogle Scholar
Selye, H 1946 The general adaptation syndrome and the diseases of adaptation. Journal of Clinical Endocrinology and Metabolism 6: 117–230CrossRefGoogle ScholarPubMed
Selye, H 1976 Stress in Health and Disease. Butterworth: Boston, USAGoogle Scholar
Shillito-Walser, E and Alexander, G 1980 Mutual recognition between ewes and lambs. Reproduction, Nutrition, Development 20(3B): 807–816CrossRefGoogle Scholar
Silanikove, N 2000 Effects of heat stress on the welfare of extensively managed domestic ruminants. Livestock Production Science 67: 1–18CrossRefGoogle Scholar
Stafford Smith, DM, Noble, IR and Jones, GK 1985 A heat balance model for sheep and its use to predict shade-seeking behaviour in hot conditions. Journal of Applied Ecology 22: 753–774CrossRefGoogle Scholar
Syme, LA and Elphick, GR 1982 Heart-rate and the behaviour of sheep in yards. Applied Animal Ethology 9: 31–35CrossRefGoogle Scholar
Taylor, PM 1998 Endocrine and metabolic effects of hypotension or halothane inhalation in sheep anaesthetized with pentobarbital. British Journal of Anaesthesia 80: 208–212CrossRefGoogle ScholarPubMed
Tikuisis, P, McLellan, TM and Selkirk, G 2002 Perceptual versus physiological heat strain during exercise-heat stress. Medicine and Science in Sports and Exercise 34: 1454–1461CrossRefGoogle ScholarPubMed
Torres-Hernandez, G and Hohenboken, W 1979 An attempt to assess traits of emotionality in crossbred ewes. Applied Animal Ethology 5: 71–83CrossRefGoogle Scholar
von Holst, D 1998 The concept of stress and its relevance for animal behaviour. Advances in the Study of Behavior 27: 1–131CrossRefGoogle Scholar
Webster, AJF, Hicks, AM and Hays, FL 1969 Cold climate and cold temperature induced changes in the heat production and thermal insulation of sheep. Canadian Journal of Physiology and Pharmacology 47: 553–562CrossRefGoogle ScholarPubMed
Wientjes, CJE 1992 Respiration in psychophysiology: methods and applications. Biological Psychology 34: 179–203CrossRefGoogle ScholarPubMed