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Long-term exposure to unpredictable and uncontrollable aversive events alters fearfulness in sheep

Published online by Cambridge University Press:  25 September 2012

A. Destrez*
Affiliation:
INRA UMR1213 Herbivores, INRA-VetAgro Sup, F-63122 Saint-Genès Champanelle, France
V. Deiss
Affiliation:
INRA UMR1213 Herbivores, INRA-VetAgro Sup, F-63122 Saint-Genès Champanelle, France
C. Leterrier
Affiliation:
INRA UMR 85 Physiologie de la Reproduction et des Comportements, INRA-CNRS-Université de Tours-IFCE, F-37380 Nouzilly, France
X. Boivin
Affiliation:
INRA UMR1213 Herbivores, INRA-VetAgro Sup, F-63122 Saint-Genès Champanelle, France
A. Boissy
Affiliation:
INRA UMR1213 Herbivores, INRA-VetAgro Sup, F-63122 Saint-Genès Champanelle, France
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Abstract

Numerous studies have investigated the emotional effects of various acute, potentially alarming events in animals, but little is known about how an accumulation of emotional experiences affects fearfulness. Fearfulness is a temperament trait that characterizes the propensity of an individual to be frightened by a variety of alarming events. The aim of this study was to investigate a putative alteration of fearfulness in sheep repeatedly exposed to various aversive events. Forty-eight 5-month-old female lambs were used. Over a period of 6 weeks, 24 of them (treated group) were exposed daily to various unpredictable and uncontrollable aversive events related to predatory cues, social context and negative handling that can occur under farming conditions. The other 24 lambs (control group) were housed in standard farming conditions (predictable food distribution and group handling). Fearfulness (behavioural and physiological responses) was assessed before and after the treatment period by subjecting the lambs to three standardized tests: individual exposure to suddenness and then to novelty in a test arena, and group exposure to a motionless human in the home pen. As biomarkers of stress, leukocyte counts, heart rate and cortisol concentrations were measured in the lambs in their home pens. Before the treatment, the emotional responses of the groups did not differ. After the treatment, treated lambs approached the human less often, had less contact with the novel object and vocalized more than controls in individual tests, suggesting that long-term exposure to unpredictable and uncontrollable aversive events increases subsequent fearfulness in sheep. In addition, treated lambs had lower leukocyte counts, heart rate and cortisol levels, pointing to a chronic stress state. These findings suggest that increased fearfulness may be used as a sign of chronic stress in farm animals.

Type
Behaviour, welfare and health
Copyright
Copyright © The Animal Consortium 2012

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References

Alexander, G, Stevens, D 1979. Discrimination of colours and grey shades by Merino ewes: tests using coloured lambs. Applied Animal Ethology 5, 215231.CrossRefGoogle Scholar
Arnould, C, Malosse, C, Signoret, JP, Descoins, C 1998. Which chemical constituents from dog feces are involved in its food repellent effect in sheep? Journal of Chemical Ecology 24, 559576.CrossRefGoogle Scholar
Baldock, NM, Sibly, RM 1990. Effects of handling and transportation on the heart rate and behaviour of sheep. Applied Animal Behaviour Science 28, 1539.Google Scholar
Bellingrath, S, Rohleder, N, Kudielka, BM 2010. Healthy working school teachers with high effort–reward-imbalance and overcommitment show increased pro-inflammatory immune activity and a dampened innate immune defence. Brain, Behavior, and Immunity 24, 13321339.Google Scholar
Blanchard, RJ, McKittrick, CR, Blanchard, DC 2001. Animal models of social stress: effects on behavior and brain neurochemical systems. Physiology & Behavior 73, 261271.Google Scholar
Boissy, A 1998. Fear and fearfulness in determining behavior. In Genetics and the behavior of domestic animals (ed. T Grandin), pp. 67–111. Academic Press, San Diego.Google Scholar
Boissy, A, Bouissou, MF 1994. Effects of androgen treatment on behavioral and physiological-responses of heifers to fear-eliciting situation. Hormones and Behavior 28, 6683.Google Scholar
Boissy, A, Veissier, I, Roussel, S 2001. Behavioural reactivity affected by chronic stress: an experimental approach in calves submitted to environmental instability. Animal Welfare 10, S175S185.Google Scholar
Boivin, X, Garel, JP, Mante, A, Le Neindre, P 1998. Beef calves react differently to different handlers according to the test situation and their previous interactions with their caretaker. Applied Animal Behaviour Science 55, 245257.Google Scholar
Broom, DM 1987. Applications of neurobiological studies to farm animal welfare. In Biology of stress in farm animals: an integrative approach (ed. PR Wiepkema), pp. 101110. Kluwer Academic Publishers, Dordrecht, the Netherlands.Google Scholar
Brydges, NM, Leach, M, Nicol, K, Wright, R, Bateson, M 2011. Environmental enrichment induces optimistic cognitive bias in rats. Animal Behaviour 81, 169175.Google Scholar
Calandreau, L, Favreau-Peigne, A, Bertin, A, Constantin, P, Arnould, C, Laurence, A, Lumineau, S, Houdelier, C, Richard-Yris, MA, Boissy, A, Leterrier, C 2011. Higher inherent fearfulness potentiates the effects of chronic stress in the Japanese quail. Behavioural Brain Research 225, 505510.Google Scholar
Cyr, NE, Romero, LM 2007. Chronic stress in free-living European starlings reduces corticosterone concentrations and reproductive success. General and Comparative Endocrinology 151, 8289.Google Scholar
Dalmau, A, Fabrega, E, Velarde, A 2009. Fear assessment in pigs exposed to a novel object test. Applied Animal Behaviour Science 117, 173180.Google Scholar
Dantzer, R, Mormede, P 1983. Stress in farm animals – a need for reevaluation. Journal of Animal Science 57, 618.Google Scholar
Dantzer, R, Mormede, P, Bluthe, RM, Soissons, J 1983. The effect of different housing conditions on behavioural and adrenocortical reactions in veal calves. Reproduction Nutrition Development 23, 501508.Google Scholar
Dawkins, MS 2006. A user's guide to animal welfare science. Trends in Ecology & Evolution 21, 7782.Google Scholar
de Jong, IC, Prelle, IT, van de Burgwal, JA, Lambooij, E, Korte, SM, Blokhuis, HJ, Koolhaas, JM 2000. Effects of environmental enrichment on behavioral responses to novelty, learning, and memory, and the circadian rhythm in cortisol in growing pigs. Physiology & Behavior 68, 571578.Google Scholar
Désiré, L, Veissier, I, Despres, G, Boissy, A 2004. On the way to assess emotions in animals: do lambs (Ovis aries) evaluate an event through its suddenness, novelty, or unpredictability? Journal of Comparative Psychology 118, 363374.Google Scholar
Doyle, RE, Lee, C, Deiss, V, Fisher, AD, Hinch, GN, Boissy, A 2011. Measuring judgement bias and emotional reactivity in sheep following long-term exposure to unpredictable and aversive events. Physiology & Behavior 102, 503510.CrossRefGoogle ScholarPubMed
Dwyer, CM, Bornett, HLI 2004. Chronic stress in sheep: assessment tools and their use in different management conditions. Animal Welfare 13, 293304.Google Scholar
Erhard, HW, Mendl, M, Christiansen, SB 1999. Individual differences in tonic immobility may reflect behavioural strategies. Applied Animal Behaviour Science 64, 3146.Google Scholar
Estep, DQ, Hetts, S 1992. Interactions, relationships, and bonds: the conceptual basis for scientist–animal relations. Cambridge University Press, Cambridge, UK, pp. 6–26.Google Scholar
Forkman, B, Boissy, A, Meunier-Salauen, MC, Canali, E, Jones, RB 2007. A critical review of fear tests used on cattle, pigs, sheep, poultry and horses. Physiology & Behavior 92, 340374.Google Scholar
Glaser, J-P, van Os, J, Portegijs, PJM, Myin-Germeys, I 2006. Childhood trauma and emotional reactivity to daily life stress in adult frequent attenders of general practitioners. Journal of Psychosomatic Research 61, 229236.Google Scholar
Hemsworth, PH, Barnett, JL, Hansen, C 1987. The influence of inconsistent handling by humans on the behaviour, growth and corticosteroids of young pigs. Applied Animal Behaviour Science 17, 245252.Google Scholar
Janssens, CJJG, Helmond, FA, Weigant, VM 1995. The effect of chronic stress on plasma cortisol concentrations in cyclic female pigs depends on the time of day. Domestic Animal Endocrinology 12, 167177.Google Scholar
Korte, SM 2001. Corticosteroids in relation to fear, anxiety and psychopathology. Neuroscience Biobehavioral Reviews 25, 117142.CrossRefGoogle ScholarPubMed
Ladewig, J 2000. Chronic intermittent stress: a model for the study of long-term stressors. pp. 159169, CABI Publishing, Wallingford, UK.Google Scholar
Ladewig, J, Smidt, D 1989. Behavior, episodic secretion of cortisol, and adrenocortical reactivity in bulls subjected to tethering. Hormones and Behavior 23, 344360.Google Scholar
Leonard, BE, Song, C 1996. Stress and the immune system in the etiology of anxiety and depression. Pharmacology Biochemistry and Behavior 54, 299303.Google Scholar
Lucini, D, Di Fede, G, Parati, G, Pagani, M 2005. Impact of chronic psychosocial stress on autonomic cardiovascular regulation in otherwise healthy subjects. Hypertension 46, 12011206.Google Scholar
Manteuffel, G, Puppe, B, Schön, PC 2004. Vocalization of farm animals as a measure of welfare. Applied Animal Behaviour Science 88, 163182.CrossRefGoogle Scholar
Mendl, M, Burman, O, Laughlin, K, Paul, E 2001. Animal memory and animal welfare. Animal Welfare 10, S141S159.CrossRefGoogle Scholar
Palestrini, C, Ferrante, V, Mattiello, S, Canali, E, Carenzi, C 1998. Relationship between behaviour and heart rate as an indicator of stress in domestic sheep under different housing systems. Small Ruminant Research 27, 177181.CrossRefGoogle Scholar
Rushen, J 1991. Problems associated with the interpretation of physiological data in the assessment of animal welfare. Applied Animal Behaviour Science 28, 381386.Google Scholar
Rushen, J, Taylor, AA, de Passille, AM 1999. Domestic animals’ fear of humans and its effect on their welfare. Applied Animal Behaviour Science 65, 285303.CrossRefGoogle Scholar
Scherer, KR 1999. On the sequential nature of appraisal processes: indirect evidence from a recognition task. Cognition & Emotion 13, 763793.CrossRefGoogle Scholar
Schwartzkopf-Genswein, KS, Booth-McLean, ME, Shah, MA, Entz, T, Bach, SJ, Mears, GJ, Schaefer, AL, Cook, N, Church, J, McAllister, TA 2007. Effects of pre-haul management and transport duration on beef calf performance and welfare. Applied Animal Behaviour Science 108, 1230.Google Scholar
Terlouw, EMC, Boissy, A, Blinet, P 1998. Behavioural responses of cattle to the odours of blood and urine from conspecifics and to the odour of faeces from carnivores. Applied Animal Behaviour Science 57, 921.Google Scholar
van de Weerd, HA, Day, JEL 2009. A review of environmental enrichment for pigs housed in intensive housing systems. Applied Animal Behaviour Science 116, 120.Google Scholar
Veissier, I, Boissy, A, dePassille, AM, Rushen, J, van Reenen, CG, Roussel, S, Andnason, S, Pradel, P 2001. Calves’ responses to repeated social regrouping and relocation. Journal of Animal Science 79, 25802593.CrossRefGoogle ScholarPubMed
von Borell, E, Langbein, J, Després, G, Hansen, S, Leterrier, C, Marchant-Forde, J, Marchant-Forde, R, Minero, M, Mohr, E, Prunier, A, Valance, D, Veissier, I 2007. Heart rate variability as a measure of autonomic regulation of cardiac activity for assessing stress and welfare in farm animals – a review. Physiology & Behavior 92, 293316.Google Scholar
Zager, A, Andersen, ML, Ruiz, FS, Antunes, IB, Tufik, S 2007. Effects of acute and chronic sleep loss on immune modulation of rats. American Journal of Physiology-Regulatory Integrative and Comparative Physiology 293, R504R509.Google Scholar