Provision of straw and the presence of undocked lambs reduce the behavioural and physiological expressions of pain and stress associated with tail docking in lambs: a preliminary study
Cristian Larrondo A B , Agustín Orihuela C G , Ana Strappini D , Gerardo Acosta-Jamett E , Daniel Mota-Rojas F and Carmen Gallo DA Escuela de Graduados, Facultad de Ciencias Veterinarias, Universidad Austral de Chile, Valdivia, 5090000, Chile.
B Facultad de Medicina Veterinaria y Agronomía, Universidad de las Américas, Viña del Mar, 2520000, Chile.
C Facultad de Ciencias Agropecuarias, Universidad Autónoma del Estado de Morelos. Av. Universidad 1001, Colonia Chamilpa, Cuernavaca, Morelos 62210, México.
D Instituto de Ciencia Animal, Facultad de Ciencias Veterinarias, Universidad Austral de Chile, Valdivia, 5090000, Chile.
E Instituto de Medicina Preventiva y Programa de Investigación Aplicada en Fauna Silvestre, Facultad de Ciencias Veterinarias, Universidad Austral de Chile, Valdivia, 5090000, Chile.
F Departamento de Producción Agrícola y Animal, Universidad Autónoma Metropolitana, Ciudad de México, 04960, México.
G Corresponding author. Email: aorihuela@uaem.mx
Animal Production Science - https://doi.org/10.1071/AN20237
Submitted: 17 April 2020 Accepted: 19 October 2020 Published online: 16 November 2020
Abstract
Aims: The aim of this experiment was to determine if the provision of straw and the presence of undocked twins could be used to mitigate the pain experienced by lambs having their tails docked using rubber rings.
Methods: A total of 54 twin St. Croix 60-days-old weaned lambs were assigned to one of four treatments: (i) the presence of undocked twins and no provision of straw (U); (ii) the provision of straw and no presence of undocked twins (St); (iii) the provision of straw and the presence of undocked twins (StU); and (iv) no provision of straw and no presence of undocked twins (C). Straw was provided as bed material over the concrete floor; whereas the presence of undocked twins was achieved by leaving one twin intact within each pair. From the placement of the rubber rings, the behaviour of tail-docked twins was video recorded continuously for 60 min, and blood samples were taken from these lambs immediately before placing the rubber ring (time 0), and at 0.5, 1, 1.5, 24, 48 and 72 h after, for cortisol and physio-metabolic profiles determination, and at 168 h after, for cortisol determination.
Key results: Lambs in treatment C spent three times longer in abnormal lying postures (P = 0.002) compared with St and StU lambs (6.49 ± 4.73 vs 1.78 ± 1.26 and 1.83 ± 1.94 min respectively). Lambs in all treatments experienced an increase in cortisol levels 1 h after tail docking, except for StU lambs. In addition, 48 and 72 h after tail docking, lambs in treatments St and StU had lower concentrations of cortisol than C lambs.
Conclusion: This study shows that the provision of straw and the presence of undocked twins reduce the behavioural and physiological expressions of pain associated with tail docking in lambs.
Implications: In lambs raised under intensive conditions, the addition of straw as bedding material and the presence of intact tail lambs could be a practical strategy to improve the welfare of tail-docked lambs, whereas for those lambs raised under extensive conditions, leaving intact those lambs that will be sold might serve as social buffering for their tail-docked conspecifics that will remain in the farm.
Keywords: animal welfare, pain, sheep, husbandry practice.
References
AWA (2009) ‘Management to avoid tail docking sheep. Technical advice fact sheet 2.’ Available at http://www.animalwelfareapproved.org/wp-content/uploads/2009/08/TAFS-2-Management-to-Avoid-Tail-Docking-sheep-9-22-09.pdf [Verifed 4 November 2020]Backus BL, McGlone JJ (2018) Evaluating environmental enrichment as a method to alleviate pain after castration and tail docking in pigs. Applied Animal Behaviour Science 204, 37–42.
| Evaluating environmental enrichment as a method to alleviate pain after castration and tail docking in pigs.Crossref | GoogleScholarGoogle Scholar |
Berrocal Y, Pearse D, Singh A, Andrade C, McBroom J, Puentes R, Eaton M (2007) Social and environmental enrichment improves sensory and motor recovery after severe contusive spinal cord injury in rat. Journal of Neurotrauma 24, 1761–1772.
| Social and environmental enrichment improves sensory and motor recovery after severe contusive spinal cord injury in rat.Crossref | GoogleScholarGoogle Scholar | 18001204PubMed |
Blackburn-Munro G, Blackburn-Munro RE (2001) Chronic pain, chonic stress and depression: coincidence or consequence? Journal of Neuroendocrinology 13, 1009–1023.
| Chronic pain, chonic stress and depression: coincidence or consequence?Crossref | GoogleScholarGoogle Scholar | 11722697PubMed |
Bolay H, Moskowitz MA (2002) Mechanisms of pain modulation in chronic syndromes. Neurology 59, S2–S7.
| Mechanisms of pain modulation in chronic syndromes.Crossref | GoogleScholarGoogle Scholar | 12221149PubMed |
Clark C, Murrel J, Fernyhough M, O’Rourke T, Mendl M (2014) Long-term and trans-generational effects of neonatal experience on sheep behaviour. Biotechnology Letters 10, 1–4.
Colditz G, Paull DR, Lee C (2012) Social transmission of physiological and behavioural responses to castration in suckling Merino lambs. Applied Animal Behaviour Science 136, 136–145.
| Social transmission of physiological and behavioural responses to castration in suckling Merino lambs.Crossref | GoogleScholarGoogle Scholar |
Dwyer C (2008) The welfare of the neonatal lamb. Small Ruminant Research 76, 31–41.
| The welfare of the neonatal lamb.Crossref | GoogleScholarGoogle Scholar |
Dwyer C (2009) Welfare of sheep: providing for welfare in an extensive environment. Small Ruminant Research 86, 14–21.
| Welfare of sheep: providing for welfare in an extensive environment.Crossref | GoogleScholarGoogle Scholar |
Fisher AD (2011) Addressing pain caused by mulesing in sheep. Applied Animal Behaviour Science 135, 232–240.
| Addressing pain caused by mulesing in sheep.Crossref | GoogleScholarGoogle Scholar |
Fraser D (2008) Understanding animal welfare. Acta Veterinaria Scandinavica 50, S1
| Understanding animal welfare.Crossref | GoogleScholarGoogle Scholar |
Fraser D, Broom DM (1997). Welfare terminology and concepts. In ‘Farm Animal Behavior and Welfare’. p. 143. (CABI Publishing: Wallingford, UK)
French NP, Wall R, Morgan KL (1994) Lamb tail docking: a controlled field study of the effects of tail amputation on health and productibity. The Veterinary Record 134, 463–467.
| Lamb tail docking: a controlled field study of the effects of tail amputation on health and productibity.Crossref | GoogleScholarGoogle Scholar | 8059511PubMed |
French NP, Parkin TD, Morgan KL (1996) A case control study of blowfly strike in lambs. The Veterinary Record 139, 384–388.
| A case control study of blowfly strike in lambs.Crossref | GoogleScholarGoogle Scholar | 8913010PubMed |
Futro A, Masłowska K, Dwyer C (2015) Ewes direct most maternal attention towards lambs that show the greatest pain-related behavioural responses. PLoS One 10, e0134024
| Ewes direct most maternal attention towards lambs that show the greatest pain-related behavioural responses.Crossref | GoogleScholarGoogle Scholar | 26217942PubMed |
Gabriel A, Marcus M, Honig W (2009) Environmental housing affects the duration of mechanical allodynia and the spinal astroglial activation in a rat model of chronic inflammatory pain. Brain Research 1276, 83–90.
| Environmental housing affects the duration of mechanical allodynia and the spinal astroglial activation in a rat model of chronic inflammatory pain.Crossref | GoogleScholarGoogle Scholar | 19406110PubMed |
Gabriel A, Paoletti G, Seta D, Panelli R, Marcus M, Farabollini F, Carli G, Joosten E (2010) Enriched environment and the recovery from inflammatory pain: social versus physical aspects and their interaction. Behavioural Brain Research 208, 90–95.
| Enriched environment and the recovery from inflammatory pain: social versus physical aspects and their interaction.Crossref | GoogleScholarGoogle Scholar | 19914294PubMed |
Gougoulis DA, Kyriazakis I, Fthenakis GC (2010) Diagnostic significance of behaviour changes of sheep: a selected review. Small Ruminant Research 92, 52–56.
Graham MJ, Kent JE, Molony V (2002) The influence of the site of application on the behavioural responses of lambs to tail docking by rubber ring. Veterinary Journal (London, England) 164, 240–243.
Grant C (2004) Behavioural responses of lambs to common painful husbandry procedures. Applied Animal Behaviour Science 87, 255–273.
| Behavioural responses of lambs to common painful husbandry procedures.Crossref | GoogleScholarGoogle Scholar |
Guesgen MJ, Beausoleil NJ, Minot EO, Stewart M, Stafford KJ (2014) Social context and other factors influence the behavioural expression of pain by lambs. Applied Animal Behaviour Science 159, 41–49.
| Social context and other factors influence the behavioural expression of pain by lambs.Crossref | GoogleScholarGoogle Scholar |
Hennessy M, Kaiser S, Sachser N (2009) Social buffering of the stress response: diversity, mechanisms and functions. Frontiers in Neuroendocrinology 30, 470–482.
| Social buffering of the stress response: diversity, mechanisms and functions.Crossref | GoogleScholarGoogle Scholar | 19545584PubMed |
Hinch GN (2017). Understanding the natural behaviour of sheep. In ‘Advances in sheep welfare’. pp. 1–15. (Woodhead Publishing: Duxford, UK)
Hostinar C, Sullivan R, Gunnar M (2014) Psychobiological mechanisms underlying the social buffering of the hypothalamic-pituitary-adrenocortical axis: a review of animal models and human studies across development. Psychological Bulletin 140, 256–282.
| Psychobiological mechanisms underlying the social buffering of the hypothalamic-pituitary-adrenocortical axis: a review of animal models and human studies across development.Crossref | GoogleScholarGoogle Scholar | 23607429PubMed |
Kent JE, Molony V, Robertson IS (1993) Changes in plasma cortisol concentrations in lambs of three ages after three methods of castration and tail docking. Research in Veterinary Science 55, 246–251.
| Changes in plasma cortisol concentrations in lambs of three ages after three methods of castration and tail docking.Crossref | GoogleScholarGoogle Scholar | 8235094PubMed |
Khasar SG, Burkham J, Dina OA, Brown AS, Bogen O, Alessandri-Haber N, Green PG, Reichling DB, Levine JD (2008) stress induces a switch of intracellular signaling in sensory neurons in a model of generalized pain. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 28, 5721–5730.
| stress induces a switch of intracellular signaling in sensory neurons in a model of generalized pain.Crossref | GoogleScholarGoogle Scholar |
Kikusui T, Winslow J, Mori J (2006) Social buffering: relief from stress and anxiety. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 361, 2215–2228.
| Social buffering: relief from stress and anxiety.Crossref | GoogleScholarGoogle Scholar | 17118934PubMed |
Larrondo C, Bustamante H, Gallo C (2018) Sheep farmers’ perception of welfare and pain associated with routine husbandry practices in Chile. Animals 8, 225
| Sheep farmers’ perception of welfare and pain associated with routine husbandry practices in Chile.Crossref | GoogleScholarGoogle Scholar |
Larrondo C, Bustamante H, Paredes E, Gallo C (2019) Long-term hyperalgesia and traumatic neuroma formation in tail-docked lambs. Animal Welfare 28, 443–454.
| Long-term hyperalgesia and traumatic neuroma formation in tail-docked lambs.Crossref | GoogleScholarGoogle Scholar |
Lester SJ, Mellor DJ, Ward RN, Holmes RJ (1991) Cortisol responses of young lambs to castration and tailing using different methods. New Zealand Veterinary Journal 39, 134–138.
| Cortisol responses of young lambs to castration and tailing using different methods.Crossref | GoogleScholarGoogle Scholar | 16031640PubMed |
Lester SJ, Mellor DJ, Holmes RJ, Ward RN, Stafford KJ (1996) Behavioural and cortisol responses of lambs to castration and tailing using different methods. New Zealand Veterinary Journal 44, 45–54.
| Behavioural and cortisol responses of lambs to castration and tailing using different methods.Crossref | GoogleScholarGoogle Scholar | 16031893PubMed |
Ligout S, Porter RH (2004) Effect of maternal presence on the development of social relationships among lambs. Applied Animal Behaviour Science 88, 47–59.
| Effect of maternal presence on the development of social relationships among lambs.Crossref | GoogleScholarGoogle Scholar |
Mellor DJ, Stafford KJ (2000) Acute castration and/or tailing distress and its alleviation in lambs. New Zealand Veterinary Journal 48, 33–43.
| Acute castration and/or tailing distress and its alleviation in lambs.Crossref | GoogleScholarGoogle Scholar | 16032116PubMed |
Molony V, Kent J (1997) Assessment of acute pain in farm animals using behavioral and physiological measurements. Journal of Animal Science 75, 266–272.
| Assessment of acute pain in farm animals using behavioral and physiological measurements.Crossref | GoogleScholarGoogle Scholar | 9027575PubMed |
Molony V, Kent JE, McKendrick IJ (2002) Validation of method for assessment of an acute pain in lambs. Applied Animal Behaviour Science 76, 215–238.
| Validation of method for assessment of an acute pain in lambs.Crossref | GoogleScholarGoogle Scholar |
Mota-Rojas D, Ceballos MA, Orihuela A, Corredor MA, Pérez E, Ramírez NR (2016). Painful practices in farm animals. In ‘Bienestar animal, una vision global en Iberoamérica [Animal welfare, a global vision in Ibero-America]’. (Eds D Mota-Rojas, A Velarde, SM Huertas-Canén, MN Cajíao) pp. 137–154. (Elsevier: Barcelona, Spain)
Orihuela A, Ungerfeld R (2019) Tail docking in sheep (Ovis aries): a review on the arguments for and against the procedure, advantages/disadvantages, methods, and new evidence to revisit the topic. Livestock Science 230, 103837
| Tail docking in sheep (Ovis aries): a review on the arguments for and against the procedure, advantages/disadvantages, methods, and new evidence to revisit the topic.Crossref | GoogleScholarGoogle Scholar |
Orihuela A, Mota-Rojas D, Velarde A, Strappini-Asteggiano A, Thielo de la Vega L, Borderas-Tordesillas F, Alonso-Spilsbury M (2018) Invited review: environmental enrichment to improve behaviour in farm animals. Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources 13, 1–16.
| Invited review: environmental enrichment to improve behaviour in farm animals.Crossref | GoogleScholarGoogle Scholar |
Pascual-Alonso M, Miranda-de la Lama GC, Villaroel M, Alierta S, Escós J, María GA (2015) Spatial preferences and behavioural patterns of lambs during fattening in straw enriched pens. Archivos de Zootecnia 64, 155–160.
| Spatial preferences and behavioural patterns of lambs during fattening in straw enriched pens.Crossref | GoogleScholarGoogle Scholar |
Pérez-Pedraza E, Mota-Rojas D, Ramírez R, Guerrero I, Martínez J, Lezama K, Mora-Medina P, Rosas M, Martínez V, González M (2018) Effect of the number of incisions and use of local anesthesia on the physiological indicators of surgically-castrated piglets. International Journal of Veterinary Science and Medicine 6, 159–164.
| Effect of the number of incisions and use of local anesthesia on the physiological indicators of surgically-castrated piglets.Crossref | GoogleScholarGoogle Scholar | 30564590PubMed |
Porter RH, Nowak R, Orgeur P (1995) Influence of a conspecific agemate on distress bleating by lambs. Applied Animal Behaviour Science 45, 239–244.
| Influence of a conspecific agemate on distress bleating by lambs.Crossref | GoogleScholarGoogle Scholar |
R Development Core Team (2015). ‘R: A language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna, Austria).
Rossi HL, Neubert JK (2008) Effects of environmental enrichment on thermal sensitivity in an operant orofacial pain assay. Behavioural Brain Research 187, 478–482.
Sutherland M, Tucker C (2011) The long and short of it: a review of tail docking in farm animals. Applied Animal Behaviour Science 135, 179–191.
Teixeira DL, Miranda-de la Lama GC, Villaroel M, Garcia-Belenguer S, Sañudo C, María GA (2012) Effect of straw on lamb welfare, production performance and meat quality during the finishing phase of fattening. Meat Science 92, 829–836.
| Effect of straw on lamb welfare, production performance and meat quality during the finishing phase of fattening.Crossref | GoogleScholarGoogle Scholar | 22871584PubMed |
Teixeira DL, Miranda-de la Lama GC, Pascual-Alonso M, Aguayo-Ulloa L, Villaroel M, María GA (2013) A note on lamb’s choice for different types of bedding materials. Journal of Veterinary Behavior-Clinical Applications and Welfare 8, 175–179.
| A note on lamb’s choice for different types of bedding materials.Crossref | GoogleScholarGoogle Scholar |
Teixeira DL, Miranda-de la Lama GC, Villaroel M, Escós J, María G (2014) Lack of straw during finishing affects individual and social lamb behavior. Journal of Veterinary Behavior-Clinical Applications and Welfare 9, 177–183.
| Lack of straw during finishing affects individual and social lamb behavior.Crossref | GoogleScholarGoogle Scholar |
Vachon P, Millecamps M, Low L, Thompson SJ, Pailleux F, Beaudry F, Bushnell CM, Stone LS (2013) Alleviation of chronic neuropathic pain by environmental enrichment in mice well after the establishment of chronic pain. Behavioral and Brain Functions 9, 22
| Alleviation of chronic neuropathic pain by environmental enrichment in mice well after the establishment of chronic pain.Crossref | GoogleScholarGoogle Scholar | 24025218PubMed |
van Praag H, Kempermann G, Gage FH (2000) Neural consequences of environmental enrichment. Nature Reviews. Neuroscience 1, 191–198.
| Neural consequences of environmental enrichment.Crossref | GoogleScholarGoogle Scholar | 11257907PubMed |
Wardhaugh KG, Morton R, Bedo D, Horton BJ, Mahon RJ (2007) Estimating the indcidence of fly myases in Australian sheep flocks: development of a weather-driven regression model. Medical and Veterinary Entomology 21, 153–167.
| Estimating the indcidence of fly myases in Australian sheep flocks: development of a weather-driven regression model.Crossref | GoogleScholarGoogle Scholar | 17550435PubMed |