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The impact of chronic environmental stressors on growing pigs, Sus scrofa (Part 1): stress physiology, production and play behaviour

Published online by Cambridge University Press:  07 June 2010

E. A. O’Connor ,
M. O. Parker ,
M. A. McLeman ,
T. G. Demmers ,
J. C. Lowe ,
L. Cui ,
E. L. Davey ,
R. C. Owen ,
C. M. Wathes  and
S. M. Abeyesinghe
E. A. O’Connor*
Affiliation:
Centre for Animal Welfare, Department of Veterinary Clinical Sciences, Royal Veterinary College, University of London, Hawkshead Lane, North Mymms, Hatfield, Hertfordshire, AL7 9TA, UK
M. O. Parker
Affiliation:
Centre for Animal Welfare, Department of Veterinary Clinical Sciences, Royal Veterinary College, University of London, Hawkshead Lane, North Mymms, Hatfield, Hertfordshire, AL7 9TA, UK
M. A. McLeman
Affiliation:
Centre for Animal Welfare, Department of Veterinary Clinical Sciences, Royal Veterinary College, University of London, Hawkshead Lane, North Mymms, Hatfield, Hertfordshire, AL7 9TA, UK
T. G. Demmers
Affiliation:
Centre for Animal Welfare, Department of Veterinary Clinical Sciences, Royal Veterinary College, University of London, Hawkshead Lane, North Mymms, Hatfield, Hertfordshire, AL7 9TA, UK
J. C. Lowe
Affiliation:
Centre for Animal Welfare, Department of Veterinary Clinical Sciences, Royal Veterinary College, University of London, Hawkshead Lane, North Mymms, Hatfield, Hertfordshire, AL7 9TA, UK
L. Cui
Affiliation:
Centre for Animal Welfare, Department of Veterinary Clinical Sciences, Royal Veterinary College, University of London, Hawkshead Lane, North Mymms, Hatfield, Hertfordshire, AL7 9TA, UK School of Agriculture and Biology, Group of Zoonosis and Comparative Medicine, Shanghai Jiaotong University, China
E. L. Davey
Affiliation:
Centre for Animal Welfare, Department of Veterinary Clinical Sciences, Royal Veterinary College, University of London, Hawkshead Lane, North Mymms, Hatfield, Hertfordshire, AL7 9TA, UK
R. C. Owen
Affiliation:
Centre for Animal Welfare, Department of Veterinary Clinical Sciences, Royal Veterinary College, University of London, Hawkshead Lane, North Mymms, Hatfield, Hertfordshire, AL7 9TA, UK
C. M. Wathes
Affiliation:
Centre for Animal Welfare, Department of Veterinary Clinical Sciences, Royal Veterinary College, University of London, Hawkshead Lane, North Mymms, Hatfield, Hertfordshire, AL7 9TA, UK
S. M. Abeyesinghe
Affiliation:
Centre for Animal Welfare, Department of Veterinary Clinical Sciences, Royal Veterinary College, University of London, Hawkshead Lane, North Mymms, Hatfield, Hertfordshire, AL7 9TA, UK
*
†E-mail: eoconnor@rvc.ac.uk
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Abstract

Commercially farmed animals are frequently housed in conditions that impose a number of concurrent environmental stressors. For pigs housed indoors, elevated levels of mechanical noise, atmospheric ammonia and low light intensities are commonplace. This experiment examined the effects on growing pigs of chronic exposure to combinations of commercially relevant levels of these potential stressors. Four-week-old hybrid female pigs (n = 224) were housed under experimentally manipulated conditions of nominally either <5 or 20 ppm atmospheric concentration of ammonia (24 h), a light intensity of 40 lux or 200 lux (12 h) and mechanical noise at either ⩽60 or 80 dB(A) (24 h) for 15 weeks in a fully factorial arrangement (23) of treatments. The response of pigs to these environmental factors was assessed using a suite of physiological, production and behavioural measures. These included indicators of hypothalamic–pituitary–adrenal (HPA) axis activation such as salivary cortisol and adrenal morphometry, as well as body weight, food conversion efficiency and general health scores. Play behaviour was recorded as it is thought to be inversely related to stress. Chronic exposure to ammonia produced the strongest effect, shown by lower concentrations of salivary cortisol and larger adrenal cortices in the pigs reared under 20 ppm ammonia, which may have been indicative of a period of HPA activation leading to a downregulation of cortisol production. The pigs in the ammoniated rooms also performed less play behaviour than pigs in non-ammoniated rooms. There was evidence for an interaction between high noise and ammonia on the health scores of pigs and for brighter light to ameliorate the effect of ammonia on salivary cortisol. However, there was no measurable impact of these potential stressors on the productivity of the pigs or any of the other physiological parameters measured. We conclude that there should be little concern in terms of performance about the physical stressors tested here, within current European Union legal limits. However, 20 ppm ammonia may have had an adverse influence on the well-being of growing pigs. In this study, all other aspects of the pigs’ husbandry were optimal; therefore, it is possible that under less favourable conditions, more pronounced effects of ammonia, noise and dim light would be observed.

Keywords

pigsstressammonialightnoise
Type
Full Paper
Information
animal , Volume 4 , Issue 11 , November 2010 , pp. 1899 - 1909
Copyright
Copyright © The Animal Consortium 2010

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References

Algers, B, Ekesbo, I, Strömberg, S 1978. Noise measurements in farm animal environments. Acta Veterinaria Scandinavica 68, 1–19.Google Scholar
Boissy, A, Manteuffel, G, Jensen, MB, Moe, RO, Spruijt, B, Keeling, LJ, Winckler, C, Forkman, B, Dimitrov, I, Langbein, J, Bakken, M, Veissier, I, Aubert, A 2007. Assessment of positive emotions in animals to improve their welfare. Physiology & Behavior 92, 375–397.Google Scholar
Bolker, BM, Brooks, ME, Clark, CJ, Geange, SW, Poulsen, JR, Stevens, MHH, White, J-SS 2009. Generalized linear mixed models: a practical guide for ecology and evolution. Trends in Ecology & Evolution 24, 127–135.CrossRefGoogle ScholarPubMed
Bushong, DM, Friend, TH, Knabe, DA 2000. Salivary and plasma cortisol response to adrenocorticotropin administration in pigs. Laboratory Animals 34, 171–181.Google Scholar
Chrousos, GP 1995. The hypothalamic-pituitary-adrenal-axis and immune-mediated inflammation. The New England Journal of Medicine 332, 1351–1363.Google Scholar
Clark, LS, Cowan, DF, Pfeiffer, DC 2006. Morphological changes in the Atlantic bottlenose dolphin (Tursiops truncatus) adrenal gland associated with chronic stress. Journal of Comparative Pathology 135, 208–216.Google Scholar
Cook, NJ, Schaefer, AL, Lepage, P, Morgan Jones, S 1996. Salivary vs. serum cortisol for the assessment of adrenal activity in swine. Canadian Journal of Animal Science 76, 329–335.Google Scholar
Cordoni, G 2009. Social play in captive wolves (Canis lupus): not only an immature affair. Behaviour 146, 1363–1385.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, 571–578.Google Scholar
de Jong, IC, Ekkel, ED, Van de Burgwal, JA, Lambooij, E, Korte, SM, Ruis, MAW, Koolhaas, JM, Blokhuis, HJ 1998. Effects of strawbedding on physiological responses to stressors and behavior in growing pigs. Physiology & Behavior 64, 303–310.CrossRefGoogle ScholarPubMed
defra 2003. Economic evaluation of the pig industry restructuring scheme. Agra CEAS Consulting in association with the Department of Agricultural Sciences, Imperial College, University of London.Google Scholar
defra 2007. Welfare of farmed animals (England) regulations (SI 2007 No 2078) Section 8: codes of recommendation for the welfare of livestock: pigs.Google Scholar
Done, SH, Chennells, DJ, Gresham, ACJ, Williamson, S, Hunt, B, Taylor, LJ, Bland, V, Jones, P, Armstrong, D, White, RP, Demmers, TGM, Teer, N, Wathes, CM 2005. Clinical and pathological responses of weaned pigs to atmospheric ammonia and dust. The Veterinary Record 157, 71.Google Scholar
Drummond, JG, Curtis, SE, Simon, J, Norton, HW 1980. Effects of aerial ammonia on growth and health of young pigs. Journal of Animal Science 50, 1085–1091.Google Scholar
Ekkel, ED, Dieleman, SJ, Schouten, WGP, Portela, A, Cornelissen, G, Tielen, MJM, Halberg, F 1996. The circadian rhythm of cortisol in the saliva of young pigs. Physiology & Behavior 60, 985–989.Google Scholar
Foury, A, Geverink, NA, Gil, M, Gispert, M, Hortós, M, Font i Furnols, M, Carrion, D, Blott, SC, Plastow, GS, Mormède, P 2007. Stress neuroendocrine profiles in five pig breeding lines and the relationship with carcass composition. Animal 1, 973–982.Google Scholar
Golden, RN, Gaynes, BN, Ekstrom, RD, Hamer, RM, Jacobsen, FM, Suppes, T, Wisner, KL, Nemeroff, CB 2005. The efficacy of light therapy in the treatment of mood disorders: a review and meta-analysis of the evidence. The American Journal of Psychiatry 162, 656–662.Google Scholar
Greenwood, PI, Shutt, DA 1992. Salivary and plasma cortisol as an index of stress in goats. Australian Veterinary Journal 69, 161–163.Google Scholar
Groot Koerkamp, PWG, Metz, JHM, Uenk, GH, Phillips, VR, Holden, MR, Sneath, RW, Short, JL, White, RPP, Hartung, J, Seedorf, J, Schröder, M, Linkert, KH, Pedersen, S, Takai, H, Johnsen, JO, Wathes, CM 1998. Concentrations and emissions of ammonia in livestock buildings in Northern Europe. Journal of Agricultural Engineering Research 70, 79–95.CrossRefGoogle Scholar
Gustin, P, Urbain, B, Prouvost, JF, Ansay, M 1994. Effects of atmospheric ammonia on pulmonary hemodynamics and vascular permeability in pigs: interaction with endotoxins. Toxicology and Applied Pharmacology 125, 17–26.CrossRefGoogle ScholarPubMed
Harris, RBS, Gu, H, Mitchell, TD, Endale, L, Russo, M, Ryan, DH 2004. Increased glucocorticoid response to a novel stress in rats that have been restrained. Physiology & Behavior 81, 557–568.Google Scholar
Hötzel, MJ, Lopez, EJC, de Oliveira, PAV, Guidoni, AL 2009. Behaviour and performance of pigs finished on deep bedding with wood shavings or rice husks in summer. Animal Welfare 18, 65–71.Google Scholar
Hyun, Y, Ellis, M, Riskowski, G, Johnson, RW 1998. Growth performance of pigs subjected to multiple concurrent environmental stressors. Journal of Animal Science 76, 721–727.Google Scholar
Janssens, C, Helmond, FA, Wiegant, VM 1994. Increased cortisol response to exogenous adrenocorticotropic hormone in chronically stressed pigs – influence of housing conditions. Journal of Animal Science 72, 1771–1777.CrossRefGoogle ScholarPubMed
Janssens, CJ, Helmond, FA, Loyens, LW, Schouten, WG, Wiegant, VM 1995. Chronic stress increases the opioid-mediated inhibition of the pituitary-adrenocortical response to acute stress in pigs. Endocrinology 136, 1468–1473.Google Scholar
Jasnow, AM, Drazen, DL, Huhman, KL, Nelson, RJ, Demas, GE 2001. Acute and chronic social defeat suppresses humoral immunity of male Syrian Hamsters (Mesocricetus auratus). Hormones and Behavior 40, 428–433.Google Scholar
Jones, JB, Burgess, LR, Webster, AJF, Wathes, CM 1996. Behavioural responses of pigs to atmospheric ammonia in a chronic choice test. Animal Science 63, 437–445.Google Scholar
Kanitz, E, Otten, W, Tuchscherer, M 2005. Central and peripheral effects of repeated noise stress on hypothalamic-pituitary-adrenocortical axis in pigs. Livestock Production Science 94, 213–224.Google Scholar
Kanitz, E, Tuchscherer, M, Puppe, B, Tuchscherer, A, Stabenow, B 2004. Consequences of repeated early isolation in domestic piglets (Sus scrofa) on their behavioural, neuroendocrine, and immunological responses. Brain, Behavior and Immunity 18, 35–45.Google Scholar
Kenward, MG, Roger, JH 1997. Small sample inference for fixed effects from restricted maximum likelihood. Biometrics 53, 983–997.CrossRefGoogle ScholarPubMed
Korte, SM, Olivier, B, Koolhaas, JM 2007. A new animal welfare concept based on allostasis. Physiology & Behavior 92, 422–428.CrossRefGoogle ScholarPubMed
Littell, RC, Milliken, GA, Stroup, WW, Wolfinger, RD, Schabenberger, O 2006. SAS for mixed models. SAS Institute Inc., Cary, NC, USA.Google Scholar
Miller, GE, Chen, E, Zhou, ES 2007. If it goes up, must it come down? Chronic stress and the hypothalamic-pituitary-adrenocortical axis in humans. Psychological Bulletin 133, 25–45.CrossRefGoogle ScholarPubMed
Monjan, AA, Collector, MI 1977. Stress-induced modulation of the immune response. Science 196, 307–308.Google Scholar
Mormede, P, Andanson, S, Auperin, B, Beerda, B, Guemene, D, Malnikvist, J, Manteca, X, Manteuffel, G, Prunet, P, van Reenen, CG, Richard, S, Veissier, I 2007. Exploration of the hypothalamic-pituitary-adrenal function as a tool to evaluate animal welfare. Physiology & Behavior 92, 317–339.Google Scholar
Muller-Schwarze, D, Stagge, B, Muller-Schwarze, C 1982. Play behavior: persistence, decrease, and energetic compensation during food shortage in deer fawns. Science 215, 85–87.CrossRefGoogle ScholarPubMed
Newberry, RC, Wood-Gush, DGM, Hall, JW 1988. Playful behaviour of piglets. Behavioural Processes 17, 205–216.CrossRefGoogle ScholarPubMed
Otten, W, Kanitz, E, Puppe, B, Tuchscherer, M, Brüssow, KP, Nürnberg, G, Stabenow, B 2004. Acute and long term effects of chronic intermittent noise stress on hypothalamic-pituitary-adrenocortical and sympatho-adrenomedullary axis in pigs. Animal Science 78, 271–283.CrossRefGoogle Scholar
Palagi, E, Paoli, T 2007. Play in adult Bonobos (Pan paniscus): modality and potential meaning. American Journal of Physical Anthropology 134, 219–225.CrossRefGoogle ScholarPubMed
Parker, MO, O'Connor, EA, McLeman, MA, Demmers, TGM, Lowe, JC, Owen, RC, Davey, EL, Wathes, CM, Abeyesinghe, SM 2010. The impact of chronic environmental stressors on growing pigs, Sus scrofa (Part 2): social behaviour. Animal, doi:10.1017/S1751731110001084.Google Scholar
Partonen, T, Lonnqvist, J 2000. Bright light improves vitality and alleviates distress in healthy people. Journal of Affective Disorders 57, 55–61.Google Scholar
Piccoli, B, Parazzoli, S, Zaniboni, A, Demartini, G, Fraschini, F 1991. Non-visual effects of light mediated via the optical route: review of the literature and implications for occupational medicine. La Medicina del Lavoro 82, 213–232.Google Scholar
Reiter, RJ 1991. Pineal gland interface between the photoperiodic environment and the endocrine system. Trends in Endocrinology & Metabolism 2, 13–19.Google Scholar
Ruis, MAW, te Brake, JHA, Engel, B, Buist, WG, Blokhuis, HJ, Koolhaas, JM 2001. Adaptation to social isolation – acute and long-term stress responses of growing gilts with different coping characteristics. Physiology & Behavior 73, 541–551.Google Scholar
Ruis, MAW, Te Brake, JHA, Engel, B, Ekkel, ED, Buist, WG, Blokhuis, HJ, Koolhaas, JM 1997. The circadian rhythm of salivary cortisol in growing pigs: effects of age, gender, and stress. Physiology & Behavior 62, 623–630.Google Scholar
Sapolsky, RM, Romero, LM, Munck, AU 2000. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Reviews 21, 55–89.Google Scholar
Seedorf, J, Hartung, J 1999. Survey of ammonia concentrations in livestock buildings. The Journal of Agricultural Science 133, 433–437.Google Scholar
Selye, H 1936. A syndrome produced by diverse nocuous agents. Nature 138, 32.Google Scholar
Siviy, S, Panksepp, J 1985. Energy balance and play in juvenile rats. Physiology & Behavior 35, 438–441.Google Scholar
Siviy, SM, Atrens, DM 1992. The energetic costs of rough and tumble play in the juvenile rat. Developmental Psychobiology 25, 137–148.Google Scholar
Smith, JH, Wathes, CM, Baldwin, BA 1996. The preference of pigs for fresh air over ammoniated air. Applied Animal Behaviour Science 49, 417–424.Google Scholar
Sorrells, AD, Eicher, SD, Scott, KA, Harris, MJ, Pajor, EA, Lay, DCJ, Richert, BT 2006. Postnatal behavioral and physiological responses of piglets from gilts housed individually or in groups during gestation. Journal of Animal Science 84, 757–766.Google Scholar
Stombaugh, DP, Teague, HS, Roller, WL 1969. Effects of atmospheric ammonia on the pig. Journal of Animal Science 28, 844–847.Google Scholar
Sutherland, MA, Niekamp, SR, Rodriguez-Zas, SL, Salak-Johnson, JL 2006. Impacts of chronic stress and social status on various physiological and performance measures in pigs of different breeds. Journal of Animal Science 84, 588–596.CrossRefGoogle ScholarPubMed
Talling, JC, Waran, NK, Wathes, CM, Lines, JA 1996. Behavioural and physiological responses of pigs to sound. Applied Animal Behaviour Science 48, 187–202.Google Scholar
Talling, JC, Lines, JA, Wathes, CM, Waran, NK 1998. The acoustic environment of the domestic pig. Journal of Agricultural Engineering Research 71, 1–12.Google Scholar
Taylor, N, Prescott, N, Perry, G, Potter, M, Sueur, CL, Wathes, C 2006. Preference of growing pigs for illuminance. Applied Animal Behaviour Science 96, 19–31.Google Scholar
Ulrich-Lai, YM, Figueiredo, HF, Ostrander, MM, Choi, DC, Engeland, WC, Herman, JP 2006. Chronic stress induces adrenal hyperplasia and hypertrophy in a subregion-specific manner. American Journal of Physiology-Endocrinology and Metabolism 291, E965–E973.Google Scholar
UK Health and Safety Executive 2001. EH40/2001 Occupational Exposure Limits.Google Scholar
Vanderschuren, LJMJ, Niesink, RJM, Ree, JM 1997. The neurobiology of social play behavior in rats. Neuroscience & Biobehavioral Reviews 21, 309–326.Google Scholar
Veissier, I, Boissy, A 2007. Stress and welfare: two complementary concepts that are intrinsically related to the animal’s point of view. Physiology & Behavior 92, 429–433.Google Scholar
von Borell, E 2000. Stress and coping in farm animals. Archiv Tierzucht/Archives Animal Breeding 43, 144–152.Google Scholar
von Borell, E, Özpinar, A, Eslinger, KM, Schnitz, AL, AZhao, Y, Mitloehner, FM 2007. Acute and prolonged effects of ammonia on hematological variables, stress responses, and behavior of nursery pigs. Journal of Swine Health and Production 15, 137–145.Google Scholar
Wathes, CM, Demmers, TGM, Teer, N, White, RP, Taylor, LL, Bland, V, Jones, P, Armstrong, D, Gresham, ACJ, Hartung, J, Chennells, DJ, Done, SH 2004. Production responses of weaned pigs after chronic exposure to airborne dust and ammonia. Animal Science 78, 87–97.Google Scholar
Yoshioka, G, Imaeda, N, Ohtani, T, Hayashi, K 2005. Effects of cortisol on muscle proteolysis and meat quality in piglets. Meat Science 71, 590–593.CrossRefGoogle ScholarPubMed