Hostname: page-component-8448b6f56d-cfpbc Total loading time: 0 Render date: 2024-04-23T15:48:12.054Z Has data issue: false hasContentIssue false
  • English
  • Français

An initial investigation into the effects of isolation and enrichment on the welfare of laboratory pigs housed in the PigTurn® system, assessed using tear staining, behaviour, physiology and haematology

Published online by Cambridge University Press:  01 January 2023

SP DeBoer ,
JP Garner ,
RR McCain ,
DC Lay Jr ,
SD Eicher  and
JN Marchant-Forde
SP DeBoer
Affiliation:
Department of Animal Sciences, Purdue University, West Lafayette, IN 47907, USA USDA-ARS, Livestock Behavior Research Unit, West Lafayette, IN 47907, USA
JP Garner
Affiliation:
Department of Animal Sciences, Purdue University, West Lafayette, IN 47907, USA Department of Comparative Medicine, Stanford University, Stanford, CA 94305, USA
RR McCain
Affiliation:
Purdue Translational Pharmacology CTSI Core Facility, West Lafayette, IN 47907, USA
DC Lay Jr
Affiliation:
USDA-ARS, Livestock Behavior Research Unit, West Lafayette, IN 47907, USA
SD Eicher
Affiliation:
USDA-ARS, Livestock Behavior Research Unit, West Lafayette, IN 47907, USA
JN Marchant-Forde*
Affiliation:
USDA-ARS, Livestock Behavior Research Unit, West Lafayette, IN 47907, USA
*
* Contact for correspondence and requests for reprints: Jeremy.marchant-forde@ars.usda.gov
Get access Rights & Permissions [Opens in a new window]

Abstract

In some parts of the world, the laboratory pig (Sus scrofa) is often housed in individual, sterile housing which may impose stress. Our objectives were to determine the effects of isolation and enrichment on pigs housed within the PigTurn® — a novel penning system with automated blood sampling — and to investigate tear staining as a novel welfare indicator. Twenty Yorkshire × Landrace weaner pigs were randomly assigned to one of four treatments in a 2 × 2 factorial combination of enrichment (non-enriched [NE] or enriched [E]) and isolation (visually isolated [I] or able to see another pig [NI]). Pigs were catheterised and placed into the PigTurns® 48 h post recovery. Blood was collected automatically twice daily to determine white blood cell (WBC) differential counts and assayed for cortisol. Photographs of the eyes were taken daily and tear staining was quantified using a 0-5 scoring scale and Image-J software to measure stain area and perimeter. Behaviour was video recorded and scan sampled to determine time budgets. Data were analysed as an REML using the MIXED procedure of SAS. Enrichment tended to increase proportion of time standing and lying laterally and decrease plasma cortisol, tear-stain area and perimeter. There was a significant isolation by enrichment interaction. Enrichment given to pigs housed in isolation had no effect on plasma cortisol, but greatly reduced it in non-isolated pigs. Tear-staining area and perimeter were highest in the NE-I treatment compared to the other three treatments. Eosinophil count was highest in the E-NI treatment and lowest in the NE-I treatment. The results suggest that in the absence of enrichment, being able to see another animal but not interact may be frustrating. The combination of no enrichment and isolation maximally impacted tear staining and eosinophil numbers. However, appropriate enrichment coupled with proximity of another pig would appear to improve welfare.

Keywords

animal welfarecortisolenrichmentisolationpigstear staining
Type
Research Article
Information
Animal Welfare , Volume 24 , Issue 1 , February 2015 , pp. 15 - 27
Copyright
© 2015 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

Armario, A, Montero, J and Balasch, J 1986 Sensitivity of cor-ticosterone and some metabolic variables to graded levels of low intensity stresses in adult male rats. Physiology & Behavior 37: 559–561. http://dx.doi.org/10.1016/0031-9384(86)90285-4CrossRefGoogle Scholar
Averós, X, Brossard, L, Dourmad, JY, de Greef, KH, Edge, HL, Edwards, SA and Meunier-Salaün, MC 2010 A meta-analysis of the combined effect of housing and environmental enrichment characteristics on the behavior and performance of pigs. Applied Animal Behaviour Science 127: 73–85. http://dx.doi.org/10.1016/j.applanim.2010.09.010CrossRefGoogle Scholar
Averós, X, Herranz, A, Sánchez, R and Gosálvez, LF 2009 Effect of the duration of commercial journeys between rearing farms and growing-finishing farms on the physiological stress response of weaned piglets. Livestock Science 122: 339–344. http://dx.doi.org/10.1016/j.livsci.2008.09.019CrossRefGoogle Scholar
Balcombe, J, Barnard, N and Sandusky, C 2004 Laboratory routines cause animal stress. Contemporary Topics in Laboratory Animal Science 43: 42–51Google ScholarPubMed
Burn, CC, Peters, A and Mason, GJ 2006 Acute effects of cage cleaning at different frequencies on laboratory rat behaviour and welfare. Animal Welfare 15: 161–171Google Scholar
Chieffi, G, Baccari, G, Di Matteo, L, d'lstria, M, Minucci, S and Varriale, B 1996 Cell biology of the Harderian Gland. International Review of Cytology 63: 1–80Google Scholar
DeBoer, S, Koopmans, S and Slangen, J 1990 Plasma cate-cholamine, corticosterone and glucose responses to repeated stress in rats: effect of interstressor interval length. Physiology & Behavior 47: 1117–1124. http://dx.doi.org/10.1016/0031-9384(90)90361-7CrossRefGoogle Scholar
DeBoer, SP, Garner, JP, Lay, DC Jr, Eicher, SD, Lucas, JR and Marchant-Forde, JN 2013 Does the presence of a human effect the preference of enrichment items in young isolated pigs? Applied Animal Behaviour Science 143: 96–103. http://dx.doi.org/10.1016/j.applanim.2012.10.007CrossRefGoogle Scholar
DeBoer, SP and Marchant-Forde, JN 2013 Tear staining as a potential welfare indicator in pigs. In: Hotzel, MJ and Pinheiro Machado, LC (eds) Proceedings of 47th Congress of the International Society for Applied Ethology p 125. 2-6 June 2013, Florianopolis, BrazilGoogle Scholar
De Jonge, F, Bokkers, E, Schouten, W and Helmond, F 1996 Rearing piglets in a poor environment: developmental aspects of social stress in pigs. Physiology & Behavior 60: 389–396. http://dx.doi.org/10.1016/S0031-9384(96)80009-6CrossRefGoogle Scholar
Dreyfuss, F and Czaczkes, J 1959 Blood cholesterol and uric acid of healthy medical students under the stress of an examination. AMA Archives of Internal Medicine 103: 708–711. http://dx.doi.org/10.1001/archinte.1959.00270050030006CrossRefGoogle ScholarPubMed
Dreyfuss, F and Feldman, S 1952 Eosinopenia induced by emotional stress. Acta Medica Scandinavica 144: 107. http://dx.doi.org/10.1111/j.0954-6820.1952.tb15672.xCrossRefGoogle ScholarPubMed
Elmore, MRP, Garner, JP, Johnson, AK, Richert, BT and Pajor, EA 2010 A flooring comparison: the impact of rubber mats on the health, behavior and welfare of group-housed sows at breeding. Applied Animal Behaviour Science 123: 7–15. http://dx.doi.org/10.1016/j.applanim.2009.11.012CrossRefGoogle Scholar
Faul, F, Erdfelder, E, Buchner, A and Lang, A-G 2009 Statistical power analyses using G*Power 3.1: tests for correlation and regression analyses. Behavior Research Methods 41: 1149–1160. http://dx.doi.org/10.3758/BRM.41.4.1149CrossRefGoogle ScholarPubMed
Forssberg, A, Tribukait, B and Vikterlöf, K-J 1961 Early blood leucocyte changes in mice and guinea pigs following X-irradiation and stress caused by operative manipulations. Acta Physiologica Scandinavica 52: 1–7. http://dx.doi.org/10.1111/j.1748-1716.1961.tb02193.xCrossRefGoogle ScholarPubMed
Fox, M 1986 Laboratory Animal Husbandry: Ethology, Welfare and Experimental Variables. State University of New York Press: Albany, NY, USAGoogle Scholar
Guide for the Care and Use of Agriculture Animals in Research and Teaching (GUCAA) 2010 Environmental Enrichment, Third Edition. Federation of Animal Science Societies: Champaign, IL, USAGoogle Scholar
Guy, JH, Meads, ZA, Shiel, RS and Edwards, SA 2013 The effect of combining different environmental enrichment materials on enrichment use by growing pigs. Applied Animal Behaviour Science 144: 102–107. http://dx.doi.org/10.1016/j.applan-im.2013.01.006CrossRefGoogle Scholar
Harkness, JE and Ridgway, MD 1980 Chromodaccryorrhea in laboratory rats (Rattus norvegicus); etiologic considerations. Laboratory Animal Science 30: 841–844Google Scholar
Haussmann, M, Carroll, J, Weesner, G, Daniels, M, Matteri, R and Lay, D 2000 Administration of ACTH to restrained, preg-nant sows alters their pigs’ hypothalamic-pituitary-adrenal (HPA) axis. Journal of Animal Science 78: 2399–2411CrossRefGoogle Scholar
Herskin, M and Jensen, K 2000 Effects of different degrees of social isolation on the behaviour of weaned piglets kept for exper-imental purposes. Animal Welfare 9: 237–249Google Scholar
Jackson, PGG and Cockroft, PD 2007 Diseases of the respira-tory system. In: Handbook of Pig Medicine pp 70–82. Saunders Ltd: London, UK. http://dx.doi.org/10.1016/B978-0-7020-2828-1.50008-6CrossRefGoogle Scholar
Jain, N 1993 Essentials of Veterinary Hematology. Blackwell Publishing: Philadelphia, USAGoogle Scholar
Klont, R, Hulsegge, B, Hoving-Bolink, A, Gerritzen, M, Kurt, E, Winkelman-Goedhart, H, de Jong, I and Kranen, R 2001 Relationships between behavioral and meat quality characteristics of pigs raised under barren and enriched housing conditions. Journal of Animal Science 79: 2835–2843CrossRefGoogle ScholarPubMed
Lewis, N 1999 Frustration of goal-directed behaviour in swine. Applied Animal Behaviour Science 64: 19–29. http://dx.doi.org/10.1016/S0168-1591(99)00025-8CrossRefGoogle Scholar
Line, S, Morgan, K and Markowitz, H 1989 Heart rate and acti-vity of rhesus monkeys in response to routine events. Laboratory Primate Newsletter 28: 9–12Google Scholar
Louch, C, Meyer, R and Emlen, J 1953 Effect of stress on diur-nal fluctuations in eosinophils of the laboratory mouse. Experimental Biology and Medicine 84: 668–671. http://dx.doi.org/10.3181/00379727-82-20213CrossRefGoogle Scholar
Mack, LA, Lay, DC Jr, Eicher, SD, Johnson, AK, Richert, BT and Pajor, EA 2014 Group space allowance has little effect on sow health, productivity, or welfare in a free-access stall system Journal of Animal Science 92: 2554–2567. http://dx.doi.org/10.2527/jas.2013-7352CrossRefGoogle ScholarPubMed
Marchant-Forde, AEM and Marchant-Forde, JN 2014 Social status and tear staining in nursery pigs. In: Manteca, X, Estevez, I, Marin, RH and Averos, X (eds) Proceedings of 48th Congress of the International Society for Applied Ethology p 145. 29 July-2 August 2014, Vitoria-Gasteiz, SpainGoogle Scholar
Marchant-Forde, JN, Lay, DC Jr, McMunn, KA, Cheng, HW, Pajor, EA and Marchant-Forde, RM 2014 Postnatal piglet hus-bandry practices and well-being: the effects of alternative techni-ques delivered in combination. Journal of Animal Science 92: 1150–1160. http://dx.doi.org/10.2527/jas.2013-6929CrossRefGoogle Scholar
Marchant-Forde, JN, Matthews, DL, Poletto, R, McCain, RR, Mann, DD, DeGraw, RT, Hampsch, JM, Peters, S, Knipp, GT and Kissinger, CB 2012 Plasma cortisol and noradrenalin con-centrations in pigs: automated sampling of freely moving pigs hou-sed in the PigTurn versus manually sampled and restrained pigs. Animal Welfare 21: 197–205. http://dx.doi.org/10.7120/09627286.21.2.197CrossRefGoogle Scholar
Mason, G, Wilson, D, Hampton, C and Würbel, H 2004 Non-invasively assessing disturbance and stress in laboratory rats by scoring chromodacryorrhoea. Alternatives to Laboratory Animals 32(S1): 153–159CrossRefGoogle ScholarPubMed
McCafferty, RE and Pinkstaff, CA 1970 A study of sexual dimorphism in Harderian glands of the miniature pig. Anatomical Record 166: 340Google Scholar
Moberg, G and Mench, J 2000 The Biology of Animal Stress: Basic Principles and Implications for Animal Welfare. CABI Publishing: New York, USACrossRefGoogle Scholar
Moynihan, J, Brenner, G and Koota, G 1990 The effects of handling on antibody production, mitogen responses, spleen cell number, and lymphocyte subpopulations. Life Science 46: 1937–1944. http://dx.doi.org/10.1016/0024-3205(90)90509-PCrossRefGoogle ScholarPubMed
Moynihan, J, Koota, G and Brenner, G 1989 Repeated interperi-toneal injections of saline attenuate the antibody response to a sub-sequent intraperitoneall injection of antigen. Brain, Behavior and Immunity 3: 90–96. http://dx.doi.org/10.1016/0889-1591(89)90008-1CrossRefGoogle Scholar
Payne, AP 1994 The Harderian gland: a tercentennial review. Journal of Anatomy 185: 1–49Google ScholarPubMed
Register, KB 2012 Atrophic rhinitis of swine. OIE Manual of Diagnostic Tests and Vaccines for Terrestrial Animals. OIE: Paris, FranceGoogle Scholar
Reinhardt, V and Reinhardt, A 2002 Comfortable Quarters for Laboratory Animals, Ninth Edition. Animal Welfare Institute: Washington DC, USAGoogle Scholar
Rothenberg, ME and Hogan, SP 2006 The eosinophil. Annual Review of Immunology 24: 147–174. http://dx.doi.org/10.1146/annurev.immunol.24.021605.090720CrossRefGoogle ScholarPubMed
Ruis, M, te Brake, J, Engel, B, Buist, W, Blokhuis, H and Koolhaas, J 2001 Adaptation to social isolation: acute and long-term stress responses of growing gilts with different coping char-acteristics. Physiology & Behavior 73: 541–551. http://dx.doi.org/10.1016/S0031-9384(01)00548-0CrossRefGoogle Scholar
Russell, WMS and Burch, RL 1959 The Principles of Humane Experimental Technique. Methuen & Co Ltd: London, UK. http://altweb.jhsph.edu/publications/humane_exp/het-toc.htmGoogle Scholar
Seggie, J and Brown, G 1975 Stress response patterns of plas-ma corticosterone, prolactin, and growth hormone in the rat, fol-lowing handling or exposure to novel environment. Canadian Journal of Physiology and Pharmacology 53: 629–637. http://dx.doi.org/10.1139/y75-087CrossRefGoogle ScholarPubMed
Sharp, J, Zammit, T and Azar, T 2001 Stress-like responses to common procedures in rats: effect of the estrous cycle. Contemporary Topics in Laboratory Animal Science 41: 15–22Google Scholar
Sharp, J, Zammit, T and Azar, T 2002 Stress-like responses to common procedures in male rats housed alone or with other rats. Contemporary Topics in Laboratory Animal Science 41: 8–14Google ScholarPubMed
Sharp, J, Zammit, T and Azar, T 2003 Stress-like responses to common procedures in individually and group-housed female rats. Contemporary Topics in Laboratory Animal Science 42: 9–18Google ScholarPubMed
Smith, ME, Gopee, NV and Ferguson, SA 2009 Preferences of minipigs for environmental enrichment objects. Journal of the American Association for Laboratory Animal Science 48: 391–394Google ScholarPubMed
Stolba, A and Wood-Gush, D 1989 The behavior of pigs in a semi-natural environment. Animal Production 48: 419–425. http://dx.doi.org/10.1017/S0003356100040411Google Scholar
Straw, BE, Dewey, CE and Wilson, MR 2006 Differential diag-nosis of disease. In: Straw, BE, Zimmerman, JJ, D’Allaire, S and Taylor, DJ (eds) Diseases of Swine, Ninth Edition. Blackwell Publishing Ltd: Oxford, UKGoogle Scholar
Street, BR and Gonyou, HW 2008 Effects of housing finishing pigs in two group sizes and at two floor space allocations on production, health, behavior, and physiological variables. Journal of Animal Science 86: 982–991. http://dx.doi.org/10.2527/jas.2007-0449CrossRefGoogle ScholarPubMed
Tuchscherer, M, Kanitz, E, Puppe, B and Tuchscherer, A 2006 Early social isolation alters behavioral and physiological responses to an endotoxin challenge in piglets. Hormones & Behavior 50: 753–761. http://dx.doi.org/10.1016/j.yhbeh.2006.06.026CrossRefGoogle Scholar
Tuchscherer, M, Kanitz, E, Puppe, B, Tuchscherer, A and Stabenow, B 2004 Effects of postnatal social isolation on hormonal and immune responses of pigs to an acute endotoxin challenge. Physiology & Behavior 82: 503–511. http://dx.doi.org/10.1016/j.physbeh.2004.04.056CrossRefGoogle Scholar
Tuyttens, FAM, Wouters, F, Struelens, E, Sonck, B and Duchanteau, L 2008 Synthetic lying mats improve lying comfort of gestating sows. Applied Animal Behaviour Science 114: 76–85. http://dx.doi.org/10.1016/j.applanim.2008.01.015CrossRefGoogle Scholar
Van de Weerd, H, Van Loo, P, Van Zutphen, L, Koolhaas, J and Baumans, V 1997 Preferences for nesting material as envi-ronmental enrichment for laboratory mice. Lab Animal 31: 133–143. http://dx.doi.org/10.1258/002367797780600152CrossRefGoogle Scholar
Von Borell, E, Ozpinar, A, Eslinger, KM, Schnitz, AL, Zhao, Y and Mitloehner, EM 2007 Acute and prolonged effects of ammonia on hematological variables, stress responses, performance, and behav-ior of nursery pigs. Journal of Swine Health and Production 15: 137–145Google Scholar
Warnier, A and Zayan, R 1985 Effects of confinement upon behavioural hormonal responses and production indices in fattening pigs. In: Zayan, R (ed) Social Space for Domestic Animals pp 128–150. Martinus Nijhoff: Dordrecht, The Netherlands. http://dx.doi.org/10.1007/978-94-009-5040-5_14CrossRefGoogle Scholar
Wiepkema, P and Koolhaas, J 1993 Stress and animal welfare. Animal Welfare 2: 195–218Google Scholar
Wood-Gush, D, Duncan, I and Fraser, D 1975 Social stress and welfare problems in agricultural animals. In: Hafez, ESE (ed) The Behavior of Domestic Animals pp 182–200. Bailliere Tindal: London, UKGoogle Scholar
Würbel, H, Chapman, R and Rutland, C 1998 Effect of feed and environmental enrichment on development of stereotypic wire-gnawing in laboratory mice. Applied Animal Behaviour Science 60: 69–81. http://dx.doi.org/10.1016/S0168-1591(98)00150-6CrossRefGoogle Scholar
Würbel, H and Garner, JP 2007 Refinement of rodent research through environmental enrichment and systematic randomization. NC3Rs #9: 1–9. www.nc3rs.org.ukGoogle Scholar