Hostname: page-component-7479d7b7d-fwgfc Total loading time: 0 Render date: 2024-07-11T04:35:42.889Z Has data issue: false hasContentIssue false
  • English
  • Français

A meta-analysis on the effects of the housing environment on the behaviour, mortality, and performance of growing rabbits

Published online by Cambridge University Press:  01 January 2023

R Sommerville ,
R Ruiz  and
X Averós
R Sommerville
Affiliation:
Compassion in World Farming, River Court, Mill Lane, Godalming, Surrey GU7 1EZ, UK The Brooke, 5th Floor Friars Bridge Court, 41-45 Blackfriars Road, London SE1 8NZ, UK
R Ruiz
Affiliation:
Neiker-Tecnalia, Department of Animal Production, 01080 Vitoria-Gasteiz, Spain
X Averós*
Affiliation:
Neiker-Tecnalia, Department of Animal Production, 01080 Vitoria-Gasteiz, Spain
*
* Contact for correspondence and requests for reprints: xaveros@neiker.eus
Get access Rights & Permissions [Opens in a new window]

Abstract

Although the number of rabbits (Oryctolagus cuniculus) produced in Europe is important, they are under-represented in welfare research. Studies on the effects of housing conditions have focused on performance and mortality. We conducted a meta-analysis to further understand the impact of the housing environment on growing rabbits. Whilst providing a robust quantifiable review, meta-analyses are restricted to existing literature. We included information on behaviour, mortality and performance. Twenty-seven peer-reviewed and conference publications, with a total of 99 experimental treatments, were used. We collected information about rabbit age, bodyweight, sex and breed; allometric space allowance, pen height, group size, environmental temperature, floor type, substrate and enrichment use, lighting, diet and medicated feed. Predictive equations for each response variable were calculated using multiple regression models. Higher space allowance was found to increase locomotor and social activity, and to reduce resting and comfort behaviour. Restricted pen height increased ingestive behaviour; comfort behaviours decreased as space allowance increased, although these might have been confounded with self-directed behaviours in literature. Mortality remained stable at varying space allowances, but increased with larger group sizes and enrichment objects. Growth rate, feed intake and feed conversion were reduced with higher space allowances and larger group sizes, and by provision of substrate and enrichment objects. Findings suggest that higher space allowance and unrestricted pen height are beneficial for rabbit behaviour, but might have undesired consequences if considered independent from other aspects. The challenge of promoting welfare in commercial conditions was highlighted, as a number of parameters which improved behavioural expression reduced performance. In certain cases welfare inputs complemented performance, including providing non-medicated feed and higher space allowance in cooler climates. Although our results should be interpreted with caution given the limitations of the included variables, they are expected to contribute to the improvement of current and new rabbit housing systems to optimise welfare.

Keywords

animal welfarebehaviourgrowing rabbitmeta-analysismortalityperformance
Type
Articles
Information
Animal Welfare , Volume 26 , Issue 2 , May 2017 , pp. 223 - 238
Copyright
© 2017 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

Aubret, JM and Duperray, J 1992 Effect of cage density on the performance and health of the growing rabbit. Journal of Applied Rabbit Research 15: 656–660Google Scholar
Averós, X, Brossard, L, Dourmad, JY, de Greef, K, Edge, HL, Edwards, SA and Meunier-Salaün, MC 2010a Quantitative assessment of the effects of space allowance, group size and floor characteristics on the lying behaviour and performance of pigs. Animal 4: 777–783. https://doi.org/10.1017/S1751731109991613CrossRefGoogle Scholar
Averós, X, Brossard, L, Dourmad, JY, de Greef, K, Edge, HL, Edwards, SA and Meunier-Salaün, MC 2010b A meta-analysis of the combined effect of housing and environmental enrichment characteristics on the behaviour and performance of pigs. Applied Animal Behaviour Science 127: 73–85. https://doi.org/10.1016/j.applanim.2010.09.010CrossRefGoogle Scholar
Averós, X, Brossard, L, Dourmad, JY, de Greef, KH, Edwards, SA and Meunier-Salaün, MC 2012 Meta-analysis on the effects of the physical environment, animal traits, feeder and feed characteristics on the feeding behaviour and performance of growing-finishing pigs. Animal 6: 1275–1289. https://doi.org/10.1017/S1751731112000328CrossRefGoogle ScholarPubMed
BAWC 2012 Opinion from the Belgian Animal Welfare Council. http://www.health.belgium.be/filestore/19082320_EN/Eng%20Advies%20WG%20Konijnen.pdfGoogle Scholar
Borenstein, M, Hedges, LV, Higgins, JPT and Rothstein, HR 2009 Introduction to Meta-Analysis. John Wiley and Sons Ltd: West Sussex, UK. https://doi.org/10.1002/9780470743386CrossRefGoogle Scholar
Buijs, S, Keeling, LJ and Tuyttens, FAM 2011 Behaviour and use of space in fattening rabbits as influenced by cage size and enrichment. Applied Animal Behaviour Science 134: 229–238. https://doi.org/10.1016/j.applanim.2011.06.008Google Scholar
Cani, PD, Neyrinck, AM, Maton, N and Delzenne, NM 2005 Oligofructose promotes satiety in rats fed a high-fat diet: involve-ment of glucagon-like peptide-1. Obesity Research 13: 1000–1007. https://doi.org/10.1038/oby.2005.117CrossRefGoogle Scholar
Cervera, C, Blas, E and Fernandez-Carmona, J 1997 Growth of rabbits under different environmental temperatures using high fat diets. World Rabbit Science 5: 71–75Google Scholar
Chiericato, GM, Boiti, C, Canali, C, Rizzi, C and Ravarotto, L 1995 Effects of heat stress and age on growth performance and endocrine status of male rabbit. World Rabbit Science 3: 125–131Google Scholar
Dixon, LM, Hardiman, JR and Cooper, JJ 2010 The effects of spatial restriction on the behaviour of rabbits (Oryctolagus cunicu-lus). Journal of Veterinary Behavior 5: 302–308. https://doi.org/10.1016/j.jveb.2010.07.002CrossRefGoogle Scholar
Dorey, NR, Udell, MAR and Wynne, CDL 2009 Breed differ-ences in dogs’ sensitivity to human points: A Meta-analysis. Behavioural Processes 81: 400–415. https://doi.org/10.1016/j.beproc.2009.03.011CrossRefGoogle Scholar
Douglas, SL, Szyszka, O, Stoddart, K, Edwards, SA and Kyriazakis, I 2014 A meta-analysis to identify animal and manage-ment factors influencing gestating sow efficiency. Journal of Animal Science 92: 1–11. https://doi.org/10.2527/jas.2014-7986CrossRefGoogle Scholar
Douglas, SL, Szyszka, O, Stoddart, K, Edwards, SA and Kyriazakis, I 2015 Animal and management factors influencing grower and finisher pig performance and efficiency in European systems: a meta-analysis. Animal 9: 1210–1220. https://doi.org/10.1017/S1751731115000269CrossRefGoogle ScholarPubMed
EFSA 2005 Scientific Opinion of the Scientific Panel on Animal Health and Welfare on ‘The impact of the current housing and husbandry systems on the health and welfare of farmed domestic rabbit’. The EFSA Journal 267: 1–31Google Scholar
Egger, M, Smith, GD and Phillips, AN 1997 Meta-analysis: principles and procedures. British Medical Journal 315: 1533–1537. https://doi.org/10.1136/bmj.315.7121.1533CrossRefGoogle ScholarPubMed
Estevez, I, Andersen, I-L and Nævdal, E 2007 Group size, den-sity and social dynamics in farm animals. Applied Animal Behaviour Science 103: 185–204. https://doi.org/10.1016/j.appla-nim.2006.05.025CrossRefGoogle Scholar
FAOSTAT 2013 Statistical Database of the Food and Agriculture Organization. http://faostat3.fao.orgGoogle Scholar
Fayez, I, Marai, M, Alnaimy, A and Habeeb, M 1994 Thermoregulation in rabbits. Cahiers Options Méditérranéennes 8: 33–41Google Scholar
Fraser, D, Phillips, PA, Thompson, BK and Tennessen, T 1991 Effect of straw on the behaviour of growing pigs. Applied Animal Behaviour Science 30: 307–318. https://doi.org/10.1016/0168-1591(91)90135-KGoogle Scholar
Fratkin, JL, Sinn, DL, Patall, EA and Gosling, SD 2013 Personality consistency in dogs: A meta-analysis. PLoS ONE 8: e54907. https://doi.org/10.1371/journal.pone.0054907CrossRefGoogle ScholarPubMed
Frias, AC and Sgarbieri, VC 1998 Guar gum effects on food intake, blood serum lipids and glucose levels of Wistar rats. Plant Foods for Human Nutrition 53: 15–28. https://doi.org/10.1023/A:1008052216477CrossRefGoogle ScholarPubMed
Fraser, D 2003 Assessing animal welfare at the farm and group level: the interplay of science and values. Animal Welfare 12: 433–443Google Scholar
Fulponi, L 2006 Private voluntary standards in the food system: The perspective of major food retailers in OECD countries. Food Policy 31: 1–13. https://doi.org/10.1016/j.foodpol.2005.06.006CrossRefGoogle Scholar
Gunn, D and Morton, DB 1995 Inventory of the behaviour of New Zealand White rabbits in laboratory cages. Applied Animal Behaviour Science 45: 277–292. https://doi.org/10.1016/0168-1591(95)00627-5CrossRefGoogle Scholar
Hamer, RM and Simpson, OM 2002 SAS® tools for meta-analysis. Proceedings of the Twenty-Seventh Annual SAS® Users Group International Conference. 14-17 April 2002, Orlando, Florida, USA. SAS Institute Inc: Cary, NC, USA. http://www2.sas.com/proceedings/sugi27/p250-27.pdfGoogle Scholar
Hansen, LT and Berthelsen, H 2000 The effect of environmen-tal enrichment on the behaviour of caged rabbits (Oryctolagus cuniculus). Applied Animal Behaviour Science 68: 163–178. https://doi.org/10.1016/S0168-1591(00)00093-9CrossRefGoogle Scholar
Hess, L 2004 Dermatologic diseases. In: Quesenberry, KE and Carpenter, JW (eds) Ferrets, Rabbits and Rodents: Clinical Medicine and Surgery, Second Edition pp 194–202. Saunders: St Louis, Missouri, USA. https://doi.org/10.1016/B0-72-169377-6/50021-6CrossRefGoogle Scholar
Huls, WL, Brooks, DL and Bean-Knudsen, D 1991 Response of adult New Zealand White rabbits to enrichment objects and paired housing. Laboratory Animal Science 41: 609–612Google ScholarPubMed
Lebas, F, Coudert, P, de Rochambeau, H and Thébault, RG 1997 Housing and equipment. The Rabbit – Husbandry, Health and Production (new revised version), FAO Animal Production and Health Series, no. 21 pp 125–147. Food and Agriculture Organization of the United Nations: Rome, ItalyGoogle Scholar
Lipsey, MW and Wilson, DB 2000 Practical Meta-Analysis. Sage Publications: Thousand Oaks, CA, USAGoogle Scholar
Maertens, L and De Groote, G 1985 L'influence de la densité d'occupation sur les résultats d'engraissement des lapins de chair. Revue de l’Agriculture 38: 463–471. [Title translation: The influence of occupancy density on fattening results of flesh rabbits]Google Scholar
Maertens, L, Tuyttens, F and Van Poucke, E 2004 Group housing of broiler rabbits: performances in enriched vs barren pens. Proceedings of the 8th World Rabbit Congress pp 1247–1250.7-10 September 2004, Puebla, Mexico. World Rabbit Science Association: Castanet-Tolosan, FranceGoogle Scholar
Mbanya, JN, Ndoping, BN, Fomunyam, RT, Noumbissi, A, Mbomi, ES, Fai, EN and Teguia, A 2004 The effect of stocking den-sity and feeder types on the performance of growing rabbits under conditions prevailing in Cameroon. World Rabbit Science 12: 259–268Google Scholar
McGlone, JJ and Newby, BE 1994 Space requirements for fin-ishing pigs in confinement: behavior and performance while group size and space vary. Applied Animal Behaviour Science 39: 331–338. https://doi.org/10.1016/0168-1591(94)90166-XCrossRefGoogle Scholar
Mirabito, L 2007 Logement et bien-être du lapin: plus de questions que de réponses? INRA Productions Animales 20: 59–64. [Title translation: Housing and welfare of rabbits: more questions than answers]CrossRefGoogle 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. CABI Publishing: Wallingford, Oxon, UK. https://doi.org/10.1079/9780851993591.0001CrossRefGoogle Scholar
Morton, DB, Jennings, M, Batchelor, GR, Bell, D, Birke, L, Davies, K, Eveleigh, JR, Gunn, D, Heath, M, Howard, B, Koder, P, Phillips, J, Poole, T, Sainsbury, AW, Sales, GD, Smith, DJA, Stauffacher, M and Turner, RJ 1993 Refinements in rabbit husbandry: Second report of the BVAAWF/FRAME/RSPCA/UFAW joint working group on refine-ment. Laboratory Animals 27: 301–329. https://doi.org/10.1258/002367793780745633CrossRefGoogle Scholar
Newberry, RC 1995 Environmental enrichment: Increasing the biological relevance of captive environments. Applied Animal Behaviour Science 44: 229–243. https://doi.org/10.1016/0168-1591(95)00616-ZCrossRefGoogle Scholar
Petherick, JC and Phillips, CJC 2009 Space allowances for con-fined livestock and their determination from allometric principles. Applied Animal Behaviour Science 117: 1–12. https://doi.org/10.1016/j.applanim.2008.09.008CrossRefGoogle Scholar
Petrie, A and Watson, P 2006 Statistics for Veterinary and Animal Science, Second Edition. Blackwell Publishing Ltd: Oxford, UKGoogle Scholar
Pettit-Riley, R, Estevez, I and Russeck-Cohen, R 2002 Effects of crowding and access to perches on aggressive behaviour in broilers. Applied Animal Behaviour Science 79: 11-25. https://doi.org/10.1016/S0168-1591(02)00116-8CrossRefGoogle Scholar
Podberscek, AL, Blackshaw, JK and Beattie, AW 1991 The behaviour of group penned and individually caged laboratory rab-bits. Applied Animal Behaviour Scienc e 28: 353-363. https://doi.org/10.1016/0168-1591(91)90167-VCrossRefGoogle Scholar
Sauvant, D, Schmidely, P, Daudin, JJ and St-Pierre, NR 2008 Meta-analyses of experimental data in animal nutrition. Animal 2:1203–1214. https://doi.org/10.1017/S1751731108002280CrossRefGoogle ScholarPubMed
Schmidely, P, Glasser, F, Doreau, M and Sauvant, D 2008 Digestion of fatty acids in ruminants: a meta-analysis of flows and variation factors 1. Total fatty acids. Animal 2: 677–690. https://doi.org/10.1017/S1751731108001717CrossRefGoogle ScholarPubMed
St-Pierre, NR 2001 Integrating quantitative findings from multi-ple studies using mixed model methodology. Journal of Dairy Science 84: 741–755. https://doi.org/10.3168/jds.S0022-0302(01)74530-4CrossRefGoogle Scholar
Statistical Analysis Systems Institute (SAS) 2011 SAS/STAT User's Guide, version 9.3. SAS Institute: Cary, NC, USAGoogle Scholar
Szendrő, Z and Dalle Zotte, A 2011 Effect of housing conditions on production and behaviour of growing meat rabbits: A review. Livestock Science 137: 296–303. https://doi.org/10.1016/j.livsci.2010.11.012CrossRefGoogle Scholar
Szendrő, Z and Luzi, F 2006 Group size and stocking density. In: Maertens, L and Coudert, P (eds) Recent Advances in Rabbit Sciences pp 121–126. Institute for Agricultural and Fisheries Research (ILVO): Melle, BelgiumGoogle Scholar
Thomas, L and Juanes, F 1996 The importance of statistical power analysis: an example from Animal Behaviour. Animal Behaviour 52: 856–859. https://doi.org/10.1006/anbe.1996.0232CrossRefGoogle Scholar
Trocino, A and Xicatto, G 2006 Animal welfare in reared rabbits: a review with emphasis on housing systems. World Rabbit Science 14: 77–93Google Scholar
Van de Weerd, HA and Day, JEL 2009 A review of environ-mental enrichment for pigs housed in intensive housing systems. Applied Animal Behaviour Science 116: 1–20. https://doi.org/10.1016/j.applanim.2008.08.001CrossRefGoogle Scholar
Verga, M, Luzi, F and Carenzi, C 2007 Effects of husbandry and management systems on physiology and behaviour of farmed and laboratory rabbits. Hormones and Behavior 52: 122–129. https://doi.org/10.1016/j.yhbeh.2007.03.024CrossRefGoogle ScholarPubMed