Effect of pasture availability and genotype on welfare, immune function, performance and meat characteristics of growing rabbits


  • Cecilia Mugnai
  • Alessandro Dal Bosco University of Perugia
  • Raffaella Cardinali
  • Pilar Garcia Rebollar
  • Livia Moscati
  • Cesare Castellini




rabbit, pasture, innate immunity, behaviour, carcass, meat quality


To analyse the effect of pasture availability and genotype on innate immunological status,morphological organisation of lymphoid follicles, behaviour, performance and carcass and meat characteristics, 80 growing rabbits (40 Leprino of Viterbo and 40 New Zealand White, NZW) were reared in bicellular standard cages (control) or in a wired pen, provided with an external grass pasture (pasture). Blood samples and behaviour observations (10 rabbits per group) were performed at different ages (weaning, 49 and 89 d). At the end of the trial, 10 rabbits per group were slaughtered to study meat quality/composition and vermiform appendix structure. Leprino rabbits showed higher serum lysozyme values than NZW for all ages and rearing systems. Leprino rabbits showed the highest values in caged animals (29.6 and 32.4 mg/mL, respectively at 49 and 89 d of age), while NZW animals did so in the pen (2.2 and 0.00 g/mL, respectively at 49 and 89 d of age). Haemolytic Complement Assay increased with age in Leprino (43.7 vs. 48.6 and 51.2 μg/mL, respectively for cage and pen), but decreased in NZW (68.6 vs. 25.8 and 41.1 μg/mL, respectively for cage and pen). Plasma TBARs was always higher in Leprino rabbits (16.0 vs. 7.0 μmol malondialdehyde/L at 29 d of age; 17.9 vs. 8.0 μmol malondialdehyde/L at 49 d of age; 20.0 vs. 11.4 μmol malondialdehyde/L at 89 d of age), whereas plasma tocopherol showed an inverse trend (32.9 vs. 46.6 mg/L at 29 d of age; 32.5 vs. 44.4 mg/L at 49 d of age; 31.2 vs. 42.4 mg/L at 89 d of age). Mortality rate of Leprino rabbits was highest in the cage system, while mortality was highest in NZW housed in the pen. Productive performance, carcass traits and fatty acid composition of meat were strongly affected by genotype and rearing system. Regarding genotype effect, Leprino showed lower daily gains (31.9 and 29.6 vs. 44.2 and 40.0 g, respectively for cage and pen system), live (2563 and 2418 vs. 2902 and 2650, respectively for cage and pen system) and carcass weights (1561 and 1465 vs. 1763 and 1580, respectively for cage and pen system). Pasture availability improved the meat nutritional quality and, in particular, the n-6/n-3 ratio was optimal and the total tocopherol content was suitable to assure a good oxidative stability.


Download data is not yet available.

Author Biographies

Cecilia Mugnai

Alessandro Dal Bosco, University of Perugia

Raffaella Cardinali

Pilar Garcia Rebollar

Livia Moscati

Cesare Castellini


Amadori M., Archetti I.L., Frassinelli M., Bagni M., Olzi E., Caronna G., Lanterni M. 1997. An immunological approach to the evaluation of welfare in Holstein Frisian cattle. Annali Istituto Zooprofilattico Sperimentale della Lombardia e dell’Emilia, Brescia.

Andersson K., Andersson I., Essen-Gustavsson B. 1990. Fakta Husdjur, 12. Swedish University of Agricultural Sciences.

Barta V., Barta O. 1993. Testing of Hemolitic Complement and its components. Vet. Clin. Imm. Lab., Bar-Lab, Blacksburg, USA.

Berthelsen H., Hansen L.T., 1999. The effect of hay on the behaviour of caged rabbits (Oryctolagus cuniculus). Anim. Welfare, 8: 149-157.

Berthelsen H., Hansen L.T. 2000. The effect of environmental enrichment on the behaviour of caged rabbits (Oryctolagus cuniculus). Appl. Anim. Behav. Sci., 68: 163-178. doi:10.1016/S0168-1591(00)00093-9

Blasco A., Ouhayoun J. 1996. Harmonization of criteria and terminology in rabbit meat research. Revised proposal. World Rabbit Sci., 4: 93-99. doi:10.4995/wrs.1996.278

Blasco A. 1996. Genetics of litter size and does fertility in the rabbit. In Proc.: 6th World Rabbit Congress. July 9-12, 1996 Toulouse, France, Vol. 2: 219-228.

Carroll S.F., Martinez R.J. 1979. Role of rabbit lysozyme in in vitro serum and plasma serum bactericidal reactions against Bacillus subtilis infection. Infect. Immun., 25: 810-819.

Castellini C., Cardinali R., Rebollar P.G., Dal Bosco A., Jimeno V., Cossu M.E. 2007. Feeding fresh chicory (Chicoria intybus) to young rabbits: Performance, development of astrointestinal tract and immune functions of appendix and Peyer's patch. Anim Feed Sci Tech., 134: 56-65. doi:10.1016/j.anifeedsci.2006.05.007

Cavani C., Bianchi M., Lazzaroni C., Luzi F., Minelli G., Petracci M., 2000. Influence of type of rearing, slaughter age and sex on fattening rabbit: II. Meat quality. World Rabbit Sci., 8: 567- 572.

Cheeke PR. 1987. Digestive physiology. In: Rabbit feeding and nutrition. Orlando: Academic Press, 15-33. doi:10.1016/B978-0-08-057078-5.50008-X

Dal Bosco A., Castellini C., Bernardini M. 2000. Productive performance and carcass and meat characteristics of cage-or open-raised rabbits. World Rabbit Sci., 8: 579-583.

Dal Bosco A., Castellini C., Mugnai C. 2002. Rearing rabbits on a wire net floor or straw litter: behaviour, growth and meat qualitative traits. Livest. Prod. Sci., 75: 149-156. doi:10.1016/S0301-6226(01)00307-4

Dal Bosco A., Castellini C., Bianchi L., Mugnai C. 2004. Effect of dietary α-linolenic acid and vitamin E on the fatty acid composition, storage stability and sensory traits of rabbit meat. Meat Sci., 66: 407-413. doi:10.1016/S0309-1740(03)00127-X

Dalle Zotte A., Ouhayoun J. 1998. Effect of genetic origin, diet and weaning weight on carcass composition, muscle physicochemical and histochemical traits in the rabbit. Meat Sci. 50: 471-478. doi:10.1016/S0309-1740(98)00060-6

Dalle Zotte A., Ragno E. 2005. Influence of the paternal genetic origin and season on the live performances and the carcass yield of rabbits reared in the organic production system. Ital. J. Anim. Sci., 4: 544-546.

Dantzer R., Mormède P. 1981. Can physiological criteria be used to assess welfare in pigs? In: W. Sybesma (Ed.) The Welfare of Pigs. pp 53-73. Martinus Nijhoff, The Hague. doi:10.1007/978-94-011-9574-4_5

Daszkiewicz T., Gugołek A., Janiszewski P., Kubiak D., Czoik M. 2012. The effect of intensive and extensive production systems on carcass quality in New Zealand White rabbits. World Rabbit Sci., 20: 25-33. doi:10.4995/wrs.2012.945

Dasso J.F., Obiakor H., Bach H., Anderson A.O., Mage R.G. 2000. A morphological and immunohistological study of the human and rabbit appendix for comparison with the avian bursa. Dev. Comp. Immunol., 24: 797-814. doi:10.1016/S0145-305X(00)00033-1

Disciplinare per l’allevamento biologico del coniglio 2001. Associazione Italiana per l’Agricoltura Biologica.

Enser M., Hallett K.G., Hewett B., Fursey G.A.J., Wood J.D., Harrington G. 1988. Fatty acid content and composition of UK beef and lamb muscle in relation to production system and implications for human nutrition. Meat Sci., 49: 329-341. doi:10.1016/S0309-1740(97)00144-7

Ferrian S., Guerrero I., Blas E., García-Diego F.J., Viana D., Pascual J.J., Corpa J.M., 2012. How selection for reproduction or foundation for longevity could have affected blood lymphocyte populations of rabbit does under conventional and heat stress conditions. Vet. Immunol. Immunop., 150: 53-60. doi:10.1016/j.vetimm.2012.08.007

Folch J., Lees M., Sloane-Stanley H. 1957. A simple method for the isolation and purification of total lipids from animal tissue. J. Biol. Chem., 226: 497-509.

Fortun-Lamothe L., Boullier S. 2004. Interactions between gut microflora and digestive mucosal immunity, and strategies to improve digestive health in young rabbits. In Proc.: 8th World Rabbit Congress, 7-10 Sept. 2004, Puebla (Mexico), 1035- 1067.

Forrester-Anderson I.T., Mcnitt J., Way R., Way M. 2006. Fatty acid content of pasture-reared fryer rabbit meat. J. Food Comp. Anal., 19: 715-719. doi:10.1016/j.jfca.2006.02.011

Gondret F., Combes S., Lefaucheur L., Lebret B. 2005. Effects of exercise during growth and alternative rearing systems on muscle fibers and collagen properties. Repr. Nutr. Dev., 45: 69-86. doi:10.1051/rnd:2005003

Grandin T., Deesing M.J. 1998. Genetics and the behaviour of domestic animals. T. Grandin (Editor), Academic Press, San Diego, California, USA, 319-341

Gunn-Dore D., Morton D.B. 1995. Inventory of the behaviour of New Zealand White rabbits in laboratory cages. Appl. Anim. Behav. Sci., 45: 277-292. doi:10.1016/0168-1591(95)00627-5

Gurr M.I. 1984. The chemistry and biochemistry of plant fats and their nutritional importance. In: Fats in Animal Nutrition. J. Wiseman, ed. Butterworths, London, UK., 3-22. doi:10.1016/B978-0-408-10864-5.50007-3

Halliwell B., Chirico S. 1993. Lipid peroxidation: its mechanism, measurement and significance. Am. J. Clin. Nutr., 57: 715S-725S.

Hansen L.T., Berthelsen H. 2000. The effect of environmental enrichment on the behaviour of caged rabbits (Oryctolagus cuniculus). Appl. Anim. Behav. Sci., 68: 163-178. doi:10.1016/S0168-1591(00)00093-9

Hernández P., Gondret F. 2006. Rabbit Meat Quality. In: Maertens L., Coudert P. (Eds.). Recent Advances in Rabbit Sciences. ILVO, Merelbeke, Belgium, 269-290.

Hewavitharana A.K., Lanari M.C., Becu C. 2004. Simultaneous determination of vitamin E homologs in chicken meat by liquid chromatography with fluorescence detection. J. Chromat., A 1025: 313-317.

Huls W.L., Brooks D.L., Bean-Knudsen D. 1991. Response of adult New Zealand White rabbits to enrichment objects and paired housing. Lab. Anim. Sci., 41: 609-612.

ISSFAL 2004. International society for the study of fatty acids and lipids. Report of the Sub-Committee on “Recommendations for intake of polyunsaturated fatty acids in healthy adults”. Available from: http://www.issfal.org.uk/ Accessed March 2013.

Korkeala H., Mäki-Petais O.T., Alanko T., Sorvettula O. 1986. Determination of pH in meat. Meat Sci., 18: 121-125. doi:10.1016/0309-1740(86)90088-4

Laemmli U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227: 680- 685. doi:10.1038/227680a0

Lambertini L., Vignola G., Zaghini G. 2001. Alternative pen housing system for fattening rabbits: effects of group density and litter. World Rabbit Sci., 9: 141-147. doi:10.4995/wrs.2001.457

Lukefahr S., Hohenboken W.D., Cheeke P.R., Patton N.M. 1983. Appraisal of nine genetic groups of rabbits for carcass and lean yield traits. J. Anim. Sci., 57:899-907.

Marchetti B., Morale M.C., Testa N., Tirolo C., Canaglia S., Amor S., Dijkstra C.D., Barden N. 2001. Stress, the immune system and vulnerability to degenerative disorders of the central nervous system in transgenic mice expressing glucocorticoid receptor antisense RNA. Brain Res. Rev., 37: 259-272. doi:10.1016/S0165-0173(01)00130-8

Martin P., Bateson P. 1986. Measuring Behaviour: an introductory guide. Cambridge University Press, Cambridge, UK.

Matthews L.R., 1996. Behaviour and Welfare of Extensively Farmed Animals. Animal welfare and sustainability of production under extensive conditions: a non-EU perspective. Appl. Anim. Behav. Sci., 49: 41-46. doi:10.1016/0168-1591(95)00666-4

McNitt J., Way R., Way M., Forrester-Anderson I. 2003. Growth of fryers reared and (or) finished using controlled grazing in movable pens. World Rabbit Sci., 11: 189-198. doi:10.4995/wrs.2003.507

Metzger Sz., Kustos K., Szendrő Zs., Szabó A., Eiben C.S., Nagy I. 2003. The effect of housing system on carcass traits and meat quality of rabbit. World Rabbit Sci., 11: 1-11. doi:10.4995/wrs.2003.492

Ministere de l'Alimentation, de l'Agriculture et de la Peche. 2010. Available at: http://agriculture.gouv.fr/IMG/pdf/ccf_ janvier_2010-homologue.pdf Accessed February 2014.

Miranda A., De la Cruz F., Zamudio S.R. 2006. Immobility response elicited by clamping the neck induces antinociception in a “tonic pain” test in mice. Life Sci. 79: 1108-1113. doi:10.1016/j.lfs.2006.03.018

Monahan F.J. 2000. Oxidation of lipids in muscle foods: Fundamental and applied concerns. E Decker, C Faustman, C.J Lopez-Bote (Eds.), Antioxidants in muscle foods, Wiley, New York (2000), 3-23.

Moscati L., Mugnai C., Dal Bosco A., Castellini C., Mourvaki E., Cardinali R. 2008. Rabbit welfare: preliminary study for a multifunctional evaluation. World Rabbit Sci., 4: 213-220. doi:10.4995/wrs.2008.616

Mugnai C., Dal Bosco A., Castellini C. 2009. Effect of rearing system and season on the performance and egg characteristics of Ancona laying hens. Ital. J. Anim. Sci., 8: 175-188.

Osserman E.F., Lawlor D.P. 1966. Serum and urinary lysozyme (muramidase) in monocytic and monomyelocitic leukemia. J. Exp. Med., 124: 921-952. doi:10.1084/jem.124.5.921

Ouhayoun J. 1998. Influence of the diet on rabbit meat quality. In: De Blas, C, Wisemann, J. (Eds), The Nutrition of the Rabbit. CABI Publishing, Oxon, UK.

Paci G., Schiavone A., Lisi E., Peiretti P.G., Bagliacca M., Mussa P.P. 2005. Meat quality characteristics in local population of rabbit reared with organic system. Ital. J. Anim. Sci., 4: 562-568.

Pinheiro V., Silva S.R., Silva J.A., Outor-Monteiro D., Mourão J.L. 2008. Growth and carcass characteristics of rabbits housed in open-air or standard systems. In Proc 9th World Rabbit Congress, 10-13 June, 2008, Verona, Italy, 1421-1424.

Pla M. 2008. A comparison of the carcass traits and meat quality of conventionally and organically produced rabbits. Livest. Sci., 115: 1-12. doi:10.1016/j.livsci.2007.06.001

Pla M., Hernández P., Ariño B., Ramírez J.A., Díaz I. 2007. Prediction of fatty acid content in rabbit meat and discrimination between conventional and organic production systems by NIRS methodology. Food Chem., 100: 165-170. doi:10.1016/j.foodchem.2005.09.029

Prieur D.J., Olson H.M., Young, D.M. 1974. Lysozyme Deficiency-An Inherited Disorder of Rabbits. Am. J. Pathol., 77: 283-298.

Prickett P.S., Miller N.J., McDonald F.G. 1933. The lysozyme content of milk from various species and its relation to the fecal flora of their nurslings ft. Bact., 25: 61-62.

Rainard P. 2003. The complement in milk and defense of the bovine mammary gland against infections. Vet. Res., 34: 647- 670. doi:10.1051/vetres:2003025

Rauw W.M., Kanis E., Noordhuizen-Stassen E.N., Grommers, F.J. 1998. Undesirable side effect of selection for high production efficiency in farm animals: a review. Livest Prod Sci., 56: 15-33. doi:10.1016/S0301-6226(98)00147-X

Ramírez J.A., Díaz I., Pla M., Gil M., Blasco A., Oliver M.A. 2005. Fatty acid composition of leg meat and perirenal fat of rabbits selected by growth rate. Food Chem., 90: 251-256. doi:10.1016/j.foodchem.2004.04.001

Reid K.B. 1995. The complement system. A major effector mechanism in humoral immunity. The Immunologist, 3: 206- 211.

Schütz K.E., Jensen P. 2001. Effects of resource allocation on behavioural strategies: a comparison of red junglefowl (Gallus gallus) and two domesticated breeds. Poult. Ethol., 107: 753 -759. doi:10.1046/j.1439-0310.2001.00703.x

StataCorp 2005. Stata Statistical Software: Release 9. College Station, TX: StataCorp.LP.

Tarladgis B.G., Watts B.M., Younathan M.T., Dugan L.Jr. 1960. A distillation method for the quantitative determination of malonaldehyde in rancid foods. J. Am. Oil Chem. Soc., 37:44- 48. doi:10.1007/BF02630824

Weinstein P.D., Mage R.G., Anderson A.O. 1994. The appendix functions as a mammalian bursal equivalent in the developing rabbit. Adv. Exp. Med. Biol., 355: 249-254. doi:10.1007/978-1-4615-2492-2_42

Zgur S., Kermauner A. 2005. Carcass traits of four rabbit genotypes. Ital. J. Anim. Sci., 4: 172-174.