New concepts and objectives for protein-amino acid nutrition in rabbits: a review.

 R. Carabaño, M.J. Villamide, J. García, N. Nicodemus, A. Llorente, S. Chamorro, D. Menoyo, P. García Rebollar, A.I. García Ruiz, J.C. De Blas

Abstract

In the European context, the new legislation to avoid mineral contamination and the ban on antibiotics as growth promoters has led to the definition of new objectives in respect of nitrogen supply. The present study summarizes the state of nitrogen nutrition in rabbits and reviews the role of protein and amino acids in rabbit health and the new nitrogen value of protein sources based on true ileal digestibility (TID) for future recommendations. The main sources of nitrogen for microbial growth are ammonia, urea and protein (endogenous and dietary). The surplus of nitrogen flow to the caecum increases mortality rates during fattening by favouring the growth of potential pathogenic bacteria. Accordingly, feeding strategies to reduce ileal nitrogen flow have been reviewed. A large reduction of dietary protein level might have negative consequences on growth performances and mortality. In order to formulate balanced low protein diets, data on ileal and faecal amino acid digestibility of 14 raw materials is summarized. The use of this different unit for amino acid digestibility is also discussed.

Keywords

amino acids; ileal digestibility; microbial growth; intestinal health; nutrition; rabbits

Full Text:

PDF

References

Adams C.E. 1983. Reproductive performance of rabbits on a low protein diet. Lab. Anim., 17: 340-345.

Adamson I., Fisher H. 1971. The amino acid requirements of the growing rabbit: Qualitative needs. Nutr. Rep. Int., 4: 59-64.

Adamson I., Fisher H. 1973. Amino acid requirement of the growing rabbit: An estimate of quantitative needs. J. Nutr., 103: 1306-1310.

Blas E., Falcao L., Gidenne T., PinheiroV., García A.I., Carabaño R. 2000. Measurement of ileal digestibility in rabbits: An interlaboratory study to compare two markers and two frequencies of digesta collections. World Rabbit Sci., 8: 131-138.

Baylos M., Menoyo D., Chamorro S., Sainz A., Nicodemus N., de Blas C., Carabaño R. 2008. Effect of dietary level and source of glutamine on intestinal health in the postweaning period. In Proc.: 9th World Rabbit Congress, 10-13 June, 2008. Verona, Italy.

Campín J., Eiras P., Rebollar P.G., Carabaño R. 2003. Estudio del tejido linfoide asociado al intestino en gazapos en torno al destete. ITEA, 24: 660-662.

Cano J.L., Blas E., Soler M.D., Moya V.J., Guillén M.I. 2004. Immune response induced by feed in growing rabbits. In Proc.: 8th World Rabbit Congress, 7-10 September, 2004. Puebla, Mexico. 765-770.

Carabaño R., Merino J.M. 2003. Efecto de la cecotrofia sobre la composición química de la digesta y sobre la digestibilidad ileal. ITEA, 24: 657-659.

Carabaño R., de Blas C., García A.I. 2000. Recent advances in nitrogen nutrition in rabbits. World Rabbit Sci., 8: 14-28.

Carabaño R., García J., de Blas J.C. 2001. Effect of fibre source on ileal apparent digestibility of non-starch polysaccharides in rabbits. Anim. Sci., 72: 343-350.

Carabaño R., Badiola I., Chamorro S., García J., García-Ruiz A.I., García-Rebollar P., Gomez-Conde M.S., Gutiérrez I., Nicodemus N., Villamide M.J., de Blas J.C. 2008. New trends in rabbit feeding: Influence of nutrition on intestinal health. Spanish J. Agri. Res., 6: 15-25.

Chamorro S., Gomez Conde M.S., Perez De Rozas A.M., Badiola I., Carabaño R., de Blas J.C. 2007a. Effect on digestion and performance of dietary protein content and increased substitution of lucerne hay with soya-bean protein concentrate in starter diets for young rabbits. Animal, 1: 651-659.

Chamorro S., Carabaño R., Badiola I., García J., de Blas J.C. 2007b. Effet d’une supplémentation alimentaire en glutamine et en arginine sur la croissance, quelques paramètres de la flore iléale et caecale et la santé intestinale chez le lapereau, sevré précocement et atteint par le syndrome de l’EEL. In Proc.: 12èmes Journées Recherche Cunicole, November, Le Mans, France, 89-92.

Chamorro S., Carabaño R., Grant G., García J., de Blas J.C. 2007c. Efecto de la adición de glutamina y arginina sobre la mortalidad y barrera intestinal de gazapos. In Proc.: II Congreso Ibérico Cunicultura. June, Vila-Real, Portugal, 91-94.

Cheeke P.R. 1971. Arginine, lysine and methionine needs of the growing rabbits. Nutr. Rep. Int., 3: 123-128.

Colin M. 1974. Supplémentation en lysine d’un régime a base de tourteau de sésame chez le lapin. Effets sur les performances de croissance et le bilan azoté estimé par deux méthodes. Ann. Zootech., 23: 119-132.

Colin M. 1975a. Effets sur la croissance du lapin de la supplémentation en l-lysine et en dl-méthionine de régimes végétaux simplifiés. Ann. Zootech., 24: 465-474.

Colin M. 1975b. Effet de la teneur en arginine du régime sur la croissance et le bilan azoté chez le lapin: relation avec le taux de lysine. Ann. Zootech., 24: 629-638.

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.

Davidson J., Spreadbury D. 1975. Nutrition of the New Zealand White rabbit. Proc. Nutr. Soc., 34, 75-83.

De Blas J.C., Mateos G.G. 1998. Feed formulation. In: de Blas J.C., Wiseman J.(Eds). The Nutrition of the Rabbit. CABI Publishing. CAB International, Wallingford, Oxon, UK, 241-253.

De Blas J.C., Pérez E., Fraga M.J., Rodriguez J.M., Gálvez J.F. 1981. Effect of diet on feed intake and growth of rabbits from weaning to slaughter at different ages and weights. J. Anim. Sci., 52: 12251232.

De Blas J.C., Fraga MJ., Rodriguez J.M. 1985. Units for feed evaluation and requirements for commercially grown rabbits. J. Anim. Sci., 60: 1021-1028.

De Blas J.C., Taboada E., Nicodemus N., Campos R., Piquer J., Mendez J. 1998. Performance response of lactating and growing rabbits to dietary threonine content. Anim. Feed Sci. Technol., 70: 151-160.

Dojana N., Costache M., Dinischiotu A. 1998. The activity of some digestive enzymes in domestic rabbits before and after weaning. Anim. Sci.: 66, 501-507.

Emaldi O., Crociani F., Matteuzzi D. 1979. Bacteria in the caecal content, soft and hard faeces of rabbit. J. Appl. Bacteriol., 46: 169172.

Feugier A., Smit M.N., Fortun-Lamothe L., Gidenne T. 2006. Fibre and protein requirements of early-weaned rabbits and the interaction with weaning age: effects on digestive health and growth performance. Anim. Sci., 82: 493-500.

Forsythe S.J., Parker D.S. 1985. Ammonia nitrogen turnover in the rabbit caecum and exchange with plasma urea. Br. J. Nutr., 54, 285292.

Fraga M.J. 1998. Protein digestion. In: de Blas J.C., Wiseman J. (ed). The Nutrition of the Rabbit. CABI Publishing. CAB International, Wallingford, Oxon, UK, 39-54.

Fraga M.J., de Blas J.C., Pérez E., Rodríguez J.M., Pérez C.J., Gálvez J.F. 1983. Effect of diet on chemical composition of rabbits slaughtered at fixed body weights. J. Anim. Sci., 56: 1097-1104.

Fraga M.J., Pérez de Ayala P., Carabaño R., de Blas J.C. 1991. Effect of type of fiber on the rate of passage and on the contribution of soft feces to nutrient intake of finishing rabbits. J. Anim. Sci., 69: 1566-1574.

Gaman E., Fisher H. 1970. The essentiality of arginine, lisyne and methionine for growing rabbits. Rep. Int., 1: 57-64.

García A.I., de Blas J.C, Carabaño R. 2004. Effect of diet (casein-based or protein-free) and caecotrophy on ileal endogenous nitrogen and amino acid flow in rabbits. Anim. Sci., 79: 231-240.

García A.I., de Blas J.C, Carabaño R. 2005. Comparison of different methods for nitrogen and amino acid evaluation in rabbit diets. Anim. Sci., 80: 169-178.

García J., Pérez-Alba L., Alvarez C., Rocha R., Ramos M., de Blas J.C. 1995. Prediction of nutritive value of lucerne hay in diets for growing rabbits. Anim. Feed Sci. Technol., 54, 33-44.

García J., Nicodemus N., Carabaño R, de Blas J.C. 2002. Effect of inclusion of defatted grape seed meal in the diet on digestion and performance of growing rabbits. J. Anim. Sci., 80, 162-170.

García-Palomares J., Carabaño R., García-Rebollar P., de Blas J.C., Corujo A., García-Ruiz A.I. 2006a. Effects of a dietary protein reduction and enzyme supplementation on growth performance in the fattening period. World Rabbit Sci., 14: 231-236.

García-Palomares J., Carabaño R., García-Rebollar P., de Blas J.C., García A.I. 2006b. Effects of dietary protein reduction during weaning on the performance of does and suckling rabbits. World Rabbit Sci., 14: 23-26.

García-Ruiz A.I., García-Palomares J., García-Rebollar P., Chamorro S., Carabaño R., de Blas J.C. 2006. Effect of protein source and enzyme supplementation on ileal protein digestibility and fattening performance in rabbits. Span. J. Agric. Res., 4: 297-303.

Gidenne T. 1992. Effect of fibre level, particle size and adaptation period on digestibility and rate of passage as measured at the ileum and in the faeces in the adult rabbit. Br. J. Nutr., 67: 133-147.

Gidenne T., García J. 2006. Nutritional strategies improving the digestive health of the weaned rabbit. In: Maertens L., Coudert P. (ed) Recent advances in rabbit sciences. Ilvo, Merelbeke, Belgium, 211-227.

Gómez-Conde M.S., García J., Chamorro S., Eiras P., García Rebollar P.G., Perez De Rozas A., Badiola I., de Blas J.C., Carabaño R. 2007. Neutral detergent-soluble fiber improves gut barrier function in 25 day-old weaned rabbits. J. Anim. Sci., 85: 3313-3321.

Gutiérrez I., García P., Carabaño R., de Blas J.C. 2000. Effect of supplementation with animal plasma and antibiotics on jejunal morphology of early-weaned rabbits. World Rabbit Sci., 8: 263267.

Gutiérrez I., Espinosa A., García J., Carabaño R., de Blas J.C. 2003. Effect of source of protein on digestion and growth performance of early-weaned rabbits. Anim. Research, 52: 461-472.

Haffar A., Laval A. Guillou J.P. 1988. Entérotoxémie à Clostridium spiroforme chez des lapins adultes. Le Point Vétérinaire, 20: 99102.

Hill R.R.H. 1986. Digestion of mucin polysaccharides in vitro by bacteria isolated from the rabbit cecum. Curr. Microbiol., 14: 117120.

Hoover W.H., Heitmann R.N. 1975. Cecal nitrogen metabolism and amino acid absorption in the rabbit. J. Nutr., 105, 245-252.

INRA 1984. L’alimentation des animaux monogastriques: Porc, Lapin, Volailles. In: Blum J.C. (ed). Institute de la Recherche Agronomique, Paris, France.

INRA 2002. Tables de composition et de valeur nutritive des matières premières destinées aux animaux d’élevage. In: Sauvant D., Perez J.M., Tran G. (ed). INRA Editions, Paris, France.

Knight K.L., Crane M.A. 1994. Generating the antibody repertoire in rabbits. Adv. Immunol., 56: 179-218.

Lanning D., Sethupathi P., Rhee K.J., Zhai S.K., Knight K.L. 2000. Intestinal microflora and diversification of the rabbit antibody repertoire. J. Immunol., 165: 2012-2019.

Lebas F. 1988. Rabbits. Liv. Prod. Sci., 19: 289-298.

Lebas F., Laplace J.P. 1972. Mensurations viscérales chez le lapin. I. Croissance du foie, des reins et des divers segments intestinaux entre 3 et 11 semaines d’age. Ann Zootech., 21: 337-347.

Lebas F., Cousin M.C., Sardi G. 1973. Effet de la teneur en protéines de rations a base de soja ou de sésame sur la croissance du lapin. Ann. Zootech., 22: 83-92.

Le Floc’h N., Séve B. 2000. Le devenir des protéines et des acides aminés dans l’intestin du porc: de la digestion à l’apparition dans la veine porte. Prod. Anim., 13: 303-314.

Llorente A., García A.I., Nicodemus N., Villamide M.J., Carabaño R. 2005. Utilización de una nueva metodología para la determinación de la digestibilidad ileal aparente y real en la valoración nitrogenada de la harina de girasol en conejos. In Proc.: XI Jornadas sobre Producción Animal ITEA, May, Zaragoza, Spain, 26, 497-499.

Llorente A., García A.I., Nicodemus N., Villamide M.J., Carabaño R. 2006. Digestibilidad ileal aparente y verdadera de aminoácidos de harinas de girasol, productos de soja y guisante en conejos. In Proc.: XXXI Symposium de Cunicultura de Asescu, May, Lorca, Spain, 117-124.

Llorente A., Villamide M.J, García A.I., Carabaño R. 2007a. Digestibilidad de la proteína de los aminoácidos de cereales y sus subproductos en conejos. In Proc.: II Congreso Ibérico de Cunicultura, June, Vila-Real, Portugal, 87-90.

Llorente A., Villamide M.J, García A.I., Chamorro S., Carabaño R. 2007b. Prédiction de la digestibilité iléale azotée par méthodes in vitro. In Proc.: 12èmes Journées Recherche Cunicole, November, Le Mans, France, 93-96.

Maertens L., de Groote G. 1988. The effect of the dietary protein-energy ratio and lysine content on the breeding results of does. Archiv Fur Geflugelkunde, 52: 89-95.

Maertens L., Štruklec M. 2006. Technical note: preliminary results with a tannin extract on the performance and mortality of growing rabbits in an enteropathy-infected environment. World Rabbit Sci. 14: 189-192.

Maertens L, Luzi F, DeGroote G. 1997. Effect of dietary protein and amino acids on the performance, carcass composition and N-excretion of growing rabbits. Ann. Zootech., 46: 255-268.

Maertens L., Cavani C., Petracci M. 2005. Nitrogen and phosphorus excretion on commercial rabbit farms: calculations based on the input-output balance. World Rabbit Sci., 13: 3-16.

McWard G.W, Nicholson L.B., Poulton B.R. 1967. Arginine requirement of the young rabbit. J. Nutr., 92: 118-120.

Merino J.M., Carabaño R. 1992. Effect of type of fibre on ileal and fecal digestibilities. J. Appl. Rabbit Res., 15: 931-937.

Motta Ferreira W., Fraga M. J., Carabaño R. 1996. Inclusion of grape pomace, in substitution for alfalfa hay, in diets for growing rabbits. Anim. Sci., 63: 167-174.

Moughan P.J., Schultze W.E., Smith W.C. 1988. Amino acid requirements of growing meat rabbit. 1. The amino acid composition of rabbit whole-body tissue-a theoretical estimate of ideal amino acid balance. Anim. Prod., 55: 153-162.

NRC 1977. Nutrient requirements of rabbits. National Academy of Science. Washington DC, USA.

Parigi Bini R., Xiccato G., Cinetto M. 1990. Energy and protein retention and partition in pregnant and non-pregnant rabbit does during the first pregnancy. Cuni-Science, 6: 19-29.

Parigi Bini R., Xiccato G., Cinetto M. 1991. Utilizzazione e ripartizione dell’energia e della proteina digeribile in coniglie non gravide durante la prima lattazione. Zootec. Nutr. Anim., 17: 107-120.

Parigi Bini R., Xiccato G., Cinetto M., Dalle Zotte A. 1992. Energy and protein utilization and partition in rabbit does concurrently pregnant and lactating. Anim. Prod., 55: 153-162.

Partridge G.G. 1989. Nutrition of farmed rabbits. Proc Nutr. Soc., 48: 93-101.

Partridge G.G., Allan S.J. 1982. The effects of different intakes of crude protein on nitrogen utilization in the pregnant lactating rabbit. Anim. Prod., 35: 145-155.

Partridge G.G., Lobley G.E., Fordyce R.A. 1986. Energy and nitrogen metabolism of rabbits during pregnancy, lactation, and concurrent pregnancy and lactation. Br. J. Nutr., 56: 199-207.

Penney R.L., Folk Jr. G.E., Galask R.P., Petzold C.R. 1986. The microflora of the alimentary tract of rabbit in relation to pH, diet and cold. J. Appl. Rabbit Res., 9: 152-156.

Proto V. 1976. Fisiologia della nutrizione del coniglio con particolare riguardo alla ciecotrofia. Rivista di Coniglicoltura 13: 15-33.

Ramos M.A., Carabaño R., Boisen S. 1992. An in vitro method for estimating digestibility in rabbits. J. Appl. Rabbit Res., 15: 938-946.

Reeds P.J., Burrin D.G., Stoll B., Jahoor F. 2000. Intestinal glutamate metabolism. J. Nutr., 130: 978S-982S.

Rerat A. 1978. Digestion and absorption of carbohydrates and nitrogenous matters in the hindgut of the omnivorous nonruminant animal. J. Anim. Sci., 46: 1808-1837.

Sanchez W.K., Cheeke P.R., Patton N.M. 1985. Effect of dietary crude protein level on the reproductive performance and growth of New Zealand white rabbits. J. Anim Sci., 60: 1029-1039.

Sirotek K., Santos E., Benda V., Marounek M. 2003. Isolation, identification and characterization of rabbit caecal mucinolytic bacteria. Acta Vet. Brno., 72: 365-370.

Spreadbury D. 1978. A study of the protein and amino acid requirements of the growing New Zealand White rabbit with emphasis on lysine and the sulphur containing amino acids. Brit. J. Nutr., 39: 601-603.

Taboada E., Méndez J., Mateos G.G., de Blas J.C. 1994. The response of highly productive rabbits to dietary lysine content. Liv. Prod. Sci., 40: 329-337.

Taboada E., Méndez J., de Blas J.C. 1996. The response of highly productive rabbits to dietary sulphur amino acid content for reproduction and growth. Reprod. Nutr. Develop., 36: 191-203.

Thacker E.J., Brandt C.S. 1955. Coprophagy in the rabbit. J. Nutr., 55: 375-385.

Trocino A., Xiccato G., Sartori A., Queaque P.I. 2000. Feeding plans at different protein levels: effects on growth performance, meat quality and nitrogen excretion in rabbits. In Proc.: 7th World Rabbit Congress, 4-7 July, 2000, Valencia, Spain. Vol. C, 467-474.

Vente-Spreeuwenberg M.A.M., Verdonk J.M.A.J., Bakker G.C.M., Beynen A.C., Verstegen M.W.A. 2004. Effect of dietary protein source on feed intake and intestinal morphology in newly weaned piglets. Livest. Prod. Sci., 86, 169-177.

Villamide M.J., Maertens L., de Blas C., Pérez J.M. 1998. Feed evaluation. In: de Blas J.C., Wiseman J. (ed). The Nutrition of the Rabbit. CABI Publishing. CAB International, Wallingford, Oxon, UK, 89-101.

Xiccato G. 1996. Nutrition of lactating does. In Proc.: 6th World Rabbit Congress, 9-12 July, 1996. Toulouse. France. Vol. 1, 29-47.

Xiccato G., Parigi Bini R., Cinetto M., Dalle Zotte A. 1992. The influence of feeding and protein levels on energy and protein utilisation by rabbit does. J. Appl. Rabbit Res., 15: 965-972.

Xiccato G., Trocino A., De Boever J.L., Maertens L., Carabaño R., Pascual J.J., Pérez J.M., Gidenne T., Falcao-E-Cunha L. 2003. Prediction of chemical composition, nutritive value and ingredient composition of European compound feeds for rabbits by near infrared reflectance spectroscopy (NIRS). Anim. Feed Sci. Technol., 104: 153-168.

Xiccato G., Trocino A., Nicodemus N. 2006. Nutrition of the young and growing rabbit: a comparative approach with the doe. In: Maertens L., Coudert P. (ed) Recent advances in rabbit sciences. Ilvo, Merelbeke, Belgium, 239-246.

Yoshida T., Kandatsu M. 1960. Studies on cecum digestion. V. Nitrogen in the water-soluble fraction of cecal contents, hard feces, and soft feces of the rabbit. Jap. J. Zootech. Sci., 31: 181-187.

Yoshida T., Kandatsu M. 1964. Studies on cecum digestion. VI. Free amino acids in the cecal contents, hard feces, and soft feces of the rabbit. Jap. J. Zootech. Sci., 35: 64-69.

Yoshida T., Pleasants J.R., Reddy B.S., Wostmann B.S. 1968. Efficiency of digestion in germfree and conventional rabbits. Brit. J. Nutr., 22: 723-737.

Yoshida T., Pleasants J.R., Reddy B.S., Wostmann B.S. 1971. Amino acid composition of cecal contents and feces in germfree and conventional Rabbits. J. Nutr., 101: 1423-1430.

Yoshida T., Pleasants J.R., Reddy B.S., Wostmann B.S. 1972. The pH values and nitrogen fractionations of cecal contents and feces of germfree and conventional rabbits. Jap. J. Zootech. Sci., 43: 284289.

Abstract Views

3364
Metrics Loading ...

Metrics powered by PLOS ALM


 

Cited-By (articles included in Crossref)

This journal is a Crossref Cited-by Linking member. This list shows the references that citing the article automatically, if there are. For more information about the system please visit Crossref site

1. Effect of dietary supplementation of spirulina (Arthrospira platensis) and thyme (Thymus vulgaris) on apparent digestibility and productive performance of growing rabbits
Zsolt Gerencsér, Zsolt Szendro, Zsolt Matics, István Radnai, Melinda Kovács, István Nagy, Marco Cullere, Alessandro Dal Bosco, Antonella Dalle Zotte
World Rabbit Science  vol: 22  issue: 1  first page: 1  year: 2014  
doi: 10.4995/wrs.2014.1351



 

 Universitat Politècnica de València

 

Official journal of the World Rabbit Science Association (WRSA)

 

e-ISSN: 1989-8886     ISSN: 1257-5011   https://doi.org/10.4995/wrs