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Understanding the equine cecum-colon ecosystem: current knowledge and future perspectives

Published online by Cambridge University Press:  23 August 2010

A. S. Santos*
Affiliation:
Animal Production Group, Animal and Veterinary Research Center, University of Trás-os-Montes and Alto Douro, PO Box 1013, 5001-801, Vila Real, Portugal
M. A. M. Rodrigues
Affiliation:
Animal Production Group, Animal and Veterinary Research Center, University of Trás-os-Montes and Alto Douro, PO Box 1013, 5001-801, Vila Real, Portugal
R. J. B. Bessa
Affiliation:
Interdisciplinary Centre of Research in Animal Health, Faculdade de Medicina Veterinária, Technical University of Lisbon, Lisboa, Portugal
L. M. Ferreira
Affiliation:
Animal Production Group, Animal and Veterinary Research Center, University of Trás-os-Montes and Alto Douro, PO Box 1013, 5001-801, Vila Real, Portugal
W. Martin-Rosset
Affiliation:
Institut National de la Recherche Agronomique, Center of Research of Clermont-Ferrand, Theix, 63122 Saint-Genés-Champanelle, France
*
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Abstract

Having evolved as a grazing animal, a horse’s digestive physiology is characterized by rapid gastric transit, a rapid but intense enzymatic digestion along the small intestine, and a long and intense microbial fermentation in the large intestine. The process of understanding and describing feed degradation mechanisms in the equine digestive system in general, and in the hindgut ecosystem in particular, is essential. Regardless of its importance for the nutritional status of the host, the significance of the cecum-colon ecosystem has not yet been fully understood, and few reports have focused deeply on the contribution of the hindgut microbial population to the nitrogen and energy requirements of the horse. Compared to ruminal activity, very little is known about hindgut ecosystem activity in the horse. Information concerning the metabolism of this microbial population and its requirements is lacking. The use of internal bacterial markers for quantifying microbial outflow in ruminants is widely reported. These techniques can be applied to cecum-colon microbial quantification, contributing to a better characterization of this ecosystem. It is likely wrong to believe that the optimization strategy in the hindgut is similar to what happens in the rumen – that is, to maximize microbial growth and, therefore, fermentation. If we consider the type of substrate that, in normal conditions, arrives in the hindgut, we can expect it to be nitrogen limiting, providing limited nitrogen-based substrates for microbial fermentation. In this review paper, we intend to gather existing information on the equine ecosystem and to provide future perspectives of research.

Type
Review
Copyright
Copyright © The Animal Consortium 2010

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References

Baruc, CI, Dawson, KA, Baker, IP 1983. The characterization of nitrogen metabolism of equine caecal bacteria. In Proceedings of the 8th Equine Nutrition and Physiology Symposium, 28–30 April 1983, Lexington, Kentucky, pp. 151–156.Google Scholar
Bennett, DK 1980. Stripes do not a zebra make. Part 1. A cladistic analysis of Equus. Systematic Zoology 29, 272287.CrossRefGoogle Scholar
Bessa, RJB, Maia, MRG, Jerónimo, E, Belo, AT, Cabrita, ARJ, Dewhurst, RJ, Fonseca, AJM 2009. Using microbial fatty acids to improve understanding of the contribution of solid associated bacteria to microbial mass in the rumen. Animal Feed Science and Technology 150, 197206.CrossRefGoogle Scholar
Bochröder, B, Schubert, R, Bodecker, D 1994. Studies on the transport in vitro of lysine, histidine, arginine and ammonia across the mucosa of the equine colon. Equine Veterinary Journal 26, 131133.CrossRefGoogle ScholarPubMed
Coenen, M, Mosseler, A, Vervuert, I 2006. Fermentative gases in breath indicate that inulin and starch start to be degraded by microbial fermentation in the stomach and small intestine of the horse in contrast to pectin and cellulose. Journal of Nutrition 136, 2108S2110S.CrossRefGoogle ScholarPubMed
Daly, K, Shirazi-Beechey, SP 2003. Design and evaluation of group-specific oligonucleotide probes for quantitative analysis of intestinal ecosystems: their application to assessment of equine colonic microflora. FEMS Microbiology Ecology 44, 243252.CrossRefGoogle ScholarPubMed
Daly, K, Stewart, CS, Flint, HJ, Shirazi-Beechey, SP 2001. Bacterial diversity within the equine large intestine as revealed by molecular analysis of cloned 16S rRNA genes. FEMS Microbiology Ecology 38, 141151.CrossRefGoogle Scholar
de Fombelle, A, Julliand, V, Drogoul, C, Jacotot, E 2001. Feeding and microbial disorders in horses: 1-effects of an abrupt incorporation of two levels of barley in a hay diet on microbial profile and activities. Journal of Equine Veterinary Science 21, 439445.Google Scholar
de Fombelle, A, Varloud, M, Goachet, AG, Jacotot, E, Philippeau, C, Drogoul, C, Julliand, V 2003. Characterization of the microbial and biochemical profile of the different segments of the digestive tract in horses given two distinct diets. Animal Science 77, 293304.CrossRefGoogle Scholar
Demeyer, DI 1991. Quantitative aspects of microbial metabolismin the rumen and hindgut. In Rumen microbial metabolism and ruminant digestion (ed. JP Jouany), pp. 217237. INRA Publications, Paris.Google Scholar
Diedrich, M, Henschel, KP 1990. The natural occurrence of unusual fatty-acids. 1. Odd numbered fatty-acids. Nahrung 34, 935943.CrossRefGoogle Scholar
Drogoul, C, Poncet, C, Tisserand, JL 2000. Feeding ground and pelleted hay rather than chopped hay to ponies: 1. Consequences for in vivo digestibility and rate of passage of digesta. Animal Feed Science and Technology 87, 117130.CrossRefGoogle Scholar
Drogoul, C, de Fombelle, A, Julliand, V 2001. Feeding and Microbial disorders in horses: 2. Effect of three hay:grain ratios on digesta passage rate and digestibility in ponies. Journal of Equine Veterinary Science 21, 487491.CrossRefGoogle Scholar
Edwards, JE, Huws, SA, Kim, EJ, Lee, MRF, Kingston-Smith, AH, Scollan, ND 2008. Advances in microbial ecosystem concepts and their consequences for ruminant agriculture. Animal 2, 653660.Google Scholar
Glade, MJ 1984. The influence of dietary fiber digestibility on the nitrogen requirements of mature horses. Journal of Animal Science 58, 638646.Google Scholar
Goodson, J, Tyznik, WJ, Cline, JH, Dehority, BA 1988. Effects of an abrupt diet change from hay to concentrate on microbial numbers and physical environment in the cecum of the pony. Applied and Environmental Microbiology 54, 19461950.CrossRefGoogle ScholarPubMed
Hespell, RB, Bryant, MP 1979. Efficiency of rumen microbial growth: some theoretical and experimental factors on YATP. Journal of Animal Science 49, 16401659.CrossRefGoogle ScholarPubMed
Hill, J 2007. Impacts of nutritional technology on feeds offered to horses: a review of effects of processing on voluntary intake, digesta characteristics and feed utilisation. Animal Feed Science and Technology 138, 92117.CrossRefGoogle Scholar
Hintz, HF, Schryver, HF 1972. Nitrogen utilization in ponies. Journal of Animal Science 34, 592595.CrossRefGoogle ScholarPubMed
Hintz, HF, Cymbaluk, NF 1994. Nutrition of the horse. Annual Review of Nutrition 14, 243267.CrossRefGoogle ScholarPubMed
Hintz, HF, Hogue, DE, Walker, EF Jr, Lowe, JE, Schryver, HF 1971. Apparent digestion in various segments of the digestive tract of ponies fed diets with varying roughage-grain ratios. Journal of Animal Science 32, 245248.CrossRefGoogle ScholarPubMed
Houpt, TR, Houpt, KA 1971. Nitrogen conservation by ponies fed a low-protein ration. American Journal of Veterinary Research 32, 579588.Google Scholar
Hyslop, JJ 2006. In situ and mobile bag methodology to measure the degradation profile of processed feeds in different segments of the equine digestive tract. Livestock Science 100, 1832.Google Scholar
Institut National de la Recherche Agronomique (INRA) 1990. Alimentation des chevaux (ed. W Martin-Rosset). INRA Publications, Paris, France.Google Scholar
Janis, C 1976. The evolutionary strategy of the equidae and the origins of rumen and cecal digestion. Evolution 30, 757774.CrossRefGoogle ScholarPubMed
Julliand, V 1998. Ecologie microbienne du système digestif des équidés: nouvelles approches: conséquenses pratiques. Compte rendu de la 24ème Journée de la Recherche Equine, Haras Nationaux edition, 4 mars 1998, Paris, pp. 105–113.Google Scholar
Julliand, V, Tisserand, JL 1992. Alimentation du poney : importante de la qualite de l’azote sur la flore microbienne caecale. Compte rendu de la 18éme Journée de la Recherche Equine, Haras Nationaux ed., 4 mars 1992, Paris, pp. 2–11.Google Scholar
Julliand, V, Prevost, H, Tisserand, JL 1993. Preliminary study of the cecal bacterial flora in the pony: quantification and diet effect. Annales de Zootechnie 42, 183.Google Scholar
Julliand, V, de Vaux, A, Millet, L, Fonty, G 1999. Identification of Ruminococcus flavefaciens as the predominant cellulolytic bacterial species of the equine cecum. Applied and Environmental Microbiology 65, 37383741.Google Scholar
Julliand, V, de Fombelle, A, Drogoul, C, Jacotot, E 2001. Feeding and microbial disorders in horses: part 3 – effects of three hay: grain ratios on microbial profile and activities. Journal of Equine Veterinary Science 21, 543546.CrossRefGoogle Scholar
Kaneda, T 1991. Iso and anteiso-fatty acids in bacteria: biosynthesis, function, and taxonomic significance. Microbiology and Molecular Biology Reviews 55, 288302.Google ScholarPubMed
Kern, DL, Slyter, LL, Weaver, JM, Leffel, EC, Samuelsons, G 1973. Pony cecum vs. steer rumen: the effect of oats and hay on the microbial ecosystem. Journal of Animal Science 37, 463469.Google Scholar
Kern, DL, Slyter, LL, Leffel, EC, Weaver, JM, Oltjen, RR 1974. Ponies vs. steers: microbial and chemical characteristics of intestinal ingesta. Journal of Animal Science 38, 559564.CrossRefGoogle ScholarPubMed
Lin, C, Stahl, DA 1995. Taxon-specific probes for the cellulolytic genus Fibrobacter reveal abundant and novel equine-associated populations. Applied and Environmental Microbiology 61, 13481351.Google Scholar
Macheboeuf, D, Maranji, M, Poncet, C, Martin-Rosset, W 1995. Study of nitrogen digestion from different hays by the mobile nylon bag technique in horses. Annales de Zootechnie 44, 219.CrossRefGoogle Scholar
Mackie, RI, Wilkins, CA 1988. Enumeration of anaerobic bacterial microflora of the equine gastrointestinal tract. Applied and Environmental Microbiology 54, 21552160.Google Scholar
Maczulak, AE, Dawson, KA, Baker, JP 1985. Nitrogen utilization in bacterial isolates from the equine cecum. Applied and Environmental Microbiology 50, 14391443.CrossRefGoogle ScholarPubMed
Martin-Rosset, W 2008. Energy requirements and allowances of exercising horses. In Nutrition of exercising horses (ed. M Saastamoinen and W Martin-Rosset), EAAP no 125, pp. 103138. Wageningen Academic Publishers, Wageningen, The Netherlands.Google Scholar
Martin-Rosset, W, Tisserand, JL 2004. Evaluation and expression of protein allowances and protein value of feeds in the MADC system for the performance horse. In Nutrition of the performance horse: which system in Europe for evaluating the nutritional requirements? (ed. V Julliand and W Martin-Rosset), EAAP no 111, pp. 103140. Wageningen Academic Publishers, Wageningen, The Netherlands.Google Scholar
Martin-Rosset, W, Doreau, M, Thivend, P 1987. Digestion de régimes à base de foin ou d’ensilage de maïs chez le cheval en croissance. Reproduction Nutrition Development 27, 291292.Google Scholar
Martin-Rosset, W, Andrieu, J, Vermorel, M, Dulphy, JP 1984. Valeur nutritive des aliments pour le cheval. In Le Cheval (ed. R Jarrige and W Martin-Rosset), pp. 209238. INRA Publications, Paris.Google Scholar
Martin-Rosset, W, Doreau, M, Boulot, S, Miraglia, N 1990. Influence of level of feeding and physiological state on diet digestibility in light and heavy breed horses. Livestock Production Science 25, 257264.Google Scholar
Martin-Rosset, W, Vermorel, M, Doreau, M, Tisserand, JL, Andrieu, J 1994. The French horse feed evaluation systems and recommended allowances for energy and protein. Livestock Production Science 40, 3756.Google Scholar
McMeniman, NP, Elliot, R, Groenendyk, S, Dowsett, KF 1987. Synthesis and absorption of cysteine from the hindgut of the horse. Equine Veterinary Journal 19, 192194.Google Scholar
Medina, B, Girard, ID, Jacotot, E, Julliand, V 2002. Effect of a preparation of Saccharomyces cerevisiae on microbial profiles and fermentation patterns in the large intestine of horses fed a high fiber or a high starch diet. Journal of Animal Science 80, 26002609.Google Scholar
Merry, RJ, McAllan, AB 1983. A comparison of the chemical composition of mixed bacteria harvested from the liquid and solid fractions of rumen digesta. British Journal of Nutrition 50, 701709.Google Scholar
Meyer, H 1983. Intestinal protein and N metabolism in the horse. In Proceedings of the Horse Nutrition Symposium, 5–7 October 1983, Uppsala, Sweden, pp. 113–137.Google Scholar
Michalet-Doreau, B, Fernandeza, I, Peyrona, C, Millet, L, Fonty, G 2001. Fibrolytic activities and cellulolytic bacterial community structure in the solid and liquid phases of rumen contents. Reproduction Nutrition Development 41, 187194.CrossRefGoogle ScholarPubMed
Micol, D, Martin-Rosset, W 1995. Feeding systems for horses on high forage diets in the temperate zones. In Proceedings of the 4th International Symposium on the Nutrition of Herbivores (ed. M Journet, E Grenet, M-H Farce, M Thériez and C Demarquilly), 11–15 September 1995, Clermont-Ferrand, France, pp. 569584. INRA editions, Paris.Google Scholar
Miraglia, N, Poncet, C, Martin-Rosset, W 1992. Effect of feeding level, physiological state and breed on the rate of passage of particulate matter through the gastroentestinal tract of the horse. Annales de Zootechnie 41, 69.Google Scholar
Miraglia, N, Poncet, C, Martin-Rosset, W 2003. Effect of feeding level physiological status and breed on the digesta passage of forage based diets in the horse. In Proceedings of the 18th Equine Nutrition and Physiology Symposium, 4–7 June 2003, East Lansing, MI, USA, pp. 275–280.Google Scholar
Moore-Colyer, MJS, Hyslop, JJ, Longland, AC, Cuddeford, D 2002. The mobile bag technique as a method for determining the degradation of four botanically diverse fibrous feedstuffs in the small intestine and total digestive tract of ponies. British Journal of Nutrition 88, 729740.Google Scholar
Moore, BE, Dehority, BA 1993. Effects of diet and hindgut defaunation on diet digestibility and microbial concentrations in the cecum and colon of the horse. Journal of Animal Science 71, 33503358.Google Scholar
Nicoletti, JN, Wohlt, J, Glade, MJ 1980. Nutrition utilization by ponies and steers is affected by dietary forage rations. Journal of Animal Science 51 (suppl. 1), 25.Google Scholar
National Research Council (NRC) 1989. Nutrient requirements of horses, 5th revised edition. National Academy of Sciences, Washington, DC, USA.Google Scholar
National Research Council (NRC) 2007. Nutrient requirements of horses, 6th revised edition. National Academy of Sciences, Washington, DC, USA.Google Scholar
Potter, GD 2004. Protein requirements of horses for maintenance and work. In Nutrition of the performance horse. Which system in Europe for evaluating the nutritional requirements? (ed. V Julliand and W Martin-Rosset), EAAP no 111, pp. 149156. Wageningen Academic Publishers, Wageningen, The Netherlands.Google Scholar
Preston, TR, Leng, RA 1987. Digestive physiology of ruminants. In Matching ruminant production systems with available resources in the tropics and subtropics (ed. Penambul Books), pp. 2148. Penambul Books Ltd, Armidale, NSW, Australia.Google Scholar
Prior, RL, Hintz, HF, Lowe, JE, Visek, WJ 1974. Urea recycling and metabolism of ponies. Journal of Animal Science 38, 565571.CrossRefGoogle ScholarPubMed
Robinson, DW, Slade, LM 1974. The current status of knowledge on the nutrition of equines. Journal of Animal Science 39, 10451066.Google Scholar
Russell, JB 2007. The energy spilling reactions of bacteria and other organisms. Journal of Molecular Microbiology and Biotechnology 13, 111.Google ScholarPubMed
Russell, JB, Cook, MC 1995. Energetics of bacterial growth: balance of anabolic and catabolic reactions. Microbiological Reviews 59, 4862.Google Scholar
Santos, AS, Jerónimo, E, Ferreira, LM, Rodrigues, MAM, Bessa, RJB 2007. Chemical composition of liquid and solid associated bacteria in the cecum and colon of horses. In Proceedings of the 58th EAAP Annual Meeting, 27–30 August 2007, Dublin, Ireland, 293p.Google Scholar
Santos, AS, Jerónimo, E, Ferreira, LM, Rodrigues, MAM, Bessa, RJB 2008. Fatty acid composition of liquid and solid associated bacteria in the cecum and colon of horses. In Proceedings of the 59th EAAP Annual Meeting, 24–27 August 2008, Vilnius, Lituania, 221p.Google Scholar
Slade, LM, Robinson, DW, Casey, KE 1970. Nitrogen metabolism in nonruminant herbivores. I. The influence of nonprotein nitrogen and protein quality on the nitrogen retention of adult mares. Journal of Animal Science 30, 753760.Google Scholar
Slade, LM, Robinson, DW, Al-Rabbat, F 1973. Ammonia turnover in the large intestine. In Proceedings of the 3rd Equine Nutrition and Physiology Symposium, Gainesville, FL, USA, pp. 1–12.Google Scholar
Slade, LM, Bishop, R, Morris, JG, Robinson, DG 1971. Digestion and absorption of 15N-labelled microbial protein in the large intestine of the horse. British Veterinary Journal 127, XIXII.CrossRefGoogle ScholarPubMed
Schmitz, M, Abrens, F, Hagemeister, H 1990. Beitrag der absorption von aminosäuren im Dikdarm zur Proteinversorgung bei Pferd, Rind und Schwein. Journal of Animal Physiology and Animal Nutrition 64, 1213.Google Scholar
Tisserand, JL 1975. Contribution à l’étude de la digestion dans le caecum du cheval. Compte rendu de la 1ère Journée de la Recherche Equine, 5 mars 1975, Paris, 3p.Google Scholar
Tisserand, JL, Masson, C 1976. Effects comparés de trois régimes: foin, luzerne déshydratée agglomérée et maïs plante entiére déshydratée agglomérée sur l’activité biochimique du caecum du poney. Compte rendu de la 2ème Journée de la Recherche Equine, Paris, pp. 73–80.Google Scholar
Udén, P, Van Soest, PJ 1982. Comparative digestion of timothy (Phileum pratense) fibre by ruminants, equines and rabbits. British Journal of Nutrition 47, 267272.Google Scholar
Van Weyenberg, S, Sales, J, Janssens, GPJ 2006. Passage rate of digesta through the equine gastrointestinal tract: a review. Livestock Science 99, 312.CrossRefGoogle Scholar
Varloud, M, Fonty, G, Roussel, A, Guyonvarch, A, Julliand, V 2007. Postprandial kinetics of some biotic and abiotic characteristics of the gastric ecosystem of horses fed a pelleted concentrate meal. Journal of Animal Science 85, 25082516.Google Scholar
Vermorel, M, Martin-Rosset, W 1997. Concepts, scientific bases, structure and validation of the French horse net energy system (UFC). Livestock Production Science 47, 261275.Google Scholar
Vlaeminck, B, Fievez, V, Cabrita, ARJ, Fonseca, AJM, Dewhurst, RJ 2006a. Factors affecting odd- and branched-chain fatty acids in milk: a review. Animal Feed Science and Technology 131, 389417.Google Scholar
Vlaeminck, B, Fievez, V, Demeyer, D, Dewhurst, RJ 2006b. Effect of forage: concentrate ratio on fatty acid composition of rumen bacteria isolated from ruminal and duodenal digesta. Journal of Dairy Science 89, 26682678.Google Scholar
Vlaeminck, B, Dufour, C, Van Vuuren, AM, Cabrita, ARJ, Dewhurst, RJ, Demeyer, D, Fievez, V 2005. Use of odd and branched-chain fatty acids in rumen contents and milk as a potential microbial marker. Journal of Dairy Science 88, 10311042.Google Scholar
Weimer, PJ, Waghorn, GC, Odt, CL, Mertens, DR 1999. Effect of diet on populations of three species of ruminal cellulolytic bacteria in lactating dairy cows. Journal of Dairy Science 82, 122134.CrossRefGoogle ScholarPubMed
Wolter, R, Gouy, D, Durix, A, Letourneau, JC, Carcelen, M, Landreau, J 1978. Digestibilité et activité biochimique intracaecale chez le poney recevant un même aliment complet présenté sous forme granulée, expansée ou semi-expansée. Annales de Zootechnie 27, 4760.Google Scholar
Woodward, AD, Holcombe, SJ, Staniar, WP, Colvin, C, Liesman, J, Trottier, NL 2009. Differential mRNA abundance of amino acid tranporters B0,+, CAT-1, LAT-2 and LAT-3 in five segments of the equine intestine. Journal of Equine Veterinary Science 29, 348349.Google Scholar
Woodward, AD, Holcombe, SJ, Steibel, JP, Staniar, WP, Colvin, C, Trottier, NL 2010. Cationic and neutral amino acid transporter transcript abundances are differentially expressed in the equine intestinal tract. Journal of Animal Science 88, 10281033.Google Scholar
Wootton, JF, Argenzio, RA 1975. Nitrogen utilization within equine large intestine. American Journal of Physiology 229, 10621067.Google Scholar