Abstract
Buffalo is an amazing ruminant with high tolerance to low-quality roughage. Due to the special breeding environment, there are few reports on the digestibility of roughage in buffalo because it is difficult to quantify ingestion and egestion. To find more applicable method to determine the digestibility of low-quality roughage in buffalo, this study was conducted to compare total feces collection (TFC) method with the following three indirect techniques: Cr2O3 (chromic oxide), AIA (acid-insoluble ash), and ADL (acid detergent lignin), to determine rice straw digestibility in buffalo. Six non-pregnant, non-lactating female buffaloes were used in this experiment and the nutritional compositions of the rice straw and feces were measured. Using Cr2O3 and AIA methods, the digestibility of dry matter (DM), ash, organic matter (OM), nitrogen free extract (NFE), crude protein (CP), ether extract (EE), crude fiber (CF), neutral detergent fiber (NDF), acid detergent fiber (ADF), cellulose (CEL), hemicellulose (HC), and ADL did not have statistically significant differences compared with TFC (P > 0.05). However, the digestibility of DM, ash, OM, NFE, EE, CF, NDF, ADF, and ADL determined using ADL method were significantly lower than those using the TFC (P < 0.05). The feces recovery of Cr2O3 and AIA was 95.89% and 97.14%, which were higher than that of ADL (88.90%). In summary, compare with ADL method, TFC, Cr2O3, and AIA methods are more accurate to determine the roughage digestibility of buffalo. Furthermore, Cr2O3 and AIA methods are applicable and convenient to evaluate the roughage digestibility of buffalo under extensive feeding system.
Similar content being viewed by others
References
Arbabi, S., Ghoorchi, T. and Parvar, R., 2016. A comparison of apparent digestibility of nutrient in caspian horse feeds as determined by total collection of faeces, acid insoluble ash and lignin methods, Iranian Journal of Applied Animal Science, 6, 461–466.
Association of Official Analytical Chemists (AOAC), 1995. Official Methods of Analysis, 16th ed. Association of Official Analytical Chemists, Arlington, VA, USA.
Bakker, G. and Jongbloed, A.W., 1994. The effect of housing system on apparent digestibility in pigs, using the classical and marker (chromic oxide, acid-insoluble ash) techniques, in relation to dietary composition, Journal of the Science of Food and Agriculture, 64, 107–115.
Barbosa, N.G.S., Rodriguez, N.M., Fernandes, P.C.C., Garcia, A., Nahum, B.D.S., Saliba, E.S., Borges, I., Ávila, S.C., Menezes, B.P., Ribeiro, O.A.V., Oliveira, M.E.C. and Quinzeiro Neto, T., 2010. Intake and digestibility of river buffalo steers (Bubalus bubalis) fed different levels of palm kernel cake: effect of diet neutral detergent fiber, digestible energy, crude protein and extract ether. In: G.A. Brudeli. E.M. Patiño and J.L. Konrad, Embrapa Amazônia Oriental-Artigo em anais de congresso (ALICE), Revista Veterinaria, 21, 146–150.
Bergero, D., Miraglia, N., Abba, C. and Polidori, M., 2004. Apparent digestibility of Mediterranean forages determined by total collection of faeces and acid-insoluble ash as internal marker, Livestock Production Science, 85, 235–238.
Bilal, M.Q., Suleman, M. and Raziq, A., 2006. Buffalo: black gold of Pakistan. Livestock Research for Rural Development, 18, 140–151.
Block, E., Kilmer, L.H. and Muller, L.D., 1981. Acid insoluble ash as a marker of digestibility for sheep fed corn plants or hay and for lactating dairy cattle fed hay Ad Libitum, Journal of Animal Science, 52, 1164–1169.
Brestenský, M., Nitrayová, S., Heger, J. and Patráš, P., 2017. Chromic oxide and acid-insoluble ash as markers in digestibility studies with growing pigs and sows, Journal of Animal Physiology and Animal Nutrition, 101, 46–52.
Buntinx, S.E., Pond, K.R., Fisher, D.S. and Burns, J.C., 1992. Evaluation of the Captec chrome controlled-release device for the estimation of fecal output by grazing sheep, Journal of Animal Science, 70, 2243–2249.
Carvalho, A.L.D., Oliveira, V.D., Moraes, W.D., Cubas, Z.S., Rinaldi, A.R., Oliveira, M.J.D., Almeida, R.P.D. and Bordignon, L.A.F., 2013. Comparison of methods for determination of nutrient digestibility of a dry kibble diet for ocelots, Pesquisa Veterinária Brasileira, 33, 71–74.
Clawson, A.J., Reid, J.T., Sheffy, B.E. and Willman, J.P., 1955. Use of chromium oxide in digestion studies with swine, Journal of Animal Science, 14, 700–709.
Cochran, R.C., Adams, D.C., Wallace, J.D. and Galyean, M.L., 1986. Predicting digestibility of different diets with internal markers: evaluation of four potential markers, Journal of Animal Science, 63, 1476–1483.
Cruz, L.C., 2010. Recent developments in the buffalo industry of Asia, Revista Veterinaria, 21, 7–19.
Dabrowski, K. and Dabrowska, H., 1981. Digestion of protein by rainbow trout (Salmo gairdneri Rich.) and absorption of amino acids within the alimentary tract, Comparative Biochemistry and Physiology Part A: Physiology, 69, 99–111.
De Marco, M., Miraglia, N., Peiretti, P.G. and Bergero, D., 2012. Apparent digestibility of wheat bran and extruded flax in horses determined from the total collection of feces and acid-insoluble ash as an internal marker, Animal, 6, 227–231.
De Silva, S.S., 1985. Evaluation of the use of internal and external markers in digestibility studies. In: C.Y. Cho, C.B. Cowey and T. Watanabe (eds), Finfish Nutrition in Asia: Methodological approaches to research and development, IDRC, Ottawa, ON, CA, 96–102.
Dixon, J., Gulliver, A. and Gibbon, D., 2001. Global farming systems study: challenges and priorities to 2030, Synthesis and Global Overview, FAO.
Fahey, G.C., McLaren, G.A. and Williams, J.E., 1979. Lignin digestibility by lambs fed both low-quality and high-quality roughages, Journal of Animal Science, 48, 941–946.
FAOSTAT. 2017. http://www.fao.org/faostat/zh/?#data/QA. Accessed Dec.20.2019.
Fenton, T.W. and Fenton, M., 1979. An improved procedure for the determination of chromic oxide in feed and feces, Canadian Journal of Animal Science, 59, 631–634.
Freitas, D.D., Berchielli, T.T., Silveira, R.N.D., Soares, J.P.G., Fernandes, J.J. and Pires, A.V., 2002. Produção fecal e fluxo duodenal de matéria seca e matéria orgânica estimados por meio de indicadores, Revista Brasileira de Zootecnia, 31, 1521–1530.
Gandra, J.R., Freitas Jr, J.E., Barletta, R.V., Maturana Filho, M., Gimenes, L.U., Vilela, F.G., Baruselli, P.S. and Rennó, F.P., 2011. Productive performance, nutrient digestion and metabolism of Holstein (Bos taurus) and Nellore (Bos taurus indicus) cattle and Mediterranean Buffaloes (Bubalis bubalis) fed with corn-silage based diets, Livestock Science, 140, 283–291.
Gao, W., Zhang, B., Lv, B., Liu, C. and Chen, D., 2015. Ruminal degradability and intestinal digestibility of individual amino acids in mixed diets with different crude protein levels measured by the modified in vitro three-step and mobile nylon bag technique, Animal Science Journal, 87, 547–556.
Glencross, B.D., Booth, M. and Allan, G.L., 2007. A feed is only as good as its ingredients - a review of ingredient evaluation strategies for aquaculture feeds, Aquaculture Nutrition, 13, 17–34.
Goddard, J.S. and McLean, E., 2001. Acid-insoluble ash as an inert reference material for digestibility studies in tilapia, Oreochromis aureus, Aquaculture, 194, 93–98.
Grant, R.J., Van Soest, P.J., McDowell, R.E. and Perez Jr, C.B., 1974. Intake, Digestibility and metabolic loss of napier grass by cattle and buffaloes when fed wilted, chopped and wholes, Journal of Animal Science, 39, 423–434.
Guzman-Cedillo, A.E., Corona, L., Castrejon-Pineda, F., Rosiles-Martínez, R. and Gonzalez-Ronquillo, M., 2017. Evaluation of chromium oxide and titanium dioxide as inert markers for calculating apparent digestibility in sheep, Journal of Applied Animal Research, 45, 275–279.
Jasra, A.W. and Johnson, D.E., 2000. Validity of lignin as an internal marker in digestion studies on rangelands, Pakistan Journal of Agricultural Research, 16, 59–63.
Kanani, J., Philipp, D., Coffey, K.P., Kegley, E.B., West, C.P., Gadberry, S., Jennings, J, Young, A.N. and Rhein, R.T., 2014. Comparison of acid-detergent lignin, alkaline-peroxide lignin, and acid-detergent insoluble ash as internal markers for predicting fecal output and digestibility by cattle offered bermudagrass hays of varying nutrient composition, Journal of Animal Science and Biotechnology, 5, 7.
Kavanagh, S., Lynch, P.B., O’mara, F. and Caffrey, P.J., 2001. A comparison of total collection and marker technique for the measurement of apparent digestibility of diets for growing pigs, Animal Feed Science and Technology, 89, 49–58.
Kierstein, G., Vallinoto, M., Silva, A., Schneider, M.P., Iannuzzi, L. and Brenig, B., 2004. Analysis of mitochondrial d-loop region casts new light on domestic water buffalo (Bubalus bubalis) phylogeny, Molecular Phylogenetics and Evolution, 30, 308–324.
Kotb, A.R. and Luckey, T.D., 1972. Markers in nutrition, Nutrition Abstracts and Reviews, 42, 813–845.
Lachmann-Sevilla, M., Araujo-Febres, O. and Vergara-Lopez, J., 2003. Evaluation of acid detergent lignin as marker to predict digestibility in sheeps, Revista Cientifica-facultad de Ciencias Veterinarias, 13, 484-489.
Lærke, H.N., Kasprzak, M.M. and Knudsen, K.B., 2012. Evaluation of two external markers for measurement of ileal and total tract digestibility of pigs fed human-type diets, Journal of Animal Science, 90, 384–386.
Lied, E., Julshamn, K. and Braekkan, O.R., 1982. Determination of protein digestibility in Atlantic cod (Gadus morhua) with internal and external indicators, Canadian Journal of Fisheries and Aquatic Sciences, 39, 854–861.
Ly, J., Ty, C. and Samkol, P., 2002. Studies on the use of acid insoluble ash as inert marker in digestibility trials with Mong Cai pigs, Livestock Research for Rural Development, 14, 14.
Mandell, I.B., Nicholson, H.H. and Christison, G.I., 1988. The effects of barley processing on nutrient digestion within the gastrointestinal tract of beef cattle fed mixed diets, Canadian Journal of Animal Science, 68, 191–198.
Martawidjaja, M. 2003. Utilization of rice straw as feed substitution for small ruminants. Wartazoa, Indonesian Bulletin of Animal and Veterinary Sciences, 13, 119–127.
Mc Geough, E.J., O’Kiely, P. and Kenny, D.A., 2010. A note on the evaluation of the acid-insoluble ash technique as a method for determining apparent diet digestibility in beef cattle, Irish Journal of Agricultural and Food Research, 49, 159–164.
McCarthy, J.F., Aherne, F.X. and Okai, D.B., 1974. Use of HCl insoluble ash as an index material for determining apparent digestibility with pigs, Canadian Journal of Animal Science, 54, 107–109.
Minson, D.J., 1971. Influence of lignin and silicon on a summative system for assessing the organic matter digestibility of Panicum, Australian Journal of Agricultural Research, 22, 589–598.
Miraglia, N., Poncet, C. and Rosset, W.M., 1992. Effect of feeding level, physiological state and breed on the rate of passage of particulate matter through the gastrointestinal tract of the horse, Annales de Zootechnie, 41, 69.
Moughan, P.J., Smith, W.C., Schrama, J. and Smits, C., 1991. Chromic oxide and acid-insoluble ash as faecal markers in digestibility studies with young growing pigs, New Zealand Journal of Agricultural Research, 34, 85–88.
Nanda, A.S. and Nakao, T., 2003. Role of buffalo in the socioeconomic development of rural Asia: current status and future prospectus, Animal Science Journal, 74, 443–455.
Oliveira, K.D., Costa, C, Bittar, C.M.M., Santos, V.P.D., Oliveira, V.A.B. and Sá, J.C.D. 2012. Indigestible cellulose and lignin in determining feces production and apparent digestibility in horses, Acta Scientiarum. Animal Sciences, 34, 267–272.
Penning, P.D. and Johnson, R.H., 1983. The use of internal markers to estimate herbage digestibility and intake: 2. Indigestible acid detergent fibre, The Journal of Agricultural Science, 100, 133–138.
Prigge, E.C., Varga, G.A., Vicini, J.L. and Reid, R.L., 1981. Comparison of ytterbium chloride and chromium sesquioxide as fecal indicators, Journal of Animal Science, 53, 1629–1633.
Rodríguez, N.M., Saliba, E.O.S. and Guimarães-Júnior, R., 2007. Uso de indicadores para estimar consumo y digestibilidad de pasto. LIPE, lignina purificada y enriquecida. Revista Colombiana de Ciencias Pecuarias, 20, 12.
Rohr, K., Brandt, M., Lebzien, P. and Schafft, H., 1984. Measurement of duodenal flow in dairy cows by either total collection or spot sampling, using a special cannula, Canadian Journal of Animal Science, 64, 116–117.
Roth, J., and Myers, P. 2004. Bubalus bubalis. Retrieved from https://animaldiversity.org/site/accounts/ information/Bubalus_bubalis.html. Accessed 10 January, 2020.
Ruiz, R., Van Soest, P.J., Van Amburgh, M.E., Fox, D.G. and Robertson, J.B., 2001. Use of chromium mordanted neutral detergent residue as a predictor of fecal output to estimate intake in grazing high producing Holstein cows, Animal Feed Science and Technology, 89, 155-164.
Sales, J. and Janssens, G.P.J., 2003a. Acid-insoluble ash as a marker in digestibility studies: a review, Journal of Animal and Feed Sciences, 12, 383–401.
Sales, J. and Janssens, G.P.J., 2003c. The use of markers to determine energy metabolizability and nutrient digestibility in avian species, World’s Poultry Science Journal, 59, 314–327.
Schäfers, S., Bulang, M., Meyer, U., Lindwedel, A., Hüther, L. and Dänicke, S., 2018. Suitability of n-alkanes and chromium (III) oxide as digestibility markers in calves at the end of the milk feeding period supplemented with a prebiotic, Animal Nutrition, 4, 84–89.
Siqueira, R.F., Gomes, R.C., Rodrigues, P.H.M., Fukushima, R.S., Lorenzo, C.L.F. and Gobesso, A.A.O., 2009. Use of cutin for determining apparent digestibility of diets for horses, Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 61, 1373–1381.
Soares, L.F.P., Guim, A., Andrade Ferreira, M.D., Modesto, E.C., Batista, Â.M.V. and Barros Sales Monteiro, P.D., 2011. Assessment of indicators and collection methodology to estimate nutrient digestibility in buffaloes, Revista Brasileira de Zootecnia, 40, 2005–2010.
Sunvold, G.D. and Cochran, R.C., 1991. Evaluation of acid detergent lignin, alkaline peroxide lignin, acid insoluble ash, and indigestible acid detergent fiber as internal markers for prediction of alfalfa, bromegrass, and prairie hay digestibility by beef steers, Journal of Animal Science, 69, 4951–4955.
Tacon, A.G. and Rodrigues, A.M., 1984. Comparison of chromic oxide, crude fibre, polyethylene and acid-insoluble ash as dietary markers for the estimation of apparent digestibility coefficients in rainbow trout, Aquaculture, 43, 391–399.
Thacker, P.A. and Qiao, S., 2001. Further modifications to the mobile nylon bag technique to determine nutrient digestibility for swine, Asian-Australasian Journal of Animal Sciences, 14, 1149–1156.
Thonney, M.L., Duhaime, D.J., Moe, P.W. and Reid, J.T., 1979. Acid insoluble ash and permanganate lignin as indicators to determine digestibility of cattle rations, Journal of Animal Science, 49, 1112–1116.
Van Keulen, J.Y. and Young, B.A., 1977. Evaluation of acid-insoluble ash as a natural marker in ruminant digestibility studies, Journal of Animal Science, 44, 282–287.
Van Soest, P.J., 1963. Use of detergents in the analysis of fibrous feeds. 2. A rapid method for the determination of fiber and lignin, Journal of the Association of Official Agricultural Chemists, 46, 829–835.
Van Soest, P.V., Robertson, J.B. and Lewis, B.A., 1991. Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition, Journal of Dairy Science, 74, 3583–3597.
Varloud, M., De Fombelle, A., Goachet, A.G., Drogoul, C. and Julliand, V., 2004. Partial and total apparent digestibility of dietary carbohydrates in horses as affected by the diet, Animal Science, 79, 61–72.
Vasconcellos, R.S., Carciofi, A.C., Oliveira, L.D., Prada, F. and Pereira, G.T., 2007. Utilização de indicadores para estimar a digestibilidade aparente em gatos, Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 59, 466–472.
Vega, R.S., Del Barrio, A.N., Sangel, P.P., Katsube, O., Canaria, J.C., Herrera, J.V., Lapitan, R.M., Orden, E.A., Fujihara, T. and Kanai, Y., 2010. Eating and rumination behaviour in Brahman grade cattle and crossbred water buffalo fed on high roughage diet, Animal Science Journal, 81, 574–579.
Velásquez, A.V., Da Silva, G.G., Sousa, D.O., Oliveira, C.A., Martins, C.M.M.R., Dos Santos, P.P.M., Balieiro, J.C.C., Rennó, F.P. and Fukushima, R.S., 2018. Evaluating internal and external markers versus fecal sampling procedure interactions when estimating intake in dairy cows consuming a corn silage-based diet, Journal of Dairy Science, 101, 5890–5901.
Vogtmann, H., Pfirter, H.P. and Prabucki, A.L., 1975. A new method of determining metabolisability of energy and digestibility of fatty acids in broiler diets, British Poultry Science, 16, 531–534.
Wanapat, M., Ngarmsang, A., Korkhuntot, S., Nontaso, N., Wachirapakorn, C., Beakes, G. and Rowlinson, P., 2000. A comparative study on the rumen microbial population of cattle and swamp buffalo raised under traditional village conditions in the northeast of Thailand, Asian Australasian Journal of Animal Sciences, 13, 918–921.
Wanapat, M., Polyorach, S., Boonnop, K., Mapato, C. and Cherdthong, A., 2009. Effects of treating rice straw with urea or urea and calcium hydroxide upon intake, digestibility, rumen fermentation and milk yield of dairy cows, Livestock Science, 125, 238–243.
Warriach, H.M., McGill, D.M., Bush, R.D., Wynn, P.C. and Chohan, K.R., 2015. A review of recent developments in buffalo reproduction - a review, Asian-Australasian Journal of Animal Sciences, 28, 451.
Williams, C.H., David, D.J. and Iismaa, O., 1962. The determination of chromic oxide in faeces samples by atomic absorption spectrophotometry, The Journal of Agricultural Science, 59, 381–385.
Yindee, M., Vlamings, B. H., Wajjwalku, W., Techakumphu, M., Lohachit, C., Sirivaidyapong, S., Thitaram, C., Amarasinghe, A.A.A.W.K., Alexander, P.A.B.D.A., Colenbrander, B. and Lenstra, J.A., 2010. Y-chromosomal variation confirms independent domestications of swamp and river buffalo, Animal Genetics, 41, 433–435.
Zicarelli, F., Calabrò, S., Piccolo, V., D’Urso, S., Tudisco, R., Bovera, F., Cutrignelli, M.I. and Infascelli F., 2008. Diets with different forage/concentrate ratios for the Mediterranean Italian buffalo: In vivo and In vitro digestibility, Asian-Australasian Journal of Animal Sciences, 21, 75–82.
Acknowledgments
Thanks for Professor Xianghua Yan’s assistance in the experimental design of this paper.
Funding
This article is financially supported by the National Key Research and Development Program (2018YFD0501605 and 2017YFD0501701) and the Fundamental Research Funds for the Central Universities (2662016PY052, 2662016QD038 and 2662018PY037).
Author information
Authors and Affiliations
Contributions
Yong Wu, Liguo Yang, and Xiang Li conceived and designed the study; Yong Wu and Liujie Shi extracted the data; Zhen Wang, Yong Wu, and Luncheng Cui analyzed the data; Zhen Wang and Xiang Li wrote the manuscript; and Zhen Wang, Luncheng Cui, Liujie Shi, Xiang Li, Changjiu He, and Xiang Li revised the paper.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethics approval
The experimental design of the feeding and digestibility trials was approved by Laboratory Animal Use and Care Committee in Hubei Science and Technology Agency. This experiment is in line with national regulations regarding animal welfare ethics. Ethical approval number is HZAUBU-2015-005.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Wang, Z., Wu, Y., Shi, L. et al. Evaluation and mining the applicable methods of roughage digestibility determination for buffalo (Bubalus bubalis). Trop Anim Health Prod 52, 2639–2646 (2020). https://doi.org/10.1007/s11250-020-02292-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11250-020-02292-9