Abstract
The objective of this study was to evaluate the influence of tree foliage species supplemented in ruminant diets based on Pennisetum purpureum on the in vitro digestibility and fermentation, microbial biomass synthesis and enteric methane production. Seven experimental diets were evaluated, including a control treatment based on P. purpureum (PT) grass, and six additional treatments supplemented with 30.0% foliage from Neomillspaughia emargiata (NE), Tabernaemontana amygdalifolia (TA), Caesalpinia gaumeri (CG), Piscidia piscipula (PP), Leucaena leucocephala (LL) and Havardia albicans (HA). A randomised complete block design repeated in two periods (block) was used. The highest gas production (P < 0.05) was recorded in treatments TA and PT (237 and 228 mL g−1, respectively). The highest in vitro digestibility of dry matter (IVDMD) and organic matter (IVOMD) (P < 0.05) was recorded in the control treatment PT (57.9% and 66.1%, respectively). Treatments LL, NE, TA and PP promoted greater microbial biomass synthesis (290, 223, 220 and 213 mg g−1, respectively) (P < 0.05). The proportion of propionic acid also increased in these latter treatments and in treatments CG and HA (P < 0.05). Additionally, treatments LL, PP, NE and TA decreased methane production (25.8, 29.5, 30.6 and 31.8 L kg−1 of digested dry matter, respectively). In conclusion, supplementation with L. leucocephala, P. piscipula, N. emargiata and T. amygdalifolia in ruminant diets based on P. purpureum is one feed alternative that can promote greater efficiency and synthesis of microbial biomass, increase the proportions of propionic and butyric acid and decrease the production of enteric methane by 15.6 to 31.6%.
Similar content being viewed by others
References
Alayón, G.J.A., Jiménez, F.G., Piñeiro, V.Á.T., Canul, S.J., Albores, M.S., Villanueva, L.G., Nahed, T.J. and Ku, V.J.C., 2018. Estrategias de mitigación de gases de efecto invernadero en la ganadería, Agroproductividad, 11(2), 11–15
Albores, M.S., Alayón, J.A.G., Ayala, A.J.B., Solorio, F.J.S., Aguilar, C.F.P., Olivera, L.C. and Ku, J.C.V., 2017. Effects of feeding ground pods of Enterolobium cyclocarpum Jacq. Griseb on dry matter intake, rumen fermentation, and enteric methane production by Pelibuey sheep fed tropical grass, Tropical Animal Health and Production, 49(4), 857–866
Archimède, H., Eugène, M., Magdeleine, C. M., Boval, M., Martin, C., Morgavi, D. P., Lecomte, P., Doreau, M., 2011. Comparison of methane production between C3 and C4 grasses and legumes, Animal Feed Science and Technology, 166, 59–64
Archimède, H., Martin, C., Periacarpin, F., Rochette, Y., Silou, T., Etienne, C., Anais and Doreau, M., 2014. Methane emission of Blackbelly rams consuming whole sugarcane forage compared with Dichanthium sp. Hay, Animal Feed Science and Technology, 190, 30–37
Association Official Analytical Chemists (AOAC), 1990. Official Methods of Analysis. 15th ed (Arlington, Virginia, U.S.A.)
Bayssa, M., Negesse, T. and Tolera, A., 2016. Leaf biomass yield, chemical composition, in vitro gas and methane production and rumen degradation characteristics of some woody plant species in Afar rangeland of north eastern Ethiopia, Middle-East Scientific Research, 24(4), 1252–1265
Bhatta, R., Saravanan, M., Baruah, L. and Prasad, C.S., 2015. Effects of graded levels of tannin-containing tropical tree leaves on in vitro rumen fermentation, total protozoa and methane production, Journal Applied Microbiology, 118(3), 557–564
Blümmel, M. and Lebzien, P., 2001. Predicting ruminal microbial efficiencies of dairy rations by in vitro techniques, Livestock Production Science, 68(2–3), 107–117
Blümmel, M., Steingass, H. and Becker, K., 1997. The relationship between in vitro gas production, in vitro microbial biomass and 15N incorporation and its implications for the prediction of voluntary feed intake of roughages, British Journal of Nutrition, 77(6), 911–921
Bonnet, O.J., Meuret, M., Tischler, M.R., Cezimbra, I.M., Azambuja, J.C. and Carvalho, P.C., 2015. Continuous bite monitoring: a method to assess the foraging dynamics of herbivores in natural grazing conditions, Animal Production Science, 55(3), 339–349
Carulla, J.E., Kreuzer, M., Machmüller, A. and Hess, H.D., 2005. Supplementation of Acacia mearnsii tannin decreases methanogenesis and urinary nitrogen in forage-fed sheep, Australian Journal of Agricultural Research, 56(9), 961–970
Cherdthong, A., Wanapat, M., Rakwongrit, D., Khota, W., Khantharin, S., Tangmutthapattharakun, G. and Phesatcha, K., 2014. Supplementation effect with slow-release urea in feed blocks for Thai beef cattle nitrogen utilization, blood biochemistry, and hematology, Tropical Animal Health and Production, 46(2), 293–298
Cuartas, C.A., Naranjo, J.F., Tarazona, A.M., Murgueitio, E., Chará, J.D., Ku, V.J.C., Solorio, F., Flores, M., Solorio, B. and Barahona, R., 2014. Contribution of intensive silvopastoral systems to the adaptation and mitigation of climate change, Revista Colombiana de Ciencias Pecuarias, 27(2), 76–94
Denek, N., Aydin, S.S. and Can, A., 2017. The effects of dried pistachio (Pistachio vera L.) by-product addition on corn silage fermentation and in vitro methane production, Journal Applied Animal Research, 45(1), 185–189
Ellis, J., Dijkstra, J., France, J., Parsons, A.J., Edwards, G.R., Rasmussen, S., Kebreab, E. and Bannink, A., 2012. Effect of high-sugar grasses on methane emissions simulated using a dynamic model, Journal Dairy Science, 95(1), 272–285
Elmasry, A.M.A., Mendoza, G.D., Miranda, L.A., Vázquez, G., Salem, A.Z.M. and Hernández, P.A., 2016. Effects of types and doses of yeast on gas production and in vitro digestibility of diets containing maize (Zea mays) and lucerne (Medicago sativa) or oat hay, South African Journal Animal Science, 46(4), 391–397
García, E., 1973. Modificación al sistema climático de Koppen, (Instituto de Geografía, UNAM, México)
Gaviria, X., Naranjo, R.J.F., Bolívar, V.D.M. and Barahona, R.R., 2015. Consumo y digestibilidad en novillos cebuínos en un sistema silvopastoril intensivo, Archivos de Zootecnia, 64(245), 21–27
Gemeda, B.S. and Hassen, A., 2015. Effect of tannin and species variation on in vitro digestibility, gas, and methane production of tropical browse plants, Asian-Australasian Journal of Animal Sciences, 28(2), 188–199
Gerber, P.J., Steinfeld, H., Herderson, B., Mottet, A., Opio, C., Dijkman, J., Falcucci, A. and Tempio, G., 2013. Tackling climate change through livestock a global assessment of emission and mitigation opportunities, (Food and Agriculture Organization (FAO), Roma)
Gómez, T., González, C., Ortiz, S.L., Vera, J.C.K., Pinto, C.A. and García, J.R.S., 2017. Dominancia, composición química-nutritiva de especies forrajeras y fitomasa potencial en una selva secundaria, Agricultura, Sociedad y Desarrollo, 14(4), 617–634
Gunun, P., Gunun, N., Cherdthong, A., Wanapat, M., Polyorach, S., Sirilaophaisan, S., Wachirapakorn, C. and Kang, S., 2017. In vitro rumen fermentation and methane production as affected by rambutan peel powder, Journal of Applied Animal Research, 46(1), 626–631
Gurbuz, Y., 2009. Efectos del contenido de taninos condensados de algunas especies de leguminosas en la emisión de gas metano, Revista Cubana de Ciencias Agrícolas 43(3), 265–273
Hess, H.D., Monsalve, L.M., Lascano, C.E., Carulla, J.E., Díaz, T.E. and Kreuzer, M., 2003. Supplementation of a tropical grass diet with forage legumes and Sapindus saponaria fruits: effects on in vitro ruminal nitrogen turnover and methanogenesis, Australian Journal of Agricultural Research, 54(7), 703–713
Hoehn, A.N., Titgemeyer, E.C., Nagaraja, T.G., Drouillard, J.S., Miesner, M.D. and Olson, K.C., 2018. Effects of high condensed-tannin substrate, prior dietary tannin exposure, antimicrobial inclusion, and animal species on fermentation parameters following a 48 h in vitro incubation, Journal of Animal Science, 96(1), 343–353
Hristov, A.N., Oh, J., Firkins, J.L., Dijkstra, J., Kebreab, E., Waghorn, G., Makkar, H.P.S., Adesogan, A.T., Yang, W., Lee, W., Gerber, P.J., Henderson, B. and Tricarico, J.M., 2013. Mitigation of methane and nitrous oxide emissions from animal operations: A review of enteric methane mitigation options, Journal of Animal Science, 91(11), 5045–5069
Hu, W., Liu, J., Wu, Y., Guo, Y. and Ye, J., 2006. Effects of tea saponins on in vitro ruminal fermentation and growth performance in growing Boer goat, Archives of Animal Nutrition, 60(1), 89–97
Jansson, I., 2001. Hierarchical summer browsing by goats in the dry savanna of south-western Botswana, Minor Field Studies No. 165, (Swedish University, Upsala, Sweden)
Jolly, S. and Wallace, A., 2007. Best Practice for Production Feeding of Lambs: A Review of the Literature. Meat and Livestock Australia Limited, (Sydney, Australia, NSW)
Kajikawa, H., Tajima, K., Mitsumori, M. and Takenaka, A., 2007. Effects of amino nitrogen on fermentation parameters by mixed ruminal microbes when energy or nitrogen is limited, Journal of Animal Science, 78(2), 121–128
Krause, D.O., Smith, W.J. and McSweeney, C.S., 2004. Use of community genome arrays (CGAs) to assess the effects of Acacia angustissima on rumen ecology, Microbiology, 150(9), 2899–2909
Krishnamoorthy, U., Rymer, C. and Robinson, P.H., 2005. The in vitro gas production technique: limitations and opportunities, Animal Feed Science and Technology, 123–124, 1–7
Ku, V.J.C., Ayala, B.A.J., Solorio, S. F.J., Briceño, P.E.G., Ruiz, G.A., Piñeiro, V.A.T., Barros, R.M., Soto, A.A., Espinoza, H.J.C., Albores, M.S., Chay, C.A.J., Aguilar, P.C.F. and Ramírez, A.L., 2013. Tropical tree foliages and shrubs as feed additives in ruminant rations. In: A. Fattah and Z.M. Salem (eds) Nutritional Strategies of Animal Feed Additives, Nova Sci. Publishers, New York, 59–76
Leng, R.A., 2011. The rumen a fermentation vat or a series of organized structured microbial consortia: implications for the mitigation of enteric methane production by feed additives, Livestock Research for Rural Development, http://www.lrrd.org/lrrd23/12/leng23258.htm. Accessed 15 may 2018
Lila, Z.A., Mohammed, N., Kanda, S., Kamada, T. and Itabashi, H., 2003. Effect of Sarsaponin on Ruminal Fermentation with Particular Reference to Methane Production in vitro, Journal Dairy Science, 86(10), 3330–3336
Lorenz, M., Alkhafadji, M., Stringano, L., Nilsson, E., Mueller-Harvey, S.I. and Udén, P., 2014. Relationship between condensed tannin structures and their ability to precipitate feed proteins in the rumen, Journal Science of Food and Agriculture, 94(5), 963–968
Makkar, H.P.S., 2003. Chemical, protein precipitation and bioassays for tannins, tannin levels and activity in unconventional feeds, and effects and fate of tannins. In: H.P.S. Makkar (ed), Quantification of Tannins in Tree and Shrub Foliage, Springer, Dordrecht, 1–42
Makkar, H.P.S., Blümmel, M. and Becker, K., 1995. Formation of complexes between polyvinyl pyrrolidones or polyethylene glycols and tannins, and their implication in gas production and true digestibility in in vitro techniques, British Journal of Nutrition, 73(6), 897–913
Makkar, H.P., Siddhuraju, P., Becker, K., Siddhuraju, P. and Becker, K., 2007. Plant secondary metabolites, (Humana Press Inc., Totowa, New Jersey, USA)
McAllister, T.A. and Newbold, C.J., 2008. Redirecting rumen fermentation to reduce methanogenesis, Australian Journal Experimental Agriculture, 48(2), 7–13
McCullough, H., 1967. The determination of ammonia in whole blood by direct colorimetric method, Clinica Chemica Acta, 17(2), 297–304
Menke, K.H. and Steingass, H., 1988. Estimation of the energetic feed value obtained from chemical analysis and in vitro gas production using rumen fluid, Animal Research Development, 28, 7–55
Min, B.R., Solaiman, S., Terrill, T., Ramsay, A. and Mueller, H.I., 2015. The effects of tannins-containing ground pine bark diet upon nutrient digestion, nitrogen balance, and mineral retention in meat goats, Journal of Animal Science Biotechnology, 6(1), 1–8
Miranda, F. and Hernández, X.E., 1963. Los tipos de vegetación de México y su clasificación, Boletín de la Sociedad Botánica de México, 28, 29–179
Miranda, R.L.A., Vázquez, M.P., Améndola, M.R., Sandoval, G.L. and González, O.R., 2015. Cuantificación de las fracciones fermentables de alfalfa y tuna por la técnica de producción de gas, In: Asociación Latinoamericana de Producción Animal (ed), XXIV Congreso de la asociación Latinoamericana de producción animal y XL Congreso de la sociedad Chilena de producción animal. Puerto Varas, Chile, 575
Monforte, B.G.E., Sandoval, C.C.A., Ramírez, A.L. and Capetillo, L.C.M., 2005. Defaunating capacity of tropical fodder trees: Effects of polyethylene glycol and its relationship to in vitro gas production, Animal Feed Science and Technology, 123-124(1), 313–327
Montgomery, D.C., 2013. Design and Analysis of Experiments 8the ed, (Wiley & Sons, New Jersey)
Naranjo, J.F., Cuartas, C.A., Murgueitio, E., Chará, J. and Barahona, R., 2012: Balance de gases de efecto invernadero en sistemas silvopastoriles intensivos con Leucaena leucocephala en Colombia, Livestock Research for Rural Development, http://www.lrrd.org/lrrd24/8/nara24150.htm, Accessed 15 may 2018
National Research Council, 2016. Nutrient Requirements of Beef Cattle: Eighth Revised Edition., https://doi.org/10.17226/19014, Accessed 28 may 2018
Newbold, C.J., López, S., Nelson, N., Ouda, J.O., Wallace, R.J. and Moss, A.R., 2005. Propionate precursors and other metabolic intermediates as possible alternative electron acceptors to methanogenesis in ruminal fermentation in vitro, British Journal Nutrition, 94(1), 27–35
Niderkorn, V., Baumont, R., Le Morvan, A. and Macheboeuf, D., 2011. Occurrence of associative effects between grasses and legumes in binary mixtures on in vitro rumen fermentation characteristics, Journal of Animal Science, 89(4), 1138–1145
Paengkoum P., Phonmun, T., Liang, J.B., Huang, X.D., Tan, H.Y. and Jahromi, M.F., 2015. Molecular weight, protein binding affinity and methane mitigation of condensed tannins form mangosteen-peel (Garcinia mangostana L.), Asian-Australasian Journal of Animal Science, 28 (10), 1442–1448
Pal, K., Patra, A. K., Sahoo, A. and Kumawat, P. K. 2015. Evaluation of several tropical tree leaves for methane production potential, degradability and rumen fermentation in vitro, Livestock Science, 180, 98–105
Patra, A. K., 2010. Aspects of nitrogen metabolism in sheep-fed mixed diets containing tree and shrub foliages, British journal of nutrition, 103(9), 1319–1330
Patra, A.K. and Saxena, J., 2011. Exploitation of dietary tannins to improve rumen metabolism and ruminant nutrition, Journal of the Science of Food and Agriculture, 91(1), 24–37
Patra, A.K., Min, B.R., Saxena, J., 2012. Dietary tannins on microbial ecology of the gastrointestinal tract in ruminants, In: A.K. Patra (ed.) Dietary phytochemicals and microbes, Springer, Netherlands, 237–262
Patra, A., Park, T., Kim, M. and Yu, Z., 2017. Rumen methanogens and mitigation of methane emission by anti-methanogenic compounds and substances, Journal of Animal Science and Biotechnology, 8(1), 1–18
Pell, A.N. and Schofield, P., 1993. Computerized monitoring of gas production to measure forage digestion in vitro, Journal Dairy Science, 76(4), 1063–1073
Piñeiro, V.A.T., Canul, J.R.S., Alayón, J.A.G., Chay, A.J.C., Ayala, A.J.B., Aguilar, C.F.P., Solorio, F.J.S. and Ku, J.C.V., 2015. Potential of condensed tannins for the reduction of emissions of enteric methane and their effect on ruminant productivity, Archivos de Medicina Veterinaria, 47(3), 263–272
Piñeiro, V.A.T., Canul, J.R.S., Casanova, L.F., Chay, C.A.J., Ayala, B.J.A., Aguilar, C.F.P., Solorio, F.J.S. and Ku, J.C.V., 2017. Enteric methane emission in sheep fed Pennisetum purpureumand tropical trees containing condensed tannins, Revista Mexicana de Ciencias Pecuarias, 8(2), 111–119
Piñeiro, V.A.T., Jiménez, F.G., Alayon, G.J.A., Chay, C.A.J., Ayala, B.A.J., Aguilar, P.C.F. and Ku, V.J.C., 2018. Effects of quebracho tannin extract on intake, digestibility, rumen fermentation, and methane production in crossbred heifers fed low-quality tropical grass, Tropical Animal Health and Production, 50(1), 29–36
Puchala, R., Min, B.R., Goetsch, A.L. and Sahlu, T., 2005. The effect of condensed tannin-containing forage on methane emission by goats, Journal of Animal Science, 83(1), 182–186
Puchala, R., Animut, G., Patra, A.K., Detweiler, G.D., Wells, J.E., Varel, V.H., Sahlu, T. and Goetsch, A.L., 2012. Effects of different fresh-cut forages and their hays on feed intake, digestibility, heat production, and ruminal methane emission by Boer × Spanish goats, Journal of Animal Science, 90 (8), 2754–2762
Sallam, S.M.A., Nasser, M.E.A., El-Waziry, A.M., Bueno, I.C.S. and Abdalla, A.L., 2007. Use of an in vitro rumen gas production technique to evaluate some ruminant feedstuffs, Journal Applied Sciences Research, 3(1), 34–41
SAS, 2006. Institute Inc., SAS/STAT. Software, ver. 9.00. SAS, (Cary, NC, USA)
Soltan, Y.A., Morsy, A.S., Sallam, S.M.A., Louvandini, H. and Abdalla, A.L., 2012. Comparative in vitro evaluation of forage legumes (prosopis, acacia, atriplex, and leucaena) on ruminal fermentation and methanogenesis, Journal of Animal and Feed Sciences, 21(4), 759–772
Soltan, Y.A., Morsy, A.S., Sallam, S.M., Lucas, R.C., Louvandini, H., Kreuzer, M. and Abdalla, A.L., 2013. Contribution of condensed tannins and mimosine to the methane mitigation caused by feeding Leucaena leucocephala, Archives of Animal Nutrition, 67(3), 169–184
Suharti, S., Astuti, D.A., Wina, E. and Toharmat, T., 2011. Rumen microbial population in the in vitro fermentation of different ratios of forage and concentrate in the presence of whole lerak (Sapindus rarak) fruit extract, Asian-Australasian Journal of Animal Science, 24(8), 1086–1091
Szumacher, S.M. and Cieślak, A., 2010. Potential of phytofactors to mitigate rumen ammonia and methane production, Journal of Animal and Feed Sciences, 19(3), 319–337
Tan, H.Y., Sieo, C.C., Abdullah, N., Liang, J.B., Huang, X.D. and Ho, Y.W., 2011. Effects of condensed tannins from Leucaena on methane production, rumen fermentation and populations of methanogens and protozoa in vitro, Animal Feed Science and Technology, 169(3–4), 185–193
Theodorou, M.K., Williams, B.A., Dhanoa, M.S., McAllan, A.B. and France, J., 1994. A simple gas production method using a pressure transducer to determine the fermentation kinetics of ruminant feeds, Animal Feed Science and Technology, 48(3–4), 185–197
Ungerfeld, E.M., 2015. Shifts in metabolic hydrogen sinks in the methanogenesis-inhibited ruminal fermentation: a meta-analysis, Frontiers in Microbiology, 6(37), 1–17
Ungerfeld, E.M., Rust, S.R., Burnett, R., 2003. Use of some novel alternative electron sinks to inhibit ruminal methanogenesis, Reproduction Nutrition Development, 43(2), 189–202
Valencia, S.S.S., Piñeiro, V.T.A., Molina, B.I.S., Lazos, B.I.J, Uuh, N.J.J., Segura C.M.R., Ramírez, A.L., Solorio, S.F.J. and Ku, V.J.C., 2018. Potential of Samanea saman pod meal for enteric methane mitigation in crossbred heifers fed low-quality tropical grass, Agricultural and Forest Meteorology, 258, 108–116
Van Soest, P.J., 1965. Symposium on factors influencing the voluntary intake of herbage by ruminants: voluntary intake in relation to chemical composition and digestibility, Journal of Animal Science, 24(3), 834–843
Van Soest, P.J., Robertson, J.B. and Lewis, B.A., 1991. Methods for dietary fibre, neutral detergent fibre and nonstarch polysaccharides in relation to animal nutrition, Journal Dairy Science, 74 (10), 3583–3597
Vargas, J., Pabón, M. and Carulla, J., 2014. Producción de metano in vitro en mezcla de gramíneas-leguminosas del trópico alto colombiano, Archivos de Zootecnia, 63(243), 397–407
Wang, Y., Alexander, T. W. and McAllister, T. A., 2009. In vitro effects of phlorotannins from Ascophyllum nodosum (brown seaweed) on rumen bacterial populations and fermentation, Journal of the Science of Food and Agriculture, 89(13), 2252–2260.
Wischer, G., Boguhn, J., Steingaß, H., Schollenberger, M. and Rodehutscord, M., 2013. Effects of different tannin-rich extracts and rapeseed tannin monomers on methane formation and microbial protein synthesis in vitro, Animal, 7(11), 1796–1805
Wolin, M.J. and Miller, T.L., 2006. Control of rumen methanogenesis by inhibiting the growth and activity of methanogens with hydroxymethylglutaryl-SCoA inhibitors. International Congress Series, 1293, 131–137
Acknowledgments
We acknowledge Ph.D. José Enrique Botello Álvarez and MsC. Marcela Guadalupe Téllez Martínez, for their support in the laboratory of the National Institute of Technology in Celaya, Guanajuato, and to Sayuri Hernández for her assistance with the experiments.
Funding
We would like to thank the National Council of Science and Technology (CONACYT) for the scholarship granted to the first author and for financing the project “Cuantificación de emisiones de metano entérico y óxido nitroso en ganadería bovina en pastoreo y diseño de estrategias para la mitigación en el sureste de México” (CONACYT-SEP CB 2014).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The author MsC. Samuel Albores Moreno has received research grant from CONACYT. The other authors declare that they have no conflict of interest.
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
Albores-Moreno, S., Alayón-Gamboa, J.A., Miranda-Romero, L.A. et al. Effect of tree foliage supplementation of tropical grass diet on in vitro digestibility and fermentation, microbial biomass synthesis and enteric methane production in ruminants. Trop Anim Health Prod 51, 893–904 (2019). https://doi.org/10.1007/s11250-018-1772-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11250-018-1772-7