The effect of oil extracted from borago officinalis L. whole plant at flowering stage on some ruminal fermentation parameters of sheep
Subject Areas : Veterinary Clinical PathologyMohsen Kazemi 1 , Yaser Eskandari Torbaghan 2
1 - Assistant Professor, Department of Animal Science, Higher Education Complex of Torbat-e Jam, Torbat-e Jam, Iran.
2 - M.Sc. Graduate of Immunology, Khalil Abad Health Center, Mashhad University of Medical Sciences, Mashhad, Iran.
Keywords: Sheep, Ruminal fermentation, Borago officinalis L, Vegetable oil,
Abstract :
Borago officinalis L. is a plant of Boraginaceae family, which is commonly used for medicinal purposes. The oil of this plant is rich in essential compounds, which is likely to cause changes in the ruminal fermentation pattern. Hence, this study was carried out with the aim of extracting the oil of borago officinalis L. after flowering by Soxhlet apparatusand investigating its effect (at four different levels of 0, 0.15, 0.30 and 0.45 mg/ml) on some ruminal fermentation parameters in an in vitro batch culture. The findings indicated that after oil addition, there was no change in gas production parameters (except for constant rate of gas production), microbial mass yield, efficiency of microbial mass synthesis, partitioning factor and protozoal population of the culture medium, but pH was significantly (linear, p < /em>=0.04) decreased compared to the control group, and total volatile fatty acids increased (linear, p < /em>=0.0006) subsequently. Also, methane yield decreased significantly (linear, p < /em>=0.0005) when the level of oil increased in the medium, but in contrast, the degradability of dry matter, organic matter and neutral detergent fiber increased. The overall results showed that the oil extracted from Borago officinalis L. can modify the ruminal fermentation pattern responsible for animal performance and reduce the emission of methane gas. Also, it seems that 0.45 mg/ml of oil produces the maximum effect on the fermentation pattern.
References:
Agarwal, N., Shekhar, C., Kumar, R., Chaudhary, L.C. and Kamra, D.N. (2009) Effect of peppermint (Mentha piperita) oil on in vitro methanogenesis and fermentation of feed with buffalo rumen liquor. Animal Feed Science and Technology, 148(2-4): 321-327.
AOAC. (1999). Official Methods of Analysis. 16th ed., Association of Official Analytical Chemists, Washington DC, USA.
Barnett, A.J.G. and Reid, R. (1957). Studies on the production of volatile fatty acids from grass in artificial rumen. 1. Volatile fatty acids production from fresh grasses. The Journal of Agricultural Science (Cambridge), 48(3): 315-321.
Barre, D.E. and Holub, B.J. (1992). The effect of borage oil consumption on the composition of individual phospholipids in human platelets. Lipids, 27(5): 315-20.
Blummel, M., Karsli, A. and Russel, J.R. (2003). Influence of diet on growth yields of rumen microorganisms in vitro and in vivo: Influence on growth yields of variable carbon fluxes to fermentation products. British Journal of Nutrition, 90(3): 625-634.
Busquet, M., Calsamiglia, S., Ferret, A. and Kamel, C. (2006). Plant extracts affect in vitro rumen microbial fermentation. Journal of Dairy Science, 89(2): 761-771.
Calsamiglia, S., Busquet, M., Cardozo, P.W., Castillejos, L. and Ferret, A. (2007). Essential oils as modifiers of rumen microbial fermentation. Journal of Dairy Science, 90(6): 2580-2595.
Cardozo, P.W., Calsamiglia, S., Ferret, A. and Kamel, C. (2005). Screening for the effects of natural plant extracts at two pH level on in vitro rumen microbial fermentation of a high-concentrate diet for beef cattle. Journal of Animal Science, 83(11): 2572-2579.
Castillejos, L., Calsamiglia, S. and Ferret, A. (2006). Effect of essential oils active compounds on rumen microbial fermentation and nutrient flow in in vitro systems. Journal of Dairy Science, 89(7): 2649-2658.
Castillejos, L., Calsamiglia, S., Martin-Tereso, J. and Ter Wijlen, H. (2008). In vitro evaluation of effects of ten essential oils at three doses on ruminal fermentation of high concentrate feedlot-type diets. Animal Feed Science and Technology, 145(1-4): 259-270.
Conner, D.E. (1993). Naturally occurring compounds. In: Antimicrobials in Foods. Davidson, P.M. and Branen, A.L. editors. 2th ed., USA: New York, Marcel Dekker, pp: 441-468.
Dehority, B.A. (2003). Rumen Microbiology. England: Nottingham University Press, pp: 372.
Demeyer, D. and Van Nevel, C. (1995). Transformations and effects of lipids in the rumen: Three decades of research at Gent University. Archives of Animal Nutrition, 48(1-2): 119-134.
Doreau, M. and Chilliard, Y. (1997). Digestion and metabolism of dietary fat in farm animals. British Journal of Nutrition, 78(1): S15-S35.
Doreau, M., Legay, F. and Bauchart, D. (1991). Effect of source and level of supplemental fat on total and ruminal organic matter and nitrogen digestion in dairy cows. Journal of Dairy Science, 74(7): 2233-2242.
Duke, J.A. (2000). Handbook of phytochemical constituents of grass herbs and other economic plants. 2nd ed., London: CRC Press, pp: 680.
Fievez, V., Babaymo, O.J. and Demeyer, D. (2005). Estimation of direct and indirect gas production in syringes: A tool to estimate short chain fatty acid production that requires minimal laboratory facilities. Animal Feed Science and Technology, 123-124(1): 197-210.
Francis, G., Kerem, Z., Makkar, H.P.S. and Becker, K. (2002). The biological action of saponins in animal systems: reviews. British Journal of Nutrition, 88(6): 587-605.
Getachew, G., Robinson, P.H., DePeters, E.J. and Taylor, S.J. (2004). Relationships between chemical composition, dry matter degradation and in vitro gas production of several ruminant feeds. Animal Feed Science and Technology, 111(1-4): 57-71.
Guarrera, P.M., Salerno, G. and Caneva, G. (2006). Food, flavouring and feed plant traditions in the Tyrrhenian sector of Basilicata. Journal of Ethnobiology and Ethnomedicine, 37(2): 1-6.
Gudej, J. and Tomczyk, M. (1996). Badania chromatograficzne zwiazkow polifenolowych w zielu Borago officinalis L. Herba Polonica, 42(4): 252-256.
Hegarty, R.S. (1999). Reducing rumen methane emission through elimination of protozoa. Australian Journal of Agricultural Research, 50(8): 1321-1327.
Hess, H.D., Kreuzer, M., Diaz, T.E., Lascano, C.E., Carulla, J.E. and Solvia, C.R. (2003). Saponin rich tropical fruits affect fermentation and methanogenesis in faunated and defaunated fluid. Animal Feed Science and Technology, 109(1-4): 79-94.
Hristov, A.N., Kennington, L.R., McGuire, M.A. and Hunt, C.W. (2005). Effect of diets containing linoleic acid or oleic acid rich oils on ruminal fermentation and nutrient digestibility, and performance and fatty acid composition if adipose and muscle tissues of finishing cattle. Journal of Animal Science, 83(6): 1312-1321.
IPCC. (2001). Climate Change 2001: The Scientific Basis. New York: Cambridge University Press.
Jalc, D. and Ceresnakova, Z. (2002). Effect of plant oils and malate on rumen fermentation in vitro. Czech Journal of Animal Science, 47(3): 106-111.
Jalc, D., Potkanski, A., Szumacher-Strabel, M., Cieslak, A. and Certic, M. (2005). Effect of microbial oil, evening primrose oil and borage oil on rumen fermentation in vitro. Veterinary Medicine-Czech, 50(11): 480-486.
Janssen, A.M., Scheffer, J.J. and Baerheim Svendsen, A. (1987). Antimicrobial activity of essential oils: a 1976-1986 Literature review. Aspects of the test methods. Planta Medica, 53(5): 395-398.
Jenkins, T.C. (1993). Lipid metabolism in the rumen. Journal of Dairy Science, 76(12): 3851-3863.
Johnson, K.A. and Johnson, D.E. (1995). Methane emissions from cattle. Journal of Animal Science, 73(8): 2483-2492.
Jouany, J.P. and Lassalas, B. (1997). Study of the adaptation of the rumen ecosystem to the antimethanogenic effect of monensin measured in vivo. Reproduction Nutrition Development, 37(1): 69-70.
Kamra, D.N. (2005). Rumen microbial ecosystem. Current Science, 89(1): 124-135.
Keady, T.W.J. and Mayne, C.S. (1999). The effects of level of fish oil inclusion in the diet on rumen digestion and fermentation parameters in cattle offered grass silage based diets. Animal Feed Science and Technology, 81(1-2): 57-68.
Komolong, M.K., Barber, D.G. and McNeill, D.M. (2001). Post-ruminal protein supply and N retention of weaner sheep fed on a basal diet of lucerne hay (Medicago sativa) with increasing levels of quebracho tannins. Animal Feed Science and Technology, 92(1-2): 59-72.
Machmuller, A. and Kreuzer, M. (1999). Methane suppression by coconut oil and associated effects on nutrient and energy balance in sheep. Canadian Journal of Animal Science, 79(1): 65-72.
Makkar, H.P.S. (2010). In vitro screening of feed resources for efficiency of microbial protein synthesis. In: In vitro screening of plant resources for extra-nutritional attributes in ruminants, Nuclear and related methodologies. Vercoe, P.E., Makkar, H.P.S. and Schlink, A.C. editors, USA: New York, Springer, pp: 107-144.
McGuffey, R.K., Richardson, L.F. and Wilkinson, J.I.D. (2001). Ionophores for dairy cattle: current status and future outlook. Journal of Dairy Science, 84(E. Suppl.): E194-E203.
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.
Mhamdi, B., Wannes, W.A., Bourgou, S. and Marzouk, B. (2009). Biochemical characterization of borage (Borago officinalis L.) seeds. Journal of Food Biochemistry, 33(3): 331-341.
Molero, R., Ibars, A., Calsamiglia, S., Ferret, A. and Losa, R. (2004). Effects of a specific blend of essential oil compounds on dry matter and crude protein degradability in heifers fed diets with different forage to concentrate ratios. Animal Feed Science and Technology, 114(1-4): 91-104.
Morgavi, D.P., Forano, E., Martin, C. and Newbold, C.J. (2010). Microbial ecosystem and methanogenesis in ruminants. Animal, 4(7): 1024-1036.
Newbold, C.J., McIntosh, F.M., Williams, P., Losa, R. and Wallace, R.J. (2004). Effects of a specific blend of essential oil compounds on rumen fermentation. Animal Feed Science and Technology, 114(1-4): 105-112.
NRC. (2007). Nutrient requirements of small ruminants: Sheep, goats, cervids, and new world camelids. 6th ed., USA: Washington, National Academy Press, 384p.
Ørskov, E.R. and McDonald, I. (1979). The estimation of protein degradability in the rumen from incubation measurements weighted according to rate of passage. Journal of Agricultural Science, 92(2): 499-503.
Patra, A.K. and Saxena, J. (2009). A review of the effect and mode of action of saponins on microbial population and fermentation in the rumen and ruminant production. Nutrition Research Reviews, 22(2): 204-219.
Pawar, M.M., Kamra, D.N., Agarwal, N. and Chaudhary, L.C. (2014). Effects of essential oils on in vitro methanogenesis and feed fermentation with buffalo rumen liquor. Agricultural Research, 3(1): 67-74.
Pieszak, M., Mikolajczak, P.L. and Manikowska, K. (2012). Borage (Borago officinalis L.) - A valuable medicinal plant used in herbal medicine. Herba Polonica, 58(4): 95-103.
Ricci, D., Fraternale, D., Giamperi, L., Bucchini, A., Epifano, F., Burini, G., et al. (2005). Chemical composition, antimicrobial and antioxidant activity of the essential oil of Teucrium marum (Lamiaceae). Journal of Ethnopharmacology, 98(1-2): 195-200.
Russell, J.B. (1998). The importance of pH in the regulation of ruminal acetate to propionate ratio and methane production in vitro. Journal of Dairy Science, 81(12): 3222-3230.
Russell, J.B. and Houlihan, A.J. (2003). Ionophore resistance of ruminal bacteria and its potential impact on human health. FEMS Microbiology Reviews, 27(1): 65-74.
Sallam, S.M.A., Bueno, I.C.S., Brigide, P., Godoy, P.B., Vittii, D.M.S.S. and Abdalla, A.L. (2009). Efficiency of eucalyptus oil on in vitro ruminal fermentation and methane production. Nutritional and Foraging Ecology of Sheep and Goats, 85(1): 267-272.
SAS Institute INC. (2002). Sas user’s Guide: statistics. Statistical Analysis Systems Institute Inc. Cary NC.
Szumacher-Strabel, M., Cieslak, A. and Nowakowska, A. (2009.) Effect of oils rich in linoleic acid on in vitro rumen fermentation parameters of sheep, goats and dairy cows. Journal of Animal and Feed Sciences, 18(3): 440-452.
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 feed. Animal Feed Science and Technology, 48(3-4): 185-197.
Van Nevel, C.J., Prins, R.A. and Demeyer. D.I. (1974). On the inverse relationship between methane and propionate in the rumen. Zeitschrift fur Tierphysiologie, 33(3): 117-125.
Vercoe, E.P., Makkar, H.P.S. and Schlink, A.C. (2010). In vitro screening of plant resources for extra nutritional attributes in ruminants: nuclear and related methodologies. In: In vitro screening of feed resources for efficiency of microbial protein synthesis. Makkar, H.P.S. editor. USA: New York, Springer, pp: 107-144.
Wanapat, M., Cherdthong, A., Pardee, P. and Wanapat, S. (2008). Manipulation of rumen ecology by dietary lemongrass (Cymbopogon citrates Stapf.) powder supplementation. Journal of Animal Science, 86(12): 3497-3503.
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Agarwal, N., Shekhar, C., Kumar, R., Chaudhary, L.C. and Kamra, D.N. (2009) Effect of peppermint (Mentha piperita) oil on in vitro methanogenesis and fermentation of feed with buffalo rumen liquor. Animal Feed Science and Technology, 148(2-4): 321-327.
AOAC. (1999). Official Methods of Analysis. 16th ed., Association of Official Analytical Chemists, Washington DC, USA.
Barnett, A.J.G. and Reid, R. (1957). Studies on the production of volatile fatty acids from grass in artificial rumen. 1. Volatile fatty acids production from fresh grasses. The Journal of Agricultural Science (Cambridge), 48(3): 315-321.
Barre, D.E. and Holub, B.J. (1992). The effect of borage oil consumption on the composition of individual phospholipids in human platelets. Lipids, 27(5): 315-20.
Blummel, M., Karsli, A. and Russel, J.R. (2003). Influence of diet on growth yields of rumen microorganisms in vitro and in vivo: Influence on growth yields of variable carbon fluxes to fermentation products. British Journal of Nutrition, 90(3): 625-634.
Busquet, M., Calsamiglia, S., Ferret, A. and Kamel, C. (2006). Plant extracts affect in vitro rumen microbial fermentation. Journal of Dairy Science, 89(2): 761-771.
Calsamiglia, S., Busquet, M., Cardozo, P.W., Castillejos, L. and Ferret, A. (2007). Essential oils as modifiers of rumen microbial fermentation. Journal of Dairy Science, 90(6): 2580-2595.
Cardozo, P.W., Calsamiglia, S., Ferret, A. and Kamel, C. (2005). Screening for the effects of natural plant extracts at two pH level on in vitro rumen microbial fermentation of a high-concentrate diet for beef cattle. Journal of Animal Science, 83(11): 2572-2579.
Castillejos, L., Calsamiglia, S. and Ferret, A. (2006). Effect of essential oils active compounds on rumen microbial fermentation and nutrient flow in in vitro systems. Journal of Dairy Science, 89(7): 2649-2658.
Castillejos, L., Calsamiglia, S., Martin-Tereso, J. and Ter Wijlen, H. (2008). In vitro evaluation of effects of ten essential oils at three doses on ruminal fermentation of high concentrate feedlot-type diets. Animal Feed Science and Technology, 145(1-4): 259-270.
Conner, D.E. (1993). Naturally occurring compounds. In: Antimicrobials in Foods. Davidson, P.M. and Branen, A.L. editors. 2th ed., USA: New York, Marcel Dekker, pp: 441-468.
Dehority, B.A. (2003). Rumen Microbiology. England: Nottingham University Press, pp: 372.
Demeyer, D. and Van Nevel, C. (1995). Transformations and effects of lipids in the rumen: Three decades of research at Gent University. Archives of Animal Nutrition, 48(1-2): 119-134.
Doreau, M. and Chilliard, Y. (1997). Digestion and metabolism of dietary fat in farm animals. British Journal of Nutrition, 78(1): S15-S35.
Doreau, M., Legay, F. and Bauchart, D. (1991). Effect of source and level of supplemental fat on total and ruminal organic matter and nitrogen digestion in dairy cows. Journal of Dairy Science, 74(7): 2233-2242.
Duke, J.A. (2000). Handbook of phytochemical constituents of grass herbs and other economic plants. 2nd ed., London: CRC Press, pp: 680.
Fievez, V., Babaymo, O.J. and Demeyer, D. (2005). Estimation of direct and indirect gas production in syringes: A tool to estimate short chain fatty acid production that requires minimal laboratory facilities. Animal Feed Science and Technology, 123-124(1): 197-210.
Francis, G., Kerem, Z., Makkar, H.P.S. and Becker, K. (2002). The biological action of saponins in animal systems: reviews. British Journal of Nutrition, 88(6): 587-605.
Getachew, G., Robinson, P.H., DePeters, E.J. and Taylor, S.J. (2004). Relationships between chemical composition, dry matter degradation and in vitro gas production of several ruminant feeds. Animal Feed Science and Technology, 111(1-4): 57-71.
Guarrera, P.M., Salerno, G. and Caneva, G. (2006). Food, flavouring and feed plant traditions in the Tyrrhenian sector of Basilicata. Journal of Ethnobiology and Ethnomedicine, 37(2): 1-6.
Gudej, J. and Tomczyk, M. (1996). Badania chromatograficzne zwiazkow polifenolowych w zielu Borago officinalis L. Herba Polonica, 42(4): 252-256.
Hegarty, R.S. (1999). Reducing rumen methane emission through elimination of protozoa. Australian Journal of Agricultural Research, 50(8): 1321-1327.
Hess, H.D., Kreuzer, M., Diaz, T.E., Lascano, C.E., Carulla, J.E. and Solvia, C.R. (2003). Saponin rich tropical fruits affect fermentation and methanogenesis in faunated and defaunated fluid. Animal Feed Science and Technology, 109(1-4): 79-94.
Hristov, A.N., Kennington, L.R., McGuire, M.A. and Hunt, C.W. (2005). Effect of diets containing linoleic acid or oleic acid rich oils on ruminal fermentation and nutrient digestibility, and performance and fatty acid composition if adipose and muscle tissues of finishing cattle. Journal of Animal Science, 83(6): 1312-1321.
IPCC. (2001). Climate Change 2001: The Scientific Basis. New York: Cambridge University Press.
Jalc, D. and Ceresnakova, Z. (2002). Effect of plant oils and malate on rumen fermentation in vitro. Czech Journal of Animal Science, 47(3): 106-111.
Jalc, D., Potkanski, A., Szumacher-Strabel, M., Cieslak, A. and Certic, M. (2005). Effect of microbial oil, evening primrose oil and borage oil on rumen fermentation in vitro. Veterinary Medicine-Czech, 50(11): 480-486.
Janssen, A.M., Scheffer, J.J. and Baerheim Svendsen, A. (1987). Antimicrobial activity of essential oils: a 1976-1986 Literature review. Aspects of the test methods. Planta Medica, 53(5): 395-398.
Jenkins, T.C. (1993). Lipid metabolism in the rumen. Journal of Dairy Science, 76(12): 3851-3863.
Johnson, K.A. and Johnson, D.E. (1995). Methane emissions from cattle. Journal of Animal Science, 73(8): 2483-2492.
Jouany, J.P. and Lassalas, B. (1997). Study of the adaptation of the rumen ecosystem to the antimethanogenic effect of monensin measured in vivo. Reproduction Nutrition Development, 37(1): 69-70.
Kamra, D.N. (2005). Rumen microbial ecosystem. Current Science, 89(1): 124-135.
Keady, T.W.J. and Mayne, C.S. (1999). The effects of level of fish oil inclusion in the diet on rumen digestion and fermentation parameters in cattle offered grass silage based diets. Animal Feed Science and Technology, 81(1-2): 57-68.
Komolong, M.K., Barber, D.G. and McNeill, D.M. (2001). Post-ruminal protein supply and N retention of weaner sheep fed on a basal diet of lucerne hay (Medicago sativa) with increasing levels of quebracho tannins. Animal Feed Science and Technology, 92(1-2): 59-72.
Machmuller, A. and Kreuzer, M. (1999). Methane suppression by coconut oil and associated effects on nutrient and energy balance in sheep. Canadian Journal of Animal Science, 79(1): 65-72.
Makkar, H.P.S. (2010). In vitro screening of feed resources for efficiency of microbial protein synthesis. In: In vitro screening of plant resources for extra-nutritional attributes in ruminants, Nuclear and related methodologies. Vercoe, P.E., Makkar, H.P.S. and Schlink, A.C. editors, USA: New York, Springer, pp: 107-144.
McGuffey, R.K., Richardson, L.F. and Wilkinson, J.I.D. (2001). Ionophores for dairy cattle: current status and future outlook. Journal of Dairy Science, 84(E. Suppl.): E194-E203.
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.
Mhamdi, B., Wannes, W.A., Bourgou, S. and Marzouk, B. (2009). Biochemical characterization of borage (Borago officinalis L.) seeds. Journal of Food Biochemistry, 33(3): 331-341.
Molero, R., Ibars, A., Calsamiglia, S., Ferret, A. and Losa, R. (2004). Effects of a specific blend of essential oil compounds on dry matter and crude protein degradability in heifers fed diets with different forage to concentrate ratios. Animal Feed Science and Technology, 114(1-4): 91-104.
Morgavi, D.P., Forano, E., Martin, C. and Newbold, C.J. (2010). Microbial ecosystem and methanogenesis in ruminants. Animal, 4(7): 1024-1036.
Newbold, C.J., McIntosh, F.M., Williams, P., Losa, R. and Wallace, R.J. (2004). Effects of a specific blend of essential oil compounds on rumen fermentation. Animal Feed Science and Technology, 114(1-4): 105-112.
NRC. (2007). Nutrient requirements of small ruminants: Sheep, goats, cervids, and new world camelids. 6th ed., USA: Washington, National Academy Press, 384p.
Ørskov, E.R. and McDonald, I. (1979). The estimation of protein degradability in the rumen from incubation measurements weighted according to rate of passage. Journal of Agricultural Science, 92(2): 499-503.
Patra, A.K. and Saxena, J. (2009). A review of the effect and mode of action of saponins on microbial population and fermentation in the rumen and ruminant production. Nutrition Research Reviews, 22(2): 204-219.
Pawar, M.M., Kamra, D.N., Agarwal, N. and Chaudhary, L.C. (2014). Effects of essential oils on in vitro methanogenesis and feed fermentation with buffalo rumen liquor. Agricultural Research, 3(1): 67-74.
Pieszak, M., Mikolajczak, P.L. and Manikowska, K. (2012). Borage (Borago officinalis L.) - A valuable medicinal plant used in herbal medicine. Herba Polonica, 58(4): 95-103.
Ricci, D., Fraternale, D., Giamperi, L., Bucchini, A., Epifano, F., Burini, G., et al. (2005). Chemical composition, antimicrobial and antioxidant activity of the essential oil of Teucrium marum (Lamiaceae). Journal of Ethnopharmacology, 98(1-2): 195-200.
Russell, J.B. (1998). The importance of pH in the regulation of ruminal acetate to propionate ratio and methane production in vitro. Journal of Dairy Science, 81(12): 3222-3230.
Russell, J.B. and Houlihan, A.J. (2003). Ionophore resistance of ruminal bacteria and its potential impact on human health. FEMS Microbiology Reviews, 27(1): 65-74.
Sallam, S.M.A., Bueno, I.C.S., Brigide, P., Godoy, P.B., Vittii, D.M.S.S. and Abdalla, A.L. (2009). Efficiency of eucalyptus oil on in vitro ruminal fermentation and methane production. Nutritional and Foraging Ecology of Sheep and Goats, 85(1): 267-272.
SAS Institute INC. (2002). Sas user’s Guide: statistics. Statistical Analysis Systems Institute Inc. Cary NC.
Szumacher-Strabel, M., Cieslak, A. and Nowakowska, A. (2009.) Effect of oils rich in linoleic acid on in vitro rumen fermentation parameters of sheep, goats and dairy cows. Journal of Animal and Feed Sciences, 18(3): 440-452.
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 feed. Animal Feed Science and Technology, 48(3-4): 185-197.
Van Nevel, C.J., Prins, R.A. and Demeyer. D.I. (1974). On the inverse relationship between methane and propionate in the rumen. Zeitschrift fur Tierphysiologie, 33(3): 117-125.
Vercoe, E.P., Makkar, H.P.S. and Schlink, A.C. (2010). In vitro screening of plant resources for extra nutritional attributes in ruminants: nuclear and related methodologies. In: In vitro screening of feed resources for efficiency of microbial protein synthesis. Makkar, H.P.S. editor. USA: New York, Springer, pp: 107-144.
Wanapat, M., Cherdthong, A., Pardee, P. and Wanapat, S. (2008). Manipulation of rumen ecology by dietary lemongrass (Cymbopogon citrates Stapf.) powder supplementation. Journal of Animal Science, 86(12): 3497-3503.
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