The Effect of Tannins in Grape Pomace and Oak Leaf on the in vitro Organic Matter Digestibility and in situ Disappearance of Sheep

Document Type: Research Article

Authors

1 Department of Animal Science, Faculty of Agriculture, Tarbiat Modartes University, Tehran, Iran

2 Department of Animal Science, Faculty of Agriculture, Bu Ali Sina University, Hamedan, Iran

Abstract

The effect of grape pomace (Vitis vinifera) and in oak leaf (Quercus libani) tannins by three runs of in vitro gas production on the organic matter digestibility (OMD) and in situ dry matter (DM) and crude protein (CP) disappearance were studied in four sheeps. Polyethylene glycol (PEG) was used to deactivate the tannins. In vitro gas production was recorded at 2, 4, 6, 8, 12, 48, 72, 96 and 120 h of incubation. The chemical composition (g/kg DM) of grape pomace and oak leaf were 940, 940 organic matter (OM); 94, 116 crude protein (CP); 568, 515 neutral detergent fiber (NDFom); 467, 316 acid detergent fiber (ADFom); 242, 93; (lignin (sa)); 70.5, 82 total phenols (TP); 49.7, 73 total tannins (TT); 79, 5.4 condensed tannin (CT) and 40, 70 hydrolysable tannin (HT). Using grape pomace and oak leaf decreased OMD, short chain fatty acids (SCFA), insoluble but fermentable fraction (b) and fermentation rate (c) comparing to control (P<0.05). The addition of PEG increased in vitrogas production (IVGP) at all times of incubation. Kinetics of gas production, OMD and SCFA were also increased by PEG incorporation (P<0.05). The increase in gas production (%) (IGP) in grape pomace (GP) diet was higher than those in oak leaf (OL) diet. The amounts of total protozoa, Isotricha, Dasytricha, subfamily of Entodiniinae, Diplodiniinae and Ophrioscolecinae were decreased by addition of grape pomace and oak leaf. The addition of PEG increased total protozoa, subfamily of Entodiniinae, Diplodiniinae andOphrioscolecinae populations in grape pomace diet (P<0.05), but increased Isotricha, Dasytricha andsubfamily of Diplodiniinae in oak leaf diet (P<0.05). The effective degradability (ED) (g/kg DM) of DM and CP for alfalfa, grape pomace and oak leafwere (646.6, 357.7 and 362.3) and (821, 227.3 and 202), respectively based on in situ fermentation. In conclusion, using grape pomace and oak leaf have positively modified NH3-N concentration and protozoa population. Diet containing grape pomace and oak leaf had lower fermentability than the diet containing alfalfa. Supplementation of PEG in GP and OL diets improved the fermentability of these diets.

Keywords


Abarghuei M.J., Rouzbehan Y. and Alipour D. (2010). The influence of the grape pomace on the ruminal parameters of sheep. Livest. Sci. 132, 73-79.
Abarghuei M.J., Rouzbehan Y. and Alipour D. (2011). Effect of oak (Quercus libani oliv.) leave tannin on ruminal fermentation of sheep. J. Agric. Sci. Technol. 13, 1021-1032.
Abreu A., Carulla J.E., Lascano C.E., Diaz T.E., Kreuzer M. and Hess H.D. (2004). Effects of Sapindus saponaria fruits on rumen fermentation and duodenal nitrogen flow of sheep fed a tropical grass diet with and without legume. J. Anim. Sci. 82, 1392-1400.
Alipour D. and Rouzbehan Y. (2007). Effects of ensiling grape pomace and addition of polyethylene glycol on in vitro gas production and microbial biomass yield. Anim. Feed Sci. Technol. 137, 138-149.
Anele U.Y., Arigbede O.M., Südekum K.H., Oni A.O., Jolaosho A.O., Olanite J.A., Adeosun A.I., Dele P.A., Ike K.A. and Akinol O.B. (2009). Seasonal chemical composition, in vitro fermentation and in sacco dry matter degradation of four indigenous multipurpose tree species in Nigeria. Anim. Feed Sci. Technol. 154, 47-57.
AOAC. (1990). Official Methods of Analysis, 15th Edition. Association of Official Analytical Chemists,Washington, DC, USA.
Baumgärtel T., Kluth H., Epperlein K. and Rodehutscord M. (2007). A note on digestibility and energy value for sheep of different grape pomace. Small Rumin. Res. 67, 302-306.
Benchaar C., McAllister T.A. and Chouinard P.Y. (2008). Digestion, ruminal fermentation, ciliate protozoal populations, and milk production from dairy cows fed Cinnamaldehyde, quebracho condensed tannin, or Yucca schidigera saponin extract. J. Dairy Sci. 91, 4765-4777.
Ben Salem H.A., Nefzaoui L., Ben Salem A. and Tisser J.L. (2000). Deactivation of condensed tannins in Acacia cyanophylla  Lindl. Foliage by polyethylene glycol in feed blocks effect on feed intake, diet digestibility, nitrogen balance, microbial synthesis and growth by sheep. Livest. Prod. Sci. 64, 51-60.
Ben Salem H., Ben Salem I., Nefzaoui A. and Ben Said M.S. (2003). Effect of PEG and olive cake feed blocks supply on feed intake, digestion, and health of goat given kermes oak (Quercuscoccifera) foliage. Anim. Feed Sci. Technol. 110, 45-59.
Besharati M. and Taghizadeh A. (2009). Evaluation of dried grape by-product as a tanniniferous tropical feedstuff. Anim. Feed Sci. Technol. 152, 198-203.
Belanche A., De La Fuente G., Moorby J.M. and Newbold C.J. (2012). Bacterial protein degradation by different rumen protozoal groups. J. Anim. Sci. 90, 4495-4504.
Calsamiglia S., Busquet M., Cardozo P.W., Castillejos L. and Ferret A. (2007). Invited review: essential oils as modifiers of rumen microbial fermentation. J. Dairy Sci. 90, 2580-2595.
Dehority B.A. (2003). Rumen Microbiology. British Library Cataloguing in Publication Data. First published.
Duncan D.B. (1955). Multiple ranges and multiple F-test. Biometrics. 11, 1-42.
Fatahi M. (1995). The Studyof Zagros’ Oak Forests and the Most Important Factors of its Destruction. Forests and Pastures Research Institute, Tehran, Iran.
Frutos P.G., Hervas F., Giraldes J. and Mantecon A.R. (2004). An in vitro study on the ability of polyethylene glycol to inhibit the effect of quebracho tannins and tannic acid on ruminal fermentation in sheep, goats, cows and deer.Australian J. Agric. Res. 55, 1125-1132.
Getachew G., Makkar H.P.S. and Becker K. (2001). Method of polyethylene glycol application to tannin-containing browses to improve microbial fermentation and efficiency of microbial protein synthesis from tannin-containing browses. Anim. Feed Sci. Technol. 92, 51-57.
Getachew G., Makkar H.P.S. and Becker K. (2000). Effect of polyethylene glycol on in vitro degradability of nitrogen and microbial protein synthesis from tannin-rich browse and herbaceous legumes. Br. J. Nutr. 84, 73-83.
Goncalves-Alvim S.J., Collevatti R.G. and Fernandez G.W. (2004). Effects of genetic variability and habitat of Qualea parviflora (Vochysiaceae) on herbivory by free-feeding and gall-forming insects. Ann. Bot. 94, 259-268.
Goel G., Puniya A.K., Aguilar C.N. and Kishan S. (2005). Interaction of gut microflora with tannins in feeds.Naturwissenschaften. 92, 497-503.
Hristov A.N., McAllister T.A., Van Herk F.H., Cheng K.J. Newbold C.J. and Cheeke P.R. (1999). Effect of Yucca schidigera on ruminal fermentation and nutrient digestion in heifers. J. Anim. Sci. 77, 2554-2563.
Khazaal K., Boza J. and Orskov E.R. (1994). Assessment of phenolics-related anti-nutritive effects in Mediterranean browse: a comparison between the use of the in vitro gas production technique with or without insoluble polyvinyl polypyrrolidone or nylon bag. Anim. Feed Sci. Technol. 49, 133-149.
Khazaal K., Markantonatos X., Nastis A. and Ørskov E.R. (1993). Changes with maturity in fibre composition and levels of extractable polyphenols in Greek browse: effects on in vitro gas production and in sacco dry matter degradation. J. Sci. Food Agric. 63, 237-244.
Kaitho R.J., Tamminga S. and Bruchem J. (1993). Rumen degradation and in vivo digestibility of dried Calliandra calothyrsusleaf. Anim. Feed Sci. Technol. 43, 19-30.
Makkar H.P.S., Dawra R.K. and Singh B. (1991). Tannin levels in leaves of some oak species at different stages of maturity. J. Sci. Food Agric. 54, 513-519.
Makkar H.P.S. and Singh B. (1991). Effect of drying conditions on tannin, fibre and lignin levels in mature oak (Quercus incana) leaves. J. Sci. Food Agric. 54, 323-328.
Makkar H.P.S. and Singh B. (1993). Effect of storage and urea addition on detannification and in sacco dry matter digestibility of mature oak (Quercus incana) leaves. Anim. Feed Sci. Technol. 41, 247-259.
Makkar H.P.S. (2000). Quantification of Tannins in Tree Foliage. FAO/IAEA Working Document. IAEA, Vienna, Austria.
Makkar H.P.S. (2003). Effects and fate tannins in ruminant animals, adaptation to tannins, and strategies to overcome detrimental effects of feeding tannin-rich feeds.Small Rumin. Res. 49, 241-256.
Makkar H.P.S. (2004). Recent advances in the in vitro gas method for evaluation of nutritional quality of feed resources. Pp. 55-88 in Assessing Quality and Safety of Animal Feeds. FAO Animal Production and Health Series 160. FAO, Rome.
Makkar H.P.S. (2010). In vitro screening of feed resources for efficiency of microbial protein synthesis. Pp. 107-144 inin vitro Screening of Plant Resources for Extra-nutritional Attributes in Ruminants: Nuclear and Related Methodologies. P.E. Vercoe, H.P.S. Makkar and A.C. Schlink, Eds. IAEA, Dordrecht, the Netherlands.
McSweeney C.S., Palmer B., Bunch R. and Krause D.O. (2001a). Microbial interaction with tannins: nutritional consequences for ruminants. Anim. Feed Sci. Technol. 91, 83-93.
McSweeney C.S., Palmer B., Bunch R. and Krause D.O. (2001b). Effect of the tropical forage Calliandra Calothyrsus on microbial protein synthesis and ecology in the rumen. J. Appl. Microbiol. 90, 78-88.
Menke K.H. and Steingass H. (1988). Estimation of the energetic feed value obtained from chemical analysis and gas production using rumen fluid. Anim. Res. Dev. 28, 7-55.
Min B.R., Attwood G.T., Reilly K., Sun W., Peters J.S., Barry T.N. and McNabb W.C. (2002). Lotus corniculatus condensed tannins decrease in vivo populations of proteolytic bacteria and affect nitrogen metabolism in the rumen of sheep. Canadian J. Microbiol. 48, 911-921.
Min B.R., PinchakW.E., Fulford J.D. and Puchala R. (2005). Effect of feed additives on in vitro and in vivo rumen characteristics and frothy bloat dynamics in steers grazing wheat pasture. Anim. Feed Sci. Technol. 123, 615-629.
Molan A.L., Attwood G.T., Min B.R. and McNabb W.C. (2001). The effect of condensed tannins from Lotus pedunculatus and Lotus corniculatus on the growth of proteolytic rumen bacteria in vitro and their possible mode of action. Canadian J. Microbiol. 47, 626-633.
Moujahed N., Kayouli C., Thewis A., Beckers Y. and Rezgui S. (2000). Effects of multinutrient blocks and polyethylene glycol 4000 supplies on intake and digestion by sheep fed Acacia cyanophylla Lindl. Foliage-based diets. Anim. Feed Sci. Technol. 88, 219-238.
Ørskov E.R. and McDonald P. (1979). The estimation of protein digestibility in the rumen from incubation measurements weighed according to rate of passage. J. Agric. Sci. Camb. 92, 499-503.
Patra A.K. and Saxena J. (2011). Exploitation of dietary tannins to improve rumen metabolism and ruminant nutrition. J. Sci. Food Agric. 91, 24-37.
Reed J.D. (1995). Nutritional toxicology of tannins and related polyphenols in forage legumes. J. Anim. Sci. 73, 1516-1528.
Robertson J.B. and Van Soest P.J. (1981). The detergent system of analysis. Pp. 123-124 in The Analysis of Dietary Fibre in Food. W.P.T. James and O. Theander, Eds. Marcel Dekker, New York, NY, USA, Basel, Switzerland.
Singh B., Sahoo A., Sharma R. and Bhat T.K. (2005). Effect of polyethylene glycol on gas production parameters and nitrogen disappearance of some tree forages. Anim. Feed Sci. Technol. 124, 351-364.
Salawu M.B., Acamovic T., Stewart C.S. and Maasdorp B. (1997). Assesment of the nutritive value of Calliandra calothyrsus: its chemical composition and the influence of tannins, pipecolic acid and polyethylene glycol on in vitroorganic matter digestibility. Anim. Feed Sci. Technol. 69, 207-217.
Spanghero M., Salem A.Z.M. and Robinson P.H. (2009). Chemical composition, including secondary metabolites and rumen fermentability of seeds and pulp of Californian (USA) and Italian grape pomaces. Anim. Feed Sci. Technol. 152, 243-255.
SASInstitute. (2001). Users Guide: Statistics, Version 8.2. SAS Institue, Carry, NC, USA.
Van Soest P.J., Robertson J.B. and Lewis B.A. (1991). Methods for dietary fibre, neutral detergent fibre and non-starch carbohydrate in relation to animal nutrition. J. Dairy Sci. 74, 3583-3597.
Van SoestP.J. (1994). Nutritional Ecology of the Ruminant. Cornell University Press, Ithaca, NY, USA.
Vitti D.M.S.S., Abdalla A.L., Bueno I.C.S., Silva Filhob J.C., Costa C., Bueno M.S., Nozella E.F., Longo C., Vieira E.Q., Cabral Filho S.L.S., Godoy P.B. and Mueller-Harvey I. (2005). Do all tannins have similar nutritional effects? A comparison of three Brazilian fodder legumes. Anim. Feed Sci. Technol. 119, 345-361.
Waghorn G.C., Ulyatt M.J., John A. and Fisher M. (1987). The effect of condensed tannins on the site of digestion of amino acids and other nutrients in sheep fed on Lotus corniculatus. Br. J. Nutr. 57, 115-126.
Wallace R.J., McEwan N.R., McIntosh F.M., Teferedegne B. and Newbold C.J. (2002). Natural products as manipulators of rumen fermentation. Asian-Australas J. Anim. Sci. 15, 1458-1468.
Williams A.G. and Coleman G.S. (1991). The Rumen Protozoa. Springer-Verlag New York Inc., New York.
Yildiz S., Kaya I., Unal Y., AksuElmali D., Kaya S., Censiz M., Kaya M. and Oncuer A. (2005). Digestion and body weight change in Tuj lambs receiving oak (Quercus hartwissiana) leaves with and without PEG. Anim. Feed Sci. Technol. 122,159-172.
Yousef Elahi M. and Rouzbehan Y. (2008). Characterization of Quercuc persica, Quercus infectoria, Quercus libani as ruminant feeds. Anim. Feed Sci. Technol. 140, 78-89
 
Abarghuei M.J., Rouzbehan Y. and Alipour D. (2010). The influence of the grape pomace on the ruminal parameters of sheep. Livest. Sci. 132, 73-79.
Abarghuei M.J., Rouzbehan Y. and Alipour D. (2011). Effect of oak (Quercus libani oliv.) leave tannin on ruminal fermentation of sheep. J. Agric. Sci. Technol. 13, 1021-1032.
Abreu A., Carulla J.E., Lascano C.E., Diaz T.E., Kreuzer M. and Hess H.D. (2004). Effects of Sapindus saponaria fruits on rumen fermentation and duodenal nitrogen flow of sheep fed a tropical grass diet with and without legume. J. Anim. Sci. 82, 1392-1400.
Alipour D. and Rouzbehan Y. (2007). Effects of ensiling grape pomace and addition of polyethylene glycol on in vitro gas production and microbial biomass yield. Anim. Feed Sci. Technol. 137, 138-149.
Anele U.Y., Arigbede O.M., Südekum K.H., Oni A.O., Jolaosho A.O., Olanite J.A., Adeosun A.I., Dele P.A., Ike K.A. and Akinol O.B. (2009). Seasonal chemical composition, in vitro fermentation and in sacco dry matter degradation of four indigenous multipurpose tree species in Nigeria. Anim. Feed Sci. Technol. 154, 47-57.
AOAC. (1990). Official Methods of Analysis, 15th Edition. Association of Official Analytical Chemists,Washington, DC, USA.
Baumgärtel T., Kluth H., Epperlein K. and Rodehutscord M. (2007). A note on digestibility and energy value for sheep of different grape pomace. Small Rumin. Res. 67, 302-306.
Benchaar C., McAllister T.A. and Chouinard P.Y. (2008). Digestion, ruminal fermentation, ciliate protozoal populations, and milk production from dairy cows fed Cinnamaldehyde, quebracho condensed tannin, or Yucca schidigera saponin extract. J. Dairy Sci. 91, 4765-4777.
Ben Salem H.A., Nefzaoui L., Ben Salem A. and Tisser J.L. (2000). Deactivation of condensed tannins in Acacia cyanophylla  Lindl. Foliage by polyethylene glycol in feed blocks effect on feed intake, diet digestibility, nitrogen balance, microbial synthesis and growth by sheep. Livest. Prod. Sci. 64, 51-60.
Ben Salem H., Ben Salem I., Nefzaoui A. and Ben Said M.S. (2003). Effect of PEG and olive cake feed blocks supply on feed intake, digestion, and health of goat given kermes oak (Quercuscoccifera) foliage. Anim. Feed Sci. Technol. 110, 45-59.
Besharati M. and Taghizadeh A. (2009). Evaluation of dried grape by-product as a tanniniferous tropical feedstuff. Anim. Feed Sci. Technol. 152, 198-203.
Belanche A., De La Fuente G., Moorby J.M. and Newbold C.J. (2012). Bacterial protein degradation by different rumen protozoal groups. J. Anim. Sci. 90, 4495-4504.
Calsamiglia S., Busquet M., Cardozo P.W., Castillejos L. and Ferret A. (2007). Invited review: essential oils as modifiers of rumen microbial fermentation. J. Dairy Sci. 90, 2580-2595.
Dehority B.A. (2003). Rumen Microbiology. British Library Cataloguing in Publication Data. First published.
Duncan D.B. (1955). Multiple ranges and multiple F-test. Biometrics. 11, 1-42.
Fatahi M. (1995). The Studyof Zagros’ Oak Forests and the Most Important Factors of its Destruction. Forests and Pastures Research Institute, Tehran, Iran.
Frutos P.G., Hervas F., Giraldes J. and Mantecon A.R. (2004). An in vitro study on the ability of polyethylene glycol to inhibit the effect of quebracho tannins and tannic acid on ruminal fermentation in sheep, goats, cows and deer.Australian J. Agric. Res. 55, 1125-1132.
Getachew G., Makkar H.P.S. and Becker K. (2001). Method of polyethylene glycol application to tannin-containing browses to improve microbial fermentation and efficiency of microbial protein synthesis from tannin-containing browses. Anim. Feed Sci. Technol. 92, 51-57.
Getachew G., Makkar H.P.S. and Becker K. (2000). Effect of polyethylene glycol on in vitro degradability of nitrogen and microbial protein synthesis from tannin-rich browse and herbaceous legumes. Br. J. Nutr. 84, 73-83.
Goncalves-Alvim S.J., Collevatti R.G. and Fernandez G.W. (2004). Effects of genetic variability and habitat of Qualea parviflora (Vochysiaceae) on herbivory by free-feeding and gall-forming insects. Ann. Bot. 94, 259-268.
Goel G., Puniya A.K., Aguilar C.N. and Kishan S. (2005). Interaction of gut microflora with tannins in feeds.Naturwissenschaften. 92, 497-503.
Hristov A.N., McAllister T.A., Van Herk F.H., Cheng K.J. Newbold C.J. and Cheeke P.R. (1999). Effect of Yucca schidigera on ruminal fermentation and nutrient digestion in heifers. J. Anim. Sci. 77, 2554-2563.
Khazaal K., Boza J. and Orskov E.R. (1994). Assessment of phenolics-related anti-nutritive effects in Mediterranean browse: a comparison between the use of the in vitro gas production technique with or without insoluble polyvinyl polypyrrolidone or nylon bag. Anim. Feed Sci. Technol. 49, 133-149.
Khazaal K., Markantonatos X., Nastis A. and Ørskov E.R. (1993). Changes with maturity in fibre composition and levels of extractable polyphenols in Greek browse: effects on in vitro gas production and in sacco dry matter degradation. J. Sci. Food Agric. 63, 237-244.
Kaitho R.J., Tamminga S. and Bruchem J. (1993). Rumen degradation and in vivo digestibility of dried Calliandra calothyrsusleaf. Anim. Feed Sci. Technol. 43, 19-30.
Makkar H.P.S., Dawra R.K. and Singh B. (1991). Tannin levels in leaves of some oak species at different stages of maturity. J. Sci. Food Agric. 54, 513-519.
Makkar H.P.S. and Singh B. (1991). Effect of drying conditions on tannin, fibre and lignin levels in mature oak (Quercus incana) leaves. J. Sci. Food Agric. 54, 323-328.
Makkar H.P.S. and Singh B. (1993). Effect of storage and urea addition on detannification and in sacco dry matter digestibility of mature oak (Quercus incana) leaves. Anim. Feed Sci. Technol. 41, 247-259.
Makkar H.P.S. (2000). Quantification of Tannins in Tree Foliage. FAO/IAEA Working Document. IAEA, Vienna, Austria.
Makkar H.P.S. (2003). Effects and fate tannins in ruminant animals, adaptation to tannins, and strategies to overcome detrimental effects of feeding tannin-rich feeds.Small Rumin. Res. 49, 241-256.
Makkar H.P.S. (2004). Recent advances in the in vitro gas method for evaluation of nutritional quality of feed resources. Pp. 55-88 in Assessing Quality and Safety of Animal Feeds. FAO Animal Production and Health Series 160. FAO, Rome.
Makkar H.P.S. (2010). In vitro screening of feed resources for efficiency of microbial protein synthesis. Pp. 107-144 inin vitro Screening of Plant Resources for Extra-nutritional Attributes in Ruminants: Nuclear and Related Methodologies. P.E. Vercoe, H.P.S. Makkar and A.C. Schlink, Eds. IAEA, Dordrecht, the Netherlands.
McSweeney C.S., Palmer B., Bunch R. and Krause D.O. (2001a). Microbial interaction with tannins: nutritional consequences for ruminants. Anim. Feed Sci. Technol. 91, 83-93.
McSweeney C.S., Palmer B., Bunch R. and Krause D.O. (2001b). Effect of the tropical forage Calliandra Calothyrsus on microbial protein synthesis and ecology in the rumen. J. Appl. Microbiol. 90, 78-88.
Menke K.H. and Steingass H. (1988). Estimation of the energetic feed value obtained from chemical analysis and gas production using rumen fluid. Anim. Res. Dev. 28, 7-55.
Min B.R., Attwood G.T., Reilly K., Sun W., Peters J.S., Barry T.N. and McNabb W.C. (2002). Lotus corniculatus condensed tannins decrease in vivo populations of proteolytic bacteria and affect nitrogen metabolism in the rumen of sheep. Canadian J. Microbiol. 48, 911-921.
Min B.R., PinchakW.E., Fulford J.D. and Puchala R. (2005). Effect of feed additives on in vitro and in vivo rumen characteristics and frothy bloat dynamics in steers grazing wheat pasture. Anim. Feed Sci. Technol. 123, 615-629.
Molan A.L., Attwood G.T., Min B.R. and McNabb W.C. (2001). The effect of condensed tannins from Lotus pedunculatus and Lotus corniculatus on the growth of proteolytic rumen bacteria in vitro and their possible mode of action. Canadian J. Microbiol. 47, 626-633.
Moujahed N., Kayouli C., Thewis A., Beckers Y. and Rezgui S. (2000). Effects of multinutrient blocks and polyethylene glycol 4000 supplies on intake and digestion by sheep fed Acacia cyanophylla Lindl. Foliage-based diets. Anim. Feed Sci. Technol. 88, 219-238.
Ørskov E.R. and McDonald P. (1979). The estimation of protein digestibility in the rumen from incubation measurements weighed according to rate of passage. J. Agric. Sci. Camb. 92, 499-503.
Patra A.K. and Saxena J. (2011). Exploitation of dietary tannins to improve rumen metabolism and ruminant nutrition. J. Sci. Food Agric. 91, 24-37.
Reed J.D. (1995). Nutritional toxicology of tannins and related polyphenols in forage legumes. J. Anim. Sci. 73, 1516-1528.
Robertson J.B. and Van Soest P.J. (1981). The detergent system of analysis. Pp. 123-124 in The Analysis of Dietary Fibre in Food. W.P.T. James and O. Theander, Eds. Marcel Dekker, New York, NY, USA, Basel, Switzerland.
Singh B., Sahoo A., Sharma R. and Bhat T.K. (2005). Effect of polyethylene glycol on gas production parameters and nitrogen disappearance of some tree forages. Anim. Feed Sci. Technol. 124, 351-364.
Salawu M.B., Acamovic T., Stewart C.S. and Maasdorp B. (1997). Assesment of the nutritive value of Calliandra calothyrsus: its chemical composition and the influence of tannins, pipecolic acid and polyethylene glycol on in vitroorganic matter digestibility. Anim. Feed Sci. Technol. 69, 207-217.
Spanghero M., Salem A.Z.M. and Robinson P.H. (2009). Chemical composition, including secondary metabolites and rumen fermentability of seeds and pulp of Californian (USA) and Italian grape pomaces. Anim. Feed Sci. Technol. 152, 243-255.
SASInstitute. (2001). Users Guide: Statistics, Version 8.2. SAS Institue, Carry, NC, USA.
Van Soest P.J., Robertson J.B. and Lewis B.A. (1991). Methods for dietary fibre, neutral detergent fibre and non-starch carbohydrate in relation to animal nutrition. J. Dairy Sci. 74, 3583-3597.
Van SoestP.J. (1994). Nutritional Ecology of the Ruminant. Cornell University Press, Ithaca, NY, USA.
Vitti D.M.S.S., Abdalla A.L., Bueno I.C.S., Silva Filhob J.C., Costa C., Bueno M.S., Nozella E.F., Longo C., Vieira E.Q., Cabral Filho S.L.S., Godoy P.B. and Mueller-Harvey I. (2005). Do all tannins have similar nutritional effects? A comparison of three Brazilian fodder legumes. Anim. Feed Sci. Technol. 119, 345-361.
Waghorn G.C., Ulyatt M.J., John A. and Fisher M. (1987). The effect of condensed tannins on the site of digestion of amino acids and other nutrients in sheep fed on Lotus corniculatus. Br. J. Nutr. 57, 115-126.
Wallace R.J., McEwan N.R., McIntosh F.M., Teferedegne B. and Newbold C.J. (2002). Natural products as manipulators of rumen fermentation. Asian-Australas J. Anim. Sci. 15, 1458-1468.
Williams A.G. and Coleman G.S. (1991). The Rumen Protozoa. Springer-Verlag New York Inc., New York.
Yildiz S., Kaya I., Unal Y., AksuElmali D., Kaya S., Censiz M., Kaya M. and Oncuer A. (2005). Digestion and body weight change in Tuj lambs receiving oak (Quercus hartwissiana) leaves with and without PEG. Anim. Feed Sci. Technol. 122,159-172.
Yousef Elahi M. and Rouzbehan Y. (2008). Characterization of Quercuc persica, Quercus infectoria, Quercus libani as ruminant feeds. Anim. Feed Sci. Technol. 140, 78-89