Comparative Evaluation of Enzymatic Crude Protein Degradation in Selected Legume Forages

Authors

DOI:

https://doi.org/10.24925/turjaf.v12i10.1762-1771.7016

Keywords:

Alfalfa, Sainfoin, Common vetch, Streptomyces griseus protease, Protein degradation

Abstract

For protein evaluation of feedstuffs for ruminants, the Streptomyces griseus protease test offers a purely enzymatic approach to estimate ruminal protein degradation. This study was conducted to determine the enzymatic crude protein (CP) degradability of alfalfa, sainfoin, and common vetch hays, which are commonly used in ruminant nutrition. To estimate CP degradation, fifteen samples from each type of hay were incubated in vitro with a commercial protease extracted from Streptomyces griseus. The incubation was carried out for 1, 4, 24, and 48 hours in a borate-phosphate buffer at pH 8. Significant differences in CP degradability values were found among all three types of hay across all incubation periods. For all incubation periods, sainfoin had the lowest CP degradability values (P < 0.05), due to its high content of cell wall components and condensed tannins (CTs). For incubation periods longer than 1 hour, common vetch had the highest CP degradability values, followed by alfalfa and sainfoin, respectively (P < 0.05). As a result, the use of the protease enzyme extracted from Streptomyces griseus was confirmed as an effective method for estimating the CP degradability of selected legume forages in the laboratory, eliminating the need for animal testing. However, since plant proteins are often embedded within carbohydrate complexes, it is recommended that future tests consider the combined use of protease and carbohydrase, particularly for sainfoin, which is rich in cell wall components and condensed tannins.

References

Abdelgadir, I. E. O., Cochran, R. C., Titgemeyer, E. C., & Vanzant, E. S. (1997). In vitro determination of ruminal protein degradability of alfalfa and prairie hay via a commercial protease in the presence or absence of cellulase or driselase. Journal of Animal Science, 75(8), 2215-2222. https://doi.org/10.2527/1997.7582215x

Alzueta, C., Rebolé, A., Barro, C., Treviño, J., & Caballero, R. (1995). Changes in nitrogen and carbohydrate fractions associated with the field drying of vetch (Vicia sativa L.). Animal Feed Science and Technology, 52(3-4), 249-255. https://doi.org/10.1016/0377-8401(94)00727-Q

Antoniewicz, A.M., & Kosmala, I. (1998). Use of in vitro digestion by protease from Streptomyces griseus, ficin or pancreatin for the estimation of ruminal effective degradability of dried lucerne forage. In: In vitro techniques for measuring nutrient supply to ruminants, British Society of Animal Science (pp. 118-119). https://doi.org/10.1017/S0263967X00032377

AOAC. (2003). Official methods of analysis of the association of official’s analytical chemists, 17th edn. Association of official analytical chemists, Arlington, Virginia.

Arieli, A., Shahar, K., Mabjeesh, S. J., Zamwel, S., & Sklan, D. (1999). Estimation of the digestible energy of ruminant feedstuffs by the combined bag technique. Journal of Dairy Science, 82(3), 566-573. https://doi.org/10.3168/jds.S0022-0302(99)75268-9

Aufrère, J. (1999). Estimation of in situ degradability of feed proteins in the rumen by a laboratory method using a protease. In: Tisserand J.-L. (ed.). Evaluation of the Nutritive Value of Mediterranean Roughages (pp. 73-78), Zaragoza : CIHEAM.

Aufrère, J., & Cartailler, D. (1988). Mise au point d’une méthode de laboratoire de révision de la dégradabilité des protéines alimentaires des aliments concentrés dans le rumen. Annales de Zootechnie, 37(4), 255-270.

Aufrère, J., Dudilieu, M., & Poncet, C. (2008). In vivo and in situ measurements of the digestive characteristics of sainfoin in comparison with lucerne fed to sheep as fresh forages at two growth stages and as hay. Animal, 2(9), 1331–1339. https://doi.org/10.1017/S1751731108002450

Aufrère, J., Graviou, D., Demarquilly, C., Verite, R., Michalet-Doreau, B., & Chapoutot, P. (1991). Predicting in situ degradability of feed proteins in the rumen by two laboratory methods (solubility and enzymatic degradation). Animal Feed Science and Technology, 33(1-2), 97-116. https://doi.org/10.1016/0377-8401(91)90049-X

Barry, T. N., & McNabb, W. C. (1999). The implications of condensed tannins on the nutritive value of temperate forages fed to ruminants. British Journal of Nutrition, 81(4), 263-272. https://doi.org/10.1017/S0007114599000501

Berard, N. C., Wang, Y., Wittenberg, K. M., Krause, D. O., Coulman, B. E., McAllister, T. A., & Ominski, K. H. (2011). Condensed tannin concentrations found in vegetative and mature forage legumes grown in western Canada. Canadian Journal of Plant Science, 91(4), 669-675. https://doi.org/10.4141/cjps10153

Broderick, G. A., & Albrecht, K. A. (1997). Ruminal in vitro degradation of protein in tannin‐free and tannin‐containing forage legume species. Crop Science, 37(6), 1884-1891. https://doi.org/10.2135/cropsci1997.0011183X003700060037x

Butkutė, B., Benetis, R., Padarauskas, A., Cesevičienė, J., Dagilytė, A., Taujenis, L., & Lemežienė, N. (2017). Young herbaceous legumes-a natural reserve of bioactive compounds and antioxidants for healthy food and supplements. Journal of Applied Botany & Food Quality, 90, 346–353. https://doi.org/10.5073/JABFQ.2017.090.043

Buxton, D. R. (1989). In vitro digestion kinetics of temperate perennial forage legume and grass stems. Crop Science, 29(1), 213-219. https://doi.org/10.2135/cropsci1989.0011183X002900010046x

Cassida, K. A., Griffin, T. S., Rodriguez, J., Patching, S. C., Hesterman, O. B., & Rust, S. R. (2000). Protein degradability and forage quality in maturing alfalfa, red clover, and birdsfoot trefoil. Crop Science, 40(1), 209-215. https://doi.org/10.2135/cropsci2000.401209x

Castillo, C., & Hernández, J. (2021). Ruminal fistulation and cannulation: a necessary procedure for the advancement of biotechnological research in ruminants. Animals, 11(7), 1870. https://doi.org/10.3390/ani11071870

Cherney, D. J. R., Volenec, J. J., & Cherney, J. H. (1992). Protein solubility and degradation in vitro as influenced by buffer and maturity of alfalfa. Animal Feed Science And Technology, 37(1-2), 9-20. https://doi.org/10.1016/0377-8401(92)90116-N

Coblentz, W.K., Abdelgadir, I.E.O., Cochran, R.C., Fritz, J.O., Fick, W.H., Olson, K.C., & Turner, J.E. (1999). Degradability of forage proteins by in situ and in vitro enzymatic methods. Journal of Dairy Science, 82(2), 343-354. https://doi.org/10.3168/jds.S0022-0302(99)75241-0

Coblentz, W. K., Fritz, J. O., Cochran, R. C., Rooney, W. L., & Bolsen, K. K. (1997). Protein degradation in response to spontaneous heating in alfalfa hay by in situ and ficin methods. Journal of Dairy Science, 80(4), 700-713. https://doi.org/10.3168/jds.S0022-0302(97)75989-7

Coblentz, W. K., & Grabber, J. H. (2013). In situ protein degradation of alfalfa and birdsfoot trefoil hays and silages as influenced by condensed tannin concentration. Journal of Dairy Science, 96(5), 3120–3137. https://doi.org/10.3168/jds.2012-6098

Colombatto, D., Mould, F. L., Bhat, M. K., & Owen, E. (2007). Influence of exogenous fibrolytic enzyme level and incubation pH on the in vitro ruminal fermentation of alfalfa stems. Animal Feed Science and Technology, 137(1-2), 150-162. https://doi.org/10.1016/j.anifeedsci.2006.10.001

Cone, J. W., Gelder, A. H. V., Steg, A., & Vuuren, A. M. V. (1996). Prediction of in situ rumen escape protein from in vitro incubation with protease from Streptomyces griseus. Journal of the Science of Food and Agriculture, 72(1), 120-126. https://doi.org/10.1002/(SICI)1097-0010(199609)72:1<120: AID-JSFA630>3.0.CO;2-3

Cone, J. W., Gelder, A. H. V., Mathijssen-Kamman, A. A., & Hindle, V. A. (2004). Rumen escape protein in grass and grass silage determined with a nylon bag and an enzymatic technique. Animal Feed Science and Technology, 111, 1-9. https://doi.org/10.1016/j.anifeedsci.2003.08.004

Curzer, H. J., Perry, G., Wallace, M. C., & Perry, D. (2016). The three Rs of animal research: what they mean for the institutional animal care and use committee and why. Science and Engineering Ethics, 22, 549-565. https://doi.org/10.1007/s11948-015-9659-8

Delgado, I., Muñoz, F., & Andueza, D. (2014). Evaluation of the competition between alfalfa and sainfoin sown in mixture. In: Baumont, R., Carrère, P., Jouven, M., Lombardi, G., López-Francos, A., Martin, B., Peeters, A., Porqueddu, C. (Eds.) Joint Meeting of the “Mountain Pastures, Mediterranean Forage Resources (pp. 139–142), Zaragoza: CIHEAM / INRA / FAO.

Du, W., Hou, F., Tsunekawa, A., Kobayashi, N., Ichinohe, T., & Peng, F. (2019). Effects of the diet inclusion of common vetch hay versus alfalfa hay on the body weight gain, nitrogen utilization efficiency, energy balance, and enteric methane emissions of crossbred Simmental cattle. Animals, 9(11), 983. https://doi.org/10.3390/ani9110983

Edmunds, B., Südekum, K. H., Spiekers, H., & Schwarz, F. J. (2012). Estimating ruminal crude protein degradation of forages using in situ and in vitro techniques. Animal feed science and technology, 175(3-4), 95-105. https://doi.org/10.1016/J.ANIFEEDSCI.2012.04.003

Faría-Mármol, J., González, J., Rodríguez, C.A., & Alvir, M.R. (2002). Effect of diet forage to concentrate ratio on rumen degradability and post-ruminal availability of protein from fresh and dried lucerne. Animal Science 74, 337-345. https://doi.org/10.1017/S1357729800052498

Gea, A., Stringano, E., Brown, R. H., & Mueller-Harvey, I. (2011). In situ analysis and structural elucidation of sainfoin (Onobrychis viciifolia) tannins for high-throughput germplasm screening. Journal of Agricultural and Food Chemistry, 59(2), 495-503. https://doi.org/10.1021/jf103609p

Getachew, G., Pittroff, W., DePeters, E. J., Putnam, D. H., Dandekar, A., & Goyal, S. (2008). Influence of tannic acid application on alfalfa hay: in vitro rumen fermentation, serum metabolites and nitrogen balance in sheep. Animal, 2(3), 381-390. https://doi.org/10.1017/S1751731107001486

Gonzales, G., Smagghe, G., Grootaert, C., Zotti, M., Raes, K., & Camp, J. (2015). Flavonoid interactions during digestion, absorption, distribution and metabolism: a sequential structure–activity/property relationship-based approach in the study of bioavailability and bioactivity. Drug Metabolism Reviews, 47, 175 - 190. https://doi.org/10.3109/03602532.2014.1003649

González, J., Ouarti, M., Rodríguez, C. A., & Alvir, M. R. (2006). Effects of considering the rate of comminution of particles and microbial contamination on accuracy of in situ studies of feed protein degradability in ruminants. Animal Feed Science and Technology, 125(1-2), 89-98. https://doi.org/10.1016/j.anifeedsci.2005.05.013

Haj Ayed, M., González, J., Caballero, R., & Alvir, M. R. (2001). Effects of maturity on nutritive value of field-cured hays from common vetch and hairy vetch. Animal Research, 50(1), 31-42. https://doi.org/10.1051/animres:2001103

Hristov, A. N., Bannink, A., Crompton, L. A., Huhtanen, P., Kreuzer, M., McGee, M., & Yu, Z. (2019). Invited review: Nitrogen in ruminant nutrition: A review of measurement techniques. Journal of Dairy Science, 102(7), 5811-5852. https://doi.org/10.3168/jds.2018-15829

Hvelplund, T., Weisbjerg, M.R., (2000). In situ techniques for the estimation of protein degradability and postrumen availability. In: Givens, D.I., Owen, E., Axford, R.F.E., Omed, H.M. (Eds.), Forage Evaluation in Ruminant Nutrition. CAB International, Wallingford, UK, 233–258. https://doi.org/10.1079/9780851993447.00

Inal, F., Tamkoc, A., Alatas, M. S., Kahraman, O., Ozbilgin, A., & Coskun, B. (2018). Determination of protein degradability of alfalfa hay via buffer or protease. Italian Journal of Animal Science, 17(2), 353-358. https://doi.org/10.1080/1828051X.2017.1364986

Janicki, F. J., & Stallings, C. C. (1988). Degradation of crude protein in forages determined by in vitro and in situ procedures. Journal of Dairy Science, 71(9), 2440-2448. https://doi.org/10.3168/jds.S0022-0302(88)79829-X

Julier, B., Guines, F., Emile, J. C., & Huyghe, C. (2003). Variation in protein degradability in dried forage legumes. Animal Research, 52(5), 401-412. https://doi.org/10.1051/animres:2003029

Jung, H. G. (1989). Forage lignins and their effects on fiber digestibility. Agronomy Journal, 81(1), 33-38. https://doi.org/10.2134/agronj1989.00021962008100010006x

Jung, H.J.G., & Dietz, D.A. (1993). Cell wall lignification and degradability. In: Jung, H.G., Buxton, D.R., Hatfield, R.D. (Eds.), Forage Cell Wall Structure and Digestibility (pp. 315–346) American Society of Agronomy, Madison, WI, USA. https://doi.org/10.2134/1993.foragecellwall.c13

Karabulut, A., Canbolat, O., Kalkan, H., Gurbuzol, F., Sucu, E., & Filya, I. (2007). Comparison of in vitro gas production, metabolizable energy, organic matter digestibility and microbial protein production of some legume hays. Asian-Australasian Journal of Animal Sciences, 20(4), 517-522. https://doi.org/10.5713/ajas.2007.517

Karlsson, L., Hetta, M., Udén, P., & Martinsson, K. (2009). New methodology for estimating rumen protein degradation using the in vitro gas production technique. Animal Feed Science and Technology, 153, 193-202. https://doi.org/10.1016/J.ANIFEEDSCI.2009.06.010

Kelln, B. M., Penner, G. B., Acharya, S. N., McAllister, T. A., & Lardner, H. A. (2020). Impact of condensed tannin-containing legumes on ruminal fermentation, nutrition, and performance in ruminants: a review. Canadian Journal of Animal Science, 101(2), 210-223. https://doi.org/10.1139/cjas-2020-0096

Khalilvandi-Behroozyar, H., Dehghan-Banadaky, M., & Rezayazdi, K. (2010). Palatability, in situ and in vitro nutritive value of dried sainfoin (Onobrychis viciifolia). The Journal of Agricultural Science, 148(6), 723-733. https://doi.org/10.1017/S0021859610000523

Kosmala, I., Antoniewicz, A., De Boever, J., Hvelplund, T., & Kowalczyk, J. (1996). Use of enzymatic solubility with ficin (EC 3.4. 22.3) to predict in situ feed protein degradability. Animal Feed Science and Technology, 59(4), 245-254. https://doi.org/10.1016/0377-8401(95)00910-8

Kraiem, K., Garrett, J. E., Meiske, J. C., Goodrich, R. D., & Marten, G. C. (1990). Influence of method of forage preservation on fibre and protein digestion in cattle given lucerne, birdsfoot trefoil and sainfoin. Animal Production, 50(2), 221-230. https://doi.org/10.1017/S0003356100004670

Kumar, R., & Singh, M. (1984). Tannins: their adverse role in ruminant nutrition. Journal of Agricultural and Food Chemistry, 32(3), 447-453. https://doi.org/10.1021/jf00123a006

Li, X., Li, M., Pu, Y., Ragauskas, A. J., Klett, A. S., Thies, M., & Zheng, Y. (2018). Inhibitory effects of lignin on enzymatic hydrolysis: The role of lignin chemistry and molecular weight. Renewable Energy, 123, 664-674. https://doi.org/10.1016/j.renene.2018.02.079

Licitra, G., Lauria, F., Carpino, S., Schadt, I., Sniffen, C. J., & Van Soest, P. J. (1998). Improvement of the Streptomyces griseus method for degradable protein in ruminant feeds. Animal Feed Science and Technology, 72(1-2), 1-10. https://doi.org/10.1016/S0377-8401(97)00178-8

Licitra, G., Van Soest, P. J., Schadt, I., Carpino, S., & Sniffen, C. J. (1999). Influence of the concentration of the protease from Streptomyces griseus relative to ruminal protein degradability. Animal Feed Science and Technology, 77(1-2), 99-113. https://doi.org/10.1016/S0377-8401(98)00233-8

Liu, C., Li, D., Chen, W., Li, Y., Wu, H., Meng, Q., & Zhou, Z. (2019). Estimating ruminal crude protein degradation from beef cattle feedstuff. Scientific Reports, 9(1), 11368. https://doi.org/10.1038/s41598-019-47768-3

Lobón Ascaso, S., Blanco Alibés, M., Sanz Pascua, A., Rufino Moya, P. J., Molino Gahete, F., & Torrens, M. J. (2015). Influence of alfalfa or sainfoin grazing on productive and reproductive parameters in ewes and lambs. Sitio Argentino de Producción Animal. 45(1): 36-46.

Lorenz, M. M., Hayot Carbonero, C., Smith, L., & Udén, P. (2012). In vitro protein degradation of 38 sainfoin accessions and its relationship to tannin content by different assays. Journal of Agricultural and Food Chemistry, 60(20), 5071-5075. https://doi.org/10.1021/jf3001179

Lynch, G.L., Van der Aar, P.J., Berger, L.L., Fahey, G.C. and Merchen, N.R. (1988) Proteolysis of alcohol-treated soybean meal proteins by Bacteroides ruminocola, Bacteroides amilophilus, pepsin, trypsin, and in the rumen of steers. Journal of Dairy Science, 71, 2416–2427. https://doi.org/10.3168/jds.S0022-0302(88)79827-6

Majewska, M. P., Miltko, R., Bełżecki, G., Kędzierska, A., & Kowalik, B. (2022). Comparison of the effect of synthetic (tannic acid) or natural (oak bark extract) hydrolysable tannins addition on fatty acid profile in the rumen of sheep. Animals, 12(6), 699. https://doi.org/10.3390/ani12060699

Makkar, H. P. (2003). Effects and fate of tannins in ruminant animals, adaptation to tannins, and strategies to overcome detrimental effects of feeding tannin-rich feeds. Small Ruminant Research, 49(3), 241-256. https://doi.org/10.1016/S0921-4488(03)00142-1

Marković, J., Dinić, B., Blagojević, M., Anđelković, B., Babić, S., Petrović, M., & Terzić, D. (2015). Effects of alfalfa and red clover cultivars on protein fractions by CNCPS system of analyzis. In: Proceedings of the 4th International Congress New Perspectives and Challenges of Sustainable Livestock Production (pp. 796-802), October 7-9, Belgrade, Serbia.

Mathis, C.P., Cochran, R.C., Vanzant, E.S., Abdelgadir, I.E.O., Heldt, J.S., Olson, K.C., Johnson, D.E., Caton, J., Fulkner, D., Horn, G., Paisley, S., Mass, R., Moore, K., & Halgerson, J. (2001). A collaborative study comparing an in situ protocol with single time-point enzyme assays for estimating ruminal protein degradability of different forages. Animal Feed Science and Technology, 93(1-2), 31-42. https://doi.org/10.1016/S0377-8401(01)00273-5

Maxin, G., Graulet, B., Le Morvan, A., Picard, F., Portelli, J., & Andueza, D. (2020). Cover crops as alternative forages for ruminants: nutritive characteristics, in vitro digestibility, methane and ammonia production. Animal Production Science, 60(6), 823-832. https://doi.org/10.1071/AN19091

McDowell L.R., Conrad J.H., Ellis G.L. & Loosli J.K. (1983). Minerals for Grazing Ruminants in Tropical Regions. University of Florida, Gainesville. 86 p.

McSweeney, C. S., Palmer, B., Bunch, R., & Krause, D. O. (1999). Isolation and characterization of proteolytic ruminal bacteria from sheep and goats fed the tannin-containing shrub legume Calliandra calothyrsus. Applied and Environmental Microbiology, 65(7), 3075-3083. https://doi.org/10.1128/AEM.65.7.3075-3083.1999

Megías, C., Pastor-Cavada, E., Torres-Fuentes, C., Girón-Calle, J., Alaiz, M., Juan, R., & Vioque, J. (2009). Chelating, antioxidant and antiproliferative activity of Vicia sativa polyphenol extracts. European Food Research and Technology, 230, 353-359. https://doi.org/10.1007/s00217-009-1178-x

Meyer, J. H., & Mackie, R. I. (1986). Microbiological evaluation of the intraruminal in sacculus digestion technique. Applied and Environmental Microbiology, 51(3), 622-629. https://doi.org/10.1128/aem.51.3.622-629.1986

Min, B. R., Attwood, G. T., Reilly, K., Sun, W., Peters, J. S., Barry, T. N., & 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 Journal of Microbiology, 48(10), 911-921. https://doi.org/10.1139/w02-08

Min, B. R., & Hart, S. P. (2003). Tannins for suppression of internal parasites. Journal of Animal Science, 81 (E Suppl. 2), E102-E109. https://doi.org/10.2527/2003.8114_suppl_2E102x

Moharrery, A., & Toghyani, E. (2013). Evaluation of nutritional properties of alfalfa and sainfoin forages by gas production techniques. Journal of Livestock Science and Technologies, 1(1), 1-9.

Muetzel, S., Akpagloh, R., & Becker, K. (2005). Sapindus rarak saponins do not affect rumen protein degradation in vitro. Proceedings of the Society of Nutrition and Physiology, 14, 17.

Nocek, J. E. (1988). In situ and other methods to estimate ruminal protein and energy digestibility: a review. Journal of Dairy Science, 71(8), 2051-2069. https://doi.org/10.3168/jds.S0022-0302(88)79781-7

Nocek, J. E., & Grant, A. L. (1987). Characterization of in situ nitrogen and fiber digestion and bacterial nitrogen contamination of hay crop forages preserved at different dry matter percentages. Journal of Animal Science, 64(2), 552-564. https://doi.org/10.2527/jas1987.642552x

Okon, P., Bachmann, M., Wensch-Dorendorf, M., Titze, N., Rodehutscord, M., Rupp, C., & Zeyner, A. (2023). Feed clusters according to in situ and in vitro ruminal crude protein degradation. Animals, 13(2), 224. https://doi.org/10.3390/ani13020224

Pagella, J. H., Mayes, R. W., Pérez-Barbería, F. J., & Ørskov, E. R. (2018). The development of an intraruminal nylon bag technique using non-fistulated animals to assess the rumen degradability of dietary plant materials. Animal, 12(1), 54-65. DOI: https://doi.org/10.1017/S1751731117001203

Pallardy, S.G. (2008). Physiology of Woody Plants. 3rd ed, Amsterdam: Elsevier, 469 p.

Parissi, Z., Irakli, M., Tigka, E., Papastylianou, P., Dordas, C., Tani, E., Abraham, E.M., Theodoropoulos, A., Kargiotidou, A., Kougiteas, L., & et al. (2022). Analysis of genotypic and environmental effects on biomass yield, nutritional and antinutritional factors in common vetch. Agronomy, 12(7), 1678. https://doi.org/10.3390/agronomy12071678

Parker, R. J., & Moss, B. R. (1981). Nutritional value of sainfoin hay compared with alfalfa hay. Journal of Dairy Science, 64(2), 206-210. https://doi.org/10.3168/jds.S0022-0302(81)82555-6

Paulson, J., Jung, H.G., Raeth-Knight, M., & Linn, J. (2008). Grass vs legume forages for dairy cattle. University of Minnesota: Saint Paul, MA, USA, 119–133.

Pedersen, M. B., Dalsgaard, S., Arent, S., Lorentsen, R., Knudsen, K. E. B., Yu, S., & Lærke, H. N. (2015). Xylanase and protease increase solubilization of non-starch polysaccharides and nutrient release of corn-and wheat distillers dried grains with solubles. Biochemical Engineering Journal, 98, 99-106. https://doi.org/10.1016/j.bej.2015.02.036

Preston, T.R. (1995). Tropical Animal Feeding: A Manual for Research Workers. FAO: Rome.

Rafińska, K., Pomastowski, P., Wrona, O., Górecki, R., & Buszewski, B. (2017). Medicago sativa as a source of secondary metabolites for agriculture and pharmaceutical industry. Phytochemistry Letters, 20, 520-539. https://doi.org/10.1016/j.phytol.2016.12.006

Reed, J. D. (1986). Relationships among soluble phenolics, insoluble proanthocyanidins and fiber in East African browse species. Rangeland Ecology & Management/Journal of Range Management Archives, 39(1), 5-7.

Roe, M.B., Chase, L.E., & Sniffen, C.J. (1991). Comparison of in vitro techniques to the in situ technique for estimation of ruminal degradation of protein. Journal of Dairy Science, 74, 1632–1640. https://doi.org/10.3168/jds.S0022-0302(91)78325-2

Roe M.B., Sniffen CJ., & Chase L.E. (1990). Techniques for measuring protein fractions in feedstuffs. In: Proceedings of Cornell Nutrition Conference (pp. 81-88), Cornell University. Ithaca. NY.

Rufino-Moya, P. J., Blanco, M., Bertolín, J. R., & Joy, M. (2019). Methane production of fresh sainfoin, with or without PEG, and fresh alfalfa at different stages of maturity is similar but the fermentation end products vary. Animals, 9(5), 197. https://doi.org/10.3390/ani9050197

Russell, J. B., & Dombrowski, D. B. (1980). Effect of pH on the efficiency of growth by pure cultures of rumen bacteria in continuous culture. Applied and Environmental Microbiology, 39(3), 604-610. https://doi.org/10.1128/aem.39.3.604-610.1980

Santra, A., & Karim, S. A. (2002). Influence of ciliate protozoa on biochemical changes and hydrolytic enzyme profile in the rumen ecosystem. Journal of Applied Microbiology, 92(5), 801-811. https://doi.org/10.1046/j.1365-2672.2002.01583.x

SAS Institute Inc. (2014). SAS/STAT 9.4 User's Guide. Cary, NC: SAS Institute Inc.

Scharenberg, A., Arrigo, Y., Gutzwiller, A., Wyss, U., Hess, H. D., Kreuzer, M., & Dohme, F. (2007). Effect of feeding dehydrated and ensiled tanniferous sainfoin (Onobrychis viciifolia) on nitrogen and mineral digestion and metabolism of lambs. Archives of Animal Nutrition, 61(5), 390-405. https://doi.org/10.1080/17450390701565081

Skinner, D.Z., Abdelgadir, I.E.O., Fish, T.K., & Cochran, R.C. (1995). Influence of growth conditions on alfalfa protein degradability. In: 24th Central Alfalfa Improvement Conference (p. 13), Spearfish, SD.

Stafford, H. A. 1990. Flavonoid metabolism. CRC Press, Boca Raton, FL.

Tedeschi, L. O., Ramírez-Restrepo, C. A., & Muir, J. P. (2014). Developing a conceptual model of possible benefits of condensed tannins for ruminant production. Animal, 8(7), 1095-1105. https://doi.org/10.1017/S1751731114000974

Terrett, O. M., & Dupree, P. (2019). Covalent interactions between lignin and hemicelluloses in plant secondary cell walls. Current Opinion in Biotechnology, 56, 97-104. https://doi.org/10.1016/j.copbio.2018.10.010

Theodoridou, K., Aufrère, J., Andueza, D., Le Morvan, A., Picard, F., Stringano, E., Pourrat, J., Mueller-Harvey, I., & Baumont, R. (2011). Effect of plant development during first and second growth cycle on chemical composition, condensed tannins and nutritive value of three sainfoin (Onobrychis viciifolia) varieties and lucerne. Grass and Forage Science, 66(3), 402–414. https://doi.org/10.1111/j.1365-2494.2011.00798.x

Thorstensson, E. M., Buxton, D. R., & Cherney, J. H. (1992). Apparent inhibition to digestion by lignin in normal and brown midrib stems. Journal of the Science of Food and Agriculture, 59(2), 183-188. https://doi.org/10.1002/jsfa.2740590208

Titze, N., Chi, Y. P., Haese, E., Hartung, J., & Rodehutscord, M. (2024). Linkage of in situ ruminal degradation of crude protein with ruminal degradation of amino acids and phytate from different soybean meals in dairy cows. Journal of Dairy Science, 107(4), 2011-2025. https://doi.org/10.3168/jds.2023-23587

Tremblay, G. F., Michaud, R., & Bélanger, G. (2003). Protein fractions and ruminal undegradable proteins in alfalfa. Canadian Journal of Plant Science, 83(3), 555-559. https://doi.org/10.4141/P02-148

Turgut, L., & Yanar, M. (2004). In situ dry matter and crude protein degradation kinetics of some forages in Eastern Turkey. Small Ruminant Research, 52(3), 217-222. https://doi.org/10.1016/S0921-4488(03)00261-X

Turgut, L., Yanar, M., Kaya, A., & Tan, M. (2006). Farklı olgunluk dönemlerinde hasat edilen bazı fiğ türlerinin ham besin maddeleri içeriği ve bunların in situ rumen parçalanabilirlikleri. Atatürk Üniversitesi Ziraat Fakültesi Dergisi, 37(2), 181-186.

Van Soest, P.J., Robertson, J.D., & Lewis, B.A. (1991). Methods for dietary fibre, neutral detergent fibre and non-starch polysaccharides in relation to animal nutrition. Journal of Dairy Science, 74, 3583–3597. https://doi.org/10.3168/jds.S0022-0302(91)78551-2

Vanzant, E. S., Cochran, R. C., & Titgemeyer, E. C. (1998). Standardization of in situ techniques for ruminant feedstuff evaluation. Journal of Animal Science, 76(10), 2717-2729. https://doi.org/10.2527/1998.76102717x

Vartoukian, S. R., Palmer, R. M., & Wade, W. G. (2010). Strategies for culture of ‘unculturable’ bacteria. FEMS Microbiology Letters, 309(1), 1-7. https://doi.org/10.1111/j.1574-6968.2010.02000.x

Vinyard, J. R., & Faciola, A. P. (2022). Unraveling the pros and cons of various in vitro methodologies for ruminant nutrition: a review. Translational Animal Science, 6(4), txac130. https://doi.org/10.1093/tas/txac130

Waghorn, G. C., Douglas, G. B., Niezen, J. H., McNabb, W. C., & Foote, A. G. (1998). Forages with condensed tannins-their management and nutritive value for ruminants. In: Proceedings of the New Zealand Grassland Association (pp. 89-98). https://doi.org/10.33584/jnzg.1998.60.2315

Wang, Y., Frutos, P., Gruber, M. Y., Ray, H., & McAllister, T. A. (2006). In vitro ruminal digestion of anthocyanidin-containing alfalfa transformed with the maize Lc regulatory gene. Canadian Journal of Plant Science, 86(4), 1119-1130. https://doi.org/10.4141/P06-001

Zhou, K., Bao, Y., & Zhao, G. (2019). Effects of dietary crude protein and tannic acid on rumen fermentation, rumen microbiota and nutrient digestion in beef cattle. Archives of Animal Nutrition, 73(1), 30-43. https://doi.org/10.1080/1745039X.2018.1545502

Downloads

Published

15.10.2024

How to Cite

Oral, H. H. (2024). Comparative Evaluation of Enzymatic Crude Protein Degradation in Selected Legume Forages . Turkish Journal of Agriculture - Food Science and Technology, 12(10), 1762–1771. https://doi.org/10.24925/turjaf.v12i10.1762-1771.7016

Issue

Section

Research Paper