DOI QR코드

DOI QR Code

Meta-analysis on Methane Mitigating Properties of Saponin-rich Sources in the Rumen: Influence of Addition Levels and Plant Sources

  • Jayanegara, Anuraga (Department of Animal Nutrition and Feed Technology, Faculty of Animal Science, Bogor Agricultural University) ;
  • Wina, Elizabeth (Indonesian Research Institute for Animal Production) ;
  • Takahashi, Junichi (Department of Animal Nutrition and Feed Technology, Faculty of Animal Science, Bogor Agricultural University)
  • Received : 2014.02.06
  • Accepted : 2014.05.06
  • Published : 2014.10.01

Abstract

Saponins have been considered as promising natural substances for mitigating methane emissions from ruminants. However, studies reported that addition of saponin-rich sources often arrived at contrasting results, i.e. either it decreased methane or it did not. The aim of the present study was to assess ruminal methane emissions through a meta-analytical approach of integrating related studies from published papers which described various levels of different saponin-rich sources being added to ruminant feed. A database was constructed from published literature reporting the addition of saponin-rich sources at various levels and then monitoring ruminal methane emissions in vitro. Accordingly, levels of saponin-rich source additions as well as different saponin sources were specified in the database. Apart from methane, other related rumen fermentation parameters were also included in the database, i.e. organic matter digestibility, gas production, pH, ammonia concentration, short-chain fatty acid profiles and protozoal count. A total of 23 studies comprised of 89 data points met the inclusion criteria. The data obtained were subsequently subjected to a statistical meta-analysis based on mixed model methodology. Accordingly, different studies were treated as random effects whereas levels of saponin-rich source additions or different saponin sources were considered as fixed effects. Model statistics used were p-value and root mean square error. Results showed that an addition of increasing levels of a saponin-rich source decreased methane emission per unit of substrate incubated as well as per unit of total gas produced (p<0.05). There was a decrease in acetate proportion (linear pattern; p<0.001) and an increase in propionate proportion (linear pattern; p<0.001) with increasing levels of saponin. Log protozoal count decreased (p<0.05) at higher saponin levels. Comparing between different saponin-rich sources, all saponin sources, i.e. quillaja, tea and yucca saponins produced less methane per unit of total gas than that of control (p<0.05). Although numerically the order of effectiveness of saponin-rich sources in mitigating methane was yucca>tea>quillaja, statistically they did not differ each other. It can be concluded that methane mitigating properties of saponins in the rumen are level- and source-dependent.

References

  1. Castro-Montoya, J. M., H. P. S. Makkar, and K. Becker. 2011. Chemical composition of rumen microbial fraction and fermentation parameters as affected by tannins and saponins using an in vitro rumen fermentation system. Can. J. Anim. Sci. 91:433-448. https://doi.org/10.4141/cjas2010-028
  2. Chwalek, M., N. Lalun, H. Bobichon, K. Ple, and L. Voutquenne-Nazabadioko. 2006. Structure-activity relationships of some hederagenin diglycosides: Haemolysis, cytotoxicity and apoptosis induction. Biochim. Biophys. Acta 1760:1418-1427. https://doi.org/10.1016/j.bbagen.2006.05.004
  3. Cottle, D. J., J. V. Nolan, and S. G. Wiedemann. 2011. Ruminant enteric methane mitigation: a review. Anim. Prod. Sci. 51:491-514. https://doi.org/10.1071/AN10163
  4. Desnoyers, M., S. Giger-Reverdin, G. Bertin, C. Duvaux-Ponter, and D. Sauvant. 2009. Meta-analysis of the influence of Saccharomyces cerevisiae supplementation on ruminal parameters and milk production of ruminants. J. Dairy Sci. 92:1620-1632. https://doi.org/10.3168/jds.2008-1414
  5. Eugene, M., H. Archimede, and D. Sauvant. 2004. Quantitative meta-analysis on the effects of defaunation of the rumen on growth, intake and digestion in ruminants. Livest. Prod. Sci. 85:81-97. https://doi.org/10.1016/S0301-6226(03)00117-9
  6. Feng, Z. H., Y. F. Cao, Y. X. Gao, Q. F. Li, and J. G. Li. 2012. Effect of gross saponin of Tribulus terrestris on ruminal fermentation and methane production in vitro. J. Anim. Vet. Adv. 11:2121-2125. https://doi.org/10.3923/javaa.2012.2121.2125
  7. Finlay, B. J., G. Esteban, K. J. Clarke, A. G. Williams, T. M. Embley, and R. P. Hirt. 1994. Some rumen ciliates have endosymbiotic methanogens. FEMS Microbiol. Lett. 117:157-161. https://doi.org/10.1111/j.1574-6968.1994.tb06758.x
  8. Firkins, J. L., M. S. Allen, B. S. Oldick, and N. R. St-Pierre. 1998. Modeling ruminal digestibility of carbohydrates and microbial protein flow to the duodenum. J. Dairy Sci. 81:3350-3369. https://doi.org/10.3168/jds.S0022-0302(98)75901-6
  9. Francis, G., Z. Kerem, H. P. S. Makkar, and K. Becker. 2002. The biological action of saponins in animal systems: A review. Br. J. Nutr. 88:587-605. https://doi.org/10.1079/BJN2002725
  10. Goel, G., H. P. S. Makkar, and K. Becker. 2008. Changes in microbial community structure, methanogenesis and rumen fermentation in response to saponin-rich fractions from different plant materials. J. Appl. Microbiol. 105:770-777. https://doi.org/10.1111/j.1365-2672.2008.03818.x
  11. Guo, S., L. Kenne, L. N. Lundgren, B. Ronnberg, and B. G. Sundquist. 1998. Triterpenoid saponins from Quillaja saponaria. Phytochemistry 48:175-180. https://doi.org/10.1016/S0031-9422(97)00716-4
  12. Guo, Y. Q., J. X. Liu, Y. Lu, W. Y. Zhu, S. E. Denman, and C. S. McSweeney. 2008. Effect of tea saponin on methanogenesis, microbial community structure and expression of mcrA gene, in cultures of rumen micro-organisms. Lett. Appl. Microbiol. 47:421-426. https://doi.org/10.1111/j.1472-765X.2008.02459.x
  13. Gutierrez, J. and R. E. Davis. 1959. Bacterial ingestion by the rumen ciliates Entodinium and Diplodinium. J. Eukaryot. Microbiol. 6:222-226.
  14. Hegarty, R. S. 1999. Reducing rumen methane emissions through elimination of rumen protozoa. Aust. J. Agric. Res. 50:1321-1328. https://doi.org/10.1071/AR99008
  15. Hess, H. D., M. Kreuzer, T. E. Diaz, C. E. Lascano, J. E. Carulla, C. R. Soliva, and A. Machmueller. 2003. Saponin rich tropical fruits affect fermentation and methanogenesis in faunated and defaunated rumen fluid. Anim. Feed Sci. Technol. 109:79-94. https://doi.org/10.1016/S0377-8401(03)00212-8
  16. Holtshausen, L., A. V. Chaves, K. A. Beauchemin, S. M. McGinn, T. A. McAllister, N. E. Odongo, P. R. Cheeke, and C. Benchaar. 2009. Feeding saponin-containing Yucca schidigera and Quillaja saponaria to decrease enteric methane production in dairy cows. J. Dairy Sci. 92:2809-2821. https://doi.org/10.3168/jds.2008-1843
  17. Hu, W. L., J. X. Liu, J. A. Ye, Y. M. Wu, and Y. Q. Guo. 2005a. Effect of tea saponin on rumen fermentation in vitro. Anim. Feed Sci. Technol. 120:333-339. https://doi.org/10.1016/j.anifeedsci.2005.02.029
  18. Hu, W. L., Y. M. Wu, J. X. Liu, Y. Q. Guo, and J. A. Ye. 2005b. Tea saponins affect in vitro fermentation and methanogenesis in faunated and defaunated rumen fluid. J. Zhejiang Univ. Sci. 6B:787-792. https://doi.org/10.1631/jzus.2005.B0787
  19. Hu, W. L., J. X. Liu, Y. M. Wu, Y. Q. Guo, and J. A. Ye. 2006. Effects of tea saponins on in vitro ruminal fermentation and growth performance in growing Boer goat. Arch. Anim. Nutr. 60:89-97. https://doi.org/10.1080/17450390500353119
  20. Jayanegara, A., M. Kreuzer, E. Wina, and F. Leiber. 2011. Significance of phenolic compounds in tropical forages for the ruminal bypass of polyunsaturated fatty acids and the appearance of biohydrogenation intermediates as examined in vitro. Anim. Prod. Sci. 51:1127-1136. https://doi.org/10.1071/AN11059
  21. Jayanegara, A., F. Leiber, and M. Kreuzer. 2012. Meta-analysis of the relationship between dietary tanin level and methane formation in ruminants from in vivo and in vitro experiments. J. Anim. Physiol. Anim. Nutr. 96:365-375. https://doi.org/10.1111/j.1439-0396.2011.01172.x
  22. Kamra, D. N., N. Agarwal, and L. C. Chaudhary. 2006. Inhibition of ruminal methanogenesis by tropical plants containing secondary compounds. Int. Congr. Ser. 1293:156-163. https://doi.org/10.1016/j.ics.2006.02.002
  23. Khiaosa-ard, R., S. F. Bryner, M. R. L. Scheeder, H. R. Wettstein, F. Leiber, M. Kreuzer, and C. R. Soliva. 2009. Evidence for the inhibition of the terminal step of ruminal α-linolenic acid biohydrogenation by condensed tannins. J. Dairy Sci. 92:177-188. https://doi.org/10.3168/jds.2008-1117
  24. Koenig, K. M., C. J. Newbold, F. M. McIntosh, and L. M. Rode. 2000. Effects of protozoa on bacterial nitrogen recycling in the rumen. J. Anim. Sci. 78:2431-2445.
  25. Kurihara, Y., J. M. Eadie, P. N. Hobson, and S. O. Mann. 1968. Relationship between bacteria and ciliate protozoa in the sheep rumen. J. Gen. Microbiol. 51:267-288. https://doi.org/10.1099/00221287-51-2-267
  26. Lassey, K. R. 2008. Livestock methane emission and its perspective in the global methane cycle. Aust. J. Exp. Agric. 48:114-118. https://doi.org/10.1071/EA07220
  27. Li, W. and W. Powers. 2012. Effects of saponin extracts on air emissions from steers. J. Anim. Sci. 90:4001-4013. https://doi.org/10.2527/jas.2011-4888
  28. Lila, Z. A., N. Mohammed, S. Kanda, T. Kamada, and H. Itabashi. 2003. Effect of sarsaponin on ruminal fermentation with particular reference to methane production in vitro. J. Dairy Sci. 86:3330-3336. https://doi.org/10.3168/jds.S0022-0302(03)73935-6
  29. Makkar, H. P. S., G. Francis, and K. Becker. 2007. Bioactivity of phytochemicals in some lesser-known plants and their effects and potential applications in livestock and aquaculture production systems. Animal 1:1371-1391.
  30. Malik, P. K. and K. K. Singhal. 2008. Influence of supplementation of wheat straw based total mixed ration with saponins on total gas and methane production in vitro. Indian J. Anim. Sci. 78:987-990.
  31. Mao, H. L., J. K. Wang, Y. Y. Zhou, and J. X. Liu. 2010. Effects of addition of tea saponins and soybean oil on methane production, fermentation and microbial population in the rumen of growing lambs. Livest. Sci. 129:56-62. https://doi.org/10.1016/j.livsci.2009.12.011
  32. McAllister, T. A. and C. J. Newbold. 2008. Redirecting rumen fermentation to reduce methanogenesis. Aust. J. Exp. Agric. 48:7-13. https://doi.org/10.1071/EA07218
  33. Monteny, G. J., A. Bannink, and D. Chadwick. 2006. Greenhouse gas abatement strategies for animal husbandry. Agric. Ecosyst. Environ. 112:163-170. https://doi.org/10.1016/j.agee.2005.08.015
  34. Morgavi, D. P., E. Forano, C. Martin, and C. J. Newbold. 2010. Microbial ecosystem and methanogenesis in ruminants. Animal 4:1024-1036. https://doi.org/10.1017/S1751731110000546
  35. Moss, A. R., J. P. Jouany, and J. Newbold. 2000. Methane production by ruminants: its contribution to global warming. Ann. Zootech. 49:231-253. https://doi.org/10.1051/animres:2000119
  36. Narvaez, N., Y. Wang, and T. McAllister. 2013. Effects of extracts of Humulus lupulus (hops) and Yucca schidigera applied alone or in combination with monensin on rumen fermentation and microbial populations in vitro. J. Sci. Food Agric. 93:2517-2522. https://doi.org/10.1002/jsfa.6068
  37. Newbold, C. J., B. Lassalas, and J. P. Jouany. 1995. The importance of methanogens associated with ciliate protozoa in ruminal methane production in vitro. Lett. Appl. Microbiol. 21:230-234. https://doi.org/10.1111/j.1472-765X.1995.tb01048.x
  38. Oleszek, W., M. Sitek, A. Stochmal, S. Piacente, C. Pizza, and P. Cheeke. 2001. Steroidal saponins of Yucca schidigera Roezl. J. Agric. Food Chem. 49:4392-4396. https://doi.org/10.1021/jf010598+
  39. Patra, A. K. and J. Saxena. 2009. The effect and mode of action of saponins on the microbial populations and fermentation in the rumen and ruminant production. Nutr. Res. Rev. 22:204-219. https://doi.org/10.1017/S0954422409990163
  40. Patra, A. K. and Z. Yu. 2013. Effective reduction of enteric methane production by a combination of nitrate and saponin without adverse effect on feed degradability, fermentation, or bacterial and archaeal communities of the rumen. Bioresour. Technol. 148:352-360. https://doi.org/10.1016/j.biortech.2013.08.140
  41. Pen, B., C. Sar, B. Mwenya, K. Kuwaki, R. Morikawa, and J. Takahashi. 2006. Effects of Yucca schidigera and Quillaja saponaria extracts on in vitro ruminal fermentation and methane emission. Anim. Feed Sci. Technol. 129:175-186. https://doi.org/10.1016/j.anifeedsci.2006.01.002
  42. Pen, B., K. Takaura, S. Yamaguchi, R. Asa, and J. Takahashi. 2007. Effects of Yucca schidigera and Quillaja saponaria with or without $\beta$ 1-4 galacto-oligosaccharides on ruminal fermentation, methane production and nitrogen utilization in sheep. Anim. Feed Sci. Technol. 138:75-88. https://doi.org/10.1016/j.anifeedsci.2006.11.018
  43. Pen, B., C. Sar, B. Mwenya, and J. Takahashi. 2008. Effects of Quillaja saponaria extract alone or in combination with Yucca schidigera extract on ruminal fermentation and methanogenesis in vitro. Anim. Sci. J. 79:193-199. https://doi.org/10.1111/j.1740-0929.2008.00517.x
  44. Santoso, B., B. Mwenya, C. Sar, Y. Gamo, T. Kobayashi, R. Morikawa, K. Kimura, H. Mizukoshi, and J. Takahashi. 2004. Effects of supplementing galacto-oligosaccharides, Yucca schidigera or nisin on rumen methanogenesis, nitrogen and energy metabolism in sheep. Livest. Prod. Sci. 91:209-217. https://doi.org/10.1016/j.livprodsci.2004.08.004
  45. SAS Institute Inc. 2008. SAS/STAT Software version 9.1. SAS Institute Inc., Cary, NC, USA.
  46. Sauvant, D., P. Schmidely, J. J. Daudin, and N. R. St-Pierre. 2008. Meta-analyses of experimental data in animal nutrition. Animal 2:1203-1214.
  47. Sliwinski, B. J., C. R. Soliva, A. Machmueller, and M. Kreuzer. 2002. Efficacy of plant extracts rich in secondary constituents to modify rumen fermentation. Anim. Feed Sci. Technol. 101:101-114. https://doi.org/10.1016/S0377-8401(02)00139-6
  48. Staerfl, S. M., M. Kreuzer, and C. R. Soliva. 2010. In vitro screening of unconventional feeds and various natural supplements for their ruminal methane mitigation potential when included in a maize-silage based diet. J. Anim. Feed Sci. 19:651-664.
  49. St-Pierre, N. R. 2001. Integrating quantitative findings from multiple studies using mixed model methodology. J. Dairy Sci. 84:741-755. https://doi.org/10.3168/jds.S0022-0302(01)74530-4
  50. Takahashi, J. 2011. Some prophylactic options to mitigate methane emission from animal agriculture in Japan. Asian Australas. J. Anim. Sci. 24:285-294. https://doi.org/10.5713/ajas.2011.r.03
  51. Thorpe, A. 2009. Enteric fermentation and ruminant eructation: the role (and control?) of methane in the climate change debate. Clim. Change 93:407-431. https://doi.org/10.1007/s10584-008-9506-x
  52. Van Nevel, C. J. and D. I. Demeyer. 1996. Control of rumen methanogenesis. Environ. Monit. Assess. 42:73-97. https://doi.org/10.1007/BF00394043
  53. Vincken, J. P., L. Heng, A. de Groot, and H. Gruppen. 2007. Saponins, classification and occurrence in the plant kingdom. Phytochemistry 68:275-297. https://doi.org/10.1016/j.phytochem.2006.10.008
  54. Voutquenne, L., C. Lavaud, G. Massiot, and Le Men-Olivier. 2002. Structure-activity relationships of haemolytic saponins. Pharm. Biol. 40:253-262. https://doi.org/10.1076/phbi.40.4.253.8470
  55. Wallace, R. J., L. Arthaud, and C. J. Newbold. 1994. Influence of Yucca schidigera extract on ruminal ammonia concentrations and ruminal microorganisms. Appl. Environ. Microbiol. 60:1762-1767.
  56. Wallace, R. J., N. R. McEwan, F. M. McIntosh, B. Teferedegne, and C. J. Newbold. 2002. Natural products as manipulators of rumen fermentation. Asian Australas. J. Anim. Sci. 15:1458-1468. https://doi.org/10.5713/ajas.2002.1458
  57. Wang, Y., T. A. McAllister, C. J. Newbold, L. M. Rode, P. R. Cheeke, and K. J. Cheng. 1998. Effects of Yucca schidigera extract on fermentation and degradation of steroidal saponins in the rumen simulation technique (RUSITEC). Anim. Feed Sci. Technol. 74:143-153. https://doi.org/10.1016/S0377-8401(98)00137-0
  58. Wang, Y., T. A. McAllister, L. J. Yanke, and P. R. Cheeke. 2000. Effect of steroidal saponin from Yucca schidigera extract on ruminal microbes. J. Appl. Microbiol. 88:887-896. https://doi.org/10.1046/j.1365-2672.2000.01054.x
  59. Wang, C. J., S. P. Wang, and H. Zhou. 2009. Influences of flavomycin, ropadiar, and saponin on nutrient digestibility, rumen fermentation, and methane emission from sheep. Anim. Feed Sci. Technol. 148:157-166. https://doi.org/10.1016/j.anifeedsci.2008.03.008
  60. Wina, E., S. Muetzel, and K. Becker. 2005. The impact of saponins or saponin-containing plant materials on ruminant production . A review. J. Agric. Food Chem. 53:8093-8105. https://doi.org/10.1021/jf048053d
  61. Wina, E., S. Muetzel, and K. Becker. 2006. Effects of daily and interval feeding of Sapindus rarak saponins on protozoa, rumen fermentation parameters and digestibility in sheep. Asian Australas. J. Anim. Sci. 19:1580-1587. https://doi.org/10.5713/ajas.2006.1580
  62. Xu, M., M. Rinker, K. R. McLeod, and D. L. Harmon. 2010. Yucca schidigera extract decreases in vitro methane production in a variety of forages and diets. Anim. Feed Sci. Technol. 159:18-26. https://doi.org/10.1016/j.anifeedsci.2010.05.005
  63. Zhao, P., D. F. Gao, M. Xu, Z. G. Shi, D. Wang, C. R. Yang, and Y. J. Zhang. 2011. Triterpenoid saponins from the genus camellia. Chem. Biodivers. 8:1931-1942. https://doi.org/10.1002/cbdv.201000265
  64. Zhou, Y. Y., H. L. Mao, F. Jiang, J. K. Wang, J. X. Liu, and C. S. McSweeney. 2011. Inhibition of rumen methanogenesis by tea saponins with reference to fermentation pattern and microbial communities in Hu sheep. Anim. Feed Sci. Technol. 166-167:93-100. https://doi.org/10.1016/j.anifeedsci.2011.04.007

Cited by

  1. Effect of Grape Pomace Powder, Mangosteen Peel Powder and Monensin on Nutrient Digestibility, Rumen Fermentation, Nitrogen Balance and Microbial Protein Synthesis in Dairy Steers vol.29, pp.10, 2015, https://doi.org/10.5713/ajas.15.0689
  2. Effects of Momordica charantia Saponins on In vitro Ruminal Fermentation and Microbial Population vol.29, pp.4, 2016, https://doi.org/10.5713/ajas.15.0402
  3. Use of Asian selected agricultural byproducts to modulate rumen microbes and fermentation vol.7, pp.1, 2016, https://doi.org/10.1186/s40104-016-0126-4
  4. Methane and nitrous oxide emissions from Canadian dairy farms and mitigation options: An updated review vol.96, pp.3, 2016, https://doi.org/10.1139/cjas-2015-0111
  5. Antiprotozoal Effect of Saponins in the Rumen Can Be Enhanced by Chemical Modifications in Their Structure vol.08, pp.1664-302X, 2017, https://doi.org/10.3389/fmicb.2017.00399
  6. Improving the antiprotozoal effect of saponins in the rumen by combination with glycosidase inhibiting iminosugars or by modification of their chemical structure vol.12, pp.9, 2017, https://doi.org/10.1371/journal.pone.0184517
  7. Special metabolites isolated from Urochloa humidicola (Poaceae) vol.89, pp.2, 2017, https://doi.org/10.1590/0001-3765201720160126
  8. on wool production, mineral balance and enteric methane emissions of Merino sheep pp.01425242, 2017, https://doi.org/10.1111/gfs.12314
  9. rumen fermentation, methane production and true digestibility at different forage to concentrate ratios vol.46, pp.1, 2018, https://doi.org/10.1080/09712119.2016.1270823
  10. Effects of replacing rice bran with tamarind seed meal in concentrate mixture diets on the changes in ruminal ecology and feed utilization of dairy steers pp.1573-7438, 2018, https://doi.org/10.1007/s11250-018-1719-z
  11. Effect of species on chemical composition, metabolizable energy, organic matter digestibility and methane production of some legume plants grown in Turkey vol.46, pp.1, 2018, https://doi.org/10.1080/09712119.2018.1480485
  12. Effect of feeding of blend of essential oils on methane production, growth, and nutrient utilization in growing buffaloes vol.31, pp.5, 2018, https://doi.org/10.5713/ajas.16.0508