Animal Production Science Animal Production Science Society
Food, fibre and pharmaceuticals from animals
RESEARCH ARTICLE

Effects of tea seed saponin supplementation on physiological changes associated with blood methane concentration in tropical Brahman cattle

C. A. Ramírez-Restrepo A E , C. J. O’Neill A , N. López-Villalobos B , J. Padmanabha C , J. K. Wang D and C. McSweeney C
+ Author Affiliations
- Author Affiliations

A CSIRO Agriculture, Australian Tropical Sciences and Innovation Precinct, James Cook Drive, Townsville, Qld 4811, Australia.

B Institute of Veterinary, Animal and Biomedical Sciences, Massey University, Palmerston North 4442, New Zealand.

C CSIRO Agriculture, Queensland BioScience Precinct, St Lucia, Brisbane, Qld 4067, Australia.

D Institute of Dairy Science, 866 Yuhangtang Road, Zhejiang University, Hangzhou, PR China.

E Corresponding author. Email: carlos.ramirez@csiro.au

Animal Production Science 56(3) 457-465 https://doi.org/10.1071/AN15582
Submitted: 14 September 2015  Accepted: 6 November 2015   Published: 9 February 2016

Abstract

A 59-day experiment compared the effects of increasing tea seed (Camellia sinensis L.) saponin (TSS) supplementation on dry matter intake (DMI), liveweight (LW), rumen fermentation, methanogenesis, blood biochemistry and animal tolerance. Six, 10, 15, 20, 25 and 30 g of powder TSS were dissolved during 5, 7, 4, 3, 3 and 2 days, respectively, and infused into the rumen of four rumen-cannulated Brahman steers (234 ± 13.6 kg LW; least-squares means ± s.e.m.) or mixed in the basal diet [BD: 0.15 Rhodes grass (Chloris gayana) hay plus a high-grain feed (0.85)] of two non-cannulated (253 ± 19.3 kg) steers. Overall, DMI was not affected, by the sequential infusion of TSS (5.3 ± 0.15 kg) or addition to the BD (5.4 ± 0.18 kg), but relative to all diets, 6 g of TSS supplementation reduced DMI (P < 0.05), while the administration above 30 g of the supplement was associated with significantly (P < 0.001) reduced DMI, scours and bloat disorders. Clinical symptoms disappeared 8 days after withdrawal of the supplement. LW increased with time (P < 0.05) and the final LW was similar for cannulated (258 ± 13.6 kg) and non-cannulated (276 ± 19.3 kg) steers. Saponin supplementation reduced total volatile fatty acid (VFA) concentration (P < 0.05), modified pattern of individual molar VFA concentrations and moderately increased ruminal pH (P < 0.05). Cannulated and non-cannulated steers fed the BD had similar daily (g) methane or yield (CH4 g/kg DMI) emissions while in respiratory chambers. However, compared with cannulated (8.0 ± 1.20 ng/mL) animals, the addition of 30 g of TSS in the BD increased (P < 0.01) blood CH4 concentration in non-cannulated (15.6 ± 1.74 ng/mL) animals. Diets supplemented with 30 g of TSS were associated with higher chloride (P < 0.01) and alkaline phosphatase (P < 0.05) blood concentrations, and lower serum concentrations of potassium and urea nitrogen (P < 0.01), iron and total lipase (P < 0.05), than was the BD. It was concluded that higher levels of TSS supplement may evoke physiological changes in the animal. However, the potential CH4 mitigation effect of this form of saponin in tropical cattle needs further investigation, alongside the derived response of the rumen microbial ecology to the tested range of supplementation.

Additional keywords: Camellia sinensis L., metabolism, physiology, ruminant.


References

Augustin JM, Kuzina V, Andesen SB, Bak S (2011) Molecular activities, biosynthesis and evolution of triterpenoid saponins. Phytochemistry 72, 435–457.
Molecular activities, biosynthesis and evolution of triterpenoid saponins.CrossRef | 1:CAS:528:DC%2BC3MXjsV2hurk%3D&md5=5dc1d449149f13a501ea794cf68a895fCAS | 21333312PubMed |

Bangham AD, Horne RW (1962) Action of saponin on biological cell membranes. Nature 196, 952–953.
Action of saponin on biological cell membranes.CrossRef | 1:CAS:528:DyaF3sXktFSnug%3D%3D&md5=142156ad6927c0ec2c62c63142475881CAS | 13966357PubMed |

Cohen SP, Haack KKV, Halstead-Nussloch GE, Bernard KF, Hatt H, Kubanek J, McCarty NA (2010) Identification of RL-TGR, a coreceptor involved in aversive chemical signalling. Proceedings of the National Academy of Sciences of the United States of America 107, 12339–12344.
Identification of RL-TGR, a coreceptor involved in aversive chemical signalling.CrossRef | 1:CAS:528:DC%2BC3cXovFyitbk%3D&md5=b24cb227c389bcdb32e19d0561f56b3dCAS | 20566865PubMed |

Coleman JJ, Okoli I, Tegos GP, Holson EB, Wagner FF, Hamblin MR, Mylonakis E (2010) Characterisation of plant-derived saponin natural products against Candida albicans. ACS Chemical Biology 5, 321–332.
Characterisation of plant-derived saponin natural products against Candida albicans.CrossRef | 1:CAS:528:DC%2BC3cXhtVamsr0%3D&md5=5110cc5d26eadfe4c059ca08be7838d1CAS | 20099897PubMed |

Dohallite J (1962) Injected saponins as abortifacients. American Journal of Veterinary Research 23, 1261–1263.

Dourmashkin RR, Dougherty RM, Harris RJC (1962) Electron microscopy observations on rous sarcoma virus and cell membranes. Nature 194, 1116–1119.
Electron microscopy observations on rous sarcoma virus and cell membranes.CrossRef | 1:STN:280:DyaF38%2FivVyqtQ%3D%3D&md5=dfbc9238966ef702328a0fdb4ab2c937CAS | 13887581PubMed |

FAO (2013) ‘Tackling climate change through livestock: a global assessment of emissions and mitigation opportunities.’ (Food and Agriculture Organization of the United Nations: Rome)

Fisher DS, Burns JC, Pond KR (1987) Modeling ad libitum dry matter intake by ruminants as regulated by distension and chemostatic feedbacks. Journal of Theoretical Biology 126, 407–418.
Modeling ad libitum dry matter intake by ruminants as regulated by distension and chemostatic feedbacks.CrossRef |

Francis G, Kerem Z, Makkar HPS, Becker K (2002) The biological action of saponins in animal systems: a review. British Journal of Nutrition 88, 587–605.
The biological action of saponins in animal systems: a review.CrossRef | 1:CAS:528:DC%2BD3sXktFKisA%3D%3D&md5=f10f0c0fe4baaf7d28977ac7be06605cCAS | 12493081PubMed |

Golub AA, Henderson BB, Hertel TW, Gerber PJ, Rose SK, Brent S (2013) Global climate policy impacts on livestock, land use, livelihoods, and food security. Proceedings of the National Academy of Sciences,USA 110, 20894–20899.
Global climate policy impacts on livestock, land use, livelihoods, and food security.CrossRef | 1:CAS:528:DC%2BC2cXnsFyrtg%3D%3D&md5=40a511569befbbbe4f7cb4b436822f30CAS |

Guo YQ, Liu JX, Lu Y, Zhu WY, Denman SE, McSweeney CS (2008) Effect of tea saponin on methanogenesis, microbial community structure and expression of mcrA gene, in cultures of rumen micro-organisms. Letters in Applied Microbiology 47, 421–426.
Effect of tea saponin on methanogenesis, microbial community structure and expression of mcrA gene, in cultures of rumen micro-organisms.CrossRef | 1:CAS:528:DC%2BD1cXhsFSjs7vP&md5=b846377745ef4d85c271106c409c9166CAS | 19146532PubMed |

Haralampidis K, Trojanowska M, Osbourn AE (2002) Biosynthesis of triterpenoid saponins in plants. Advances in Biochemical Engineering/Biotechnology 75, 31–49.
Biosynthesis of triterpenoid saponins in plants.CrossRef | 1:CAS:528:DC%2BD38XmtVWgsA%3D%3D&md5=e2bd3078c9160e0e81a73a2ba51d51a0CAS | 11783842PubMed |

Henderson B, Falcucci A, Mottet A, Early L, Werner B, Steinfeld H, Gerber P (2015) Marginal costs of abating greenhouse gases in global ruminant livestock sector. Mitigation and Adaptation Strategies for Global Change
Marginal costs of abating greenhouse gases in global ruminant livestock sector.CrossRef |

Herrero M, Thornton PK (2013) Livestock and global change: emerging issues for sustainable food systems. Proceedings of the National Academy of Sciences, USA 110, 20878–20881.
Livestock and global change: emerging issues for sustainable food systems.CrossRef | 1:CAS:528:DC%2BC2cXnsFykug%3D%3D&md5=606290a5f1413d7f8cfe64f3396f6082CAS |

Hu WL, Liu JX, Ye JA, Wu YM, Guo YQ (2005) Effects of tea saponin on rumen fermentation in vitro. Animal Feed Science and Technology 120, 333–339.
Effects of tea saponin on rumen fermentation in vitro.CrossRef | 1:CAS:528:DC%2BD2MXjvVKrsrk%3D&md5=5c32b15a640135563ee017ae3cfa2039CAS |

Hu W, Liu J, Wu Y, Guo Y, Ye J (2006) Effects of tea saponins on in vitro ruminal fermentation and growth performance in growing Boer goat. Archives of Animal Nutrition 60, 89–97.
Effects of tea saponins on in vitro ruminal fermentation and growth performance in growing Boer goat.CrossRef | 1:CAS:528:DC%2BD28XksF2jsg%3D%3D&md5=ca438814ab45bc66840577eb6a6ea50aCAS | 16529160PubMed |

Johnson IT, Gee JM, Price K, Curl C, Fenwick GR (1986) Influence of saponins on gut permeability and active nutrient transport in vitro. The Journal of Nutrition 116, 2270–2277.

Kawaguchi M, Kato T, Kamada S, Yahata A (1994) Three-month oral repeated administration toxicity study of seed saponins of Thea sinensis L. (ryokucha saponin) in rats. Food and Chemical Toxicology 32, 431–442.
Three-month oral repeated administration toxicity study of seed saponins of Thea sinensis L. (ryokucha saponin) in rats.CrossRef | 1:CAS:528:DyaK2cXksFWqsL8%3D&md5=e7e7df282f3abdaadc5d528c7e5a9f57CAS | 8206442PubMed |

Klita PT, Mathinson GW, Fenton TW, Hardin RT (1996) Effects of alfalfa root saponins on digestive function in sheep. Journal of Animal Science 74, 1144–1156.

Littell RC, Henry PR, Ammerman CB (1998) Statistical analysis of repeated measures data using SAS procedures. Journal of Animal Science 76, 1216–1231.

Mao HL, Wang JK, Zhou YY, Liu JK (2010) Effects of addition of tea saponins and soybean oil on methane production, fermentation and microbial population in the rumen of growing lambs. Livestock Science 129, 56–62.
Effects of addition of tea saponins and soybean oil on methane production, fermentation and microbial population in the rumen of growing lambs.CrossRef |

Meagher LP, Smith BL, Wilkins AL (2001) Metabolism of diosgenin derived saponins: implications for hepatogenous photosensitization diseases in ruminants. Animal Feed Science and Technology 91, 157–170.
Metabolism of diosgenin derived saponins: implications for hepatogenous photosensitization diseases in ruminants.CrossRef | 1:CAS:528:DC%2BD3MXktV2ntrw%3D&md5=617dfa3fd06abf82a70e60a4ec5d4bb5CAS |

Moses T, Pollier J, Almagro L, Buyst D, Van Montagu M, Pedreño MA, Msrtins JC, Thevelein JM, Goossens A (2014) Combinatorial biosynthesis of sapogenins and saponins in Saccharomyces cerevisiae using a C-16α hydroxylase from Bupleurum falcatum. Proceedings of the National Academy of Sciences, USA 111, 1634–1639.
Combinatorial biosynthesis of sapogenins and saponins in Saccharomyces cerevisiae using a C-16α hydroxylase from Bupleurum falcatum.CrossRef | 1:CAS:528:DC%2BC2cXhs1Siur4%3D&md5=cd27bbab80fdd8253230b69f40dffe4aCAS |

Oda K, Matsuda H, Murakami T, Katayama S, Ohgitani T, Yoshikawa M (2000) Adjuvant and haemolytic activities of 47 saponins derived from medicinal and food plants. Biological Chemistry 381, 67–74.
Adjuvant and haemolytic activities of 47 saponins derived from medicinal and food plants.CrossRef | 1:CAS:528:DC%2BD3cXit1ymt78%3D&md5=2922ca3d898b5fd40ff42fc29ed06e42CAS | 10722052PubMed |

Oleszek WA (2002) Chromatographic determination of plant saponins. Journal of Chromatography. A 967, 147–162.
Chromatographic determination of plant saponins.CrossRef | 1:CAS:528:DC%2BD38XlsVOltLc%3D&md5=dce12e7671ba81b850638a87b2977834CAS | 12219927PubMed |

Potter DA, Redmond CT, Meepagala KM, Williams DW (2009) Managing earthworm casts (Oligochaeta: Lumbricidae) in turfgrass using natural byproduct of tea oil (Camelia sp.) manufacture. Pest Management Science 66, 439–446.

Ramírez-Restrepo CA, Barry TN (2005) Alternative temperate forages containing secondary compounds for improving sustainable productivity in grazing ruminants: a review. Animal Feed Science and Technology 120, 179–201.
Alternative temperate forages containing secondary compounds for improving sustainable productivity in grazing ruminants: a review.CrossRef |

Ramírez-Restrepo CA, Barry TN, Marriner A, López-Villalobos N, McWilliam EL, Lassey KR, Clark H (2010) Effect of grazing willow fodder blocks upon methane production and blood composition in young sheep. Animal Feed Science and Technology 141, 61–81.

Ramírez-Restrepo CA, O’Neill CJ, López-Villalobos N, Padmanabha J, McSweeney C (2014) Tropical cattle methane emissions: the role of natural statins supplementation. Animal Production Science 54, 1294–1299.
Tropical cattle methane emissions: the role of natural statins supplementation.CrossRef |

Ramírez-Restrepo CA, Clark H, Muetzel S (2015) Methane emissions from young and mature dairy cattle. Animal Production Science.
Methane emissions from young and mature dairy cattle.CrossRef |

Saleem M, Nazir M, Ali MS, Hussain H, Lee YS, Riaz N, Jabbar A (2010) Antimicrobial natural products: an update on future antibiotic drug candidates. Natural Product Reports 27, 238–254.
Antimicrobial natural products: an update on future antibiotic drug candidates.CrossRef | 1:CAS:528:DC%2BC3cXht1Sntbo%3D&md5=8bef0c1ce9c3be61895035bb2f90af01CAS | 20111803PubMed |

SAS (2013) ‘User’s guide: statistics, version 9.4.’ (Statistical Analysis Software: Cary, NC)

Schmidt M, Schmidt H-J, Baumgart A, Guédon D, Netsch MI, Kreuter M-H, Schmidlin CB, Schrenk D (2005) Toxicity of green tea extracts and their constituents in rat hepatocytes in primary culture. Food and Chemical Toxicology 43, 307–314.
Toxicity of green tea extracts and their constituents in rat hepatocytes in primary culture.CrossRef | 1:CAS:528:DC%2BD2MXhtVKjuw%3D%3D&md5=8ae6b32478b5877a222e714ebdf60764CAS | 15621343PubMed |

Schulman JH, Rideal EK (1937) Molecular interaction in monolayers. II. The action of haemolytic and agglutinating agents on lipo-protein monolayers. Proceedings of the Royal Society of London. Series B, Biological Sciences 122, 46–57.
Molecular interaction in monolayers. II. The action of haemolytic and agglutinating agents on lipo-protein monolayers.CrossRef | 1:CAS:528:DyaA2sXitVyiuw%3D%3D&md5=7d4a9633f29a02861fe5535d11620075CAS |

Sjölander A, Cox JC, Barr IG (1998) ISCOMs: an adjuvant with multiple functions. Journal of Leukocyte Biology 64, 713–723.

Sparg SG, Light ME, van Staden J (2004) Biological activities and distribution of plant saponins. Journal of Ethnopharmacology 94, 219–243.
Biological activities and distribution of plant saponins.CrossRef | 1:CAS:528:DC%2BD2cXmvFWktrc%3D&md5=bf568d763a8226b42d9dad9fc1cf0e98CAS | 15325725PubMed |

Tedeschi LO, Ramírez-Restrepo CA, Muir JP (2014) Developing a conceptual model of possible benefits of condensed tannins for ruminant production. Animal 8, 1095–1105.
Developing a conceptual model of possible benefits of condensed tannins for ruminant production.CrossRef | 1:CAS:528:DC%2BC2cXpvVWkt7w%3D&md5=d060489dc4f159a2f53aa6509dac034eCAS | 24784919PubMed |

Thakur M, Melzig MF, Fuchs H, Weng A (2011) Chemistry and pharmacology of saponins: special focus on cytotoxic properties. Botanics: Targets and Therapy 1, 19–29.

Thornton PK, Herrero M (2015) Adapting to climate change in the mixed crop and livestock farming systems in sub-Saharan Africa. Nature Climate Change
Adapting to climate change in the mixed crop and livestock farming systems in sub-Saharan Africa.CrossRef |

Vincken JP, Heng L, de Groot A, Gruppen H (2007) Saponins, classification and occurrence in the plant kingdom. Phytochemistry 68, 275–297.
Saponins, classification and occurrence in the plant kingdom.CrossRef | 1:CAS:528:DC%2BD2sXntlGmsw%3D%3D&md5=0438fa453bf673b5d8fc1c673e7aa6e7CAS | 17141815PubMed |

Yuan ZP, Zhang CM, Zhou L, Zou CX, Guo YQ, Li WT, Liu JX, Wu YM (2007) Inhibition of methanogenesis by tea saponin and tea saponin plus disodium fumarate in sheep. Journal of Animal and Feed Sciences 16, 560–565.

Zhang X-F, Han Y-Y, Bao G-H, Ling T-J, Zhang L, Gao L-P, Xia T (2012) A new saponin from tea seed pomace (Camellia oleifera Abel) and its protective effect on PC12 cells. Molecules (Basel, Switzerland) 17, 11721–11728.
A new saponin from tea seed pomace (Camellia oleifera Abel) and its protective effect on PC12 cells.CrossRef | 1:CAS:528:DC%2BC38XhvVyisbfK&md5=5f118c989ff043b3955d4c03d69221c2CAS |

Zhao YL, Cai GM, Hong X, Shan LM, Xiao XH (2008) Anti-hepatitis B virus activities of triterpenoid saponin compound from potentilla anserine L. Phytomedicine 15, 253–258.
Anti-hepatitis B virus activities of triterpenoid saponin compound from potentilla anserine L.CrossRef | 1:CAS:528:DC%2BD1cXntV2hu7o%3D&md5=c6a3b24d6d679d851b3f9425eecbc5a6CAS | 18337074PubMed |

Zhou YY, Mao HL, Jiang F, Wang JK, Liu JX, McSweeney CS (2011) Inhibition of rumen methanogenesis by tea saponins with reference to fermentation pattern and microbial communities in Hu sheep. Animal Feed Science and Technology 166–167, 93–100.
Inhibition of rumen methanogenesis by tea saponins with reference to fermentation pattern and microbial communities in Hu sheep.CrossRef |



Rent Article (via Deepdyve) Export Citation Cited By (2)