Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Animal Production Science Animal Production Science Society
Food, fibre and pharmaceuticals from animals
RESEARCH ARTICLE

Effect of Leucaena leucocephala and corn oil on ruminal fermentation, methane production and fatty acid profile: an in vitro study

Agung Irawan https://orcid.org/0000-0003-1179-0469 A B D , Cuk Tri Noviandi B ,   Kustantinah B , Budi Prasetyo Widyobroto B , Andriyani Astuti B and Serkan Ates C
+ Author Affiliations
- Author Affiliations

A Vocational School, Universitas Sebelas Maret, Surakarta 57126, Indonesia.

B Faculty of Animal Science, Universitas Gadjah Mada, Yogyakarta 55281, Indonesia.

C Department of Animal and Rangeland Sciences, Oregon State University, Corvallis, OR 97333, USA.

D Corresponding author. Email: a.irawan@staff.uns.ac.id

Animal Production Science 61(5) 459-469 https://doi.org/10.1071/AN20003
Submitted: 4 January 2020  Accepted: 29 October 2020   Published: 24 November 2020

Abstract

Aims: This in vitro study aimed to examine the effect of proportions of Leucaena (Leucaena leucocephala (Lam.) de Wit) to Napier grass (Pennisetum purpureum Schumach) or levels of corn oil (CO) and their interaction on ruminal fermentation, methane (CH4) production and fatty acid profile.

Methods: The experiment was conducted as a 4 × 3 factorial arrangement following a completely randomised design with two factors. The treatments were according to the proportion of Leucaena and Napier grass (in g/kg DM, Treatment (T)1 = 0 : 750 (control), T2 = 250 : 500, T3 = 500 : 250, T4 = 750 : 0). Three levels of CO (in mg rumen fluid, CO1 = 0, CO2 = 10, CO3 = 20 respectively) were added to each of the diet, giving a total 12 dietary treatments.

Key results: Replacing Napier grass with Leucaena at 500 g/kg (T3) and 750 g/kg (T4) levels increased the molar volatile fatty acid concentration, microbial protein synthesis (P < 0.001) and ammonia nitrogen concentration (P = 0.003), whereas ruminal protozoa concomitantly decreased (P < 0.05). The addition of CO at 10 mg also reduced the number of ruminal protozoa compared with the control (P < 0.001). A significant Leucaena × CO interaction was observed on the increase of ammonia nitrogen and microbial protein synthesis, and CH4 production was simultaneously suppressed (P < 0.001). There was also a significant Leucaena × CO interaction on increasing concentration of C18:1 cis-9, C18:2 cis-10 cis-12 and α-linolenic acid, which thus contributed to the increase of n-3 polyunsaturated fatty acids accumulation in the culture (P < 0.001). However, the concentration of C18:0 was not influenced by the treatments (P > 0.05).

Conclusion: This study demonstrated that the inclusion of Leucaena into a Napier grass-based diet at 500 g/kg and 750 g/kg DM positively affected rumen fermentation, reduced CH4 formation and increased beneficial fatty acids in the rumen. Although CO had similar positive effects on CH4 production and targeted beneficial fatty acids, it reduced the microbial protein synthesis at inclusion of 20 mg/mL DM. Overall, there were synergistic interactions between Leucaena and CO in reducing CH4 production and improving the fatty acid profile in the rumen.

Implications: It is possible to improve animal productivity while reducing the environmental impact of livestock production through inclusion of tannin-containing Leucaena and CO in ruminant diets in tropical regions where C4 grasses typically have low nutritive value.

Keywords: biohydrogenation, methanogenesis, ruminant, tanniferous legume.


References

Aboagye IA, Beauchemin KA (2019) Potential of molecular weight and structure of tannins to reduce methane emissions from ruminants: a review. Animals 9, 856
Potential of molecular weight and structure of tannins to reduce methane emissions from ruminants: a review.Crossref | GoogleScholarGoogle Scholar |

AbuGhazaleh AA, Ishlak A (2014) Effects of incremental amounts of fish oil on trans fatty acids and Butyrivibrio bacteria in continuous culture fermenters. Journal of Animal Physiology and Animal Nutrition 98, 271–278.
Effects of incremental amounts of fish oil on trans fatty acids and Butyrivibrio bacteria in continuous culture fermenters.Crossref | GoogleScholarGoogle Scholar | 23581938PubMed |

Ahmed MA, Jusoh S, Alimon AR, Ebrahimi M, Samsudin AA (2018) Nutritive and anti-nutritive evaluation of Kleinhovia hospita, Leucaena leucocephala and Gliricidia sepium with respect to their effects on in vitro rumen fermentation and gas production. Tropical Animal Science Journal 41, 128–136.
Nutritive and anti-nutritive evaluation of Kleinhovia hospita, Leucaena leucocephala and Gliricidia sepium with respect to their effects on in vitro rumen fermentation and gas production.Crossref | GoogleScholarGoogle Scholar |

AOAC (2005) ‘Official methods of analysis.’ 18th edn. (Association of Analytical Chemists: Arlington, VA)

Beauchemin KA, Mcginn SM, Martinez TF, McAllister TA (2007) Use of condensed tannin extract from quebracho trees to reduce methane emissions from cattle 1. Journal of Animal Science 85, 1990–1996.
Use of condensed tannin extract from quebracho trees to reduce methane emissions from cattle 1.Crossref | GoogleScholarGoogle Scholar | 17468433PubMed |

Beauchemin KA, Kreuzer M, McAllister TA (2008) Nutritional management for enteric methane abatement: a review. Australian Journal of Experimental Agriculture 48, 21–27.
Nutritional management for enteric methane abatement: a review.Crossref | GoogleScholarGoogle Scholar |

Beauchemin KA, Mcginn SM, Benchaar C, Holtshausen L (2009) Crushed sunflower, flax, or canola seeds in lactating dairy cow diets: effects on methane production, rumen fermentation, and milk production. Journal of Dairy Science 92, 2118–2127.
Crushed sunflower, flax, or canola seeds in lactating dairy cow diets: effects on methane production, rumen fermentation, and milk production.Crossref | GoogleScholarGoogle Scholar | 19389969PubMed |

Bhatta R, Saravanan M, Baruah L, Sampath KT (2012) Nutrient content, in vitro ruminal fermentation characteristics and methane reduction potential of tropical tannin-containing leaves. Journal of the Science of Food and Agriculture 92, 2929–2935.
Nutrient content, in vitro ruminal fermentation characteristics and methane reduction potential of tropical tannin-containing leaves.Crossref | GoogleScholarGoogle Scholar | 22522493PubMed |

Chaney AL, Marbach EP (1962) Modified reagent for determination urea and ammonia. Clinical Chemistry 8, 130–132.
Modified reagent for determination urea and ammonia.Crossref | GoogleScholarGoogle Scholar | 13878063PubMed |

Costa DFA, Quigley SP, Isherwood P, Mclennan SR, Sun XQ, Gibbs SJ, Poppi DP (2017) The inclusion of low quantities of lipids in the diet of ruminants fed low quality forages has little effect on rumen function. Animal Feed Science and Technology 234, 20–28.
The inclusion of low quantities of lipids in the diet of ruminants fed low quality forages has little effect on rumen function.Crossref | GoogleScholarGoogle Scholar |

Dilzer A, Park Y (2012) Health implication of conjugated linoleic acid (CLA) in human health. Critical Reviews in Food Science and Nutrition 52, 488–513.
Health implication of conjugated linoleic acid (CLA) in human health.Crossref | GoogleScholarGoogle Scholar | 22452730PubMed |

Elghandour MMY, Vallejo LH, Salem AZM, Salem MZM, Camacho LM, Odongo NE (2017) Effects of Schizochytrium microalgae and sunflower oil as sources of unsaturated fatty acids for the sustainable mitigation of ruminal biogases methane and carbon dioxide. Journal of Cleaner Production 168, 1389–1397.
Effects of Schizochytrium microalgae and sunflower oil as sources of unsaturated fatty acids for the sustainable mitigation of ruminal biogases methane and carbon dioxide.Crossref | GoogleScholarGoogle Scholar |

Girón JEP, Restrepo LMP, Fornaguera JEC (2016) Supplementation with corn oil and palm kernel oil to grazing cows: ruminal fermentation, milk yield, and fatty acid profile. Revista Brasileira de Zootecnia 45, 693–703.
Supplementation with corn oil and palm kernel oil to grazing cows: ruminal fermentation, milk yield, and fatty acid profile.Crossref | GoogleScholarGoogle Scholar |

Gómez-Cortés P, Gallardo B, Mantecón AR, Juárez M, de la Fuente MA, Manso T (2014) Effects of different sources of fat (calcium soap of palm oil vs. extruded linseed) in lactating ewes’ diet on the fatty acid profile of their suckling lambs. Meat Science 96, 1304–1312.
Effects of different sources of fat (calcium soap of palm oil vs. extruded linseed) in lactating ewes’ diet on the fatty acid profile of their suckling lambs.Crossref | GoogleScholarGoogle Scholar | 24334053PubMed |

Harrison MT, McSweeney C, Tomkins NW, Eckard RJ (2015) Improving greenhouse gas emissions intensities of subtropical and tropical beef farming systems using Leucaena leucocephala. Agricultural Systems 136, 138–146.
Improving greenhouse gas emissions intensities of subtropical and tropical beef farming systems using Leucaena leucocephala.Crossref | GoogleScholarGoogle Scholar |

Hristov AN, Oh J, Firkins JL, Dijkstra J, Kebreab E, Waghorn G, Makkar HPS, Adesogan AT, Yang W, Lee C, Gerber PJ, Henderson B, Tricarico JM (2013) Special topics: mitigation of methane and nitrous oxide emissions from animal operations: I. A review of enteric methane mitigation options. Journal of Animal Science 91, 5045–5069.
Special topics: mitigation of methane and nitrous oxide emissions from animal operations: I. A review of enteric methane mitigation options.Crossref | GoogleScholarGoogle Scholar | 24045497PubMed |

Jayanegara A, Leiber F, Kreuzer M (2012) Meta-analysis of the relationship between dietary tannin level and methane formation in ruminants from in vivo and in vitro experiments. Journal of Animal Physiology and Animal Nutrition 96, 365–375.
Meta-analysis of the relationship between dietary tannin level and methane formation in ruminants from in vivo and in vitro experiments.Crossref | GoogleScholarGoogle Scholar | 21635574PubMed |

Jiménez-Peralta FS, Salem AZM, Mejia-Hernández P, González-Ronquillo M, Albarrán-Portillo B, Rojo-Rubio R, Tinoco-Jaramillo JL (2011) Influence of individual and mixed extracts of two tree species on in vitro gas production kinetics of high-concentrate diet fed to growing lambs. Livestock Science 136, 192–200.
Influence of individual and mixed extracts of two tree species on in vitro gas production kinetics of high-concentrate diet fed to growing lambs.Crossref | GoogleScholarGoogle Scholar |

Judy JV, Bachman GC, Fernando SC, Hales KE, Miller PS, Stowell RR, Kononoff PJ (2019) Reducing methane production with corn oil and calcium sulfate: responses on whole-animal energy and nitrogen balance in dairy cattle. Journal of Dairy Science 102, 2054–2067.
Reducing methane production with corn oil and calcium sulfate: responses on whole-animal energy and nitrogen balance in dairy cattle.Crossref | GoogleScholarGoogle Scholar | 30612805PubMed |

Khiaosa-Ard R, Bryner SF, Scheeder MRL, Wettstein H, Leiber F, Kreuzer M, Soliva CR (2009) Evidence for the inhibition of the terminal step of ruminal α-linolenic acid biohydrogenation by condensed tannins. Journal of Dairy Science 92, 177–188.
Evidence for the inhibition of the terminal step of ruminal α-linolenic acid biohydrogenation by condensed tannins.Crossref | GoogleScholarGoogle Scholar | 19109277PubMed |

Lunsin R, Wanapat M, Yuangklang C, Rowlinson P (2012) Effect of rice bran oil supplementation on rumen fermentation, milk yield and milk composition in lactating dairy cows. Livestock Science 145, 167–173.
Effect of rice bran oil supplementation on rumen fermentation, milk yield and milk composition in lactating dairy cows.Crossref | GoogleScholarGoogle Scholar |

Makkar HPS (2003) ‘Quantification of tannins in tree and shrub foliage: a laboratory manual.’ (Academic Publishers: Dordrecht, the Netherlands)

Mapato C, Wanapat M, Cherdthong A (2010) Effects of urea treatment of straw and dietary level of vegetable oil on lactating dairy cows. Tropical Animal Health and Production 42, 1635–1642.
Effects of urea treatment of straw and dietary level of vegetable oil on lactating dairy cows.Crossref | GoogleScholarGoogle Scholar | 20524063PubMed |

Matsushita M, Tazinafo NM, Padre RG, Oliveira CC, Souza NE, Visentainer JV, Macedo FAF, Ribas NP (2007) Fatty acid profile of milk from Saanen goats fed a diet enriched with three vegetable oils. Small Ruminant Research 72, 127–132.
Fatty acid profile of milk from Saanen goats fed a diet enriched with three vegetable oils.Crossref | GoogleScholarGoogle Scholar |

McAllister TA, Newbold CJ (2008) Redirecting rumen fermentation to reduce methanogenesis. Australian Journal of Experimental Agriculture 48, 7–13.
Redirecting rumen fermentation to reduce methanogenesis.Crossref | GoogleScholarGoogle Scholar |

McSweeney CS, Palmer B, McNeill DM, Krause DO (2001) Microbial interactions with tannins: nutritional consequences for ruminants. Animal Feed Science and Technology 91, 83–93.
Microbial interactions with tannins: nutritional consequences for ruminants.Crossref | GoogleScholarGoogle Scholar |

Menke BYKH, Raab L, Salewski A, Steingass H (1979) The estimation of the digestibility and metabolizable energy content of ruminant feeding stuffs from the gas production when they are incubated with rumen liquor in vitro. The Journal of Agricultural Science 93, 217–222.
The estimation of the digestibility and metabolizable energy content of ruminant feeding stuffs from the gas production when they are incubated with rumen liquor in vitro.Crossref | GoogleScholarGoogle Scholar |

Naumann HD, Tedeschi LO, Huntley NF (2017) The role of condensed tannins in ruminant animal production: advances, limitations and future directions. Revista Brasileira de Zootecnia 46, 929–949.
The role of condensed tannins in ruminant animal production: advances, limitations and future directions.Crossref | GoogleScholarGoogle Scholar |

Nguyen TTG, Wanapat M, Phesatcha K, Kang S (2017) Effect of inclusion of different levels of Leucaena silage on rumen microbial population and microbial protein synthesis in dairy cows. Asian-Australasian Journal of Animal Sciences 30, 181–186.
Effect of inclusion of different levels of Leucaena silage on rumen microbial population and microbial protein synthesis in dairy cows.Crossref | GoogleScholarGoogle Scholar |

Noviandi CT, Eun J, Peel MD, Waldron BL, Min BR, Zobell DR, Miller RL (2014) Effects of energy supplementation in pasture forages on in vitro ruminal fermentation characteristics in continuous cultures. The Professional Animal Scientist 30, 13–22.
Effects of energy supplementation in pasture forages on in vitro ruminal fermentation characteristics in continuous cultures.Crossref | GoogleScholarGoogle Scholar |

Ogimoto K, Imai S (1980) ‘Atlas of rumen microbiology.’ (Japanese Science Society Press: Tokyo, Japan)

Patra AK (2014) A meta-analysis of the effect of dietary fat on enteric methane production, digestibility and rumen fermentation in sheep, and a comparison of these responses between cattle and sheep. Livestock Science 162, 97–103.
A meta-analysis of the effect of dietary fat on enteric methane production, digestibility and rumen fermentation in sheep, and a comparison of these responses between cattle and sheep.Crossref | GoogleScholarGoogle Scholar |

Piñeiro-Vázquez A, Rodolfo Canul-solis J, Jimenez-Ferrer G, Alayón-Gamboa J, Chay-Canul A, Ayala-Burgos AJ, Aguilar-Pérez C, Ku-Vera J (2018) Effect of condensed tannins from Leucaena leucocephala on rumen fermentation, methane production and population of rumen protozoa in heifers fed low-quality forage. Asian-Australasian Journal of Animal Sciences 31, 1738–1746.
Effect of condensed tannins from Leucaena leucocephala on rumen fermentation, methane production and population of rumen protozoa in heifers fed low-quality forage.Crossref | GoogleScholarGoogle Scholar | 29103289PubMed |

Plummer DT (1987) ‘An introduction practical laboratory.’ (McGraw-Hill Book Company LTD: New Delhi, India)

Rana KK, Wadhwa M, Bakshi MPS (2006) Seasonal variations in tannin profile of tree leaves. Asian-Australasian Journal of Animal Sciences 19, 1134–1138.
Seasonal variations in tannin profile of tree leaves.Crossref | GoogleScholarGoogle Scholar |

Rira M, Morgavi DP, Genestoux L, Djibiri S, Sekhri I, Doreau M (2019) Methanogenic potential of tropical feeds rich in hydrolysable tannins. Journal of Animal Science 97, 2700–2710.
Methanogenic potential of tropical feeds rich in hydrolysable tannins.Crossref | GoogleScholarGoogle Scholar | 31192352PubMed |

Saminathan M, Gan HM, Abdullah N, Wong C, Ramiah SK, Tan HY, Sieo CC, Ho YW (2017) Changes in rumen protozoal community by condensed tannin fractions of different molecular weights from a Leucaena leucocephala hybrid in vitro. Journal of Applied Microbiology 123, 41–53.
Changes in rumen protozoal community by condensed tannin fractions of different molecular weights from a Leucaena leucocephala hybrid in vitro.Crossref | GoogleScholarGoogle Scholar | 28434189PubMed |

Seresinhe T, Madushika SAC, Seresinhe Y, Lal PK, Ørskov ER (2012) Effects of tropical high tannin non legume and low tannin legume browse mixtures on fermentation parameters and methanogenesis using gas production technique. Asian-Australasian Journal of Animal Sciences 25, 1404–1410.
Effects of tropical high tannin non legume and low tannin legume browse mixtures on fermentation parameters and methanogenesis using gas production technique.Crossref | GoogleScholarGoogle Scholar | 25049496PubMed |

Soltan YA, Morsy AS, Sallam SMA, Lucas RC, Louvandini H, Kreuzer M, Abdalla AL (2013) Contribution of condensed tannins and mimosine to the methane mitigation caused by feeding Leucaena leucocephala. Archives of Animal Nutrition 67, 169–184.
Contribution of condensed tannins and mimosine to the methane mitigation caused by feeding Leucaena leucocephala.Crossref | GoogleScholarGoogle Scholar | 23742642PubMed |

Soltan YA, Morsy AS, Lucas RC, Abdalla AL (2016) Potential of mimosine of Leucaena leucocephala for modulating ruminal nutrient degradability and methanogenesis. Animal Feed Science and Technology 223, 20–31.

Stewart EK, Beauchemin KA, Dai X, MacAdam JW, Christensen RG, Villalba JJ (2019) Effect of tannin-containing hays on enteric methane emissions and nitrogen partitioning in beef cattle. Journal of Animal Science 97, 3286–3299.
Effect of tannin-containing hays on enteric methane emissions and nitrogen partitioning in beef cattle.Crossref | GoogleScholarGoogle Scholar | 31242504PubMed |

Szczechowiak J, Szumacher-Strabel M, El-Sherbiny E, Pers-Kamczyc P, Pawlak P, Cieslak A (2016) Rumen fermentation, methane concentration and fatty acid proportion in the rumen and milk of dairy cows fed condensed tannin and/or fish-soybean oils blend. Animal Feed Science and Technology 216, 93–107.
Rumen fermentation, methane concentration and fatty acid proportion in the rumen and milk of dairy cows fed condensed tannin and/or fish-soybean oils blend.Crossref | GoogleScholarGoogle Scholar |

Tan HY, Sieo CC, Abdullah N, Liang JB, Huang XD, Ho YW (2011) Effects of condensed tannins from Leucaena on methane production, rumen fermentation and populations of methanogens and protozoa in vitro. Animal Feed Science and Technology 169, 185–193.
Effects of condensed tannins from Leucaena on methane production, rumen fermentation and populations of methanogens and protozoa in vitro.Crossref | GoogleScholarGoogle Scholar |

Top S, Preston C, Dukes JS, Tharayil N (2017) Climate influences the content and chemical composition of foliar tannins in green and senesced tissues of Quercus rubra. Frontiers in Plant Science 8, 423
Climate influences the content and chemical composition of foliar tannins in green and senesced tissues of Quercus rubra.Crossref | GoogleScholarGoogle Scholar | 28559896PubMed |

Tubiello F, Salvatore M, Cóndor Golec R, Ferrara A, Rossi S, Biancalani R, Federici S, Jacobs H, Flammini A (2014) ‘Agriculture, forestry and other land use emissions by sources and removals by sinks.’ (FAO: Rome, Italy)

Van Soest PV, Robertson J, Lewis B (1991) Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. Journal of Dairy Science 74, 3583–3597.
Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition.Crossref | GoogleScholarGoogle Scholar |

Vasta V, Ya DR, Mele M, Serra A, Luciano G, Lanza M, Biondi L, Priolo A (2010) Bacterial and protozoal communities and fatty acid profile in the rumen of sheep fed a diet containing added tannins. Applied and Environmental Microbiology 76, 2549–2555.
Bacterial and protozoal communities and fatty acid profile in the rumen of sheep fed a diet containing added tannins.Crossref | GoogleScholarGoogle Scholar | 20173064PubMed |

Waghorn G (2008) Beneficial and detrimental effects of dietary condensed tannins for sustainable sheep and goat production: progress and challenges. Animal Feed Science and Technology 147, 116–139.
Beneficial and detrimental effects of dietary condensed tannins for sustainable sheep and goat production: progress and challenges.Crossref | GoogleScholarGoogle Scholar |

Wanapat M, Mapato C, Pilajun R, Toburan W (2011) Effects of vegetable oil supplementation on feed intake, rumen fermentation, growth performance, and carcass characteristic of growing swamp buffaloes. Livestock Science 135, 32–37.
Effects of vegetable oil supplementation on feed intake, rumen fermentation, growth performance, and carcass characteristic of growing swamp buffaloes.Crossref | GoogleScholarGoogle Scholar |

Wang M, Jing Y, Liu S, Gao J, Shi L, Vercoe P (2016) Soybean oil suppresses ruminal methane production and reduces content of coenzyme F420 in vitro fermentation. Animal Production Science 56, 627–633.
Soybean oil suppresses ruminal methane production and reduces content of coenzyme F420 in vitro fermentation.Crossref | GoogleScholarGoogle Scholar |

Wu D, Xu L, Tang S, He Z, Tan Z, Han X, Zhou C, Kang J, Wang M (2015) Supplementation of increasing amounts of linoleic acid to Leymus chinensis decrease methane production and improve fatty acid composition in vitro. European Journal of Lipid Science and Technology 117, 945–953.
Supplementation of increasing amounts of linoleic acid to Leymus chinensis decrease methane production and improve fatty acid composition in vitro.Crossref | GoogleScholarGoogle Scholar |