Register      Login
Crop and Pasture Science Crop and Pasture Science Society
Plant sciences, sustainable farming systems and food quality
RESEARCH ARTICLE

Anti-methanogenic advantage of biserrula (Biserrula pelecinus) over subterranean clover (Trifolium subterraneum) from in vitro fermentation is maintained across growth stages and cutting treatments

Bidhyut Kumar Banik A B , Zoey Durmic B C , William Erskine https://orcid.org/0000-0002-2074-4299 A C E and Clinton Revell A D
+ Author Affiliations
- Author Affiliations

A Centre for Plant Genetics and Breeding, School of Agriculture and Environment, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.

B School of Agriculture and Environment, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.

C Institute of Agriculture, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.

D Department of Primary Industries and Regional Development, 3 Baron-Hay Court, South Perth, WA 6151, Australia.

E Corresponding author. Email: william.erskine@uwa.edu.au

Crop and Pasture Science 70(3) 263-272 https://doi.org/10.1071/CP18069
Submitted: 20 February 2018  Accepted: 31 January 2019   Published: 14 March 2019

Abstract

The annual forage legume biserrula (Biserrula pelecinus L.) offers a promising opportunity as a low-methanogenic, bioactive pasture for southern Australian grazing systems where subterranean clover (Trifolium subterraneum L.) is the dominant annual pasture legume. This in vitro study to assess methanogenic potential examined how growth stage and cutting of biserrula affect biomass, nutritive value and fermentative parameters including methanogenic potential compared with subterranean clover. Both species were grown in a glasshouse, where three growth-stage treatments comprised plant collection at vegetative, reproductive or maturity growth stages. Three cutting (simulated grazing) treatments included cutting at the vegetative or reproductive stage and an uncut control, with herbage collection at maturity. Methane production in biserrula was unaffected by the stage of growth. Other nutritive value and fermentative parameters varied significantly with growth stage, the highest fibre content and lowest crude protein (CP) being found at maturity. Regrowth from herbage cut at the reproductive stage had higher CP and lower biomass than other cut treatments. In biserrula, this regrowth also showed the highest fermentability of the three cutting treatments including elevated methane yield. Notwithstanding these treatment effects on fermentability, biserrula maintained its strong anti-methanogenic advantage over subterranean clover across all treatments, confirming its potential as an anti-methanogenic bioactive pasture.

Additional keywords: defoliation, in vitro fermentability.


References

AFIA (2003) Fodder analyst’s laboratory manual. In ‘A reference manual of standard methods for the analysis of fodder’. (Australian Fodder Industry Association Limited: Melbourne)

AFIA (2011) Laboratory methods manual. In ‘A reference manual of standard methods for the analysis of fodder’. (Australian Fodder Industry Association Limited: Melbourne)

AOAC (1990) ‘Official methods of analysis.’ (Association Official Analytical Chemists: Washington, DC, USA)

Aydin R, Kamalak A, Canbolat O (2007) Effect of maturity on the potential nutritive value of burr medic (Medicago polymorpha) hay. The Journal of Biological Sciences 7, 300–304.
Effect of maturity on the potential nutritive value of burr medic (Medicago polymorpha) hay.Crossref | GoogleScholarGoogle Scholar |

Ayres J, Nandra K, Turner A (1998) A study of the nutritive value of white clover (Trifolium repens L.) in relation to different stages of phenological maturity in the primary growth phase in spring. Grass and Forage Science 53, 250–259.
A study of the nutritive value of white clover (Trifolium repens L.) in relation to different stages of phenological maturity in the primary growth phase in spring.Crossref | GoogleScholarGoogle Scholar |

Baldwin RL, Thornley JH, Beever DE (1987) Metabolism of the lactating cow: II. Digestive elements of a mechanistic model. The Journal of Dairy Research 54, 107–131.
Metabolism of the lactating cow: II. Digestive elements of a mechanistic model.Crossref | GoogleScholarGoogle Scholar | 3819150PubMed |

Banik BK, Durmic Z, Erskine W, Ghamkhar K, Revell C (2013a) In vitro ruminal fermentation characteristics and methane production differ in selected key pasture species in Australia. Crop & Pasture Science 64, 935–942.
In vitro ruminal fermentation characteristics and methane production differ in selected key pasture species in Australia.Crossref | GoogleScholarGoogle Scholar |

Banik BK, Durmic Z, Erskine W, Nichols P, Ghamkhar K, Vercoe P (2013b) Variability of in vitro ruminal fermentation and methanogenic potential in the pasture legume biserrula (Biserrula pelecinus L.). Crop & Pasture Science 64, 409–416.
Variability of in vitro ruminal fermentation and methanogenic potential in the pasture legume biserrula (Biserrula pelecinus L.).Crossref | GoogleScholarGoogle Scholar |

Banik BK, Durmic Z, Erskine W, Revell CK, Vadhanabhuti J, McSweeney CS, Padmanabha J, Flematti GR, Algreiby AA, Vercoe PE (2016) Bioactive fractions from the pasture legume Biserrula pelecinus L. have an anti-methanogenic effect against key rumen methanogens. Anaerobe 39, 173–182.
Bioactive fractions from the pasture legume Biserrula pelecinus L. have an anti-methanogenic effect against key rumen methanogens.Crossref | GoogleScholarGoogle Scholar | 27060275PubMed |

Barreira JC, Visnevschi-Necrasov T, Pereira G, Nunes E, Oliveira MBP (2017) Phytochemical profiling of underexploited Fabaceae species: Insights on the ontogenic and phylogenetic effects over isoflavone levels. Food Research International 100, 517–523.
Phytochemical profiling of underexploited Fabaceae species: Insights on the ontogenic and phylogenetic effects over isoflavone levels.Crossref | GoogleScholarGoogle Scholar | 28964376PubMed |

Benchaar C, Rivest J, Pomar C, Chiquette J (1998) Prediction of methane production from dairy cows using existing mechanistic models and regression equations. Journal of Animal Science 76, 617–627.
Prediction of methane production from dairy cows using existing mechanistic models and regression equations.Crossref | GoogleScholarGoogle Scholar | 9498373PubMed |

Bernhoft A (2010) A brief review on bioactive compounds in plants. In ‘Bioactive compounds in plants—benefits and risks for man and animals’. (Ed. A Bernhoft) pp. 11–17. (The Norwegian Academy of Science and Letters: Oslo, Norway)

Blaxter K, Clapperton J (1965) Prediction of the amount of methane produced by ruminants. British Journal of Nutrition 19, 511–522.
Prediction of the amount of methane produced by ruminants.Crossref | GoogleScholarGoogle Scholar | 5852118PubMed |

Broderick G, Abrams S, Rotz C (1992) Ruminal in vitro degradability of protein in alfalfa harvested as standing forage or baled hay. Journal of Dairy Science 75, 2440–2446.
Ruminal in vitro degradability of protein in alfalfa harvested as standing forage or baled hay.Crossref | GoogleScholarGoogle Scholar | 1452848PubMed |

Buddle BM, Denis M, Attwood GT, Altermann E, Janssen PH, Ronimus RS, Pinares-Patiño CS, Muetzel S, Neil Wedlock D (2011) Strategies to reduce methane emissions from farmed ruminants grazing on pasture. Veterinary Journal 188, 11–17.
Strategies to reduce methane emissions from farmed ruminants grazing on pasture.Crossref | GoogleScholarGoogle Scholar |

Carr SJ, Howieson JG, Loi A, Michalk D (1996) Yield potential and soil type adaptation of Biserrula pelecinus—a new pasture legume for acid soils. In ‘Proceedings IVth International Symposium Plant Soil Interactions at Low pH’. 17–24 March 1996, Belo Horizonte, MG, Brazil. (Brazilian Soil Science Society: Viçosa, Minas Gerais State, Brazil)

Cassida K, Rodriguez J, Hesterman O, Griffin T, Patching S, Rust S (2000) Protein degradability and forage quality in maturing alfalfa, red clover, and birdsfoot trefoil. Crop Science 40, 209–215.
Protein degradability and forage quality in maturing alfalfa, red clover, and birdsfoot trefoil.Crossref | GoogleScholarGoogle Scholar |

Chaichi MR, Tow PG (2000) The effects of sowing rate, defoliation intensity and time of defoliation commencement on vegetative and reproductive growth of medic swards. Journal of Agricultural Science and Technology 2, 207–216.

Chaves AV, Waghorn GC, Brookes IM, Woodfield DR (2006) Effect of maturation and initial harvest dates on the nutritive characteristics of ryegrass (Lolium perenne L.). Animal Feed Science and Technology 127, 293–318.
Effect of maturation and initial harvest dates on the nutritive characteristics of ryegrass (Lolium perenne L.).Crossref | GoogleScholarGoogle Scholar |

Collins W, Rhodes I, Rossiter R, Palmer M (1983) The effect of defoliation on seed yield of two strains of subterranean clover grown in monocultures and in binary mixtures. Crop & Pasture Science 34, 671–679.
The effect of defoliation on seed yield of two strains of subterranean clover grown in monocultures and in binary mixtures.Crossref | GoogleScholarGoogle Scholar |

Conning S, Renton M, Ryan M, Nichols P (2011) Biserrula and subterranean clover can co-exist during the vegetative phase but are out-competed by capeweed. Crop & Pasture Science 62, 236–247.
Biserrula and subterranean clover can co-exist during the vegetative phase but are out-competed by capeweed.Crossref | GoogleScholarGoogle Scholar |

CSIRO (2007) ‘Nutrient requirements of domesticated ruminants.’ (CSIRO Publishing: Melbourne)

Dijkstra J, Neal HDSC, Beever DE, France J (1992) Simulation of nutrient digestion, absorption and outflow in the rumen: model description. The Journal of Nutrition 122, 2239–2256.
Simulation of nutrient digestion, absorption and outflow in the rumen: model description.Crossref | GoogleScholarGoogle Scholar | 1331382PubMed |

Durmic Z, McSweeney C, Kemp G, Hutton P, Wallace R, Vercoe P (2008) Australian plants with potential to inhibit bacteria and processes involved in ruminal biohydrogenation of fatty acids. Animal Feed Science and Technology 145, 271–284.
Australian plants with potential to inhibit bacteria and processes involved in ruminal biohydrogenation of fatty acids.Crossref | GoogleScholarGoogle Scholar |

Durmic Z, Hutton P, Revell D, Emms J, Hughes S, Vercoe P (2010) In vitro fermentative traits of Australian woody perennial plant species that may be considered as potential sources of feed for grazing ruminants. Animal Feed Science and Technology 160, 98–109.
In vitro fermentative traits of Australian woody perennial plant species that may be considered as potential sources of feed for grazing ruminants.Crossref | GoogleScholarGoogle Scholar |

Fulkerson W, Donaghy D (2001) Plant-soluble carbohydrate reserves and senescence—key criteria for developing an effective grazing management system for ryegrass-based pastures: a review. Australian Journal of Experimental Agriculture 41, 261–275.
Plant-soluble carbohydrate reserves and senescence—key criteria for developing an effective grazing management system for ryegrass-based pastures: a review.Crossref | GoogleScholarGoogle Scholar |

Fulkerson W, Neal J, Clark C, Horadagoda A, Nandra K, Barchia I (2007) Nutritive value of forage species grown in the warm temperate climate of Australia for dairy cows: grasses and legumes. Livestock Science 107, 253–264.
Nutritive value of forage species grown in the warm temperate climate of Australia for dairy cows: grasses and legumes.Crossref | GoogleScholarGoogle Scholar |

Griffin T, Cassida K, Hesterman O, Rust S (1994) Alfalfa maturity and cultivar effects on chemical and in situ estimates of protein degradability. Crop Science 34, 1654–1661.
Alfalfa maturity and cultivar effects on chemical and in situ estimates of protein degradability.Crossref | GoogleScholarGoogle Scholar |

Hides D, Lovatt J, Hayward MV (1983) Influence of stage of maturity on the nutritive value of Italian ryegrasses. Grass and Forage Science 38, 33–38.
Influence of stage of maturity on the nutritive value of Italian ryegrasses.Crossref | GoogleScholarGoogle Scholar |

Hoffman P, Sievert S, Shaver R, Welch D, Combs D (1993) In situ dry matter, protein, and fiber degradation of perennial forages. Journal of Dairy Science 76, 2632–2643.
In situ dry matter, protein, and fiber degradation of perennial forages.Crossref | GoogleScholarGoogle Scholar | 8227665PubMed |

Howieson JG, Loi A, Carr SJ (1995) Biserrula pelecinus L.—a legume pasture species with potential for acid, duplex soils which is nodulated by unique root-nodule bacteria. Australian Journal of Agricultural Research 46, 997–1010.
Biserrula pelecinus L.—a legume pasture species with potential for acid, duplex soils which is nodulated by unique root-nodule bacteria.Crossref | GoogleScholarGoogle Scholar |

Jones DIH, Wilson AD (1987) ‘Nutritive quality of forage.’ (Eds JB Hacker, JH Ternouth) (Academic Press: Sydney)

Keim JP, López IF, Berthiaume R (2014) Nutritive value, in vitro fermentation and methane production of perennial pastures as affected by botanical composition over a growing season in the south of Chile. Animal Production Science 54, 598–607.
Nutritive value, in vitro fermentation and methane production of perennial pastures as affected by botanical composition over a growing season in the south of Chile.Crossref | GoogleScholarGoogle Scholar |

Kleen J, Taube F, Gierus M (2011) Agronomic performance and nutritive value of forage legumes in binary mixtures with perennial ryegrass under different defoliation systems. The Journal of Agricultural Science 149, 73–84.
Agronomic performance and nutritive value of forage legumes in binary mixtures with perennial ryegrass under different defoliation systems.Crossref | GoogleScholarGoogle Scholar |

Langer RHM (1966) Mineral nutrition of grasses and cereals. In ‘Proceedings 12th Easter School in Agricultural Science’. University of Nottingham, 1965. (Eds FL Milthorpe, JD Ivins) (Butterworths: London)

Loi A, Carr S, Porqueddu C (1995) ‘Alternative pasture legumes and rhizobium collection in Sardinia.’ (Co-operative Research Centre for Legumes in Mediterranean Agriculture (CLIMA): Perth, W. Aust.)

Loi A, Howieson J, Carr S, Kelman W (2001) Register of Australian Herbage Plant Cultivars: B. Legumes, 25. Biserrula, Biserrula pelecinus L. (biserrula) cv. Casbah. Australian Journal of Experimental Agriculture 41, 841–842.
Register of Australian Herbage Plant Cultivars: B. Legumes, 25. Biserrula, Biserrula pelecinus L. (biserrula) cv. Casbah.Crossref | GoogleScholarGoogle Scholar |

Loi A, Howieson J, Nutt B, Carr S (2005a) A second generation of annual pasture legumes and their potential for inclusion in Mediterranean-type farming systems. Australian Journal of Experimental Agriculture 45, 289–299.
A second generation of annual pasture legumes and their potential for inclusion in Mediterranean-type farming systems.Crossref | GoogleScholarGoogle Scholar |

Loi A, Revell C, Nutt B (2005b) Casbah and Mauro Biserrula: Persistent pasture legumes for Mediterranean farming systems. Farmnote No. 37. Department of Agriculture, Western Australia, South Perth, W. Aust.

Loi A, Revell C, Nutt B (2005c) Domestication of new forage legumes improves the productivity and persistence of pastures in Mediterranean environments. In ‘Adaptation and management of forage legumes—strategies for improved reliability in mixed sward. Proceedings 1st COST 852 Workshop’. (Eds BE Frankow-Lindberg, RP Collins, A Luscher, MT Sebasria, A Helgadottir) pp. 165–175. (Swedish University of Agricultural Sciences: Ystad, Sweden)

Mahr-un-Nisa , Sarwar M, Ajmal Khan M (2004) Influence of urea treated wheat straw with or without corn steep liquor on feed consumption, digestibility and milk yield and its composition in lactating Nili-ravi buffaloes. Asian-Australasian Journal of Animal Sciences 17, 825–829.
Influence of urea treated wheat straw with or without corn steep liquor on feed consumption, digestibility and milk yield and its composition in lactating Nili-ravi buffaloes.Crossref | GoogleScholarGoogle Scholar |

Marinas A, García-González R, Fondevila M (2003) The nutritive value of five pasture species occurring in the summer grazing ranges of the Pyrenees. Animal Science 76, 461–469.
The nutritive value of five pasture species occurring in the summer grazing ranges of the Pyrenees.Crossref | GoogleScholarGoogle Scholar |

McDonald P, Edwards RA, Greenhalgh JFD (1988) ‘Animal nutrition.’ (Longman Group: Harlow, UK)

McDougall EI (1948) Studies on ruminant saliva. 1. The composition and output of sheep’s saliva. The Biochemical Journal 43, 99–109.
Studies on ruminant saliva. 1. The composition and output of sheep’s saliva.Crossref | GoogleScholarGoogle Scholar | 18889874PubMed |

Morley FHW, Katznelson J (1965) ‘Colonization in Australia by Trifolium subterraneum L.’ (Academic Press: New York and London)

Nichols PGH, Barbetti MJ, Collins WJ (1996) ‘Registered cultivars of subterranean clover: their characteristics, origin and identification.’ (Western Australian Department of Agriculture: South Perth, W. Aust.)

Nichols PGH, Loi A, Nutt BJ, Evans PM, Craig AD, Pengelly BC, Dear BS, Lloyd DL, Revell CK, Nair RM (2007) New annual and short-lived perennial pasture legumes for Australian agriculture—15 years of revolution. Field Crops Research 104, 10–23.
New annual and short-lived perennial pasture legumes for Australian agriculture—15 years of revolution.Crossref | GoogleScholarGoogle Scholar |

Nichols PGH, Revell CK, Humphries A, Howie J, Hall E, Sandral G, Ghamkhar K, Harris C (2012) Temperate pasture legumes in Australia—their history, current use and future prospects. Crop & Pasture Science 63, 691–725.
Temperate pasture legumes in Australia—their history, current use and future prospects.Crossref | GoogleScholarGoogle Scholar |

Norman H, Revell D, Mayberry D, Rintoul A, Wilmot M, Masters D (2010) Comparison of in vivo organic matter digestion of native Australian shrubs by sheep to in vitro and in sacco predictions. Small Ruminant Research 91, 69–80.
Comparison of in vivo organic matter digestion of native Australian shrubs by sheep to in vitro and in sacco predictions.Crossref | GoogleScholarGoogle Scholar |

Oddy VH, Robards GE, Low SG (1983) Prediction of in vivo dry matter digestibility from the fibre and nitrogen content of a feed. In ‘Feed information and animal production. Proceedings Second Symposium of the International Network of Feed Information Centres’. (Eds GE Robards, RG Packham) pp. 395–398. (Commonwealth Agricultural Bureaux: Farnham Royal, UK)

Okello S, Sabiiti E, Schwartz H (2005) Factors affecting in sacco dietary degradation by Ankole cattle grazing natural range pastures in Uganda. African Journal of Range & Forage Science 22, 157–166.
Factors affecting in sacco dietary degradation by Ankole cattle grazing natural range pastures in Uganda.Crossref | GoogleScholarGoogle Scholar |

Pinares-Patiño C, Waghorn G, Machmüller A, Vlaming B, Molano G, Cavanagh A, Clark H (2007) Methane emissions and digestive physiology of non-lactating dairy cows fed pasture forage. Canadian Journal of Animal Science 87, 601–613.
Methane emissions and digestive physiology of non-lactating dairy cows fed pasture forage.Crossref | GoogleScholarGoogle Scholar |

Robinson K, Bell LW, Bennett RG, Henry DA, Tibbett M, Ryan MH (2007) Perennial legumes native to Australia—a preliminary investigation of nutritive value and response to cutting. Australian Journal of Experimental Agriculture 47, 170–176.
Perennial legumes native to Australia—a preliminary investigation of nutritive value and response to cutting.Crossref | GoogleScholarGoogle Scholar |

Rossiter RC (1976) The influence of defoliation on vegetation growth in swards of three strains of subterranean clover. Crop & Pasture Science 27, 197–206.
The influence of defoliation on vegetation growth in swards of three strains of subterranean clover.Crossref | GoogleScholarGoogle Scholar |

Sarwar M, Ajmal Khan M (2003) Nitrogen retention and chemical composition of urea treated wheat straw ensiled with organic acids or fermentable carbohydrates. Asian-Australasian Journal of Animal Sciences 16, 1583–1592.
Nitrogen retention and chemical composition of urea treated wheat straw ensiled with organic acids or fermentable carbohydrates.Crossref | GoogleScholarGoogle Scholar |

Sarwar M, Mahr-un-Nisa , Ajmal Khan M, Mushtaque M (2006) Chemical composition, herbage yield and nutritive value of Panicum antidotale and Pennisetum orientale for Nili buffaloes at different clipping intervals. Asian-Australasian Journal of Animal Sciences 19, 176–180.
Chemical composition, herbage yield and nutritive value of Panicum antidotale and Pennisetum orientale for Nili buffaloes at different clipping intervals.Crossref | GoogleScholarGoogle Scholar |

Tavendale MH, Meagher LP, Pacheco D, Walker N, Attwood GT, Sivakumaran S (2005) Methane production from in vitro rumen incubations with Lotus pedunculatus and Medicago sativa, and effects of extractable condensed tannin fractions on methanogenesis. Animal Feed Science and Technology 123–124, 403–419.
Methane production from in vitro rumen incubations with Lotus pedunculatus and Medicago sativa, and effects of extractable condensed tannin fractions on methanogenesis.Crossref | GoogleScholarGoogle Scholar |

Turner N, Begg J, Wilson J (1978) Responses of pasture plants to water deficits. In ‘Plant relations in pastures’. (Ed. JR Wilson) pp. 50–66. (CSIRO: Melbourne)

Ugherughe PO (1986) Relationship between digestibility of Bromus inermis plant parts. Journal of Agronomy & Crop Science 157, 136–143.
Relationship between digestibility of Bromus inermis plant parts.Crossref | GoogleScholarGoogle Scholar |

Ulyatt M (1971) Studies on the causes of the differences in pasture quality between perennial ryegrass, short-rotation ryegrass, and white clover. New Zealand Journal of Agricultural Research 14, 352–367.
Studies on the causes of the differences in pasture quality between perennial ryegrass, short-rotation ryegrass, and white clover.Crossref | GoogleScholarGoogle Scholar |

Visnevschi-Necrasov T, Barreira JC, Cunha SC, Pereira G, Nunes E, Oliveira MBP (2015) Phylogenetic insights on the isoflavone profile variations in Fabaceae spp.: assessment through PCA and LDA. Food Research International 76, 51–57.
Phylogenetic insights on the isoflavone profile variations in Fabaceae spp.: assessment through PCA and LDA.Crossref | GoogleScholarGoogle Scholar |

Waghorn GC, Tavendale MH, Woodfield DR (2002) Methanogenesis from forage fed to sheep. Proceedings of the New Zealand Grassland Association 64, 159–165.

Warner J, Sharrow S (1984) Set stocking, rotational grazing and forward rotational grazing by sheep on western Oregon hill pastures. Grass and Forage Science 39, 331–338.
Set stocking, rotational grazing and forward rotational grazing by sheep on western Oregon hill pastures.Crossref | GoogleScholarGoogle Scholar |