The red macroalgae Asparagopsis taxiformis is a potent natural antimethanogenic that reduces methane production during in vitro fermentation with rumen fluid
Robert D. Kinley A C , Rocky de Nys B , Matthew J. Vucko B , Lorenna Machado B and Nigel W. Tomkins A
+ Author Affiliations
- Author Affiliations
A CSIRO Agriculture, Australian Tropical Science and Innovation Precinct, James Cook University, Townsville, Qld 4811, Australia.
B MACRO-Centre for Macroalgal Resources and Biotechnology, College of Marine and Environmental Sciences, James Cook University, Townsville, Qld 4811, Australia.
C Corresponding author. Email: rob.kinley@csiro.au
Animal Production Science 56(3) 282-289 https://doi.org/10.1071/AN15576
Submitted: 14 September 2015 Accepted: 23 November 2015 Published: 9 February 2016
Abstract
Livestock feed modification is a viable method for reducing methane emissions from ruminant livestock. Ruminant enteric methane is responsible approximately to 10% of greenhouse gas emissions in Australia. Some species of macroalgae have antimethanogenic activity on in vitro fermentation. This study used in vitro fermentation with rumen inoculum to characterise increasing inclusion rates of the red macroalga Asparagopsis taxiformis on enteric methane production and digestive efficiency throughout 72-h fermentations. At dose levels ≤1% of substrate organic matter there was minimal effect on gas and methane production. However, inclusion ≥2% reduced gas and eliminated methane production in the fermentations indicating a minimum inhibitory dose level. There was no negative impact on substrate digestibility for macroalgae inclusion ≤5%, however, a significant reduction was observed with 10% inclusion. Total volatile fatty acids were not significantly affected with 2% inclusion and the acetate levels were reduced in favour of increased propionate and, to a lesser extent, butyrate which increased linearly with increasing dose levels. A barrier to commercialisation of Asparagopsis is the mass production of this specific macroalgal biomass at a scale to provide supplementation to livestock. Another area requiring characterisation is the most appropriate method for processing (dehydration) and feeding to livestock in systems with variable feed quality and content. The in vitro assessment method used here clearly demonstrated that Asparagopsis can inhibit methanogenesis at very low inclusion levels whereas the effect in vivo has yet to be confirmed.
Additional keyword: greenhouse gas, ruminant, seaweed.
References
Beauchemin KA, McAllister TA, McGinn SM (2009) Dietary mitigation of enteric methane from cattle. CAB Reviews No. 035 Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources 4, 1–18.| Dietary mitigation of enteric methane from cattle. CAB Reviews No. 035Crossref | GoogleScholarGoogle Scholar |
Bergman EN (1990) Energy contributions of volatile fatty acids from the gastrointestinal tract in various species. Physiological Reviews 70, 567–590.
Clarke KR, Gorley RN (2006) ‘Primer v6 user manual/tutorial.’ (PRIMER-E Ltd: Plymouth, UK)
Cone JW, van Gelder AH, Visscher GJW, Oudshoorn L (1996) Influence of rumen fluid and substrate concentration on fermentation kinetics measured with a fully automated time related gas production apparatus. Animal Feed Science and Technology 61, 113–128.
| Influence of rumen fluid and substrate concentration on fermentation kinetics measured with a fully automated time related gas production apparatus.Crossref | GoogleScholarGoogle Scholar |
Denman SE, Tomkins NW, McSweeney CS (2007) Quantitation and diversity analysis of ruminal methanogenic populations in response to the antimethanogenic compound bromochloromethane. FEMS Microbiology Ecology 62, 313–322.
| Quantitation and diversity analysis of ruminal methanogenic populations in response to the antimethanogenic compound bromochloromethane.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsValtr7E&md5=3b4d5b31de81b675f96bb2da5d913747CAS | 17949432PubMed |
Dubois B, Tomkins NW, Kinley RD, Bai M, Seymour S, Paul NA, de Nys R (2013) Effect of tropical algae as additives on rumen in vitro gas production and fermentation characteristics. American Journal of Plant Sciences 4, 34–43.
| Effect of tropical algae as additives on rumen in vitro gas production and fermentation characteristics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXjsFart74%3D&md5=cb2a0cf330a77dc7d0039452a6a43b91CAS |
Goering HK, van Soest PJ (1970) ‘Forage fiber analyses (apparatus, reagents, procedures, and some applications) Agriculture Handbook no. 379.’ (ARS-USDA: Washington, DC)
Henry B, Charmley E, Eckard R, Caughan JB, Hegarty R (2012) Livestock production in a changing climate: adaptation and mitigation research in Australia. Crop and Pasture Science 63, 191–202.
| Livestock production in a changing climate: adaptation and mitigation research in Australia.Crossref | GoogleScholarGoogle Scholar |
Horwitz W (Ed.) (2000) ‘Official methods of AOAC international.’ 17th edn. (Association of Official Analytical Chemists International: Gaithersburg, MD)
IPCC (2014) Climate change 2014: synthesis report. Contribution of Working Groups I, II, and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. (Eds RK Paachauri, LA Meyer) (IPCC: Geneva, Switzerland)
Johnson KA, Johnson DE (1995) Methane emissions from cattle. Journal of Animal Science 73, 2483–2492.
Kinley R, Fredeen A (2015) In vitro evaluation of feeding North Atlantic stormtoss seaweeds on ruminal digestion. Journal of Applied Phycology 27, 2387–2393.
| In vitro evaluation of feeding North Atlantic stormtoss seaweeds on ruminal digestion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhvFKmtg%3D%3D&md5=feafcae1252a84710438f03f263d8319CAS |
Kirschke S, Bousquet P, Ciais P, Saunois M, Canadell JG, Dlugokencky EJ, Bergamaschi P, Bergmann D, Blake DR, Bruhwiler L, Cameron-Smith P, et al (2013) Three decades of global methane sources and sinks. Nature Geoscience 6, 813–823.
| Three decades of global methane sources and sinks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsVyqt7nN&md5=7297230dad6468f7301bd02071e5c545CAS |
Machado L, Magnusson M, Paul NA, de Nys R, Tomkins NW (2014) Effects of marine and freshwater macroalgae on in vitro total gas and methane production. PLoS One 9, e85289
| Effects of marine and freshwater macroalgae on in vitro total gas and methane production.Crossref | GoogleScholarGoogle Scholar | 24465524PubMed |
Machado L, Kinley RD, Magnusson M, de Nys R, Tomkins NW (2015a) The potential of macroalgae for beef production systems in Northern Australia. Journal of Applied Phycology 27, 2001–2005.
| The potential of macroalgae for beef production systems in Northern Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvFSntbvF&md5=bfce9daea2d88f0df908f7b0acae582bCAS |
Machado L, Magnusson M, Paul NA, Kinley RD, de Nys R, Tomkins NW (2015b) Dose-response effects of Asparagopsis taxiformis and Oedogonium sp. on in vitro fermentation and methane production. Journal of Applied Phycology
| Dose-response effects of Asparagopsis taxiformis and Oedogonium sp. on in vitro fermentation and methane production.Crossref | GoogleScholarGoogle Scholar |
Mitsumori M, Shinkai T, Takenaka A, Enishi O, Higuchi K, Kobayashi Y, Nonaka I, Asanuma N, Denman SE, McSweeney CS (2012) Responses in digestion, rumen fermentation and microbial populations to inhibition of methane by a halogenated methane analogue. British Journal of Nutrition 108, 482–491.
| Responses in digestion, rumen fermentation and microbial populations to inhibition of methane by a halogenated methane analogue.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFClu7fK&md5=83b9473bdb1c81c275a8f41dc27dae8eCAS | 22059589PubMed |
Morgavi D, Forano E, Martin C, Newbold CJ (2010) Microbial ecosystem and methanogenesis in ruminants. Animal 4, 1024–1036.
| Microbial ecosystem and methanogenesis in ruminants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmvVajtr0%3D&md5=b95aa96aedc98e44e77cbe2f14f00d3fCAS | 22444607PubMed |
NHMRC (2013) ‘Australian code for the care and use of animals for scientific purposes.’ 8th edn. (National Health and Medical Research Council: Canberra)
Olivier JGJ, van Aardenne JA, Dentener FJ, Pagliari V, Ganzeveld LN, Peters JAHW (2005) Recent trends in global greenhouse gas emissions: regional trends 1970–2000 and spatial key sources in 2000. Environmental Sciences 2, 81–99.
| Recent trends in global greenhouse gas emissions: regional trends 1970–2000 and spatial key sources in 2000.Crossref | GoogleScholarGoogle Scholar |
Patra AK (2012) Enteric methane mitigation technologies for ruminant livestock: a synthesis of current research and future directions. Environmental Monitoring and Assessment 184, 1929–1952.
| Enteric methane mitigation technologies for ruminant livestock: a synthesis of current research and future directions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjtFOjsbw%3D&md5=557523d59d2a947b93943c81b3a8200cCAS | 21547374PubMed |
Paul N, Tseng CK (2012) Seaweed. In ‘Aquaculture: farming aquatic animals and plants’. 2nd edn. (Eds JS Lucas, PC Southgate) pp. 268–284. (Blackwell Publishing Ltd: Oxford)
Paul N, de Nys R, Steinberg P (2006) Chemical defence against bacteria in the red alga Asparagopsis armata: linking structure with function. Marine Ecology Progress Series 306, 87–101.
| Chemical defence against bacteria in the red alga Asparagopsis armata: linking structure with function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjtFejsbw%3D&md5=097bd8f247e8572448e069ef89f32e15CAS |
Pellikaan WF, Hendriks WH, Uwimana G, Bongers LJGM, Becker PM, Cone JW (2011) A novel method to determine simultaneously methane production during in vitro gas production using fully automated equipment. Animal Feed Science and Technology 68, 196–220.
| A novel method to determine simultaneously methane production during in vitro gas production using fully automated equipment.Crossref | GoogleScholarGoogle Scholar |
R Core Team (2013) ‘R: A language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna, Austria) Available at http://www.R-project.org/ [Verified 11 November 2015]
Tomkins NW, Colegate S, Hunter R (2009) A bromochloromethane formulation reduces enteric methanogenesis in cattle fed grain-based diets. Animal Production Science 49, 1053–1058.
| A bromochloromethane formulation reduces enteric methanogenesis in cattle fed grain-based diets.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVWqtLnE&md5=a58afb32860a8af661d3dcc368b5abc9CAS |
Wang Y, Xu Z, Bach S, McAllister T (2008) Effects of phlorotannins from Ascophyllum nodosum (brown seaweed) on in vitro ruminal digestion of mixed forage or barley grain. Animal Feed Science and Technology 145, 375–395.
| Effects of phlorotannins from Ascophyllum nodosum (brown seaweed) on in vitro ruminal digestion of mixed forage or barley grain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpsVKrt70%3D&md5=53f3a357015651652b9adc3b16f95e73CAS |
