Asparagopsis taxiformis decreases enteric methane production from sheep
Xixi Li A F , Hayley C. Norman A , Robert D. Kinley B , Michael Laurence C , Matt Wilmot A , Hannah Bender C , Rocky de Nys D and Nigel Tomkins B EA CSIRO Agriculture, Centre for Environment and Life Sciences, Floreat, WA 6014, Australia.
B CSIRO Agriculture, Australian Tropical Sciences and Innovation Precinct James Cook University, Townsville, Qld 4811, Australia.
C College of Veterinary Medicine, Murdoch University, Murdoch, WA 6150, Australia.
D MACRO, The Centre for Macroalgal Resources and Biotechnology, College of Marine and Environmental Sciences, James Cook University, Townsville, Qld 4811, Australia.
E Meat and Livestock Australia, 527 Gregory Terrace, Fortitude Valley, Qld 4006, Australia.
F Corresponding author. Email: xixili.r@gmail.com
Animal Production Science 58(4) 681-688 https://doi.org/10.1071/AN15883
Submitted: 20 December 2015 Accepted: 2 August 2016 Published: 28 September 2016
Abstract
Asparagopsis taxiformis concentrates halogenated compounds that are known to inhibit cobamide-dependent methanogenesis in vitro and, therefore, has potential to mitigate enteric methane production. The present study investigated the effect of Asparagopsis on methane (CH4) production from sheep offered a high-fibre pelleted diet (offered at 1.2 × maintenance) at five inclusion levels of Asparagopsis for 72 days (0% (control), 0.5%, 1%, 2% and 3% organic matter basis as offered). Individual animal CH4 measurements were conducted at 21-day intervals using open-circuit respiration chambers. Asparagopsis inclusion resulted in a consistent and dose-dependent reduction in enteric CH4 production over time, with up to 80% CH4 mitigation at the 3% offered rate compared with the group fed no Asparagopsis (P < 0.05). Sheep fed Asparagopsis had a significantly lower concentration of total volatile fatty acids and acetate, but a higher propionate concentration. No changes in liveweight gain were identified. Supplementing Asparagopsis in a high-fibre diet (<2% organic matter) resulted in significant and persistent decreases in enteric methanogenesis over a 72-day period. Granulomatous and keratotic ruminal mucosa changes were identified in several sheep with Asparagopsis supplementation. While the outcomes of the present study may be extrapolated to feedlot to achieve the antimethanogenic effect associated with Asparagopsis, further work is required to define the long-term effects on productivity and animal health.
Additional keywords: halogenated compounds, macroalgae, methanogenesis, ruminal fermentation.
References
AFIA (2009) ‘Australian Fodder Industry Association laboratory methods manual.’ Publication No. 03/001 (AFIA: Melbourne)AOAC (2005) Official method 990.03. Protein (crude) in animal feed, combustion method. In ‘Official methods of analysis of AOAC International’. pp. 30–31. (AOAC International: Arlington, VA)
Australian’s National Greenhouse Accounts (2014) Quarterly update of Australia’s National Greenhouse Gas Inventory: June 2014. (Australian Government Department of the Environment and Energy) Available at https://www.environment.gov.au/climate-change/greenhouse-gas-measurement/publications/quarterly-update-australias-national-green house-gas-inventory-june-2014 [Verified 10 September 2016]
Beauchemin KA, Kreuzer M, O’Mara F, 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 | 1:CAS:528:DC%2BD1cXovVGn&md5=23b38df440406cdf954ea8c1fc39bac0CAS |
Burreson BJ, Moore RE, Roller (1976) Volatile halogen compounds in the alga Asparagopsis taxiformis (Rhodophyta). Journal of Agricultural and Food Chemistry 24, 856–861.
| Volatile halogen compounds in the alga Asparagopsis taxiformis (Rhodophyta).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XksVGju7k%3D&md5=105137499ea92acfd19c4ca7b30564c6CAS |
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 |
Faichney GJ, White GA (1983) ‘Methods for the analysis of feeds eaten by ruminants.’ (CSIRO, Division of Animal Production, Ian Clunies Ross Animal Research Laboratory: Melbourne)
Getachew G, Blümmel M, Makkar HPS, Becker K (1998) In vitro gas measuring techniques for assessment of nutritional quality of feeds: a review. Animal Feed Science and Technology 72, 261–281.
| In vitro gas measuring techniques for assessment of nutritional quality of feeds: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjvVWgsb4%3D&md5=bada1bec9779a75c46090c523c8bde02CAS |
Johnson ED, Wood AS, Stone JB, Moran ET (1972) Some effects of methane inhibition in ruminants (steers). Canadian Journal of Animal Science 52, 703–712.
| Some effects of methane inhibition in ruminants (steers).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3sXkt1SitQ%3D%3D&md5=18f5b7e380b30cae26f5c97d38da8c63CAS |
Klein L, Wright AG (2006) Construction and operation of open-circuit methane chambers for small ruminants. Australian Journal of Experimental Agriculture 46, 1257–1262.
| Construction and operation of open-circuit methane chambers for small ruminants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XpsFWltbs%3D&md5=f1f607ccd7ff7b8d3642f131dc99779eCAS |
Kraut JA, Madias NE (2007) Serum anion gap: its uses and limitations in clinical medicine. Clinical Journal of the American Society of Nephrology 2, 162–174.
| Serum anion gap: its uses and limitations in clinical medicine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht12rtrc%3D&md5=4d29aec332cd2719b4426286642c833eCAS | 17699401PubMed |
Li X (2014) Eremophila glabra reduces methane production in sheep. PhD thesis. University of Western Australia, Perth.
Lourenço SO, Barbarino E, De-Paula JC, Pereira LOdS, Marquez UML (2002) Amino acid composition, protein content and calculation of nitrogen-to-protein conversion factors for 19 tropical seaweeds. Phycological Research 50, 233–241.
| Amino acid composition, protein content and calculation of nitrogen-to-protein conversion factors for 19 tropical seaweeds.Crossref | GoogleScholarGoogle Scholar |
Machado L, Magnusson M, Paul NA, de Nys R, Tomkins N (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, Magnusson M, Paul NA, Kinley R, de Nys R, Tomkins N (2016a) Identification of bioactives from the red seaweed Asparagopsis taxiformis that promote antimethanogenic activity in vitro. Journal of Applied Phycology
| Identification of bioactives from the red seaweed Asparagopsis taxiformis that promote antimethanogenic activity in vitro.Crossref | GoogleScholarGoogle Scholar |
Machado L, Magnusson M, Paul N, Kinley R, de Nys R, Tomkins N (2016b) Dose–response effects of Asparagopsis taxiformis and Oedogonium sp. on in vitro fermentation and methane production. Journal of Applied Phycology 28, 1443–1452.
| Dose–response effects of Asparagopsis taxiformis and Oedogonium sp. on in vitro fermentation and methane production.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtVKiu7vP&md5=5c4e047f69a77fe6c33bd4c3f45df3a8CAS |
McCrabb GJ, Berger KT, Magner T, May C, Hunter RA (1997) Inhibiting methane production in Brahman cattle by dietary supplementation with a novel compound and the effects on growth. Australian Journal of Agricultural Research 48, 323–329.
| Inhibiting methane production in Brahman cattle by dietary supplementation with a novel compound and the effects on growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXislals7Y%3D&md5=218d9d20304c71a8d8d2e7871c3909f8CAS |
NHMRC (2013) ‘Australian code for the care and use of animals for scientific purposes.’ 8th edn. (National Health and Medical Research Council: Canberra)
O’Sullivan L, Murphy B, McLoughlin P, Duggan P, Lawlor PG, Hughes H, Gardiner GE (2010) Prebiotics from marine macroalgae for human and animal health applications. Marine Drugs 8, 2038–2064.
| Prebiotics from marine macroalgae for human and animal health applications.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXos12ksLw%3D&md5=55cd0c51632fdfe45e00ee5b3b45cf33CAS | 20714423PubMed |
Paul N, de Nys R, Steinberg P (2006a) 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 |
Paul NA, Cole L, de Nys R, Steinberg PD (2006b) Ultrastracutre of the gland of the red alga Asparagopsis armata (boonemaisoniaceae). Journal of Phycology 42, 637–645.
| Ultrastracutre of the gland of the red alga Asparagopsis armata (boonemaisoniaceae).Crossref | GoogleScholarGoogle Scholar |
Sawyer M, Hoover W, Sniffen C (1974) Effects of a ruminal methane inhibitor on growth and energy metabolism in the ovine. Journal of Animal Science 38, 908–914.
Suiter J (1994) Body condition scoring of sheep and goats. Farmnote 69. Department of Agriculture and Food Western Australia.
Svirbely JL, Alford WC, Von Oettingen WF (1947) Toxicity and narcotic action of mono-chloro-mono-bromo-methane with special reference to inorganic and volatile bromide in blood, urine, and brain. Federation Proceedings 6, 375
Tomkins NW, Colegate SM, Hunter RA (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 |
Wood JM, Kennedy FS, Wolfe RS (1968) Reaction of multihalogenated hydrocarbons with free and bound reduced vitamin B12. Biochemistry 7, 1707–1713.
| Reaction of multihalogenated hydrocarbons with free and bound reduced vitamin B12.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF1cXktFKhtbw%3D&md5=7d46bedbed666068348577a5fa592475CAS | 4870333PubMed |
