Increasing the proportion of Leucaena leucocephala in hay-fed beef steers reduces methane yield
A. Stifkens A B , E. M. Matthews A , C. S. McSweeney C and E. Charmley
A *
+ Author Affiliations
- Author Affiliations
A CSIRO Agriculture and Food, Private Mail Bag PO Aitkenvale, Townsville, Qld 4814, Australia.
B University of Liège, Gembloux Agro-Bio Tech, 2 Passage des Déportés, 5030 Gembloux, Belgium.
C CSIRO Agriculture and Food, 306 Carmody Road, St Lucia, Qld 4067, Australia.
Animal Production Science 62(7) 622-632 https://doi.org/10.1071/AN21576
Submitted: 19 November 2021 Accepted: 21 January 2022 Published: 22 February 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)
Abstract
Context: Leucaena leucocephala (leucaena) is a leguminous shrub adapted to higher rainfall (>600 mm) in frost-free areas of Australia. It can be a source of high-quality forage for cattle grazing tropical grass-based pastures that are seasonally deficient in the nitrogen content required for adequate levels of performance. Leucaena contains bioactive compounds that may reduce methanogenesis in the rumen, helping to achieve Australia's goal to make red meat production carbon neutral by 2030.
Aim: A study was undertaken to evaluate the response in animal performance and methane production to increasing percentages of leucaena in a hay-based diet.
Methods: Growing steers were fed diets containing 0%, 18%, 36% and 48% leucaena. Intake, liveweight gain, methane production and yield were measured in a cross-over trial with two modern cultivars of leucaena (Redlands and Wondergraze). Methane was measured in open-circuit respiration chambers.
Key results: There were no effects of cultivar on most parameters. Increasing leucaena percentage in the diet increased dry matter intake, animal performance and methane production (g/day) but reduced methane yield (g/kg dry matter intake) according to the equation: methane yield = 19.8 − 0.09 × leucaena percentage in the diet. The inclusion of polyethylene glycol to nullify potential antimethanogenic activity of tannins restored methane yield by 67%, indicating that tannins were responsible for most of the observed reduction in methane yield.
Conclusion: The results demonstrate that leucaena can improve animal performance and reduce methane yield in steers fed low-quality grasses.
Implications: Leucaena can be included in diets of grazing cattle in areas agronomically suited to its production, as a means to reduce enteric methane emissions.
Keywords: Australia, cattle, greenhouse gas, intake, legume, methane, tannin, tropical.
References
Aboagye IA, Beauchemin KA (2019) Potential of molecular weight and structure of tannins to reduce methane emission from ruminants: a review. Animals 9, 856| Potential of molecular weight and structure of tannins to reduce methane emission from ruminants: a review.Crossref | GoogleScholarGoogle Scholar |
Aboagye IA, Oba M, Koenig KM, Zhao GY, Beauchemin KA (2019) Use of gallic acid and hydrolyzable tannins to reduce methane emission and nitrogen excretion in beef cattle fed a diet containing alfalfa silage. Journal of Animal Science 97, 2230–2244.
| Use of gallic acid and hydrolyzable tannins to reduce methane emission and nitrogen excretion in beef cattle fed a diet containing alfalfa silage.Crossref | GoogleScholarGoogle Scholar | 30906949PubMed |
Animut G, Puchala R, Goetsch AL, Patra AK, Sahlu T, Varel VH, Wells J (2008) Methane emission by goats consuming different sources of condensed tannins. Animal Feed Science and Technology 144, 228–241.
| Methane emission by goats consuming different sources of condensed tannins.Crossref | GoogleScholarGoogle Scholar |
Archimède H, Rira M, Barde DJ, Labirin F, Marie-Magdeleine C, Calif B, Periacarpin F, Fleury J, Rochette Y, Morgavi DP, Doreau M (2016) Potential of tannin-rich plants, Leucaena leucocephala, Glyricidia sepium and Manihot esculenta, to reduce enteric methane emissions in sheep. Journal of Animal Physiology and Animal Nutrition 100, 1149–1158.
| Potential of tannin-rich plants, Leucaena leucocephala, Glyricidia sepium and Manihot esculenta, to reduce enteric methane emissions in sheep.Crossref | GoogleScholarGoogle Scholar | 27870287PubMed |
Australian Greenhouse Emissions Information System (2019) National greenhouse gas inventory – Paris agreement. Paris Agreement Inventory. Australian Government, Canberra, ACT, Australia. http://climatechange.gov.au. (Accessed 15 October 2021)
Beauchemin KA, McGinn SM, Martinez TF, McAllister TA (2007) Use of condensed tannin extract from quebracho trees to reduce methane missions from cattle. Journal of Animal Science 85, 1990–1996.
| Use of condensed tannin extract from quebracho trees to reduce methane missions from cattle.Crossref | GoogleScholarGoogle Scholar | 17468433PubMed |
Beutel TS, Corbet DH, Hoffmann MB, Buck SR, Kienzle M (2018) Quantifying leucaena cultivation extent on grazing land. The Rangeland Journal 40, 31–38.
| Quantifying leucaena cultivation extent on grazing land.Crossref | GoogleScholarGoogle Scholar |
Bowen MK, Chudleigh F, Buck S, Hopkins K (2016) Productivity and profitability of forage options for beef production in the subtropics of northern Australia. Animal Production Science 58, 332–342.
| Productivity and profitability of forage options for beef production in the subtropics of northern Australia.Crossref | GoogleScholarGoogle Scholar |
Cardona CAC, Naranjo-Ramírez JF, Morales AMT, Correa GA, Rosales RB (2015) Dry matter and nutrient intake and diet composition in Leucaena leucocephala-based intensive silvopastoral systems. Tropical and Subtropical Agroecosystems 18, 303–311.
Chaney AL, Marbach EP (1962) Modified reagents for determination of urea and ammonia. Clinical Chemistry 8, 130–132.
| Modified reagents for determination of urea and ammonia.Crossref | GoogleScholarGoogle Scholar | 13878063PubMed |
Charmley E, Williams SRO, Moate PJ, Hegarty RS, Herd RM, Oddy VH, Reyenga P, Staunton KM, Anderson A, Hannah MC (2016) A universal equation to predict methane production of forage-fed cattle in Australia. Animal Production Science 56, 169–180.
| A universal equation to predict methane production of forage-fed cattle in Australia.Crossref | GoogleScholarGoogle Scholar |
Coates DB, Dixon RM (2011) Developing robust faecal near infrared spectroscopy calibrations to predict diet dry matter digestibility in cattle consuming tropical forages. Journal of Near Infrared Spectroscopy 19, 507–519.
| Developing robust faecal near infrared spectroscopy calibrations to predict diet dry matter digestibility in cattle consuming tropical forages.Crossref | GoogleScholarGoogle Scholar |
Dalzell SA, Burnett DJ, Dowsett JE, Forbes VE, Shelton HM (2012) Prevalence of mimosine and DHP toxicity in cattle grazing Leucaena leucocephala pastures in Queensland, Australia. Animal Production Science 52, 365–372.
| Prevalence of mimosine and DHP toxicity in cattle grazing Leucaena leucocephala pastures in Queensland, Australia.Crossref | GoogleScholarGoogle Scholar |
Gagen EJ, Wang J, Padmanabha J, Liu J, de Carvalho IPC, Liu J, Webb RI, Al Jassam R, Morrison M, Denman SE, McSweeney CS (2014) Investigation of a new acetogen isolated from an enrichment of the tamar wallaby forestomach. BMC Microbiology 7, 1122
| Investigation of a new acetogen isolated from an enrichment of the tamar wallaby forestomach.Crossref | GoogleScholarGoogle Scholar |
Harrison MT, McSweeney CS, 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 |
Herd RM, Arthur PF, Donoghue KA, Bird SH, Bird-Gardiner T, Hegarty RS (2014) Measures of methane production and their phenotypic relationships with growth and body composition traits in beef cattle. Journal of Animal Science 92, 5267–5274.
| Measures of methane production and their phenotypic relationships with growth and body composition traits in beef cattle.Crossref | GoogleScholarGoogle Scholar | 25349368PubMed |
Hove L, Topps JH, Sibanda S, Ndlovu LR (2001) Nutrient intake and utilisation by goats fed dried leaves of the shrubs legumes Acacia angustissima, Calliandra calothyrsus and Leucaena leucocephala as supplements to native pasture hay. Animal Feed Science and Technology 91, 95–106.
| Nutrient intake and utilisation by goats fed dried leaves of the shrubs legumes Acacia angustissima, Calliandra calothyrsus and Leucaena leucocephala as supplements to native pasture hay.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) 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.
| Mitigation of methane and nitrous oxide emissions from animal operations: I. A review of enteric methane mitigation options.Crossref | GoogleScholarGoogle Scholar | 24045497PubMed |
Huang XD, Liang JB, Tan HY, Yahya R, Ho YW (2011) Effects of Leucaena condensed tannins of differing molecular weights on in vitro CH4 production. Animal Feed Science and Technology 166, 373–376.
| Effects of Leucaena condensed tannins of differing molecular weights on in vitro CH4 production.Crossref | GoogleScholarGoogle Scholar |
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 |
Jones RJ, Palmer B (2002) Assessment of condensed tannin concertation in a collection of Leucaena species using 14C-labelled polyethylene glycol (PEG 4000). Tropical Grasslands 36, 47–53.
Keeney M, Katz I, Allison MJ (1962) On the probable origin of some milk fat acids in rumen microbial lipids. Journal of the American Oil Chemists’ Society 39, 198–201.
| On the probable origin of some milk fat acids in rumen microbial lipids.Crossref | GoogleScholarGoogle Scholar |
Kennedy PM, Charmley E (2012) Methane yields from Brahman cattle fed tropical grasses and legumes. Animal Production Science 52, 225–239.
| Methane yields from Brahman cattle fed tropical grasses and legumes.Crossref | GoogleScholarGoogle Scholar |
Klein L, Baker SK (1993) Composition of the fractions of dry, mature subterranean clover digested in vivo and in vitro. In ‘Proceedings of the 17th International Grassland Congress’. Palmerston North, Hamilton, Lincoln, NZ/Rockhampton, Qld. pp. 593–595. (International Grassland Congress)
Makkar HP (2003) ‘Quantification of tannins in tree and shrub foliage: a laboratory manual.’ (Kluwer Academic Publishers: Dordrecht, The Netherlands)
Martinez-Fernandez G, Denman SE, Yang C, Cheung J, Mitsumori M, McSweeney CS (2016) Methane inhibition alters the microbial community, hydrogen flow, and fermentation response in the rumen of cattle. Frontiers in Microbiology 7, 1122
| Methane inhibition alters the microbial community, hydrogen flow, and fermentation response in the rumen of cattle.Crossref | GoogleScholarGoogle Scholar | 27486452PubMed |
Martinez-Fernandez G, Denman SE, Cheung J, McSweeney CS (2017) Phloroglucinol degradation in the rumen promotes the redirection of hydrogen when methanogenesis is suppressed. Frontiers in Microbiology 8, 1871
| Phloroglucinol degradation in the rumen promotes the redirection of hydrogen when methanogenesis is suppressed.Crossref | GoogleScholarGoogle Scholar | 29051749PubMed |
McSweeney CS, Palmer B, Bunch R, Krause DO (1999) In vitro quality assessment of tannin-containing tropical shrub legumes: protein and fibre digestion. Animal Feed Science and Technology 82, 227–241.
| In vitro quality assessment of tannin-containing tropical shrub legumes: protein and fibre digestion.Crossref | GoogleScholarGoogle Scholar |
McSweeney CS, Palmer B, Bunch R, Krause DO (2001) Effect of the tropical forage calliandra on microbial protein synthesis and ecology in the rumen. Journal of Applied Microbiology 90, 78–88.
| Effect of the tropical forage calliandra on microbial protein synthesis and ecology in the rumen.Crossref | GoogleScholarGoogle Scholar | 11155126PubMed |
Meat & Livestock Australia (2021) CN30 overview CN30: carbon neutral by 2030. Meat & Livestock Australia, Sydney, NSW, Australia. http://mla.com.au (Accessed 15 October 2021)
Molina IC, Angarita EA, Mayorga OL, Chará J, Barahona-Rosales R (2016) Effect of Leucaena leucocephala on methane production of Lucerna heifers fed a diet based on Cynodon plectostachyus. Livestock Science 185, 24–29.
| Effect of Leucaena leucocephala on methane production of Lucerna heifers fed a diet based on Cynodon plectostachyus.Crossref | GoogleScholarGoogle Scholar |
Montoya-Flores MD, Molina-Botero IC, Arango J, Romano-Muñoz JL, Solorio-Sánchez FJ, Aguilar-Pérez CF, Ku-Vera JC (2020) Effect of dried leaves of Leucaena leucocephala on rumen fermentation, rumen microbial population, and enteric methane production in crossbred heifers. Animals 10, 300
| Effect of dried leaves of Leucaena leucocephala on rumen fermentation, rumen microbial population, and enteric methane production in crossbred heifers.Crossref | GoogleScholarGoogle Scholar |
Perry LA, Al Jassim R, Gaughan JB, Tomkins NW (2017) Effect of feeding forage characteristic of wet- or dry-season tropical C4 grass in northern Australia, on methane production, intake and rumen outflow rates in Bos indicus steers. Animal Production Science 57, 2033–2041.
| Effect of feeding forage characteristic of wet- or dry-season tropical C4 grass in northern Australia, on methane production, intake and rumen outflow rates in Bos indicus steers.Crossref | GoogleScholarGoogle Scholar |
Poppi DP, McLennan SR (2010) Nutritional research to meet future challenges. Animal Production Science 50, 329–338.
| Nutritional research to meet future challenges.Crossref | GoogleScholarGoogle Scholar |
Radrizzani A, Dalzell SA, Shelton HM (2011) Effect of environment and plant phenology on prediction of plant nutrient deficiency using leaf analysis in Leucaena leucocephala. Crop & Pasture Science 62, 248–260.
| Effect of environment and plant phenology on prediction of plant nutrient deficiency using leaf analysis in Leucaena leucocephala.Crossref | GoogleScholarGoogle Scholar |
Rira M, Morgavi DP, Archimède H, Marie-Magdeleine C, Popova M, Bousseboua H, Doreau M (2015) Potential of tannin-rich plants for modulating ruminal microbes and ruminal fermentation in sheep. Journal of Animal Science 93, 334–347.
| Potential of tannin-rich plants for modulating ruminal microbes and ruminal fermentation in sheep.Crossref | GoogleScholarGoogle Scholar | 25568379PubMed |
Satter LD, Slyter LL (1974) Effect of ammonia concentration on rumen microbial protein production in vitro. British Journal of Nutrition 32, 199–208.
| Effect of ammonia concentration on rumen microbial protein production in vitro.Crossref | GoogleScholarGoogle Scholar |
Shelton M, Brewbaker JL (1998) Leucaena leucocephala – the most widely used forage tree legume. In ‘Forage tree legumes in tropical agriculture’. (Eds RC Gutteridge, HM Shelton) pp. 15–29. (Tropical Grassland Society of Australia)
Shelton M, Dalzell S (2007) Production, economic and environmental benefits of leucaena pastures. Tropical Grasslands 41, 174–190.
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 |
Suybeng B, Charmley E, Gardiner CP, Malu-Aduli BS, Malau-Aduli AEO (2020) Supplementing northern Australian beef cattle with Desmanthus tropical legume reduces in vivo methane emissions. Animals 10, 2097
| Supplementing northern Australian beef cattle with Desmanthus tropical legume reduces in vivo methane emissions.Crossref | GoogleScholarGoogle Scholar |
Suybeng B, Mwangi FW, McSweeney CS, Charmley E, Gardiner CP, Malu-Aduli BS, Malau-Aduli AEO (2021) Response to climate change: evaluation of methane emissions in northern Australian beef cattle on a high quality diet supplemented with Desmanthus using open-circuit respiration chambers and GreenFeed emission monitoring systems. Biology 10, 2097
| Response to climate change: evaluation of methane emissions in northern Australian beef cattle on a high quality diet supplemented with Desmanthus using open-circuit respiration chambers and GreenFeed emission monitoring systems.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 |
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, 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 |
Tomkins N, Harrison M, McSweeney CS, Denman S, Charmley E, Lambrides CJ, Dalal R (2019) Greenhouse gas implications of leucaena-based pastures. Can we develop an emissions reduction methodology for the beef industry? Tropical Grasslands-Forrajes Tropicales 7, 267–272.
| Greenhouse gas implications of leucaena-based pastures. Can we develop an emissions reduction methodology for the beef industry?Crossref | GoogleScholarGoogle Scholar |
Ungerfeld EM (2020) Metabolic hydrogen flows in rumen fermentation: principles and possibilities of interventions. Frontiers in Microbiology 11, 589
| Metabolic hydrogen flows in rumen fermentation: principles and possibilities of interventions.Crossref | GoogleScholarGoogle Scholar | 32351469PubMed |
van Lingen HJ, Niu M, Kebreab E, Valadares Filho SC, Rooke JA, Duthie CA, Schwarm A, Kreuzer M, Hynd PI, Caetano M, Eugène M, Martin C, McGee M, O’Kiely P, Hünerberg M, McAllister TA, Berchielli TT, Messana JD, Peiren N, Chaves AV, Charmley E, Cole NA, Lee S-S, Berndt A, Reynolds CJ, Crompton LA, Bayat A, Yáñez-Ruiz DR, Yu Z, Bannink A, Dijkstra J, Casper DP, Hristov AN (2019) Prediction of beef cattle enteric methane production, yield and intensity using an intercontinental database. Agriculture, Ecosystems & Environment 283, 106575
| Prediction of beef cattle enteric methane production, yield and intensity using an intercontinental database.Crossref | GoogleScholarGoogle Scholar |
