Individual-level correlations of rumen volatile fatty acids with enteric methane emissions for ranking methane yield in sheep fed fresh pasture
Arjan Jonker A K , Sharon Hickey B , Paul Boma A D , Chernet Woyimo Woju A E F J , Edgar Sandoval A , Sarah MacLean A , Mariana García Rendón Calzada A F , Wanjie Yu A G H I , Sarah Lewis A , Peter H. Janssen A , John C. McEwan C and Suzanne Rowe CA Grasslands Research Centre, AgResearch Ltd, Tennent Drive, Private Bag 11008, Palmerston North 4442, New Zealand.
B Ruakura Research Centre, AgResearch Ltd, 10 Bisley Road, Private Bag 3123, Hamilton 3214, New Zealand.
C Invermay Agricultural Centre, AgResearch Ltd, Puddle Alley Private Bag 50034, Mosgiel 9053, New Zealand.
D Nabuin Zonal Agricultural Research and Development Institute, National Agricultural Research Organisation, Nabuin Zardi, PO Box 132, Moroto, Uganda.
E Ethiopian Biotechnology Institute, Debrezeit Road, Addis Ababa, 1000 Ethiopia.
F Mizan-Tepi University, College of Agriculture and Natural Resources, Department of Animal Science, 21 Tepi Bushira, PO Box 260, Mizan-Tepi, Ethiopia.
G Universidad Nacional Autónoma de México, Facultad de Medicina Veterinaria y Zootecnia, Ciudad Universitaria, Av. Universidad #3000, Colonia, C.U., Coyoacán, 04510 Ciudad de México, Mexico.
H Animal Nutrition Group, Wageningen University and Research, De Elst 1, PO Box 338, 6708 WD, Wageningen, The Netherlands.
I Department of Animal Science, Animal Nutrition and Physiology, Aarhus University, Blichers Alle 20, DK-8830 Tjele, Denmark.
J Current address: Auckland Bioengineering Institute, The University of Auckland, 70 Symonds Street, Grafton, Auckland 1010, New Zealand.
K Corresponding author. Email: arjan.jonker@agresearch.co.nz
Animal Production Science 61(3) 300-305 https://doi.org/10.1071/AN20128
Submitted: 6 March 2020 Accepted: 16 September 2020 Published: 17 November 2020
Abstract
Context: Total ruminal volatile fatty acids (VFA) or acetate concentrations were previously found to be moderate correlated proxies to select sheep that are genetically low methane (CH4) emitters. However, this was based on trials, with sheep fed lucerne pellets at a fixed feeding level, which is different from pastoral farming conditions in New Zealand, where the correlated proxy would be applied.
Aim: To determine repeatability and individual-level correlation of rumen VFAs with CH4 emissions in sheep fed ad libitum cut pasture in three and four repeated periods in Experiments 1 and 2 respectively. Sheep in Experiment 1 were also fed lucerne pellets at 2.0 × maintenance-energy requirements in two periods.
Methods: Methane emissions were measured from 96 and 72 animals, in Experiments 1 and 2 respectively, in respiration chambers and rumen samples were collected via oral stomach tubing before morning feeding. Repeatability estimates between periods within feed and experiment serve as an upper threshold for the estimate of heritability and ri estimates are a proxy for genetic correlation.
Key results: Methane (g/day) production and yield (g/kg dry-matter intake) were low to moderately repeatable traits on pasture across periods (0.58 and 0.39 for CH4 production and 0.43 and 0.32 for yield in Experiments 1 and 2 respectively). On pasture, repeatability was generally greater for VFA proportions (0.13–0.32) than for VFA concentrations (0.02–0.24), while the opposite was the case on lucerne pellets. Rumen propionate as a proportion of total VFA had strong negative ri (−0.82 and −0.87) and acetate : propionate ratio (A : P; 0.82 and 0.78) and (acetate + butyrate) : (propionate + valerate) ratio (AB : PV; 0.84 and 0.82) had a strong positive ri with CH4 yield in sheep fed cut pasture, while the ri of total ruminal VFA (−0.13 and 0.35) and acetate (−0.08 and 0.38) concentrations with CH4 yield were only moderate and non-significant.
Conclusion: The VFA traits propionate proportion and A : P and AB : PV ratios had strong individual-level correlations with CH4 yield in sheep fed pasture ad libitum, suggesting that they would be useful correlated proxies to rank sheep CH4 yields.
Keywords: correlated proxy, indicator trait, reticulo-rumen fermentation, short-chain fatty acids.
References
Bain WE, Bezuidenhout L, Jopson NB, Pinares-Patiño CS, McEwan JC (2014) Rumen differences between sheep identified as being low or high methane emitters. Proceedings of the Association for the Advancement of Animal Breeding and Genetics 20, 376–378.Demeyer DI, Nevel CJ (1975) Methanogenesis, an integrated part of carbohydrate fermentation and its control. In ‘Digestion and metabolism in the ruminant’. (Eds IW McDonald, ACI Warner) pp. 366–382. (The University of New England Publishing Unit: Armidale, NSW, Australia)
Difford GF, Olijhoek DW, Hellwing ALF, Lund P, Bjerring MA, de Haas Y, Lassen J, Løvendahl P (2018) Ranking cows’ methane emissions under commercial conditions with sniffers versus respiration chambers. Acta Agriculturæ Scandinavica. Section A, Animal Science 68, 25–32.
Gilmour AR, Gogel BJ, Cullis BR, Thompson R (2009) ‘ASReml user guide release 3.0.’ (VSN International Ltd: Hemel Hempstead, UK)
Herd R, Bird SH, Donoghue KA, Arthur P, Hegarty R (2013) Phenotypic association between methane production traits, volatile fatty acids and animal breeding traits. Proceedings of the Association for the Advancement of Animal Breeding and Genetics 20, 286–289.
Janssen PH (2010) Influence of hydrogen on rumen methane formation and fermentation balances through microbial growth kinetics and fermentation thermodynamics. Animal Feed Science and Technology 160, 1–22.
| Influence of hydrogen on rumen methane formation and fermentation balances through microbial growth kinetics and fermentation thermodynamics.Crossref | GoogleScholarGoogle Scholar |
Jonker A, Hickey S, McEwan J, Rowe S, Aharoni Y, Molano G, Sandoval E, Bain W, Elmes S, Dodds K, MacLean S, Knowledr K, Bryson B, Pinares-Patino C (2018a) Rumen characteristics and total tract digestibility in low and high methane yield selection line sheep offered fresh good or poor quality pasture. Proceedings of the World Congress on Genetics Applied to Livestock Production 11, 366
Jonker A, Hickey SM, Rowe SJ, Janssen PH, Shackell G, Elmes S, Bain WE, Wing J, Greer GJ, Bryson B, MacLean S, Dodds KG, Pinares-Patiño CS, Young EA, Knowler K, Pickering NK, McEwan JC (2018b) Genetic parameters of methane emissions determined using portable accumulation chambers in lambs and ewes grazing pasture and genetic correlations with emissions determined in respiration chambers. Journal of Animal Science 96, 3031–3042.
| Genetic parameters of methane emissions determined using portable accumulation chambers in lambs and ewes grazing pasture and genetic correlations with emissions determined in respiration chambers.Crossref | GoogleScholarGoogle Scholar | 29741677PubMed |
Jonker A, Molano G, Sandoval E, Taylor PS, Antwi C, Olinga S, Cosgrove GP (2018c) Methane emissions differ between sheep offered a conventional diploid, a high-sugar diploid or a tetraploid perennial ryegrass cultivar at two allowances at three times of the year. Animal Production Science 58, 1043–1048.
| Methane emissions differ between sheep offered a conventional diploid, a high-sugar diploid or a tetraploid perennial ryegrass cultivar at two allowances at three times of the year.Crossref | GoogleScholarGoogle Scholar |
Jonker A, Hickey SM, McEwan JC, Rowe SJ, Janssen PH, MacLean S, Sandoval E, Lewis S, Kjestrup H, Molano G, Agnew M, Young EA, Dodds KG, Knowler K, Pinares-Patiño CS (2019a) Genetic parameters of plasma and ruminal volatile fatty acids in sheep fed alfalfa pellets and genetic correlations with enteric methane emissions. Journal of Animal Science 97, 2711–2724.
| Genetic parameters of plasma and ruminal volatile fatty acids in sheep fed alfalfa pellets and genetic correlations with enteric methane emissions.Crossref | GoogleScholarGoogle Scholar | 31212318PubMed |
Jonker A, MacLean S, Woyimo Woju C, Garcia Rendon Calzada M, Yu W, Molano G, Hickey S, Pinares-Patiño CS, McEwan JC, Janssen PH, Sandoval E, Lewis S, Rowe S (2019b) Excreta emissions in progeny of low and high enteric methane yield selection line sheep fed pasture of different qualities. Animal Feed Science and Technology 257, 114289
| Excreta emissions in progeny of low and high enteric methane yield selection line sheep fed pasture of different qualities.Crossref | GoogleScholarGoogle Scholar |
Kamke J, Kittelmann S, Soni P, Li Y, Tavendale M, Ganesh S, Janssen PH, Shi W, Froula J, Rubin EM, Attwood GT (2016) Rumen metagenome and metatranscriptome analyses of low methane yield sheep reveals a Sharpea-enriched microbiome characterised by lactic acid formation and utilisation. Microbiome 4, 56
| Rumen metagenome and metatranscriptome analyses of low methane yield sheep reveals a Sharpea-enriched microbiome characterised by lactic acid formation and utilisation.Crossref | GoogleScholarGoogle Scholar | 27760570PubMed |
Kittelmann S, Pinares-Patino CS, Seedorf H, Kirk MR, Ganesh S, McEwan JC (2014) Two different bacterial community types are linked with the low-methane emission trait in sheep. PLoS One 9, e103171
| Two different bacterial community types are linked with the low-methane emission trait in sheep.Crossref | GoogleScholarGoogle Scholar | 25383707PubMed |
MfE (2018) ‘New Zealand’s greenhouse gas inventory 1990–2016.’ Available at http://www.mfe.govt.nz/node/23304/ [Verified 6 March 2020]
Palarea-Albaladejo J, Rooke JA, Nevison IM, Dewhurst RJ (2017) Compositional mixed modelling of methane emissions and ruminal volatile fatty acids from individual cattle and multiple experiments. Journal of Animal Science 95, 2467–2480.
Pinares-Patiño CS, Hunt C, Martin R, West J, Lovejoy P, Waghorn GC (2012) ‘Chapter 1: New Zealand Ruminant Methane Measurement Centre, AgResearch, Palmerston North. Technical manual on respiration chamber design.’ (Ministry of Agriculture and Forestry: Wellington, New Zealand) Available at https://globalresearchalliance.org/library/livestock-research-group-technical-manual-respiration-chamber-designs-february-2014/ [Verified 6 March 2020]
Pinares-Patiño CS, Hickey SM, Young EA, Dodds KG, MacLean S, Molano G, Sandoval E, Kjestrup H, Harland R, Hunt C, Pickering NK, McEwan JC (2013) Heritability estimates of methane emissions from sheep. Animal 7, 316–321.
| Heritability estimates of methane emissions from sheep.Crossref | GoogleScholarGoogle Scholar | 23739473PubMed |
Rowe SJ, Hickey SM, Jonker A, Hess MK, Janssen PH, Johnson P, Bryson B, Knowler K, Pinares-Patino C, Bain WE, Elmes S, Young E, Wing J, Waller E, Pickering N, McEwan JC (2019) Selection for divergent methane yield in New Zealand sheep: a ten-year perspective. In ‘Proceedings of the Association of Advancement in Animal Breeding and Genetics 23rd conference’, 27 October – 1 November 2019, University of New England, Armidale, New South Wales, Australia. pp. 306–309. Available at http://www.aaabg.org/aaabghome/AAABG23papers/75Rowe23306.pdf [Verified 5 October 2020]
Swainson N, Muetzel S, Clark H (2018) Updated predictions of enteric methane emissions from sheep suitable for use in the New Zealand national greenhouse gas inventory. Animal Production Science 58, 973–979.
| Updated predictions of enteric methane emissions from sheep suitable for use in the New Zealand national greenhouse gas inventory.Crossref | GoogleScholarGoogle Scholar |
Williams SRO, Hannah MC, Jacobs JL, Wales WJ, Moate PJ (2019) Volatile fatty acids in ruminal fluid can be used to predict methane yield of dairy cows. Animals 9, 1006
| Volatile fatty acids in ruminal fluid can be used to predict methane yield of dairy cows.Crossref | GoogleScholarGoogle Scholar |
Xiang R, McNally J, Rowe S, Jonker A, Pinares-Patino CS, Oddy VH, Vercoe PE, McEwan JC, Dalrymple BP (2016) Gene network analysis identifies rumen epithelial cell proliferation, differentiation and metabolic pathways perturbed by diet and correlated with methane production. Scientific Reports 6, 39022
| Gene network analysis identifies rumen epithelial cell proliferation, differentiation and metabolic pathways perturbed by diet and correlated with methane production.Crossref | GoogleScholarGoogle Scholar | 27966600PubMed |
Xiang R, McNally J, Bond J, Tucker D, Cameron M, Donaldson AJ, Austin KL, Rowe S, Jonker A, Pinares-Patino CS, McEwan JC, Vercoe PE, Oddy H, Dalrymple BP (2018) Across-experiment transcriptomics of sheep rumen identifies expression of lipid/oxo-acid metabolism and muscle cell junction genes associated with variation in methane-related phenotypes. Frontiers in Genetics 9, 330
| Across-experiment transcriptomics of sheep rumen identifies expression of lipid/oxo-acid metabolism and muscle cell junction genes associated with variation in methane-related phenotypes.Crossref | GoogleScholarGoogle Scholar | 30177952PubMed |
Zetouni L, Henryon M, Kargo M, Lassen J (2017) Direct multitrait selection realizes the highest genetic response for ratio traits. Journal of Animal Science 95, 1921–1925.
Zetouni L, Difford GF, Lassen J, Byskov MV, Norberg E, Løvendahl P (2018) Is rumination time an indicator of methane production in dairy cows? Journal of Dairy Science 101, 11074–11085.
| Is rumination time an indicator of methane production in dairy cows?Crossref | GoogleScholarGoogle Scholar | 30292552PubMed |
