Beyond Methane: Residual Methane Emission Is Associated with Productive, Metabolic, and Sustainability Traits in Beef Cattle

Enteric methane (CH4) mitigation strategies should reduce environmental impact without compromising animal productivity. Residual methane emission (RME) has been proposed as a phenotype for identifying cattle that emit more or less methane than predicted after accounting for relevant sources of variation, but its associations with host metabolism, carcass, and integrated sustainability remain poorly characterized. This retrospective study evaluated whether Nellore steers classified according to RME differed in ruminal fermentation, serum and meat metabolomic profiles, productive performance, economic indicators, and environmental efficiency. Twenty-nine steers were classified as low (n = 10), intermediate (n = 9), or high (n = 10) residual methane emitters based on RME calculated after adjustment for the original dietary treatment, mean daily dry matter intake, and metabolic body weight. Methane emissions were measured using the GreenFeed system, while ruminal fermentation, serum and meat metabolomes (H-NMR), productive performance, carcass traits, economic indicators, carbon credit scenarios, and integrated sustainability indices were evaluated. Low-RME animals emitted 23.6% less methane than high-RME animals (p < 0.001), while showing average daily gain, carcass gain, and final carcass weight comparable to those of high-RME animals (p > 0.05). Differences in ruminal fermentation were also observed among phenotypes, with low-RME animals showing a greater propionate-to-acetate ratio and intermediate-RME animals showing greater acetate concentration and acetate-to-propionate ratio (p < 0.05). Exploratory principal component analysis revealed partial separation of serum metabolomic profiles but no overall discrimination of meat metabolomes. In contrast, sparse partial least squares analysis identified an exploratory multimetabolite pattern associated with RME, with serum glutamine, creatinine, carnitine, serine, citrate, and meat succinate among the metabolites contributing most strongly to the observed differentiation among methane emission phenotypes. Low emitters also achieved the greatest carcass margin, carbon credit revenue, eco-efficiency, and integrated sustainability score while exhibiting the shortest distance to the theoretical ideal sustainability point (p < 0.05). These findings indicate that residual methane emission represents a multidimensional biological phenotype integrating ruminal fermentation, host intermediary metabolism, productive efficiency, and environmental performance. Selecting cattle with low residual methane emissions may therefore contribute simultaneously to climate-smart beef production, improved eco-efficiency, and enhanced economic sustainability.