Ericaceous species reduce methane emissions in sheep and red deer: Respiration chamber measurements and predictions at the scale of European heathlands
Graphical abstract
Introduction
Atmospheric methane (CH4) is a potent greenhouse gas (GHG) that contributes to global warming and methane emissions from human activities have more than doubled since the 1700s (Houghton et al., 1990, p. xvi). Methane is key in GHG inventories due to its high global-warming potential (25 times more than CO2 for a 100 year time horizon) but shorter atmospheric lifespan (1/5–1/20) than CO2 (Solomon et al., 2007), which means that methane reduction might be an effective strategy of slowing global warming in the short-term, as Cain et al. (2019) models suggest. Antropogenic methane sources (i.e. agriculture, waste disposal and fossil fuels extraction) account for about 50–65% of total methane emissions [total = 542–852 Tg CH4 y−1, Stocker et al. (2013, p. 509)] and CH4 from ruminant enteric fermentation methanogenesis [87–94 Tg CH4 y−1, Stocker et al. (2013, p. 509)] contributes about 25% of methane emissions worldwide. Methanogenesis is carried out by the metabolic activities of archaeal microbes in the rumen, with hydrogen from carbohydrate fermentation reducing CO2 to form CH4. This process decreases the efficiency with which ruminants transform carbohydrates into energy, as it has been long demonstrated in calorimetric studies (Blaxter, 1962).
Plant matter constitutes one the main sources of bioenergy in the planet. Plant intracellular compounds, such as sugars and proteins, are highly digestible for vertebrates, but in most cases, constitute a small proportion of plant biomass. On the other hand, fibrous cell wall carbohydrates (mainly cellulose and hemicellulose) are abundant but their digestion in the vertebrate is dependent on the actions of the gut microbes. Although most vertebrates can, to some extent, digest fibre (cellulose, hemicellulose and xylans) through the microbial populations in the hind gut (caecum, colon and rectum), the most efficient fibre-digesters are those animals that accommodate fore-gut fermentation, as are ruminants (Church, 1988) and also pseudo-ruminant species, such as camelids, which methane emissions expressed on the basis of digestible fibre intake do not differ from the former group (Dittmann et al., 2014). Ruminants can transform and transfer the energy content of fibre to higher trophic levels (Fahey and Berger, 1988), which makes them a key link in the trophic chain to mobilise fibre as an abundant resource of energy.
Moss et al. (2000) and Martin et al. (2010) have revised the type of attempts used to reduce methanogenesis in ruminants as a means of increasing animal production efficiency. These authors categorised them into intervention on (i) rumen biome, (ii) food and (iii) and selection of low methane animal phenotypes. Some examples include the use of acetogens, alternative electron acceptors, propionate enhancers, probiotics to reduce protozoal ruminal populations, the use of feeds containing lipids or high quality/lower fibre sources of carbohydrates but at the high carbon footprint cost of producing these feeds. Although methane emissions by domestic ruminants have been quantified on a global scale (Stocker et al., 2013), our knowledge on methane emissions by domestic ruminants in extensive systems is poor, and even more limited is our information on emissions by wild ruminants. This is because data on methane emissions is lacking across ruminant species, with insufficient knowledge of their diets and seasonal variation, combined with inaccurate or non-existent data of the sizes of wild populations, as Pérez-Barbería (2017) pointed out.
Shrublands are widespread across the world, presenting a range in plant diversity from very high (e.g. South Africa fynbos) to low (UK moorland) (Hultén and Fries, 1986). The Class Calluno-Ulicetea comprises the vegetation of heathlands and grasslands dominated by Nardus stricta, mainly distributed across Europe (approx. 275,000 km2), with the largest areas being in Norway, Sweden, Iceland and the UK (Corine 2012); however, their area is fast shrinking (Fagúndez, 2013). These heathlands and grasslands comprise of mosaics of dwarf shrubs (Calluna vulgaris, Erica cinerea, Erica tetralix, Empetrum nigrum, Vaccinium myrtillus) and rough grasses (particularly Nardus) and sedges (Hultén and Fries, 1986). They are characteristic of acidic and nutrient-poor soils from dry, sandy, to boggy areas and expanses of open acidic and coniferous woodlands. Their species are stress-tolerant but poor inter-species competitors and are negatively affected by soil nutrient enrichment, as nitrogen enrichment experiments on Scottish heathland have demonstrated (Britton and Fisher, 2007).
Heathlands, including some of their soils, provide valuable ecosystem services for many reasons, including their constraining effects on global warming rate, and the provision of recreation and hunting resources (Cordingley, 2012). When heathlands develop on acidic peat soils these sites have a significant contribution to water storage, water flow regulation, migration of solutes and as land-based carbon and energy reservoirs (Rezanezhad et al., 2016). For example, in the UK, peat soils store over 3.2 billion tonnes of carbon (IUCN, 2017). Heathlands constitute areas of low human density and high biodiversity (Britton and Fisher, 2007), in which populations of valuable game resources and domestic animal stock can develop [eg. red deer (Pérez-Barbería et al., 2013), red grouse (Hudson and Newborn, 1995), sheep (Milligan et al., 2018)]. Ericaceous species constitute the principal woody perennial dietary components of hill sheep and red deer in the uplands of UK and northern Europe (Fig. 1), especially in winter, when the productivity of grass decreases substantially [sheep (Milner and Gwynne, 1974), red deer (Mitchell et al., 1977)]. In most mountain ranges and shrublands across Europe, heathlands are part of the habitat of iconic and economically important species, such as grouse, chamois, red deer, wild boar and ibex, contributing to the local economy of these otherwise poorly productive lands (Cordingley, 2012).
Despite the large size of sheep and red deer populations in many heathland areas [sheep (Milne et al., 1998), red deer (Clutton-Brock et al., 2004; Pérez-Barbería et al., 2013)] and the importance of the ecosystem services provided by heathlands (Cordingley, 2012), there is a paucity of information on methane emissions by wild red deer (Pérez-Barbería, 2017) and domestic ruminants on extensive production systems. One promising sustainable strategy of reducing methanogenesis in ruminants is the use of mixed diets of plants rich in secondary compounds, among them, polyphenolic compounds such as tannins, that are claimed to have the potential of reducing CH4 emissions, as indicated by the meta-analysis carried out by Jayanegara et al. (2012) on a collection on 30 studies, including in vivo and in vitro experiments.
Calluna and Vaccinium are common species in Palearctic heath (Hultén and Fries, 1986). Calluna vulgaris is an ericaceous perennial plant species dominant in many areas of the northern hemisphere in the European oceanic heathlands, which often forms mosaics with Vaccinium myrtillus, a genus also common in northern Asia, Greenland, Western Canada, and the Western United States (Hultén and Fries, 1986). Calluna contains a large proportion of phenolic secondary compounds (eg. tannins, condensed tannins) and many non-tannin phenolics (proanthocyanidins) (Tolera et al., 1997), and the leaves of Vaccinium are rich in tannins (Schonert and Friederi, 1970). These chemicals constitute one of the largest and most widespread groups of plant secondary compounds that ruminant herbivores ingest (Robbins, 1993, p. 252). Some of these compounds interact with proteins and carbohydrates, thus reducing the digestibility of the diet, as demonstrated on in vitro studies with increasing concentrations of condensed tannins (Tan et al., 2011); they can also interact with digestive enzymes and reduce their chemical activity (Robbins, 1993), as demonstrated by Makkar et al. (1988) using incubation in bovine rumen of substrates that varied in tannin concentration. Cutting down methane emissions from ruminant enteric fermentation by using diets containing plants that reduce rumen methanogenesis may not be straight forward, if the secondary compounds of these plants have a concomitant effect on the energy utilisation by the animal. For example, Piñeiro-Vázquez et al. (2017) found that using small concentrations (2–3%) of condensed tannins on a basal grass diet energy loss as methane was reduced (31–48%) without affecting intakes, but digestibilities were negatively affected, and similar results were obtained in vitro by Tan et al. (2011).
In this study we aimed to (i) assess how ericaceous species (Calluna and Vaccinium) in grass based diets reduce enteric methane emissions per unit of organic matter digestibility from sheep and red deer, using open-circuit respiration chambers; (ii) using the output of our models to make predictions, at the scale of European heathlands, on methane emissions from red deer and sheep on different dietary scenarios, and (iii) compare the predicted emissions against total methane emissions reported in GHG inventories at country level across Europe.
Section snippets
Animals and diets
Twenty-three castrated male sheep (Ovis aries; age = 2–3 y; body mass (kg): mean = 49.2, range = 40–65, sd = 7.8) and nine female red deer (Cervus elaphus; age = 2–5 y; body mass (kg): mean = 83.4, range = 65–97, sd = 11.4) were used. They were progressively familiarised to the experimental conditions to minimise the potential effect of stress of confinement in respiration chambers on their well-being; the process took up to 2 years in deer. Different experimental diets with varying proportions
Methane emissions in respiration chambers
The proportions of ericaceous species in the actual diet after correction for refusals ranged between 0.0 and 0.67 (mean = 0.47), mean DMI across experiments varied between 690 and 1380 g d−1 in sheep, and between 1152 and 1812 g d−1 in deer. Mean DOMI varied between 401 and 696 g d−1 in sheep, and between 746 and 1009 g d−1 in deer (Table 1). Across diets mean methane emissions from sheep ranged between 24.3 and 35.6 g kg−1 DOM, and from deer between 18.8 and 38.9 g kg−1 DOM (Table 1).
As
Discussion
Methane emissions per unit of DOMI decreased as the proportion of ericaceous species in the diet increased, this effect was stronger in red deer than in sheep, but this relationship was complex because of the significant interaction between the proportion of ericaceous species in the diet and DOMI.
Comparison of CH4 emission records across studies is not a trivial task because of differences in diet, intake level, animal species, units and methodology used, as it has been highlighted in a
Declaration of competing interest
No conflict of interest
Acknowledgements
Jim McLeod, Stuart Lamb, Sheilla Reid, David Hamilton, Donald Barrie and students of the European Union Leonardo da Vinci Programme provided assistance during the experiment. The following people and agencies provided information on population size and body weights of sheep and red deer: Ricardo García González, Sandro Lovari, Stefano Mattioli, Atidzhe Ahmed, András Náhlik, Ruth Carden, Lina Burbaitė, Carlos Fonseca, Juan Carranza, John Hetherington, José Luis Garrido Martín (Fedenca), Pablo
Authors' contribution
The experimental design and gas respiration trials were carried out by RWM and FJPB. FJP-B undertook the statistical analysis and wrote the paper. JG performed the bomb calorimetry measurements of urine samples and collaborated improving the paper. DS-P produced the heathland map and associated spatial data.
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