Ericaceous species reduce methane emissions in sheep and red deer: Respiration chamber measurements and predictions at the scale of European heathlands

https://doi.org/10.1016/j.scitotenv.2020.136738Get rights and content

Highlights

  • Methane is a potent greenhouse gas and enteric fermentation one the main sources.

  • Heathland contains ericaceous species and provides valuable ecosystem services.

  • Sheep and red deer methane emissions decreased when fed ericaceous species.

  • Sheep and deer grazing on European heathland reduces by 0.5% total methane emissions.

  • Carbon credits on heathland grazing systems might help to reduce methane emissions.

Abstract

Despite the importance of atmospheric methane as a potent greenhouse gas and the significant contribution from ruminant enteric fermentation on methane emissions at a global scale, little effort has been made to consider the influence that different plant-based natural diets have on methane emissions in grazing systems. Heathland is an ericaceous dwarf-shrub-dominated habitat widespread across the northern hemisphere, in Europe, provides valuable ecosystem services in areas with poor soils, such as water flow regulation, land-based carbon skin, energy reservoir and habitat of key game species. We (i) measured methane emissions from red deer (Cervus elaphus) and sheep (Ovis aries) fed mixed diets of natural grass plus ericaceous species (either Calluna vulgaris or Vaccinium myrtillus) using open-circuit respiration chambers; and (ii) modelled the results to estimate methane emissions from red deer and sheep populations inhabiting heathland habitats across Europe under different scenarios of grass-based mixed diets with varying proportions of ericaceous species. Our results indicated that methane emissions per unit of digestible organic matter intake decreased as the proportion of ericaceous species in diet increased, but this relationship was complex because of the significant interaction between the proportion of ericaceous species in the diet and digestible organic matter intake. According to our estimates red deer and sheep populations across European heathlands produce 129.7 kt·y−1 methane (se = 1.79) based on a hypothetical grass-ericaceous species mixed diet containing 30% of ericaceous species; this is 0.5% of total methane emissions from human activity across Europe (24,755 kt·y−1), and a reduction in methane emissions of 63.8 kt·y−1 against the same deer and sheep populations, if assumed to consume a grass-only diet. We suggest the implementation of carbon credits as a measure to value the relevance of heathland systems to promote biodiversity and its potential contribution to reduce methane emissions in ruminant grazing systems.

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 FJPsingle bondB. 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.

References (94)

  • F.J. Pérez-Barbería

    Scaling methane emissions in ruminants and global estimates in wild populations

    Sci. Total Environ.

    (2017)
  • A. Pelchen et al.

    Methane emissions from sheep

    Small Rumin. Res.

    (1998)
  • R. Puchala et al.

    Methane emissions by goats consuming Sericea lespedeza at different feeding frequencies

    Anim. Feed Sci. Technol.

    (2012)
  • F. Rezanezhad et al.

    Structure of peat soils and implications for water storage, flow and solute transport: a review update for geochemists

    Chem. Geol.

    (2016)
  • H. Tan et al.

    Effects of condensed tannins from Leucaena on methane production, rumen fermentation and populations of methanogens and protozoa in vitro

    Anim. Feed Sci. Technol.

    (2011)
  • A. Tolera et al.

    Nutritive evaluation of some browse species

    Anim. Feed Sci. Technol.

    (1997)
  • Artemisan Fundation

    Economic and Social Assessment of Hunting in Spain

    (2018)
  • K.A. Beauchemin et al.

    Methane Emissions From Feedlot Cattle Fed Barley or Corn Diets

    (2005)
  • K. Beauchemin et al.

    Use of condensed tannin extract from quebracho trees to reduce methane emissions from cattle

    J. Anim. Sci.

    (2007)
  • A. Bento et al.

    On the importance of baseline setting in carbon offsets markets

    Clim. Chang.

    (2016)
  • R. Bhatta et al.

    Diet effects on methane production by goats and a comparison between measurement methodologies

    J. Agric. Sci.

    (2008)
  • K.L. Blaxter

    The Energy Metabolism of Ruminants

    (1962)
  • K. Bouchard

    Methane Emissions and Rumen Microbial Changes in Steers Fed Condensed Tannin Containing Diets Under Western Canadian Conditions

    (2011)
  • M. Bown et al.

    Evaluation of the Energy Equations Used by the National Enteric Methane Inventory (No. MPI Technical Paper No: 2013/06)

    (2013)
  • A.J. Britton et al.

    Interactive effects of nitrogen deposition, fire and grazing on diversity and composition of low-alpine prostrate Calluna vulgaris heathland

    J. Appl. Ecol.

    (2007)
  • J.M. Brockway et al.

    Energy metabolism of the red deer

    J. Physiol.

    (1968)
  • L. Burbaitė et al.

    Red deer population and harvest changes in Europe

    Acta Zool. Litu.

    (2010)
  • J. Button

    Carbon: commodity or currency? The case for an international carbon market based on the currency model

    Harv. Environ. Law Rev.

    (2008)
  • M. Cain et al.

    Improved calculation of warming-equivalent emissions for short-lived climate pollutants

    Npj Clim. Atmospheric Sci.

    (2019)
  • J.E. Carulla et al.

    Supplementation of Acacia mearnsii tannins decreases methanogenesis and urinary nitrogen in forage-fed sheep

    Aust. J. Agric. Res.

    (2005)
  • Y. Chung et al.

    Enteric methane emission, diet digestibility, and nitrogen excretion from beef heifers fed sainfoin or alfalfa

    J. Anim. Sci.

    (2013)
  • D.C. Church

    The Ruminant Animal. Digestive Physiology and Nutrition

    (1988)
  • T.H. Clutton-Brock et al.

    Red deer stocks in the Highlands of Scotland

    Nature

    (2004)
  • J.E. Cordingley

    Ecosystem Service Provision in Dynamic Heath Landscapes (Phd)

    (2012)
  • D.J. Cottle et al.

    Ruminant enteric methane mitigation: a review

    Anim. Prod. Sci.

    (2011)
  • Deer Commission for Scotland, n.d. Annual Reports 1960–2002. Her Majesty's Stationery Office,...
  • M.T. Dittmann et al.

    Methane emission by camelids

    PLoS One

    (2014)
  • R. Dzieciolowski

    Relations between the age and size of red deer in Poland

    Acta Theriol. (Warsz.)

    (1970)
  • D.J. Eldridge et al.

    Impacts of shrub encroachment on ecosystem structure and functioning: towards a global synthesis

    Ecol. Lett.

    (2011)
  • J. Fagúndez

    Heathlands confronting global change: drivers of biodiversity loss from past to future scenarios

    Ann. Bot.

    (2013)
  • G.C. Fahey et al.

    Carbohydrate nutrition of ruminants, in

  • P. Fennessy et al.

    Energy requirements of red deer

    Proc. N. Z. Soc. Anim. Prod.

    (1981)
  • M.D. Fraser et al.

    Traditional vs modern: role of breed type in determining enteric methane emissions from cattle grazing as part of contrasting grassland-based systems

    PLoS One

    (2014)
  • J.K. Galbraith et al.

    Intake, digestibility, methane and heat production in bison, wapiti and white-tailed deer

    Can. J. Anim. Sci.

    (1998)
  • M. Giuburunca et al.

    Effects of plant secondary metabolites on methane production and fermentation parameters in in vitro ruminal cultures

    Sci. Pap. Anim. Sci. Biotechnol.

    (2014)
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