The role of small ruminants on global climate change

Global warming, as a consequence of excessive CO2 production mainly due to anthropogenic actions, is one of the main concerns of society due to the effects it can cause in the survival of humans, plants and animals. Several climatic consequences have already been reported, such as warming the oceans and changing biodiversity in various regions of the planet. One of the greenhouse gases responsible for global warming, which causes a lot of concern, is methane gas from digestion of food by ruminants. Besides that, emissions of greenhouse gases are represented also by waste management, rice cultivation, burning of residues from agriculture and soil management for agricultural production. Among ruminants, sheep and goats play an important economic role mainly in Oceania, Asia and Africa. More than 50% of small ruminants of the world are located in arid region, indicating their adaptability and future suitability to increasing temperatures. The purpose of this review is to report current knowledge about the methane emission produced by small ruminants, addressing the different interfaces of this theme, and considering possible mitigation strategies.


Introduction
The sustainability of agricultural production systems depends, among other factors, on maintaining the good quality of the environment.Climate change, greenhouse effects or global warming are terms related to the same problem, quite current, that may be influenced by anthropogenic interventions regarding the carbon and nitrogen cycle in agroecosystems.The consequences of these changes can affect the natural reproductive cycle of plants and animals, the migration of certain species of birds, even the extinction of several species, significantly affecting the planet's biodiversity (Ministry of Agriculture and Forestry [MAF], 2012).Thus, according to Skuce, Morgan, Van Dijk, and Mitchell (2013), these circumstances of anthropogenic origin are considered the greatest threat faced by the world population, since they will affect the production of food and natural resources.
Emissions of greenhouse gases (GHG) are directly related to this theme and are represented mainly by the ruminal fermentation of production animals, waste management, rice cultivation, burning of residues from agriculture and soil management for agricultural production.Approximately 80% of the anthropogenic CH 4 emissions are derived from ruminant production, especially in extensive production systems (Gill, Smith, & Wilkinson, 2010).Recognized as the third most polluting GHG, the annual growth rate of methane emissions was reported as 7% (Intergovernamental Panel on Climate Change [IPCC], 2006), with agricultural activities accounting for 70% of this value.However, according to the IPCC (2014), although the agriculture and land use sectors are responsible for 25% of the anthropogenic net greenhouse gas emissions, there are indications of declining to less than half of that share between 2010 and 2050, becoming the sector a net CO 2 sink before the end of the century, due to reforestation and changes in land management and agriculture.
The small ruminant production sector is of great relevance in the world, as sheep and goats represent approximately 56% of the world ruminant population (Food and Agriculture Organization of the United Nations [FAO], 2016).Small ruminant production plays a crucial socioeconomic role on the different continents.Besides the production of approximately 1.5 million tons of meat and 25.6 million tons of milk (FAO, 2016), this sector contributes to the preservation of landscapes and ecosystems, cooperating with biodiversity conservation and supplying products to niche markets (Marino et al., 2016).
More than 50% of the small ruminant's world population is located in arid regions, indicating the adaptability of these animals to such environmental conditions and their future suitability to regions predicted to sustain increasing temperatures.The plasticity of small ruminants is highlighted by the ability of sheep to graze in wasteland -particularly in Asian and African countries -to pasturelands in Australia.
The purpose of this review is to report current knowledge about methane emissions produced by small ruminants, addressing the different interfaces of this theme, and considering possible mitigation strategies.The contribution of small ruminants to global methane emissions are also discussed.

Methanogenesis
Unlike monogastric animals, ruminants maintain a symbiosis with microorganisms present in the first part of the gastrointestinal tract.The rumen is sheltered with a microbial population highly capable of fermenting dietary carbohydrates, recognized as the main energetic source of ruminants (Van Soest, 1994).Among the microbial groups, species of bacteria, protozoa, fungi and, with a population ranging from 0.5 to 3.0%, are the organisms of the domain Archae, also known as methanogenic bacteria (Hackmann & Spain, 2010).The ingested foods are anaerobically fermented and converted into short chain fatty acids (SCFA), mainly acetate, propionate and butyrate, branched chain fatty acids, microbial protein, vitamins from the K and B complex (Berchielli, Pires, & Oliveira, 2011) and gases from the fermentation process, such as carbon dioxide (CO 2 ), nitrous oxide (N 2 O), hydrogen (H 2 ) and methane (CH 4 ) (Sejian et al., 2017).From the synthesis of acetate and butyrate via the Embden-Meyerhof pathway, popularly known as glycolysis, H 2 is produced in the process.However, the anaerobic fermentation capacity of the lignocellulosic components is directly related to the elimination of H 2 from the ruminal environment (Kozloski, 2011).The most common form of H 2 elimination from the rumen is known as methanogenesis, in which there is a combination of four molecules of hydrogen with a molecule of carbon dioxide through the action of the microorganisms of the Archae domain.Thus, methanogenic bacteria maintain the biochemical ruminal balance from the restructuring of the NAD + , FAD + and NADP + cofactors (Martin, Morgavi, & Doreau, 2010).In contrast to acetate and butyrate, the production of propionate does not result in the release of H 2 , being the path of this SCFA considered competitive to the use of H 2 in the rumen (Martin et al., 2010).
Through flatulence and, mainly, eructation, CH 4 is eliminated from the ruminal environment and such activities are natural consequences to prevent gas accumulation (Muñoz, Yan, Wills, Murray, & Gordon, 2012).However, production and elimination of CH 4 causes energy losses in the range of 2 to 12% of the gross energy ingested by ruminants (Moss, Jouany, & Newbold, 2000).In sheep, the estimate reported by the IPCC (2006) of energy loss in methanogenesis is, on average, 6.5%.

Ruminal methane emitted by ruminants
Small ruminants are found on all continents, predominantly in countries known as emerging.According to FAO (2016), the world herd has approximately 1.2 billion sheep and 1 billion goats, growing at around 1.5% per year in the last five years (Figure 1).In relation to Brazil, the national herd reached 18.43 million sheep and 9.78 million goats in 2016, with the greatest concentration in the Northeast (63%) and South (23.9%) regions (ANUALPEC, 2017).
In Brazil, ruminal fermentation of beef cattle was the main cause (75%) of methane emissions in 2012, according to the Annual Estimates of Greenhouse Gases (Ministério da Ciência, Tecnologia e Inovação [MCTI], 2014).The dairy herd ranks second, accounting for 12% of methane emissions.The size of beef and dairy cattle populations in relation to that of small ruminants in Brazil (Figure 1) explain this difference in emissions (Table 1).Cattle reared on pasture account for 41% of direct methane emissions, and this has been considered the largest contribution within the category of ruminants (MCTI, 2014).Relative to impacts per unit of production, the meat sector represents lower potential of CH 4 emissions per kg of final product than the milk sector.In addition, small ruminants destined to meat have a lower CH4 emitting potential than cattle, when evaluated in kg CO 2-eq per kg of final product (Table 1).Sheep and goats contribute with about 6.5% of the world emissions, corresponding to 429 thousand Gg CO 2-eq , of which 59% is attributed to sheep and 41% to goats; with 299 thousand Gg CO 2-eq derived from meat and 130 thousand Gg CO 2-eq derived from milk, greater numbers than those indicated by the FAO (2016) (Table 1), demonstrating the variation in the reported data in inventories.
The contribution to the global production of meat from small ruminants is characterized by a dichotomy between regions; the world production of lamb meat is largely concentrated in Western Europe and Oceania, while goat meat production occurs in regions of lower socioeconomic development (Asia).The gas emissions derived from small ruminant meat is lower in Oceania and Western Europe (the main producers), due to intensification and greater efficiency of the production systems than in developing regions (Opio et al., 2013).
Emissions from dairy small ruminants is generally greater than from meat production, especially in regions such as Asia and Africa, due to extensive production systems and management, directed mainly for subsistence (Patra, 2014).Sheep and goats are recognized as the only species of domesticated ruminants able to live on mountain and areas with soils poor in nutrients.These animals also express the ability to excavate the soil in search of shoots and buried parts of perennial species for ingestion in dry seasons or semi-arid regions (Sejian et al., 2017), thus they are found in more inhospitable regions, and in less efficient systems, leading to longer production cycles.On the other hand, the carbon footprint of milk from small ruminants is greater than that of bovine milk, 6.5 kg CO 2-eq kg milk -1 versus 2.8 kg CO 2-eq kg milk -1 (Opio et al., 2013), due to the high productivity of dairy cattle compared to sheep and goats.

Emission of enteric methane by sheep
The commercial production of sheep meat worldwide is known by the low "carbon footprint", which makes the activity convenient to sustainable farming systems.It is estimated that the main sheepproducing countries, concentrated in Oceania and Western Europe, are contributing with the least amount of enteric CH 4 emissions, compared to goat-producing countries in developing areas.As already discussed, this is due to the greater intensification of production in developed countries, and the model of subsistence in emerging regions (Salem, 2010).According to Marino et al. (2016), greater prolificacy, leading to greater number of lambs born per lambing cycle, and short cycles for the production of meat contribute to the efficiency of the system.In fact, sheep meat production can effectively contribute to food production in an efficient and sustainable way, favoring the carbon balance of production systems.
In order to generate more robust greenhouse gas emission information from sheep production, Muetzel and Clark (2015) conducted four experiments that measured the emissions of adult and young animals fed pastures of different qualities.The result of this study (510 measurements in 115 sheep) showed that dry matter intake (DMI) in kg day -1 explained 80% of CH 4 production variation per animal (g d -1 ), and if CH 4 emissions were to be estimated using a single equation, that would be: pCH = 0.792xDMI + 3.1 where: pCH 4 : methane production (g d -1 ) DMI: dry matter intake (kg day -1 ) However, when the results were analyzed as two separate sets of data (<1 year, and > 1 year), it was identified that when the animals were younger than 1 year of age the prediction was improved, including metabolizable energy (ME) of the diet, in addition to DMI.
Therefore, estimates of digestibility and dietary intake can be used to identify corresponding seasonal changes in the production of CH 4 from ruminants managed on pasture.Thus, the emission of methane should be measured and integrated to the measurements of DM intake, energy values, fiber quality and quantity in the diet in order to know more about potential mitigations in pasture production systems (Berndt & Tomkins, 2013).
Table 2 shows annual values of methane (kg CH 4 year -1 ) from sheep of different body weights obtained from studies in different regions of the world.It can be observed that the emissions are between 5 and 15 kg CH 4 animal -1 year -1 (average of 8 kg CH 4 year -1 ) for animals of different weights and categories.Considering the Brazilian sheep herd of 17 million animals (Anuário da Pecuária Brasileira [ANUALPEC], 2017), this would result in about 130 Gg CH 4 year -1 , slightly greater than values estimated by FAO (2016).

Ruminal methane emission by goats
The lack of data on emissions by goats limits reliable estimates of ruminal methane emissions.The IPCC (2006) reports the emission of 5 kg CH 4 animal -1 year -1 for goats with 40 kg of body weight, assuming daily emission of 13 g CH 4 animal -1 day -1 , which is in agreement with the reported data in the literature (Table 2).Some authors have developed mathematical models to predict methane emission by goats.Patra and Lalhriatpuii (2016) elaborated a model based on the nutritional composition of the diet and intake variables, using a review with 42 published works.The linear model developed based on metabolizable energy intake (ME) and digestible energy (DE) accurately predicted methane production.However, the model of Patra and Lalhriatpuii (2016) does not distinguish the prediction by production type; while Fernández, Espinós, López, García-Diego, and Cervera (2013) developed models exclusively for dairy goats.The authors' model was based on body weight, milk production and diet.According to this model, it was observed that there was an overestimation of values described by IPCC (2007), showing the need for further research to refine the emission estimates.Effects of feed restriction on ruminal methane emission by goats were observed by Lima et al. (2016), mentioning that the emission decreases linearly with the reduction of the dry matter intake, although the loss of energy in the form of methane proportional to the organic matter intake did not present differences due to the food restriction.
The effect of dietary supplementation on methane emission was reported by Debruyne et al. (2018) in kids.The supplementation with coconut oil until 11 weeks of life suppressed the methanogenic activity, inhibiting the colonization of the rumen by Archea bacteria, reducing the in vitro emission of methane.Jeong et al. (2012) also observed this effect of the inclusion of vegetable oils (coconut, soybean and palm) on ruminal methane emission, reducing on average 25% of the emission in relation to animals that did not receive oils.Thus, the use of food alternatives to manipulate the ruminal microbiota to reduce ruminal methane emissions has been widely evaluated and has frequently shown positive results regarding its action.
The effect of the inclusion of condensed tannins on the diet of goats on methane emission was evaluated by Bhatta et al. (2013); this inclusion significantly reduced methane emissions at 12 and 25% of the daily emission rate, due to the inclusion of 2.8 and 5.7 g kg -1 DM from the diet, respectively.Condensed tannins inhibit methanogenesis by a direct effect on ruminal methanogens and an indirect effect on hydrogen production due to lower feed degradation (Martin et al., 2010;Tavendale et al., 2005).The direct effect can be attributed to cell death by the formation of complexes with sterols in protozoal cell membranes.This modifies ruminal fermentation by suppressing ruminal protozoa and selectively inhibiting methanogenic bacteria.Condensed tannins have an inhibitory capacity for methanogenic activity, and may be present in plants of extensive goat production regions.
Table 3 presents annual CH 4 emission data for dairy and non-dairy goats of different weights and animal categories in various regions of the world.
The values indicate an average of 6 kg CH 4 year -1 for non-dairy animals, which are the majority of the Brazilian herd located in the Northeast, and 14 kg CH 4 year -1 for dairy goats.Considering the average for non-dairy animals, it would result in 54 Gg CH 4 year -1 , close to the estimate by FAO (2016).

Factors interfering in the emission of methane
Voluntary intake of food by the animal is the main factor that affects the efficiency by which the ingested nutrients are used.The greater the voluntary intake, the higher the productivity of animals, and the lower the nutrient requirements for each unit of animal production (Mertens, 2007).In ruminants, intake is the result of a dynamic combination between the animal, the type of food, more specifically the plant in the case of grazing animals, and ruminal fermentation.
Therefore, it is essential to measure dry matter (and nutrient) intake by ruminants (Berndt & Tomkins, 2013) to estimate the production of CH 4 and the influence of dietary intake and nutritional composition on this parameter.Studies have shown that when forage intake increases, CH 4 emission also increases, indicating a positive relationship between DM intake and methane emission (Amaral et al., 2016;Charmley et al., 2016;Hammond et al., 2013;Kurihara, Magner, Hunter, & McCrabb, 1999;Moorby, Fleming, Theobald, & Fraser, 2015;Savian et al., 2014;Zhao, O'Connell, & Yan, 2016).It is also important to understand the role of the components of the diet offered to the animals, especially with regard to the type of carbohydrate, since carbohydrates are important for the production of CH 4 .For instance, carbohydrates influence ruminal pH which in turn can alter the ruminal microbiota (Johnson & Johnson, 1995).It is well known that increasing the level of starch in the diet reduces the proportion of dietary energy converted to CH 4 (Blaxter & Clapperton, 1965) mainly due to a change in fermented substrate from fiber to starch and the concomitant decline in ruminal pH.The concentration and chemical characteristics of plant fiber also influence fermentation and thus the production of CH 4 (Van Soest, 1994).
Herbivores exhibit a complex pattern of interactions with their pastoral environment, making the plant-animal relationship a cause-andeffect function between pasture structure and ingestion patterns.Carvalho (2013) stated that herbivores select plants and their morphological components to optimize nutrient intake.Thus, the ultimate goal would be to achieve the highest possible intake of metabolizable energy (Boval & Dixon, 2012).
In conjunction with research evaluating nutritional influence on rumen CH 4 emissions, preliminary studies in the area of genetic improvement in sheep are being carried out.These studies were conducted to observe heritability and repeatability in methane emissions from animals considered to be low and high emitters.The results were 0.30 ± 0.26 for heritability and 0.16 ± 0.10 for repeatability, differing also in relation to concentrate (17.8 g kg DMI -1 , pelleted) and forage based diets (Pinares-Patiño et al., 2011), suggesting that this may be a way to achieve greater mitigation potentials in small ruminant production.

Mitigation strategies on small ruminant production
Global environmental pressures indicate that the reduction of CH 4 emissions from livestock is one of the main factors to guide ruminant production research (Machmüller, 2006).The three main methods of mitigating methane emissions are: 1) nutritional strategies, the most widespread ones; 2) selection of animals by breed or genetics, and intensification of production systems; 3) modification of the ruminal environment (Marino et al., 2016).
It is known that the type of food ingested by small ruminants directly determines the proportion of SCFAs produced; thus, diets rich in non-fibrous carbohydrates (starch and sugars) result in a higher proportion of propionate during ruminal fermentation.Therefore, CH 4 production tends to be lower in diets with increased levels of concentrate (Moss et al., 2000).In addition, Castillo-González, Burrola-Barraza, Domínguez-Viveros, and Chávez-Martínez (2014) reported that the reduction of ruminal pH, with the presence of concentrate in the diet, has a deleterious effect on protozoa and cellulolytic bacteria, leading to lower production of H 2 .
The addition of enzymes optimizes the fermentation of dietary fibers and is responsible for the reduction of up to 9% in CH 4 production, since the inclusion of lipids leads to a decrease in the population of methanogenic microorganisms (Beauchemin et al., 2008).Commercial ionophores, such as monensin, lasalocid, salinomycin, and tetronasin, passes the single porous membrane of Gram-positive bacteria and interfere with cell energy production.Thus, there is inhibition of H 2 production by these microorganisms (Tedeschi, Callaway, Muir, & Anderson, 2011).
According to Herrero et al. (2016), improving reproductive indices, food availability and average daily gain (ADG) reduce the production cycle and therefore are effective in reducing GHG emissions.Moreover, the same authors estimate that better management practices will reduce GHG emissions by 0.2 Gt CO 2-eq by 2050.Accordingly, authors affirm that well-applied pasture management techniques lead to intensified production and to the reduction in CH 4 emissions per kilogram of final product (Andrade et al., 2014;DeRamus, Clement, Giampola, & Dickison, 2003;Savian et al., 2014).Berndt and Tomkins (2013) emphasize that farm management with the objective of mitigation will be observed in the emissions of kg GHG per kg of final product (milk and/or meat), and most probably not in the individual emissions of the animals.Thus, in pastoral systems, the mitigation potential can be achieved mainly by improvements in pasture management.This strategy is related to the intensification of production such as food supplementation, implantation of the intermittent pasture management system and alternative systems such as crop-livestock integration and silvopastoral systems (Berchielli, Messana, & Canesin, 2012).
However, the real challenge is to find strategies for animals kept in pastures, and these strategies be persistent in their effects.Regardless of the production system, two challenges to achieve mitigation are recurrent.The first is related to the reduction of the CH 4 production per unit of ingested food, or per unit of final product, and for this, it will require the execution of an integrated number of strategies.The second challenge refers to the application of the former strategy, since it will only occur if the profitability exceeds implementation costs (Berndt & Tomkins, 2013).Therefore, the best mitigation strategy should increase profitability of production and/or other livestock products, as well as promote a persistent reduction of methane emissions (Grainger, Williams, Clarke, Wright, & Eckard, 2010).
Regarding genetic improvement, as a tool to mitigate the adverse effects of climate change on animal production, the selection of breeds and individuals seeking high production efficiency, and also animals tolerant to these adverse effects on the wool, meat and milk production are very important strategies (Sejian et al., 2017).They are important since in the current scenario it is commonly reported effects of increase in environmental temperature and reduction in rainfall.
Another point to consider is the balance between CO 2 emissions eq.from animals and their absorption by pasture plants.The potential of soil carbon sequestration in pasture systems may be significantly greater than methane emissions from enteric fermentation or manure management (Berchielli et al., 2012;IPCC, 2014).According to Henderson et al. (2015), adjustments in grazing pressure, allowing the maximization of forage production, can lead to the sequestration of 148.4 Tg of CO 2 per year in pastures worldwide, also indicating that animal emissions can be fully offset by higher gains in carbon sequestration.Thus, when CH 4 emissions were analyzed in experiments on pasture systems, factors such as grazing intensity and their spatial distribution, carbon sequestration of pasture, and the impact of animal production alter and increase the variability of these emissions (Savian et al., 2014).
Despite being a major emitter, livestock farming shows great potential for carbon sequestration through well-managed pastures.The Brazilian national emission is slightly higher than 1 Mg CO 2- eq ha -1 , while sequestration can reach 0.78 Mg CO 2-eq ha -1 (Zen, Barioni, Bonato, Almeida, & Ritti, 2008).According to Gerber et al. (2013) carbon sequestration of pastures can significantly offset GHG emissions, with global estimates of approximately 0.6 Gt CO 2-eq year -1 .Thus, investment in pasture could increase animal production efficiency and reduce the amount of GHG emitted per kilogram of meat produced, which could reach neutral or even negative carbon balances.

Conclusion
The search for strategies that increase carbon footprint mitigation and animal adaptations to the adverse effects of climate change on small ruminant production systems is very important, since a large part of the world's herd is in regions where animals are exposed to extensive systems and thus subjected to substantial fluctuations in environmental conditions.In all regions of the world, increases in environmental temperature have been reported and predicted, indicating a trend towards a continuous increase for the next 50 years.In this way, the adaptation of animals and production systems to environmental variations and the possible lower input of resources may be fundamental for the sustainability of food production in agroecosystems.

Table 1 .
World and Brazilian emission of ruminal methane for sheep, goats and cattle.

Table 2 .
Annual methane ruminal emission of sheep, according to body weight (BW) in different regions of world.

Table 3 .
Annual methane ruminal emission of goats, according to body weight (BW) in different regions of world.