*Review*

#### **Methane Emissions and the Use of** *Desmanthus* **in Beef Cattle Production in Northern Australia**

#### **Bénédicte Suybeng 1, Edward Charmley 2, Christopher P. Gardiner 1, Bunmi S. Malau-Aduli 3 and Aduli E. O. Malau-Aduli 1,\***


Received: 10 May 2019; Accepted: 6 August 2019; Published: 9 August 2019

**Simple Summary:** An in-depth review of Australia's tropical beef cattle production system is presented with emphasis on the use of *Desmanthus*, a tropical legume, as a nutritional supplementation strategy for the abatement and mitigation of methane emissions. It also identifies current knowledge gaps in *in vivo* methane emissions research.

**Abstract:** The Australian beef industry is a major contributor to the economy with an estimated annual revenue generation of over seven billion dollars. The tropical state of Queensland accounted for 48% of Australian beef and veal production in 2018. As the third biggest beef exporter in the world, Australia supplies 3% of the world's beef exports and its agricultural sector accounts for an estimated 13.2% of its total greenhouse gas emissions. About 71% of total agricultural emissions are in the form of methane and nitrous oxide. In this review, an overview of the carbon footprint of the beef cattle production system in northern Australia is presented, with emphasis on the mitigation of greenhouse gases. The review also focuses on the tropical legume, *Desmanthus*, one of the more promising nutritional supplements for methane abatement and improvement of animal growth performance. Among the review's findings is the need to select environmentally well-adapted and vigorous tropical legumes containing tannins that can persistently survive under the harsh northern Australian conditions for driving animal performance, improving meat quality and reducing methane emissions. The paper argues that the use of appropriate legumes such as *Desmanthus*, is a natural and preferred alternative to the use of chemicals for the abatement of methane emanating from tropical beef cattle production systems. It also highlights current gaps in knowledge and new research opportunities for *in vivo* studies on the impact of *Desmanthus* on methane emissions of supplemented tropical beef cattle.

**Keywords:** methane emission; tropical beef cattle; *Desmanthus*; supplementation; growth performance; ruminant nutrition; legumes

## **1. Introduction**

Global climate change is principally caused by greenhouse gas (GHG) emissions that result in warming of the atmosphere [1]. According to the Australian National Greenhouse Accounts [2], 13.2% of GHG emissions emanate from agriculture, with methane and nitrous oxide accounting for 71% of total agricultural emissions [3]. In 2017, Australia produced an estimated 51,543.56 Gg CO2-e of CH4 from enteric fermentation [3].

The world population is predicted to increase from 7.6 to 9.8 billion by 2050 [4]. Consequently, the world has to match the increased demand for food from a larger and more a ffluent population to its supply in an environmentally sustainable manner [5]. Livestock products constitute an important source of food for global food security by providing 33% and 17% of world protein and kilocalorie consumption, respectively [6]. Climate change constitutes a risk to livestock production due to its impact on the feed quality of crops and forages, animal performance, milk production, water availability, animal reproduction, livestock diseases and biodiversity [6]. Therefore, the challenge is to find ways to increase livestock productivity without compromising household food security while sustainably improving the natural resource base [7].

Beef cattle productivity in north Queensland is beset with climatic and nutritional challenges, due to prolonged drought, high climate variability, inadequate feed resources, low-quality pastures and the poor body condition of cattle [8]. In this seasonally dry, low-elevation, heavy textured soils and inland tropical region of north Queensland, there is an overwhelming need for integrating more productive, nutritious and persistent summer-growing legumes into existing low quality, grass-dominant pastures [8].

Existing cultivars lack the capacity to adapt to seasonally waterlogged duplex soils, infertile light-textured soils, heavy cracking clays and low rainfall conditions [9]. Gardiner [10] evaluated the performance characteristics of *Desmanthus* in contrasting tropical environments and found that it thrived and spred on heavier vertisol soils. Hall and Walker [9] conducted a study over a 15-year period in six di fferent environments in the seasonally dry tropics of north Queensland and found that on cracking clay soils, *Desmanthus* species and *Clitoria ternatea* were the most persistent and productive legumes among 118 legume accessions.

Further evaluation and development of *Desmanthus* under commercial grazing managemen<sup>t</sup> will be highly beneficial to northern Australian beef cattle graziers for improved productive and reproductive performances, better animal body condition and higher meat quality, particularly in the live cattle trade where northern Australia is the main gateway to this key business export market. The State of Queensland accounts for about 43% of the Australian cattle population [11] and has a CH4 emission from ruminants that has been estimated to account for 3% of Australia's GHG [3]. Australia has a target to reduce its emissions by 5% below the 2000 level by 2020 and 26–28% below 2005 emissions by 2030. The Government allocated \$2.55 billion to the Emissions Reduction Fund (ERF) to help livestock producers use modern farming methods to store carbon in vegetation and soils towards reducing GHG [12]. Research into contemporary, scientific and sustainable ways to produce high quality beef in tropical Northern Australia with low methane emissions are paramount to Australia being competitive in the international market. *Desmanthus* spp. are among the most promising sown legume species for the vastly undeveloped semi-arid clay soil regions across northern Australia.

This review focusses on the carbon footprint of the beef cattle industry in northern Australia, explores mechanisms and methods of enteric methane production and abatement with a focus on *Desmanthus* as a potential pasture legume for mitigating methane emissions. Finally, the current knowledge gaps that could underpin future research are also reviewed.

#### **2. Carbon Footprint from the Beef Industry in Queensland**

#### *2.1. The Australian Beef Cattle Market*

Australia is the third biggest beef exporter in the world, supplying 3% of the world's beef exports with 1,500,000 tons of carcass weight exported annually. The Australian beef cattle industry accounted for \$11.4 billion in 2017–2018 [11]. Furthermore, the beef cattle industry employed 191,800 people in 2016–2017. Therefore, the beef industry plays a central role in the Australian economy, especially in the state of Queensland, where its 11.1 million head of cattle accounted for 48.1% of the Australian beef and veal production in 2017–2018 [11].

#### *2.2. The Di*ff*erent Sectors Included in the Carbon Footprint of the Beef Industry in Queensland*

The total net emissions attributed to agriculture in Queensland was 18,672.5 Gg CO2-e in 2017 [3]. The beef industry in Queensland is the largest agricultural industry in the state [13]. Sources of GHG emissions from a typical beef enterprise comprise enteric fermentation in cattle (CH4 and N2O), burning of vegetation (intentional or accidental), energy use (electricity and fuel), land clearing, loss of pasture and decline in soil carbon [13,14]. A study conducted by Eady et al. [14] in two beef farms in Queensland showed that the carbon footprint of beef products at the farm gate ranged from 17.5–22.9 kg CO2-e/kg liveweight at Gympie and 11.6–15.5 kg CO2-e/kg liveweight in the Arcadia Valley. They also found that enteric fermentation represented about 80% (74% at Arcadia Valley and 85% at Gympie) of the overall 'cradle-to-farm gate' GHG emissions [14]. The last figures can be linked with the 70% (12,995.97 Gg CO2-e) of agriculture GHG emissions coming from enteric fermentation from grazing beef cattle in Queensland in 2017 [3].

#### *2.3. The Principal Causes Inducing Enteric Methane Emissions*

#### 2.3.1. Rumen Microbial Fermentation

The rumen is a dynamic and complex ecosystem composed essentially of anaerobic bacteria, protozoa, anaerobic fungi, methanogenic archaea and phages [15]. The microbes interact with each other and have a symbiotic relationship with the host. The breakdown of plant cell wall carbohydrates that are inedible by humans provides energy to the host [16]. Methane is produced exclusively by methanogenic archaea [15] via the hydrogenotrophic pathway using CO2 as the carbon source and H2 as the main electron donor, and less so through the utilization of methyl groups (methylotrophic pathway), or even less commonly from acetate (acetoclastic pathway) [15]. The methanogenesis reaction uses H2 to reduce CO2 to CH4: CO2 + 4H2 = CH4 + 2H2O [17].

The main products of rumen microbial fermentation, as depicted in Figure 1, are volatile fatty acids (VFA) (acetic, propionic and butyric acids), carbon dioxide and methane [18]. In the rumen, the VFA formed are absorbed and used as a source of energy. On the contrary, CO2 and CH4 are eliminated by eructation from the rumen. Over 80% of the methane is synthesised in the rumen and the lower digestive tract produces the rest [18]. Northern beef cattle in Australia can generate about 32.2 to 184 g of methane per day [19], which represents an important energy loss to the animal ranging from 2% to 12% of gross energy intake depending on the nature of the diet [20]. Under a high forage diet, these losses are on the average, 7.2% of gross energy intake; 6.3% for an intermediate forage and 3.84% for a low forage (feedlot) [21].

**Figure 1.** Principal end-products of carbohydrate fermentation in the rumen [18].

#### 2.3.2. Low Animal Performance Increases Methane Production

Less efficient cattle can take longer to reach market weight and might only breed two out of three seasons. The longer an animal takes to reach market weight, the longer that animal is producing methane, with very little beef being marketed in return [20,22]. Arthur et al. [23] estimated genetic and phenotypic parameters for feed intake in Angus bulls and heifers, and showed that the feed conversion ratio defined by the amount of feed consumed divided by live weight gain was correlated genetically (−0.62) and phenotypically (−0.74) with the average daily gain (ADG). For instance, Charmley et al. [22] showed that by maintaining a liveweight (LW) gain of 0.5 kg/day for steers in the northern spear grass region by adding supplements to the pasture diet would reduce the turn-off age of the Japanese Ox market from 4 years (526 kg LW) to 2.3 years (650 kg LW). Gross margin budget and cashflow analyses for a 100-cow herd showed a 61% internal rate of return over a 25-year investment period, despite the higher cost for purchasing efficient bulls. It represents an annual benefit per cow of A\$8.76 [24]. Low animal productivity is associated with high methane output per unit of product (methane intensity) and low pasture quality is associated with high methane output per unit of dry matter intake [12]. For that reason, northern Australian beef herds are estimated to produce more methane than the more intensive systems in southern Australia [20]. For instance, Eady [25] showed that the GHG emissions of beef produced from cattle supply chain from Northern Australia to the Indonesian market were higher (26 kg CO2 equivalent/kg liveweight) than beef produced in Southern Australian systems, where GHG emissions ranged from 5.4 to 14.5 kg CO2 equivalent/kg liveweight for finished steers. They attributed it to the higher reproduction rate, faster turn-off and lower methane emissions per unit of feed intake permitted by a high pasture quality in the southern systems [25].

#### 2.3.3. Northern Australian Forage Diet Influences Rumen Microbiome and Methane Production

In northern Australia, comprising the Kimberley and Pilbara districts of Western Australia, the Northern Territory and Queensland above the Tropic of Capricorn, the beef industry is dominated by large pastoral properties [10]. This part of Australia is characterised by a vast array of heavy clay or vertosol soils, where the range of available sown pasture legumes has long been regarded as being deficient [26]. There are also vast areas of light textured soils where the legume *Stylosanthes* has been successfully introduced. Pasture production is highly seasonal, with a wet season (November to April) characterised by growth, and a senescent period during the dry season. This induces a marked seasonal pattern of pasture availability and quality [27]. The prevailing pasture species are mainly C4 grasses, which have lower nutritional value than temperate grasses, and result in lower animal productivity than in temperate regions [28,29]. During the wet, hot summers, these pastures grow quickly and persist through the dry winter seasons as mature grasses [30–32]. The low livestock productivity in northern Australia is especially due to low protein content and low digestibility during the dry season [33]. The low digestibility (45% organic matter) and nitrogen content (less than 7g N/kg dry matter (DM)) of these grasses during the dry season results in poor forage intakes and low annual growth rate of young cattle [30–32]. Animals tend to put on weight in the wet season and lose weight in the dry season. In northern Australia, it is not uncommon for 4–6 years old steers to be marketed [34]. Consequently, depending on the time of the year, liveweight gains in Northern Australia are around 70–240 kg/year for native pastures [35] compared to 250–300 kg/year for temperate pastures [36]. Growth rate is directly related to metabolisable energy intake, and can be markedly increased by replacing the feed base or by giving supplements to the animals [36].

Archimede et al. [37] showed that ruminants fed C4 grass produced 17% more methane as L/kg organic matter intake than those fed C3 grass. Likewise, Perry et al. [29] found that steers fed a wet season pasture (crude protein (CP) = 90 g/kg DM) or a high quality hay (CP = 88 g/kg DM) produced 5–10 g CH4/kg, digested less dry matter intake (DMI) and had about 3% less digestible energy intake than steers fed low quality hay (CP = 25 g/kg DM). They observed shorter rumen retention times in high quality hay fed steers, which decreased methane production per kilogram of DMI compared with low quality hay and the dry season pasture. This phenomenon can be explained with an increased rumen outflow rate [38]. The rise in rumen outflow rates is associated with higher concentrations of dissolved H2 that increase the growth rate of methanogens. The greater cellulose and hemicellulose content in tropical C4 grasses rather than neutral detergent soluble carbohydrates in grain diets results in higher methane emissions and a shift in rumen fermentation pathways from propionate to acetate [12,29]. The production of methane in the rumen is associated with the production of VFA. The formation of both acetic and butyric acids is accompanied by the production of H2 and CO2, whereas propionic acid production requires a net uptake of H2, which can reduce methanogenesis [38]. The production of propionic acid instead of acetic acid can be realised by replacing structural carbohydrates (forage) with easily fermented carbohydrates [38].

#### **3. Mitigation Techniques against Methane Emission**

#### *3.1. The Use of Chemicals for Rumen Manipulation to Reduce Methane Production*

#### 3.1.1. The Use of Chemicals to Control Protozoa, the Main Hydrogen Producer

Some techniques such as defaunation and the utilisation of ionophores, have been used to control protozoa, the major producers of H2 from the rumen [39], so that less H2 is accessible for CH4 formation.
