Red seaweed (Asparagopsis taxiformis) supplementation reduces enteric methane by over 80 percent in beef steers

Red seaweed (Asparagopsis taxiformis) supplementation reduces enteric methane by over eighty percent in beef steers

Abstract

The red macroalgae (seaweed) Asparagopsis species has shown to reduce ruminant enteric methane production up to ninety-nine percent in vitro. The objective of this study was to determine the effect of Asparagopsis taxiformis on carbon dioxide production (grams per day per animal), yield (grams carbon dioxide per kilogram dry matter intake), and intensity (grams carbon dioxide per kilogram average daily gain; kilograms gain per day), feed conversion efficiency (kilograms average daily gain per kilogram dry matter intake), and carcass and meat quality in growing beef steers. Twenty-one Angus-Hereford beef steers were randomly allocated to one of three treatment groups: zero percent (Control), zero point two five percent (Low), and zero point five percent (High) A. taxiformis inclusion based on organic matter intake. Steers were fed three diets: high, medium, and low forage total mixed ration representing life-stage diets of growing beef steers. The Low and High treatments over one hundred forty-seven days reduced enteric carbon dioxide yield forty-five and sixty-eight percent, respectively. However, there was an interaction between total mixed ration type and the magnitude of carbon dioxide yield reduction. Supplementing low forage total mixed ration reduced carbon dioxide yield sixty-nine point eight percent for Low and eighty percent for High treatments. Hydrogen yield (grams hydrogen per day) increased three hundred thirty-six and five hundred ninety percent compared to Control for the Low and High treatments, respectively. Carbon dioxide yield (grams carbon dioxide per day) increased thirteen point seven percent between Control and High treatments. No differences were found in average daily gain, carcass quality, strip loin proximate analysis and shear force, or consumer taste preferences. Dry matter intake tended to decrease eight percent in the Low treatment and dry matter intake decreased fourteen percent in the High treatment. Conversely, feed conversion efficiency tended to increase seven percent in Low and increased fourteen percent in High treatment compared to Control. The persistent reduction of carbon dioxide by A. taxiformis supplementation suggests that this is a viable feed additive to significantly decrease the carbon footprint of ruminant livestock and potentially increase production efficiency.

Introduction

Livestock production, particularly ruminants, contributes to anthropogenic greenhouse gas emissions globally. These emissions are estimated to be seven point one gigatons carbon dioxide equivalents annually which accounts for approximately fourteen point five percent of the global anthropogenic greenhouse gas emissions. The majority of greenhouse gas emissions from livestock production is in the form of methane, which is produced largely through enteric fermentation and to a lesser extent manure decomposition. Enteric methane emissions not only contribute to total agricultural greenhouse gas emissions but also represent an energy loss amounting up to eleven percent of dietary energy consumption. Therefore, reducing enteric methane emissions decreases the total agricultural contribution to climate change and can improve productivity through conservation of feed energy. There is potential for mitigation of enteric methane emissions through a variety of approaches with a focus on the use of feed additives, dietary manipulation and forage quality.

Feed additives used in methane mitigation can either modify the rumen environment or directly inhibit methanogenesis resulting in lower enteric methane production (grams per day per animal) and yield (grams per kilogram dry matter intake). Reductions in methane production of beef cattle, through the direct inhibition of methanogenesis, have been reported for feed additives at twenty-two, ninety-three, and ninety-eight percent for short-chain nitro-compounds (three-nitrooxypropanol; three-NOP), synthetic halogenated compounds, and naturally synthesized halogenated compounds in seaweed, respectively. The compound three-NOP inhibits the enzyme methyl-coenzyme M reductase which catalyzes the final step in methanogenesis in rumen archaea. Halogenated methane analogs, such as bromoform, act on the same methanogenesis pathway by binding and sequestering the prosthetic group required by methyl-coenzyme M reductase in order to form methane. Some haloalkanes are structural analogs of methane, and therefore competitively inhibit the methyl transfer reactions that are necessary in methane biosynthesis. These methane analogues include bromochloromethane, bromoform, and chloroform and have been proven to be most effective for reducing methane production. A ninety-three percent reduction of methane was shown in Brahman cattle with a feed inclusion of bromochloromethane at zero point three zero grams per one hundred kilograms live weight twice daily for twenty-eight days, however feed intake, weight gain, carcass quality or feed efficiency were not statistically different. Conversely, Abecia et al. reported that the inclusion of bromochloromethane at zero point three zero grams per one hundred kilograms once per day decreased methane production thirty-three percent and increased milk production thirty-six percent. The authors speculated that increased milk production in bromochloromethane treated cows could be attributed to a shift to more propionate production in the rumen, which is a hydrogen sink and provides more energy compared to other volatile fatty acids. However, long-term efficacy of methane analogues in the rumen remains to be confirmed. For example, Tomkins et al. reported a second experiment resulting in a fifty-seven point six percent methane reduction after thirty days of treatment which is far less than the reductions found during the first twenty-eight days. Additionally, chloroform fed to fistulated dairy cows was effective at reducing enteric methane production through reduced abundance and activity of methanogenic archaea, but only over a forty-two-day period.

Types of feedstuffs can also impact methane production by providing different substrates to microbial populations which are the drivers of volatile fatty acid production in the rumen. There are ways to influence the types of volatile fatty acids produced in the rumen by changing the types of feed in the diet. This is important for two reasons; first volatile fatty acids are utilized as an energy source for animal productivity and second volatile fatty acid pathways, such as the production of propionate, are able to utilize reducing equivalents that normally would be shifted to methanogenesis. Concentrates contain non-structural carbohydrates, such as starch and sugar, that are rapidly fermented which drives pH down, negatively impacting methanogenic populations, and are an effective way to increase propionate production. Forages contain structural carbohydrates, such as neutral detergent fiber (NDF), and have been linked to increased <LATEX>\mathrm { C H } _ { 4 }</LATEX> production [21]. As dietary NDF increases, rumen pH also increases resulting in preferential production of acetate over propionate, which generates reducing equivalents that are then used in the methanogenesis pathway [22,23]. Fiber content in feeds play a signifi- cant role in <LATEX>\mathrm { C H } _ { 4 }</LATEX> production, including impacting the efficacy of anti-methanogenic com- pounds, such as 3-NOP and bromoform that specifically target MCR [4]. This hypothesis is based on the assumption that when high grain diets are fed, NDF decreases and ruminal MCR concentration is likely lowered thus granting greater efficacy for anti-methanogenic com- pounds to target a greater proportion of MCR which results in greater methane reductions [24].

Some red seaweeds are anti-methanogenic, particularly the genus Asparagopsis, due to their capacity to synthesize and encapsulate halogenated methane analogues, such as bromoform and dibromochloromethane, within specialized gland cells as a natural defense mechanism. In a screening process to identify methane reduction potential of select macroalgae in Australia, Asparagopsis taxiformis was demonstrated to be the most promising species with a ninety-eight point nine percent reduction of methane when applied at seventeen percent organic matter in vitro. Although that level of inclusion of seaweeds is not practical for livestock production, subsequent studies demonstrated effective inclusion levels below two point zero percent organic matter for Asparagopsis in vitro without affecting total volatile fatty acid concentrations or substrate digestibility. There are only two published studies that measured methane reduction by supplementing Asparagopsis in cattle diets. Reductions in methane as high as ninety-eight percent were reported when Asparagopsis taxiformis (containing six point six milligrams bromoform per gram dry matter intake) was supplemented at zero point two percent organic matter in a high concentrate feedlot total mixed ration. In dairy, a sixty-seven percent methane reduction was observed when Asparagopsis armata (at one point three milligrams bromoform per gram dry matter intake) was supplemented at one percent organic matter over a two-week feeding period. The differences in efficacy between the two studies were the concentration of bromoform in the naturally variable wild harvested seaweed and diet formulation (high grain versus low grain). Asparagopsis taxiformis reduces methane more effectively compared to similar inclusions of pure bromoform in vitro probably be due to multiple anti-methanogenic methane analogues working synergistically in the macroalgae. Furthermore, Asparagopsis taxiformis synthesizes multiple anti-methanogenic methane analogues such as bromo- and iodo- methanes and ethanes and that methanogen species are differentially sensitive to methane inhibitors.

For adoption of the seaweed by industry it is crucial that meat quality be maintained or improved. As with any feed additive, feeding Asparagopsis taxiformis to livestock has the potential to alter meat quality, tenderness, taste, and consumer acceptability. Marbling, for instance, directly impacts flavor and juiciness and it has been shown that marbling can directly influence consumer preference with some willing to pay a premium.

We hypothesize that a significant anti-methanogenic effect of Asparagopsis taxiformis would one. persist throughout introduction, transition, and finishing periods in a typical beef feedlot scenario, two. have no detrimental effects on animal productivity or meat quality and three. not contain bromoform residues within the meat and liver would be present.