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Peer-reviewed

Research Article

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

• Breanna M. Roque,
• Marielena Venegas,
• Robert D. Kinley,
• Rocky de Nys,
• Toni L. Duarte,
• Xiang Yang,
• Ermias Kebreab

ten

• Published: March 17, 2021
• https://doi.org/10.1371/periodical.pone.0247820

Figures

Abstract

The red macroalgae (seaweed) Asparagopsis spp. has shown to reduce ruminant enteric methane (CH₄) production up to 99% in vitro. The objective of this study was to determine the effect of Asparagopsis taxiformis on CH₄ production (g/solar day per animal), yield (g CH₄/kg dry matter intake (DMI)), and intensity (g CH_iv/kg ADG); average daily gain (ADG; kg proceeds/mean solar day), feed conversion efficiency (FCE; kg ADG/kg DMI), and carcass and meat quality in growing beef steers. Twenty-1 Angus-Hereford beef steers were randomly allocated to one of three treatment groups: 0% (Control), 0.25% (Low), and 0.5% (Loftier) A. taxiformis inclusion based on organic thing intake. Steers were fed 3 diets: high, medium, and low forage total mixed ration (TMR) representing life-stage diets of growing beef steers. The Low and High treatments over 147 days reduced enteric CH₄ yield 45 and 68%, respectively. However, there was an interaction between TMR type and the magnitude of CH₄ yield reduction. Supplementing low provender TMR reduced CH₄ yield 69.viii% (P <0.01) for Low and 80% (P <0.01) for Loftier treatments. Hydrogen (H_two) yield (g H₂/DMI) increased (P <0.01) 336 and 590% compared to Control for the Low and High treatments, respectively. Carbon dioxide (CO₂) yield (yard CO₂/DMI) increased 13.7% between Control and High treatments (P = 0.03). No differences were institute in ADG, carcass quality, strip loin proximate analysis and shear force, or consumer gustation preferences. DMI tended to subtract 8% (P = 0.08) in the Depression handling and DMI decreased 14% (P <0.01) in the Loftier treatment. Conversely, FCE tended to increment 7% in Depression (P = 0.06) and increased xiv% in High (P <0.01) treatment compared to Control. The persistent reduction of CH_iv by A. taxiformis supplementation suggests that this is a viable feed additive to significantly subtract the carbon footprint of ruminant livestock and potentially increase production efficiency.

Citation: Roque BM, Venegas M, Kinley RD, de Nys R, Duarte TL, Yang 10, et al. (2021) Reddish seaweed (Asparagopsis taxiformis) supplementation reduces enteric methane by over 80 percentage in beef steers. PLoS 1 sixteen(3): e0247820. https://doi.org/x.1371/journal.pone.0247820

Editor: James E. Wells, United States Department of Agronomics, Agricultural Research Service, Usa

Received: August xiii, 2020; Accustomed: February thirteen, 2021; Published: March 17, 2021

Copyright: © 2021 Roque et al. This is an open access article distributed under the terms of the Artistic Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: All relevant data are within the newspaper and its Supporting Information files.

Funding: This inquiry received fiscal support from Elm Innovations, the David and Lucile Packard Foundation and the Grantham Foundation. Financial Support was only used to cover the costs of conducting the experiment only. Funders did not have a role in the study design, data drove and analysis, decision to publish, or preparation of the manuscript'.

Competing interests: The authors accept declared that no competing interests be.

Introduction

Livestock production, particularly ruminants, contributes to anthropogenic greenhouse gas (GHG) emissions globally. These emissions are estimated to be 7.ane Gt carbon dioxide (CO₂) equivalents annually which accounts for approximately 14.5% of the global anthropogenic GHG emissions [1]. The majority of GHG emissions from livestock product is in the grade of methyl hydride (CH_four), which is produced largely through enteric fermentation and to a lesser extent manure decomposition. Enteric CH₄ emissions not only contribute to total agricultural GHG emissions but also represent an energy loss amounting upward to eleven% of dietary free energy consumption [2]. Therefore, reducing enteric CH₄ emissions decreases the total agronomical contribution to climate change and can improve productivity through conservation of feed free energy. At that place is potential for mitigation of enteric CH₄ emissions through a variety of approaches with a focus on the use of feed additives, dietary manipulation and forage quality [3].

Feed additives used in CH₄ mitigation tin can either change the rumen environment or straight inhibit methanogenesis resulting in lower enteric CH₄ production (g/day per animal) and yield (g/kg dry affair intake [DMI]). Reductions in CH_four product of beef cattle, through the direct inhibition of methanogenesis, have been reported for feed additives at 22, 93, and 98% for short-chain nitro-compounds (3-nitrooxypropanol; 3-NOP, [four]), synthetic halogenated compounds [v], and naturally synthesized halogenated compounds in seaweed [6], respectively. The compound iii-NOP inhibits the enzyme methyl-coenzyme M reductase (MCR) which catalyzes the terminal step in methanogenesis in rumen archaea [7]. Halogenated CH_four analogs, such as bromoform, act on the same methanogenesis pathway past binding and sequestering the prosthetic group required by MCR in order to grade CH₄ [eight–10]. Some haloalkanes are structural analogs of CH₄, and therefore competitively inhibit the methyl transfer reactions that are necessary in CH_four biosynthesis [eleven,12]. These CH₄ analogues include bromochloromethane (BCM), bromoform, and chloroform and have been proven to be most effective for reducing CH₄ production. A 93% reduction of CH₄ was shown in Brahman cattle with a feed inclusion of BCM at 0.30 one thousand/100 kg LW twice daily for 28 days, however feed intake, weight gain, carcass quality or feed efficiency were non statistically unlike [5]. Conversely, Abecia et al. (2012) reported that the inclusion of BCM at 0.30 g/100 kg once per mean solar day decreased CH_iv production 33% and increased milk product 36% [13]. The authors speculated that increased milk production in BCM treated cows could exist attributed to a shift to more propionate production in the rumen, which is a hydrogen (H₂) sink and provides more free energy compared to other volatile fatty acids. However, long-term efficacy of CH_iv analogues in the rumen remains to be confirmed. For case, Tomkins et al. (2009) reported a second experiment resulting in a 57.6% CH₄ reduction after thirty days of handling which is far less than the reductions establish during the first 28 days [v]. Additionally, chloroform fed to fistulated dairy cows was effective at reducing enteric CH₄ production through reduced affluence and activity of methanogenic archaea, but only over a 42-day period [14].

Types of feedstuffs can also impact CH_four production by providing different substrates to microbial populations which are the drivers of volatile fatty acid (VFA) production in the rumen. There are means to influence the types of VFA produced in the rumen by changing the types of feed in the diet [15,16]. This is important for two reasons; commencement VFAs are utilized as an free energy source for creature productivity and second VFA pathways, such as the production of propionate, are able to utilize reducing equivalents that unremarkably would be shifted to methanogenesis [17,xviii]. Concentrates comprise non-structural carbohydrates, such as starch and sugar, that are chop-chop fermented which drives pH down, negatively impacting methanogenic populations, and are an effective fashion to increment propionate production [19,20]. Forages contain structural carbohydrates, such as neutral detergent fiber (NDF), and have been linked to increased CH_four production [21]. Equally dietary NDF increases, rumen pH too increases resulting in preferential production of acetate over propionate, which generates reducing equivalents that are and then used in the methanogenesis pathway [22,23]. Cobweb content in feeds play a significant role in CH₄ production, including impacting the efficacy of anti-methanogenic compounds, such every bit 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 compounds to target a greater proportion of MCR which results in greater methane reductions [24].

Some carmine seaweeds are anti-methanogenic, particularly the genus Asparagopsis, due to their capacity to synthesize and encapsulate halogenated CH₄ analogues, such equally bromoform and dibromochloromethane, within specialized gland cells as a natural defense machinery [25]. In a screening process to place CH₄ reduction potential of select macroalgae in Commonwealth of australia, Asparagopsis taxiformis was demonstrated to be the near promising species with a 98.9% reduction of CH₄ when practical at 17% OM in vitro [26]. Although that level of inclusion of seaweeds is not practical for livestock product, subsequent studies demonstrated effective inclusion levels beneath 2.0% OM for Asparagopsis in vitro [27,28] without affecting total VFA concentrations or substrate digestibility. There are only two published studies that measured CH_four reduction by supplementing Asparagopsis in cattle diets. Reductions in CH₄ every bit high as 98% were reported when A. taxiformis (containing 6.6 mg bromoform/1000 DMI) was supplemented at 0.2% OM in a loftier concentrate feedlot TMR [6]. In dairy, a 67% CH₄ reduction was observed when Asparagopsis armata (at 1.three mg bromoform/one thousand DMI) was supplemented at 1% OM over a 2-week feeding flow [29]. The differences in efficacy between the two studies were the concentration of bromoform in the naturally variable wild harvested seaweed and diet conception (loftier grain versus low grain) [half dozen]. A. taxiformis reduces CH_iv more effectively compared to like inclusions of pure bromoform in vitro probably be due to multiple anti-methanogenic CH_iv analogues working synergistically in the macroalgae [thirty]. Furthermore, A. taxiformis synthesizes multiple anti-methanogenic CH₄ analogues such equally bromo- and iodo- methanes and ethanes [31] and that methanogen species are differentially sensitive to CH₄ inhibitors [32].

For adoption of the seaweed past industry it is crucial that meat quality be maintained or improved. As with whatsoever feed condiment, feeding A. taxiformis to livestock has the potential to modify meat quality, tenderness, sense of taste, and consumer acceptability. Marbling, for example, straight impacts flavour and juiciness and information technology has been shown that marbling can directly influence consumer preference with some willing to pay a premium [33].

We hypothesize that a significant anti-methanogenic result of A. taxiformis would 1.) persist throughout introduction, transition, and finishing periods in a typical beef feedlot scenario, 2.) have no detrimental effects on brute productivity or meat quality and 3.) not comprise bromoform residues within the meat and liver would be present.

Materials and methods

This report was approved by the Institutional Fauna Care and Use Commission of the University of California, Davis (Protocol No. 20803).

Written report design, animals, and diets

Twenty-one Angus-Hereford cantankerous beef steers, blocked past weight, were randomly allocated to 1 of iii handling groups: 0% (Control, n = 7), 0.25% (Low, north = seven), and 0.5% (High, n = 6) inclusion rates of A. taxiformis based on OM intake. The unbalanced number of steers between handling groups was due to an unexpected animal injury during the concluding 3 weeks of the trial to which all information from this steer was removed from statistical analysis. The steers used in this study were obtained from the Shasta Livestock Auction Yard (Cottonwood, CA), all of which were sourced from the same ranch, and were approximately 8 months of age weighing approximately 352 ± 9 kg at the start of the trial. Each steer was randomly assigned to an private pen, fitted with its ain feed bunk, and were fed twice per twenty-four hours at 0600 and 1800 hours at 105% of the previous day'due south intake.

The experiment followed a completely randomized blueprint, with a 2-week covariate period, used as a baseline catamenia, before treatment began followed by three-week data collection intervals for 21-weeks; a total of 147 days (Fig ane). During data drove intervals, alfalfa pellets offered through the gas measuring device (GreenFeed organization, C-Lock, Inc., Rapid Urban center, SD) were included as function of daily feed intake. Steers were fed 3 diets during the written report; high (starter diet; 63 days), medium (transition nutrition; 21 days), and low (finisher diet; 63 days) provender TMRs, which are typical life-stage TMRs of growing beefiness steers (Table ane). Samples from the three diets and alfalfa pellets were nerveless once per calendar week and numberless of A. taxiformis were randomly sampled and analyzed (Table 2) for dry out matter, acrid detergent fiber, NDF, lignin, starch, crude fat, total digestible nutrient and mineral content (Cumberland Valley Belittling Services, Waynesboro, PA). Steers were offered water advertising libitum.

The A. taxiformis used equally a feed additive was provided by Republic Scientific and Industrial Research System (CSIRO) Australia. The seaweed was collected during the gametophyte phase from Humpy Island, Keppel Bay, QLD (23o13'01"South, 150o54'01"E) by Middle for Macroalgal Resource and Biotechnology of James Cook University, Townsville, Queensland, Australia. Once collected, the A. taxiformis was frozen, stored at −15°C, then freeze dried at Forager Nutrient Co., Cherry-red Hills, Tasmania, Australia, and afterwards footing using a Hobart D340 mixer (Troy, OH, USA) and 3mm sieve. Total seaweed inclusion ranged from 46.seven to 55.7 g/solar day for Depression and 76.1 to 99.4 yard/mean solar day for High handling. The seaweed used in the study contained bromoform at a concentration of 7.8 mg/g dry out weight equally determined by Bigelow Analytical Services (East Boothbay, ME, USA). To increase palatability and adhesion to feed, 200 ml of molasses and 200 ml of water was mixed with the A. taxiformis supplement, then the molasses-water-A. taxiformis mixture was homogenously incorporated into the TMR, by hand mixing, for each treatment beast. The Command group also received 200 ml of both molasses and h2o with their daily feed to ensure A. taxiformis was the only departure between the three treatments.

Sample collection and assay

Marsh gas, CO₂, and H₂ gas emissions from steers were measured using the GreenFeed system (C-Lock Inc., Rapid Urban center, SD, United states). Gas emissions were measured during the covariate (baseline) period and experimental menstruation during weeks three, 6, 9, 12, 15, eighteen, and 21. In each measurement period, gas emission data were collected during 3 consecutive days equally follows: starting at 0700, 1300, and 1900 hours (sampling twenty-four hours one); 0100, k, and 1600 hours (sampling twenty-four hour period 2); and 2200 and 0400 hours (sampling mean solar day three). Eructated gas samples from each steer were taken at random across each handling grouping. The GreenFeed machine was manually moved to each steer pen where the steer was allowed to enter the machine by choice and induced to consume from the machine for 3 to v minutes, followed by a 2-infinitesimal background gas sample collection. 1 GreenFeed unit of measurement was used for all gas emissions samples and took approximately 140 minutes to consummate each timepoint. The GreenFeed organisation was calibrated earlier each measurement catamenia with a standard gas mixture containing (mol %): 5000 ppm CO_ii, 500 ppm CH₄, 10 ppm H_ii, 21% O_two and nitrogen as a balance (Air Liquide America Specialty Gases, Rancho Cucamonga, CA). Recovery rates for CO₂, CH_four, and H₂ observed in this written report were within +/− 3% of the known quantities of gas released. Alfalfa pellets were offered at each sampling event equally bait feed and was kept beneath ten% of the full DMI during each iii-mean solar day measurement period. The composition of alfalfa pellets is shown in Table 2. Feed residuals were collected daily before the forenoon feeding to decide the previous mean solar day'due south intake. Feed intake and feed costs were recorded daily and bodyweight (BW) was measured in one case weekly, using a Silencer Ranch Model hydraulic squeeze chute (Dubas Equipment Stapleton, NE) equipped with a calibration, at 0500 before morning time feeding to reduce variability due to gut fill.

Afterward the feeding trial was completed, all 20 steers were sent to a USDA-inspected commercial packing found (Cargill Meat Solutions, Fresno, California) for slaughter. On the day of slaughter, steers were marked and followed throughout the process. On the first 24-hour interval, livers were collected, placed in individually labelled freezer bags and stored on dry out water ice until placed in a −20°C freezer. Carcasses were aged for 48 hours in a big cooler and and so graded by a certified USDA grader. Straight later grading, carcasses were sent to fabrication where the strip loin from the left side of each carcass was cut and saved for further assay. All xx strip loins were vacuum packed and so stored on water ice and transported back to the University of California, Davis where they were cryovac packaged and stored at iv°C in night for 14 days. After 14-day of aging, strip loins were cut into steaks (2.45 cm thickness) and individually vacuum packaged and stored at −twenty°C. Samples of steaks and livers were analyzed by Bigelow Analytical Services (Eastward Boothbay, ME, Usa) for bromoform concentrations following a modified protocol described by Paul et al. (2009) [25]. The limits of bromoform detection and quantification were 0.06 mg/kg and 0.20 mg/kg, respectively. Steaks were likewise analyzed for proximate analysis by Midwest Labs (Omeha, Nebraska) for moisture (AOAC 950.46), protein (AOAC 992.15), fat (AOAC 991.36), ash (AOAC 900.02, 920.155, 920.153), calories (21 CFR P101.9), carbohydrates (100 –Moisture–Protein–Fat—Ash), and iodine (USP 233) concentration.

To test for objective tenderness, slice shear strength (SSF) and Warner-Brazler shear forcefulness (WBSF) were measured following the protocol described by [34]. One steak from each beast was thawed overnight and cooked to an internal temperature of 71°C. Within 1 to 2 minutes after cooking, the SSF were measured using machine texture analyzer (TMS Pro Texture Analyzer, Food Technology corporation, Sterling, VA, USA) with a crosshead at the speed of 500 mm/minute. To exam WBSF, cooked steaks were cooled at 4°C overnight, and and so four cores were cut using WEN 8-inch 5 Speed Drill Press from one steak from each animal parallel to the muscle fiber orientation. The WBSF was measured using the TMS Pro texture analyzer with a Warner Bratzler blade (two.eight mm wide) and a crosshead at speed of 250 mm/minute. The average meridian forces for all four cores were recorded.

A consumer sensory panel was conducted at UC-Davis. Strip steaks were thawed at 4°C for 24 hours and then cooked to an internal temperature of 71°C using a George Foreman clamshell (Spectrum Brands, Middleton, WS, USA). Internal temperature was taken from the geometric heart of each steak using a K thermocouple thermometer (AccuTuff 351, model 35100, Cooper-Atkins Corporation, Middlefield, CT, Usa). Following cooking, steaks were rested for 3 minutes then cut into 1.five cm^three pieces. Each steak was randomly assigned a unique three digit number, placed into glass bowls covered in tin foil then stored in an insulated food warmer (Carlisle model PC300N03, Oklahoma, OK, USA) for longer than thirty minutes prior to the start of each sensory evaluation session. A full of 112 participants evaluated steak samples during i of the 5 sessions held over a 4-twenty-four hours period. Each participant evaluated a total of three steak samples, one from each treatment group, with a minimum of 2 ane.5 cm^three pieces per steak. Each participant was asked to evaluate tenderness, flavor, juiciness, and overall acceptance using a ix-point hedonic scale (ane = Dislike extremely and 9 = Similar extremely).

Statistical assay

Statistical analysis was performed using R statistical software (version 3.6.1; The R Foundation for Statistical Computing, Vienna, Austria). The linear mixed-effects models (lme) procedure was used with the steer as the experimental unit. GreenFeed emission data were averaged per steer and gas measurement menses, which was and so used in the statistical assay. The statistical model included treatment, diet, treatment × diet interactions, and the covariate term, with the error term assumed to be normally distributed with mean = 0 and constant variance. Individual beast was used as random consequence, whereas all other factors were considered fixed. Information was analyzed equally repeated measures with an autoregressive 1 correlation structure. Statistical significance was established when P ≤ 0.05 and a trend at 0.05 > P ≤ 0.10. The consumer sensory evaluation data were analyzed using the Kruskal-Wallis test. The Dunn's test with P-value adjustment following Bonferroni methods was used for postal service-hoc pair-wise comparisons.

Dry out thing intake (DMI) and cost per kg of gain (CPG) data was averaged by week and used in the statistical assay. Boilerplate daily gain (ADG) was calculated by subtracting initial BW from final BW then dividing past the number of experimental days for each diet regimen and the duration of the study (i.due east. 63 days on high forage (starter) TMR, 21 days on medium forage (transition) TMR, then 63 days on low forage (finisher) TMR with total study elapsing of 147 days). Feed conversion efficiency (FCE) was calculated by dividing ADG by DMI for each diet regimen and the duration of the study. Carbon Dioxide (CO_two), CH₄, and H_ii emissions are reported every bit production (yard/day), yield (one thousand/kg DMI), and intensity (g/kg ADG).

Results

Gas parameters

The emissions as production (g/day), yield (g/kg DMI), and intensity (g/kg ADG) of CH_iv, H₂, and CO₂ gases from the steers in the three treatment groups (Command, Low, and Loftier) are presented in Fig ii (for the duration of the trial) and Table 3 (divided by the three diet regimes). Inclusion of A. taxiformis in the TMR had a significant linear reduction in enteric CH₄ production, yield, and intensity. For the elapsing of the experimental flow, CH₄ production, yield and intensity declined by 50.6 and 74.9%, 45 and 68%, and fifty.9 and 73.ane% for Depression and High treatments, respectively, compared to Control. Hydrogen production, yield, and intensity significantly increased by 318 and 497%, 336 and 590%, and 380 and 578% in the Depression and Loftier treatments, respectively, for the duration of the experiment. Carbon dioxide (CO₂) production and intensity factors were non affected by either Depression or High treatments, however, CO_two yield was significantly greater in High treatment compared to Command (P = 0.03).

Fig ii. Asparagopsis taxiformis inclusion furnishings on methane, hydrogen and carbon dioxide emissions over a 147-day menstruation.

Means, standard deviations, and statistical differences of methane, hydrogen, and carbon dioxide production (g/d) (A1,B1,C1), yield (g/kg dry thing intake (DMI)) (A2,B2,C2), and intensity (g/kg average daily proceeds) (A3,B3,C3) for 0%, 0.25% (Low), and 0.50% (Loftier) Asparagopsis taxiformis inclusion. Means within a graph with unlike alphabets differ (P < 0.05).

https://doi.org/ten.1371/journal.pone.0247820.g002

An interaction was observed between diet formulation and magnitude of CH₄ reduction and H₂ formation for production, yield, and intensity factors (Table 3). Methane production, yield, and intensity in steers on the high provender TMR and supplemented with A. taxiformis reduced by 36.4 and 58.7%, 32.7 and 51.9%, and 36.9 and 56.4% for Low and High treatments, respectively. Hydrogen production, yield, and intensity increased by 177 and 360%, 198 and 478%, and 256 and 524% for the Depression and Loftier treatments, respectively. Methane production, yield, and intensity in steers fed the medium forage TMR and supplemented with A. taxiformis was reduced past 51.8 and 86.8%, 44.6 and 79.7%, and 54.4% and 82.four%% for the Low and High treatments, respectively. Furthermore, H_ii production, yield and intensity significantly increased past 326 and 535%, 404 and 753%, and 341 and 626% for the Low and High treatments, respectively. Steers fed low forage TMR and supplemented with A. taxiformis reduced CH₄ production, yield, and intensity by 72.4 and 81.9%, 69.8 and fourscore.0%, and 67.5 and 82.6% for Depression and High treatments, respectively. Additionally, H₂ production, yield, and intensity increased by 419 and 618%, 503 and 649%, and 566 and 559% for the Depression and High treatments, respectively. No significant differences were found in CO₂ product, yield, or intensity in whatever of the three diets.

Animal product parameters

Dry out matter intake (DMI), ADG, feed conversion efficiency (ADG/DMI; FCE) and cost per proceeds ($USD/kg weight gain; CPG) every bit impacted by treatment groups (Command, Low, and High) for the entire experimental period is presented in Table 4 and for the individual TMRs in Table 5. Initial BW, final BW, carcass weight and full weight gained are shown in Tabular array 4. During the unabridged experiment (Tabular array 4), DMI in Depression treatment tended (P = 0.08) to decrease by viii% and High treatment DMI significantly reduced by 14% (P < 0.01) whereas no pregnant effects were observed in ADG by either Low or High handling groups when compared to Control. With the reduction of DMI in Depression and High treatments and similar ADG among all 3 treatments, FCE tended to increase vii% (P = 0.06) in Depression treatment and increased 14% (P < 0.01) in High treatment. No pregnant differences betwixt initial BW, concluding BW, total gains, CPG or carcass weight were found betwixt Command and treatment groups. While no significant differences were found in CPG, there was a $0.37 USD/kg gain differential between High and Command and $0.18 USD/kg proceeds differential betwixt Depression and Control.

Decreases in DMI were also found over the three dissimilar TMR diets (Tabular array 5) where steers fed the loftier and medium forage TMR and the High treatment decreased their DMI 18.5 (P = 0.01) and 18.0% (P < 0.01), respectively. No significant effects were observed in ADG, CPG, or FCE by the Depression or High treatment groups during the private TMR diets. Additionally, toll differentials for Loftier treatment were $0.29, $0.twoscore, and $0.34 USD/kg gain and for Low treatment were $0.fifteen, $0.49, and $0.34 USD/kg gain for the loftier, medium, and low forage TMRs, respectively.

Carcass and meat quality parameters

There was no statistical difference between treatment groups for rib eye expanse (Tabular array six). No effects were constitute betwixt Control, Low, and High treatments in moisture, protein, fat, ash, carbohydrates, or calorie content of strip loins (Table 6). The average WBSF values for the Control, Low and High groups were two.81, ii.66 and ii.61 kg, respectively. Additionally, the SSF averages were measured as 17.i for Command, 16.75 for Low and 17.4 kg for High treatments. No pregnant differences (P > 0.05) were found in shear force resistance amongst treatment groups. Hateful scores of all sensory attributes (tenderness, juiciness, and flavor) by consumer panels were not significantly different (P > 0.05) among treatment groups (Table 6). The gustatory modality panel considered all steaks, regardless of treatment grouping, to be moderately tender and juicy. This was consequent with the sense of taste panel stating that they moderately liked the flavor of all steaks regardless of treatment group. At that place was no difference (P > 0.05) in overall acceptability among treatment groups. There was a linear increase in iodine concentrations in both Depression (P < 0.01) and High (P < 0.01) compared to Control. Iodine concentrations for the Control treatment group were below detection levels, which was set at 0.10 mg/g (Tabular array 6). Nonetheless, 5 out of seven steers in Low handling grouping had iodine levels above the detection level with a treatment boilerplate of 0.08 mg/1000 (P < 0.01). All 6 steers in the Loftier handling grouping were establish to comprise iodine levels above the detection level with concentration levels ranging betwixt 0.xiv–0.17 mg/one thousand with a mean of 0.15 mg/g (P < 0.01). Bromoform concentrations for all treatment groups were below detection levels, which were 0.06 mg/kg.

Give-and-take

Enteric methyl hydride production, yield, and intensity

This report demonstrated that dietary inclusion of A. taxiformis induces a consequent and considerable reduction in enteric CH₄ production from steers on a typical feedlot style nutrition. Enteric CH₄ is the largest contributor to GHG emissions from livestock production systems. Significant reductions in CH₄ yield, which is standardized by DMI, when Asparagopsis is supplemented to beef cattle diets has been established in this written report and are similar to the reductions found in previous studies [6,29,35]. While CH₄ intensities have been previously reported for dairy cows fed A. armata [29], this is the starting time report to measure CH₄ intensity differences in beefiness cattle fed A. taxiformis. Intensity reports are of import to determine the amount of methane being produced per unit of output for ruminant livestock systems. At that place is a concern that feed additives and other CH₄ reducing agents decrease in efficacy over time [fourteen]. This study provided prove that the seaweed inclusion was effective in reducing CH₄ emissions, which persisted for the duration of the study of 147 days (Fig three). Notably, until this study the longest exposure to A. taxiformis had been demonstrated for steers in a study catastrophe after a 90-d finishing menstruum [6]. To date, only iii in vivo studies have been published using Asparagopsis spp. to reduce enteric CH₄ emissions in feedlot Brangus steers [6], lactating dairy cattle [29], and sheep [35]. All studies bear witness considerable yet variable reductions in enteric CH₄ emissions. The differences in efficacy are likely due to levels of seaweed inclusion, formulation of the diets, and differences in seaweed quality based on bromoform concentrations.

Fig 3. Asparagopsis taxiformis inclusion furnishings on methane emissions during the 21 week experimental flow.

Methane product [1000 CH_iv/day] (A) and methane yield [m CH_iv/kg DMI] (B) from beefiness steers supplemented with Asparagopsis taxiformis at 0%, 0.25%, and 0.five% of basal full mixed ration on an organic affair basis during the 21 week experimental flow. Data points are treatment means for each gas drove timepoint and error bars represent standard errors.

https://doi.org/x.1371/periodical.pone.0247820.g003

It has been previously hypothesized that NDF levels can also influence the rate at which CH₄ is reduced with the inclusion of inhibitors [4,24]. In the electric current study, the magnitude of reductions in CH₄ product were negatively correlated (r² = 0.89) with NDF levels in the three nutrition regimens that contained 33.1% (high forage), 25.eight% (medium forage), and 18.6% (low forage) NDF levels. Enteric CH_iv production was reduced 32.7, 44.half-dozen and 69.8% in steers on the Low handling and 51.9, 79.seven, and 80.0% on High treatment with high, medium and depression provender TMRs, respectively. The low forage TMR, containing the lowest NDF levels, was the most sensitive to the inclusion of A. taxiformis with CH₄ reductions above 70% at equivalent inclusion levels compared to the higher forage TMRs. Vyas et al (2018) showed like trends of greater methane reduction potential in high grain, low NDF, diets in combination with the anti-methanogenic compound iii-NOP [24]. It has been hypothesized to increase efficacy by a reduction in rumen MCR concentration when low NDF is fed, thus increasing the MCR targeting capability of the anti-methanogenic feed additive. An lxxx.6% reduction of CH_four yield in sheep fed diets containing 55.six% NDF, even so, the level of A. taxiformis intake by the sheep was unclear but was offered at 6 times the Loftier treatment in our report [35]. A 42.7% reduction in CH₄ yield was observed in lactating dairy cattle fed a diet containing xxx.1% NDF at 1% inclusion rate of A. armata [29]. The high forage TMR in our study had a similar NDF level to the dairy report, yet, had approximately double the reduction of CH_iv, fifty-fifty when consuming 50% less seaweed. These differences relate to a large degree to the quality of seaweed in terms of the concentration of bromoform, which was 1.32 mg/thousand in the dairy study [29] compared to vii.82 mg/g in the current study. The aforementioned collection of A. taxiformis was used in a previously published in vivo study focused on Brangus feedlot steers for a duration of 90 days [6]. This seaweed had bromoform concentration of half-dozen.55 mg/thousand, which was marginally lower than our study and may be due to variation in the drove, sampling, analysis techniques, or storage weather. Despite the marginally lower bromoform concentration in the seaweed and using 0.20% inclusion rate of A. taxiformis on OM basis, the CH_iv yield was reduced by up to 98% in Brangus feedlot steers. The diet used by Kinley et al. (2020) included 30.vi% NDF, which was similar to our loftier cobweb nutrition [6]. The greater efficacy of A. taxiformis in that written report could exist due to collective feed formulation differences such as the free energy dense component of barley versus corn, which is typical of Australian and American feedlots, respectively. Additionally, information technology could be due to benign interaction with the ionophore, monensin, that was used in the Australian study. Monensin has non been used in whatsoever other feed formulation in other in vivo studies with the inclusion of Asparagopsis species. Apply of monensin in diets has shown to decrease CH₄ yields by up to 6% in feedlot steers while besides having an enhanced upshot in diets containing greater NDF levels [36]. A potential enhancing interaction of the seaweed with monensin is of groovy involvement and farther investigation volition elucidate this potential that could have pregnant benign economical and ecology impact for formulated feeding systems that use monensin.

Enteric hydrogen and carbon dioxide emissions

Increases in H₂ yield have typically been recorded when anti-methanogenic feed additives are used, and with the improver of Asparagopsis species in dairy cattle (1.25–3.75 fold) [29] and Brangus feedlot steers (3.8–17.0 fold) [6]. Similar increases in H₂ yield have been reported in feed additives that reduce enteric CH₄ emissions targeting methanogens. For example, in lactating dairy cows supplemented with 3-NOP, H₂ yield increased 23–71 fold [37]. Bromochloromethane (BCM) fed to goats increased H₂ (mmol/head per day) 5–35 fold, while chloroform fed to Brahman steers increased H_ii yield 316 fold [38,39]. Although feeding Asparagopsis spp. increased overall H_ii yield (Fig 4), the magnitude was considerably lower (ane.25–17 fold) compared to alternative CH₄ reducing feed additives (five–316 fold), with similar levels of reductions in CH₄. This indicates that there may be a redirection of H₂ molecules that would otherwise be utilized through the germination of CH_four and redirected into unlike pathways that could be beneficial to the animal. For example, increased propionate to acetate concentrations have been recorded in in vitro [40,41] and in vivo [six] using A. taxiformis and BCM [42] for CH_four mitigation which may indicate that some of the excess H₂ is being utilized for propionate production.

Fig 4. Asparagopsis taxiformis inclusion effects on hydrogen emissions during the 21-week experimental period.

Hydrogen product [g H₂/24-hour interval] (A) and Hydrogen yield [g H_ii/kg DMI] (B) from beef steers supplemented with Asparagopsis taxiformis at 0%, 0.25%, and 0.5% of basal total mixed ration on an organic thing basis during the 21 week experimental period. Data points are handling ways for each gas collection timepoint and mistake bars represent standard errors.

https://doi.org/10.1371/journal.pone.0247820.g004

Similar to the lactating dairy cattle written report with i% A. armata supplementation [29], the CO₂ yield in the electric current study also increased in the High group (Fig ii). Withal, in the current written report no differences in CO₂ production were seen. Typically, CO₂ and H_ii are used in the methanogenesis pathway to class CH_four thus increases in exhaled CO₂ is expected with the add-on of anti-methanogenic compounds. The fact that only CO_ii yield increased may exist due to decreases in DMI, which could accept reduced overall CO₂ generation thus resulting in no increases seen in CO_two production factors.

Animal production parameters

Dry affair intake reductions observed in this study were consistent with previous studies in lactating dairy cows where decreases in DMI were found to be 10.7 and 37.9% at 0.50 and ane.0% inclusion rate of A. armata [29], respectively. Decreases in DMI have also been reported in cattle fed other anti-methanogenic feed additives in a linear dose-response manner. For instance, Tomkins et al (2009) reported 3 to xix% reductions in DMI in steers supplemented with BCM at dosages between 0.15 and 0.lx grand/100 kg alive weight [5]. Additionally, Martinez-Fernandez et al (2016) found 1.vii to 15% reductions in DMI when chloroform was direct applied to the rumen, through a rumen fistula, at dosages between 1 to 2.6 grand/100g liveweight [39]. In dissimilarity, Kinley et al (2020) reported no significant differences in DMI at the highest A. taxiformis level of 0.twenty% [6]. Still, the inclusion level was less than our study'southward lowest inclusion rate, then based on previous experiment's observation of reduced DMI in a dose-response mode [29], it was expected to take lower outcome on DMI. Decreases in DMI are normally associated with lower productivity due to lower levels of nutrients and dietary energy consumed. However, there was no significant divergence in ADG betwixt steers in the High treatment and Control (boilerplate 1.56 kg/day) groups despite consuming fourteen% less feed. The results were in agreement with a previous study [29], in which milk production was not compromised at a 0.5% OM inclusion level despite reductions in DMI. The FCE (ADG/DMI) increased significantly in High treatment group, suggesting that inclusion rates of A. taxiformis at 0.5% improves overall feed efficiency in growing beefiness steers. Since a big proportion of on farm costs is the purchase of feed, an improved feed efficiency is particularly heady for producers to decrease feed costs while as well producing the aforementioned corporeality of total weight gains. Total gains were between 224 kg (Depression) to 236 kg (High) combined with an average cost differential of ~$0.18 USD/kg gain (Low) and ~$0.37 USD/kg gain (Loftier). A producer finishing 1000 head of beef cattle has the potential to reduce feed costs past $40,320 (Depression) to $87,320 (High) depending on seaweed dosage. While the CPG in this study were non statistically significant, this may be due to low beast numbers in each treatment and warrants further investigation on a larger feedlot setting to reduce animate being variability.

Bromoform and iodine residues

Bromoform is the major active ingredient responsible for CH₄ reduction when fed to cattle [43]. Yet, high levels of bromoform are suspected to exist hazardous for humans and mice. While bromoform intake limits are yet to be defined for cattle specifically, the Us EPA (2017) has suggested a reference dose for bromoform, an estimated level of daily oral exposure without negative effects, to be 0.02 mg/kg BW/day for human consumption [44]. Information technology is essential that nutrient products from livestock consuming the seaweed are confirmed as safe for consumption and that bromoform residues are non transferred to the edible tissues and offal of bovines at levels detrimental to nutrient safety. Previous studies have demonstrated that bromoform was not detectable in the kidney, musculus, fatty deposits, blood, feces, and milk in either Brangus feedlot steers [6], dairy cows [29], or sheep [35]. Strip loin and liver samples from steers were collected and in agreement with previous studies, no bromoform was detected in this study.

The National Academies of Sciences, Applied science, and Medicine recommendations for daily iodine intake in growing beef cattle is 0.5 mg/g DMI and maximum tolerable limit is fifty mg/1000 DMI [45]. Based on DMI intake from steers in this report, recommended daily iodine intake levels were 5.two mg/twenty-four hour period and 4.85 mg/day and maximum limits are 521 mg/day and 485 mg/day for Low and High handling groups, respectively. The iodine level in the A. taxiformis fed in the current report contained 2.27 mg/g, therefore, maximum daily intake of seaweed iodine was 106–127 mg/day and 173–225 mg/twenty-four hour period for the Low and Loftier handling groups, respectively. While these levels do not exceed maximum tolerable limits, they exceed daily iodine intake recommendations for cattle, therefore it was appropriate to exam for iodine remainder levels in meat used for homo consumption. The US Food and Nutrition Board of the National Academy of Sciences has set a tolerable upper intake level (UL) for human being consumption of foods, which is defined as the highest level of daily intake that poses no adverse wellness effects [46]. The iodine UL ranges betwixt 200 ug/solar day to 1,100 ug/day depending on age, gender, and lactation demographics. Strip loins tested for iodine residues had levels of 0.08 and 0.xv ug/g from steers in treatments Depression and Loftier, respectively. These iodine residues are far under the UL limits for human consumption. For case, UL for a person under 3 years of age is 200 ug/twenty-four hours meaning that this person would take to consume more than 2.5 kg/day and 1.3 kg/day of meat from a Depression and High steers, respectively, to accomplish the UL. An adult over the age of 18 has an UL of 1,100 ug/twenty-four hour period and would have to eat more than 13.8 kg/day and 7.3 kg/twenty-four hour period of meat from a Depression and Loftier steers, respectively, to achieve their UL of iodine intake. At the inclusion levels and iodine concentration of A. taxiformis used in this report the margin of condom is extremely loftier and the likelihood of iodine toxicity from consuming the meat is extremely low. The health hazards of consistently consuming any meat at such levels is much college than the iodine toxicity risks. Depression level iodine in meat may provide for provision of iodine to populations that suffer from natural iodine deficiency, a common issue in populations with low intake of marine food products [47].

Carcass and meat quality parameters

Marbling scores ranged from 410–810 while all carcasses, regardless of treatment, graded as either choice or prime. The value placed on tenderness in the marketplace is high and has even been found that consumers are likely to pay premiums for more tender beef [48]. Many factors tin can greatly affect meat tenderness, such equally animals' age at slaughter, brood, marbling, and diet [49–51]. All animals used in the current study were of similar historic period and breed. Additionally, no significant deviation in average marbling scores was observed. The lack of significant differences seen in these factors further supports that the supplementation of A. taxiformis at the current dosage did not affect the tenderness of meat. This is in agreement with Kinley et al. (2020)'s meat taste assessment where no differences between Command and A. taxiformis supplemented beefiness cattle were found [6]. The combination of both the current study as well every bit the Kinley et al (2020) written report [vi] indicates that the supplementation of A. taxiformis at or below 0.5% to cattle does not significantly impact overall meat quality nor alter the sensory properties of the steaks.

Conclusions

This report demonstrated that the use of A. taxiformis supplemented to beef cattle diets reduced enteric CH_four emissions for a duration of 21 weeks without any loss in efficacy. The efficacy was highly correlated with the proportion of NDF in the diet equally demonstrated through the typical stepwise transition to a feedlot finishing diet conception. Additionally, supplementing A. taxiformis had no measurable bromoform residues, no detrimental iodine residual effects in the production, and did not alter meat quality or sensory properties. Importantly, the apply of A. taxiformis impacts DMI and not ADG, therefore increasing overall feed efficiency (FCE) in growing beef steers. This study besides demonstrated a potential to reduce the cost of production per kg of weight gain. These feed cost reductions in combination with significantly reduced CH₄ emissions have a potential to transform beef product into a more economically and environmentally sustainable red meat manufacture.

Next steps for the use of Asparagopsis as a feed-additive would be to develop aquaculture techniques in ocean and land-based systems globally, each addressing local challenges to produce a consistent and high-quality product. Processing techniques are evolving with the aim of stabilizing every bit feed supplement and the economic science of the supply chain. The techniques include utilization of already fed components every bit carriers and formats such equally suspensions in oil which may exist washed using fresh or dried seaweed, and options in typical feed formulations such as mixtures are being explored [52]. Transportation of the candy or unprocessed seaweed should be kept to a minimum, and then cultivation in the region of utilize is recommended specially to avoid long-haul shipping.

Supporting information

S1 Table. Original data.

Information sets used for statistical assay of animal production, gas emissions, carcass parameters, and taste panel between Command, 0.25% OM inclusion of Asparagopsis taxiformis (Low), and 0.50% OM inclusion of Asparagopsis taxiformis (Loftier) handling groups.

https://doi.org/ten.1371/journal.pone.0247820.s001

(XLSX)

Acknowledgments

The authors acknowledge Meat and Livestock Australia, James Cook University and CSIRO for the supply of A. taxiformis used in the trial, in detail T.L. Neoh for sample preparation. Nosotros are grateful to undergraduate interns: A. Neveu, A. Wilson, A. Yiao, B. Wong, C. Grub, C. Martinez, C. Mielke, D. Maqueda, Eastward. Anderson, J. DeGuzman, J. Fang, J. Infante, J. Jordan, K. Allchin, 1000. Garcia, K. Martin, 50. Arkangel, G. Cervantes, Grand. Venegas, Chiliad. Zack, P. Nguyen, P. Petschl, Due south. Calderon, S. Leal, S. Lee, T. Lee, and V. Escobar that participated in the trial. We appreciate Dr. Craig Burnell and Steve Archer (Bigelow Labs in Due east Boothbay, ME, United states) for developing methods to measure bromoform concentration in Asparagopsis taxiformis, meat, liver, and feces collected in this study.

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Source: https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0247820