Elsevier

Journal of Cleaner Production

Volume 234, 10 October 2019, Pages 132-138
Journal of Cleaner Production

Inclusion of Asparagopsis armata in lactating dairy cows’ diet reduces enteric methane emission by over 50 percent

https://doi.org/10.1016/j.jclepro.2019.06.193Get rights and content

Highlights

  • Methane production by cows reduced up to 67% due to seaweed inclusion in diet.

  • Methane emissions reduced by up to 43% when normalized by how much cows consumed.

  • Adjusted for milk production methane emissions reduced by up to 60%.

  • Hydrogen and carbon dioxide emissions increased as methane emission decreased.

Abstract

Livestock production, particularly enteric methane production, contributes to greenhouse gas emissions globally. Various mitigation strategies developed to reduce enteric emissions have limited success. Although in vitro studies have shown a considerable reduction in methane emissions using Asparagopsis spp., no studies have been conducted to investigate the effect of any species of Asparagopsis in dairy cattle. Our objective was to evaluate quantitatively the response of cows consuming Asparagopsis armata on methane production (g/kg), yield (g/kg feed intake) and intensity (g/kg milk yield). Twelve post-peak lactating Holstein cows were randomly assigned to three treatments (control, 0.5% and 1% inclusion levels of A. armata on organic matter basis) in a 3 × 3 Latin square design with three 21-day periods. Enteric methane emissions were measured using the GreenFeed system. Methane production by cows decreased significantly by 26.4% at the low (0.5%) level of A. armata inclusion and 67.2% at the high (1%) level of inclusion. Feed intake was reduced by 10.8 and 38.0%, in cows fed the low and high level of macroalgae inclusion, respectively. Methane yield decreased significantly by 20.3 and 42.7% in cows fed diet including 0.5% and 1% A. armata inclusion levels, respectively (P = <0.0001). Methane intensity significantly decreased by 26.8% from cows fed at 0.5% level and 60% at the 1.0% A. armata inclusion level. Bromoform concentrations in milk were not significantly different between treatments. Our in vivo results showed that A. armata has potential to be used as a feed additive to reduce enteric methane emissions.

Introduction

The livestock sector contributes 14.5% of global GHG emissions (Gerber et al., 2013), with global methane emissions contributing to about 2.1 Gt CO2 equivalent in 2010 (Smith et al., 2014). There are considerable differences in contribution of enteric methane in different regions and countries of the world. The main source of anthropogenic methane emissions in the United States is generated by enteric fermentation of livestock (25%; NASEM, 2018). US EPA (2019) estimated the total methane emissions from enteric fermentation in the United States to be 6.46 Tg in 2017, which is equivalent to 27% of the nation's anthropogenic methane emissions. Enteric methane is a natural by-product of microbial fermentation of nutrients in the digestive tract of animals. Enteric methane emissions represent up to 11% of dietary gross energy consumed by ruminants and in North American dairy cattle it is estimated to be about 5.7% of gross energy intake (Moraes et al., 2014).

Hristov et al. (2013) reported that mitigation options including nitrates, ionophores, tannins, direct-fed microbials and vaccines may offer opportunities to reduce enteric methane emissions; however, the results have been inconsistent. Knapp et al. (2014) estimated that nutrition and feeding approaches may contribute to reducing methane emission intensity (i.e., emissions per milk yield) by 2.5–15%, whereas rumen modifiers had little success in sustained methane emissions without compromising milk production. Methane inhibitors may be a more successful approach in reducing emissions from enteric fermentation. For example, 3-nitrooxypropanol (3NOP) has been reported to substantially decrease methane emissions from ruminants (Duin et al., 2016).

Seaweeds have been a traditional part of livestock diet and have been used since the recording of agricultural practices began (Evans and Critchley 2014). There have been several studies on seaweeds to characterize their effects as livestock feeds and their potential to manipulate rumen fermentation and methane production. Maia et al. (2016) evaluated several seaweeds and reported that their efficacy is impacted by the formulation of the basal feed of the livestock. The utility of seaweeds as feeds is impacted by the composition of the biomass which in turn is a result of many inherent factors such as species, growth stage, habitat, and external factors such as temperature, light, and nutrient availability. A key feature is the circumstantial production and accumulation of secondary metabolites (Paul et al., 2006) that may have a bioactive impact on the animals or from the perspective of methane production, on the microbial consortium that thrives in a rumen. Many seaweeds have been demonstrated to reduce methane production by rumen methanogens but with variable effects on fermentative health and substrate digestibility (Machado et al., 2014). The effectiveness of the seaweeds has been shown to have a relationship with the level of inclusion in the diet (Kinley et al., 2016; Machado et al., 2016a, Machado et al., 2016b; Li et al., 2018) and only Asparagopsis has been demonstrated to remain effective and dramatically antimethanogenic without negative impacts on rumen function and at low inclusion levels in animal diets (Kinley et al., 2016; Li et al., 2018).

In the development of knowledge of Asparagopsis spp. effects on rumen microbial production of methane, there has been progression through multiple in vitro studies all of which have demonstrated significant if not total reduction of methane emissions at levels of approximately 2% of diet substrates (Dubois et al., 2013; Machado et al., 2016b, Machado et al., 2016a). Even though this dietary level of the seaweed was low and considered feasible for livestock production systems, Li et al. (2018) demonstrated in animals the potential for efficacy at lower intake levels. From their study in sheep using Asparagopsis taxiformis, Li et al. (2018) reported up to 80% reduction in methane emissions. Although the project applied A. taxiformis offerings of 0.5, 1, 2, and 3% of the diet, the feed formulation provided for voluntary intake of the seaweed product which resulted in partial unavailability or refusal by the sheep. Nevertheless with reduced intake of the seaweed the results showed significant methane reduction and was the first indication that in vitro studies had over predicted the levels of Asparagopsis intake required for effective methane reduction in vivo. This created an exploratory research requirement for subsequent animal studies to characterize the optimal intake of Asparagopsis to significantly reduce methane emissions which is proposed to be variable based on diet composition.

In the systematic in vivo characterization of Asparagopsis as an antimethanogenic feed additive for ruminant livestock this study is the first demonstration of the effects in lactating dairy cattle. Based on previous in vitro and in vivo work it was hypothesized that application of Asparagopsis as a feed additive in a total mixed ration (TMR) would significantly reduce enteric methane emissions and improve productivity represented by increased milk production. The objectives of the study were to: (1) investigate the potential of the macroalgae Asparagopsis armata in reducing methane emissions in vivo; and (2) quantify methane production (g/day per cow), yield (g/kg dry matter intake (DMI)) and intensity (g/kg milk yield) as a result of inclusion of A. armata in the TMR of lactating dairy cattle.

Section snippets

Animals and experimental design

All animal procedures were approved by the UC Davis Institutional Animal Care and Use Committee. Twelve multiparous Holstein cows with an average weight of 729 ± 24.9 kg, 35.1 ± 2.19 kg/d milk yield and 201 ± 37 days in lactation were housed in a freestall barn equipped with individual animal sensor electronic recognition Calan gates (American Calan, Northwood, NH) to measure individual animal feed intake. As this was the first reported study using dairy cattle, we conducted a pretrial to

Gas parameters

The average methane, hydrogen, and carbon dioxide production for the three treatment groups is given in Fig. 1. Methane production (g/d) by cows decreased significantly by 26.4% at the low (0.5%) level of A. armata inclusion and 67.2% at the high (1%) level (Fig. 1A). Hydrogen production increased 163 and 236% by cows fed diets with low and high levels of macroalgae inclusion. Carbon dioxide production was similar between control and low level of inclusion; however, there was a significant

Discussion

Livestock systems, particularly ruminants, contribute to greenhouse gas emissions, and particularly in the form of enteric methane. A review of mitigation options for enteric methane from ruminants showed that some of the effective strategies include increasing forage digestibility, replacing grass silage with corn silage, feeding legumes, adding dietary lipids and concentrates (Hristov et al., 2013). Although effective, these types of system management options may not offer the scale of

Conclusions

The potential of the macroalgae Asparagopsis to reduce methane emissions shown in in vitro studies was investigated in vivo using dairy cattle. Adding Asparagopsis at 0.5% of diet OM resulted in reductions of 26.4% in methane production, 20.5% in methane yield (adjusted for feed intake) and 26.8% in methane intensity (adjusted for milk production) without compromising milk yield or intake. Increasing the inclusion level to 1% resulted in reductions of 67.2% methane production, 42.6% methane

Acknowledgments

This research received financial support from Elm Innovations, The 11th Hour Project of the Schmidt Family Foundation, Straus Family Creamery, Silicon Valley Community Foundation, Organic Valley and Foundation for Food and Agriculture Research. We are grateful to undergraduate interns M. Venegas, A. Aguilar, B. Martinez, S. Calderon, L. Djoneva, T. Burris, A. Wilson, L. Jones, E. Anderson, and K. Roth that participated in the trial. We appreciate Dr. Craig Sanderson for providing the

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