atmosphere

Article Estimation of Greenhouse Gas Emission from Hanwoo (Korean Native ) Manure Management Systems

Seunggun Won 1, Youngbin Yoon 1, Muhammad Mahboob Ali Hamid 1 , Arif Reza 2,3 , Soomin Shim 2, Seungsoo Kim 2, Changsix Ra 2 , Eliza Novianty 2 and Kyu-Hyun Park 2,* 1 Department of Animal Resources, College of Life and Environmental Science, Daegu University, Gyeongsan 38453, ; [email protected] (S.W.); [email protected] (Y.Y.); [email protected] (M.M.A.H.) 2 Department of Animal Industry Convergence, College of Animal Life Sciences, Kangwon National University, Chuncheon 24341, Korea; [email protected] (A.R.); [email protected] (S.S.); [email protected] (S.K.); [email protected] (C.R.); [email protected] (E.N.) 3 Department of Environmental Science, College of Agricultural Sciences, IUBAT—International University of Business Agriculture and Technology, Dhaka 1230, Bangladesh * Correspondence: [email protected]; Tel.: +82-33-250-8621

 Received: 19 June 2020; Accepted: 6 August 2020; Published: 10 August 2020 

Abstract: The agricultural sector is considered one of the major sources of greenhouse gas (GHG) emissions globally. The livestock industry as a significant contributor, is accounting for about 18% of GHG emissions measured in carbon dioxide (CO2) equivalent from agricultural practices. Depending on farming practices and climatic conditions, GHGs such as methane (CH4) and nitrous oxide (N2O) emissions from livestock agriculture can vary significantly. Country-specific emission factors are, therefore, needed for a precise estimation of GHG emissions and to avoid uncertainties. This study was aimed at estimating the CH4 and N2O emission fluxes from Hanwoo (the most famous and popular Korean native cattle) manure management systems. CH4 and N2O emission fluxes from litter in the Hanwoo cattle barn and composting lot were monitored and calculated for 52 weeks using the dynamic chamber method. The calculated monthly average fluxes of CH4 and N2O from litter in the cattle barn ranged from 0.0 to 30.0 13.7 and 0.896 0.557 to 2.925 2.853 µg/m2 s, respectively ± ± ± during the whole measurement period. While during the composting period, the monthly average of CH and N O emission fluxes were varied from 1.449 0.783 to 86.930 19.092 and 0.511 0.410 to 4 2 ± ± ± 2.629 1.105 µg/m2 s, respectively. The calculated emission fluxes of CH and N O from manure ± 4 2 management systems in this study were almost 5.4 and 2.1 times, respectively higher than the values reported for the Asian, South and North American countries in the 2006 Intergovernmental Panel on Climate Change (IPCC) Guidelines for National Greenhouse Gas Inventories. Overall, this study initiates the process along with signifies the importance of developing country-specific GHG inventories for the effective reduction of GHG emissions from the livestock sector in Korea.

Keywords: greenhouse gas; CH4;N2O; Hanwoo cattle; livestock; manure management; Korea

1. Introduction Climate change has been one of the most significant and widely discussed challenges during the last few decades worldwide, with extreme weather patterns, sea level rise, change in ocean currents, and melting icecaps and glaciers [1]. Global climate change caused by greenhouse gas (GHG) emissions has been constantly illustrated with balances of nutrients in the agricultural setting. The livestock industry as a major contributor, is responsible for about 18% of GHG emissions measured in carbon

Atmosphere 2020, 11, 845; doi:10.3390/atmos11080845 www.mdpi.com/journal/atmosphere Atmosphere 2020, 11, 845 2 of 12

dioxide (CO2) equivalent from the agricultural sector [2]. The 2006 Intergovernmental Panel on Climate Change (IPCC) guideline (GL) recognizes both CH4 and N2O gases as significant GHGs in the livestock sector and their impact on global warming [3]. CH4 and N2O have a global warming potential of 28–36 and 265–298 times that of CO2 over 100 years, respectively [4]. According to Food and Agriculture Organization (FAO), the livestock industry emits 37% of anthropogenic CH4 mainly from ruminant enteric fermentation, and 65% of anthropogenic N2O from manure management [1]. Gaseous emissions from livestock agriculture are generally affected by environmental conditions, ventilation rate, dietary composition, animal activities, animal life stage, manure properties (e.g., moisture content and pH), and manure management practices [5,6]. To measure GHG emissions, chamber-based (manual or automated) and micrometeorological (eddy covariance or gradient techniques) methods are generally used [3], while a combination of both approaches can also be adopted [7]. Compared to micrometeorological techniques, chamber-based techniques are widely used due to their simplicity, low operational cost and convenience [8]. However, chamber-based methods typically only cover short time intervals and have the drawback of biasing the environmental conditions known to affect GHG exchange such as temperature and humidity [3]. Over nearly a century, chamber measurements of trace gas fluxes between the surface of the ground and the atmosphere were carried out. Various chamber methods, including static (closed chamber/non-flow-through chamber) and dynamic (open chamber/flow-through chamber), are used to estimate GHG (CO2, CH4,N2O) fluxes with varying degrees of success [9,10]. Between the chamber techniques, the majority of studies used static chambers to measure the GHG emissions [11]. In a static chamber, the concentration of gas within the chamber increases over time because there is very little or no substitution of air in the headspace. Jørgensen et al., therefore, used fans to blend the air in the headspace to reduce bias from gradients of the vertical gas concentration [12]. On the other hand, in a dynamic chamber, continuous flow of outside air is maintained and the difference in concentration between entering and leaving air is measured. The continuous external airflow in the dynamic chambers helps to maintain a steady-state gas concentration gradient at the surface–air interface, hence, the GHG emissions can be measured uninterruptedly [13,14]. In Korea (hereafter referred as Korea), emissions from agricultural activities accounted for 3% of Korea’s total GHG emissions in 2013, showing a marginally higher increase when compared with 2006 (2.5%) [15,16] and as main contributors, CH4 and N2O represented 20% and 13% of the total emission from the agriculture sector [17]. Ji and Park reported that enteric CH4 emissions, CH4 and N2O emissions from livestock manure management in Korea showed annual growth rates of 1.7%, 2.6% and 3.2%, respectively from 1990 to 2009 [18]. The Korean government recently announced a roadmap to decrease the GHG emissions by 2030 [19], which proposed a reduction in overall GHG emissions from the agriculture sector by 5.2%. Currently, Korea is applying Tier 1 methods in IPCC 1996 GL to calculate GHG emissions livestock industries and planning to use 2006 GL by 2023. However, for a precise estimation of GHG emissions and to avoid uncertainties, the IPCC 2006 GL recommends each country to develop country-specific emission factors (EFs). Korea is one of the countries having limited grazing land for ruminants, due to a shortage in arable lands and increased pressure on agricultural production. Moreover, over the past few decades, the dietary pattern of Korean people has changed from rice to animal products including meat, milk and eggs. Additional livestock products are, therefore, needed to fulfil growing demand, which ultimately leads to a rise in GHG emission levels from livestock agriculture. Hanwoo (Bos primigenius), the most dominant Korean native cattle are raised to meet production needs. According to the Hanwoo traceability system, the number of cattle amounted to 3.07 million in 2019, representing more than 86% of the total cattle population in Korea [20]. Hanwoo cattle has been identified as the major contributor of the GHG emissions from the cattle production sector in Korea as well as showed higher enteric GHG emissions than other breeds [21,22]. However, none of the studies have estimated GHG emissions from Hanwoo cattle manure management systems, which acts as the main hindrance to developing national GHG emissions statistics for livestock sector in Korea. Considering the above, this study was, Atmosphere 2020, 11, x FOR PEER REVIEW 3 of 13

Atmosphereemission2020 fluxes, 11, 845from the Hanwoo cattle manure management systems using the dynamic chamber3 of 12 method. Atmosphere 2020, 11, x FOR PEER REVIEW 3 of 13 therefore, aimed at investigating the CH4 and N2O emission fluxes from the Hanwoo cattle manure 2. Experiments managementemission fluxes systems from using the Hanwoo the dynamic cattle chambermanure management method. systems using the dynamic chamber method. 2.2.1. Experiments Research Site and Description 2.This Experiments research was conducted from 2 November 2018 to 1 November 2019 (365 days; 52 weeks; 2.1. Research Site and Description 93 times sampling) at the Kangwon National University Annex Farm (37°56′24.1” N and 127°46′57.0” 2.1. Research Site and Description E) locatedThis research in Chuncheon, was conducted Korea. During from 2 the November study, 46 2018 Hanwoo to 1 November cattle between 2019 the (365 ages days; of 520 and weeks; 108 This research was conducted from 2 November 2018 to 1 November2 2019 (365 days; 52 weeks; 93months times sampling)were reared at thein a Kangwonsteel-made National winch-curtain University barn Annex (1071 Farmm ). Sawdust (37◦56024.1 was00 N used and as 127 bedding◦46057.0 with00 E) 93 times sampling) at the Kangwon National University Annex Farm (37°56′24.1” N and 127°46′57.0” located±10 cm inof Chuncheon,thickness at Korea.the beginning. During the A total study, of 46 24 Hanwoo pens were cattle used between in this the study. ages Each of 0 and pen 108 had months one to E) located in Chuncheon, Korea. During the study, 46 Hanwoo cattle between the ages of 0 and 108 werefour rearedcattle filled in asteel-made in with ad winch-curtainlibitum water barnsupply (1071 except m2). the Sawdust pen located was used in the as beddingbottom left with (Figure10 cm 1, months were reared in a steel-made winch-curtain barn (1071 m2). Sawdust was used as bedding with± ofcross thickness±10 marked), cm of atthickness thewhich beginning. atwas the usedbeginning. A for total storing A oftotal 24 ofthe pens 24 sila pe werensge. were The used used housed in in thisthis cattle study. study. were Each Each fedpen pen withhad hadone roughage, to one to fourpellets,four cattle and cattle filled concentrates filled in within with ad twice ad libitum libitum a day water water (09:00 supplysupply and 17:00). except except the the pen pen located located in the in thebottom bottom left (Figure left (Figure 1, 1, crosscross marked), marked), which which was was used used for for storing storing thethe silage.silage. The The housed housed cattle cattle were were fed fedwith with roughage, roughage, pellets,pellets, and and concentrates concentrates twice twice a daya day (09:00 (09:00 andand 17:00).

Figure 1. Overview of the cattle barn: (a) cattle pen, (b) inlet fan, (c) outlet fan. FigureFigure 1. Overview1. Overview of of the the cattle cattle barn:barn: ( (aa)) cattle cattle pen, pen, (b ()b inlet) inlet fan, fan, (c) outlet (c) outlet fan. fan. 2.2. Chamber Installation, Composting Facility and Data Recording 2.2. Chamber2.2. Chamber Installation, Installation, Composting Composting Facility Facility and DataData Recording Recording 2 TheThe Thesurfacesurface surface areaarea area ofof theofthe the cattlecattle cattle rearingrearing rearing barnbarn waswas 736 736736 m mm2 and2 andand as as asa dynamic aa dynamicdynamic chamber, chamber,chamber, the barn thethe barnwasbarn waswas sealedsealedsealed andand and thethe thefansfans fans werewere were placedplaced placed inin in frontfront front and andand backback of ofof the thethe barn barnbarn for forfor continuous continuouscontinuous airflow. airflow.airflow. Three ThreeThree fans were fansfans werewere fixedfixedfixed atatthe the at center thecenter center above above above the the the main main main entrance entrance entrance (Figure (Figure1). 1). 1). Airflow Airflow Airflow rate rate rate fromfrom from the thefan fan fanwas was wasmeasured measured measured with with with an airan flowairan flow air capture flow capture capture hood hood orhood balometer. or or balometer. balometer. In the present study, the CH4 and N2O emissions from the composting lot was measured using InIn thethe presentpresent study, study, the the CH CH4 4and and N N2O2O emissions emissions from from the the composting composting lot lot was was measured measured using using a a mega-dynamic chamber. The entire composting lot was covered and equipped with fans for air mega-dynamica mega-dynamic chamber. chamber. The The entire entire composting composting lot was lot coveredwas covered and equipped and equipped with fans with for fans air inflowfor air inflow and outflow similar to the cattle barn GHG estimation system. Figure 2 represents the andinflow outflow and similaroutflow to similar the cattle tobarn the GHGcattle estimationbarn GHG system. estimation Figure system.2 represents Figure the 2 schematic represents of thethe schematic of the composting facility. Most farms in Korea operate static pile for composting. Hence, composting facility. Most farms in Korea operate static pile for composting. Hence, the composting schematicthe composting of the composting facility was facility.designed Most to simula farmste compostingin Korea operate as close static as in practice.pile for composting. Hence, facilitythe composting was designed facility to was simulate designed composting to simula aste close composting as in practice. as close as in practice.

Figure 2. Side and front view of the composting facility.

Atmosphere 2020, 11, x FOR PEER REVIEW 4 of 13 Atmosphere 2020, 11, 845 4 of 12 Figure 2. Side and front view of the composting facility.

Temperature data from both the cattlecattle barnbarn andand compostingcomposting facility were collected using temperature logger logger data data (HOBO (HOBO ® Pro® Pro v2 Temperature/Relative v2 Temperature/Relative Humidity Humidity Data Data Logger, Logger, Onset, Onset, MA, MA,USA), USA), placed placed inside inside the thechamber chamber and and from from the the Korean Korean Meteorological Meteorological Data Data Open Open Portal ((www.data.kma.go.krwww.data.kma.go.kr),), respectively.respectively.

2.3. Sampling Procedure The first first and and last last samples samples from from the the dynamic dynamic chamber chamber were were taken taken on 2 onNovember 2 November 2018, and 2018, 1 andNovember 1 November 2019, 2019accordingly., accordingly. The samples The samples were ta wereken twice taken during twice the during week, the usually week, on usually Tuesday on Tuesdayand Friday. and On Friday. the sampling On the sampling day, the gas day, samples the gas we samplesre collected were collectedthree times three with times triplicates with triplicates between between9:00 to 15:00 9:00 (by to 15:00 3 h interval). (by 3 h interval). The first The sample first sample was taken was one taken hour one later hour of later closing of closing the chamber the chamber and andturning turning on the on thefan.fan. The The air airsample sample from from the the inle inlett and and outlet outlet chambers chambers were were taken taken using using a a 25 25 mL syringe (Jung Rim Syringe, Jung Rim Medical IndustrialIndustrial Co. Ltd., Seoul, Korea) through a plastic hose (outer diameterdiameter = 0.6 mm and inner diameter = 0.4 mm) connected to a pumppump (Oil-less(Oil-less DiaphragmDiaphragm Pump 35DNS, G&M Tech Inc., Yongin, Korea).Korea). The collected samples were stored in 8 mL vacuumed glass-vials (LK LAB KOREA 99429, LK Lab Korea, Na Namyangju,myangju, Korea) and sealed with butyl-rubber ® septa (Samwoo Kurex ® 1515 mm, mm, Samwoo Samwoo Kurex, Kurex, Seoul, Korea) Korea).. The The glass glass vials were vacuumed using ® a vacuum machine (VALUE (VALUE ® TF-VE245N,TF-VE245N, Teddington-France, Teddington-France, Villeneuve Villeneuve la la Garenne, Garenne, France) France) for for 5 5min min [23]. [23 ].After After collection, collection, the the glass glass vials vials were were prop properlyerly sealed sealed with with parafilm parafilm and and stored stored for further gas chromatography (GC) analysis (Figure(Figure3 3).).

(a) (b) (c)

Figure 3. Gas sampling procedure: ( (aa)) vacuuming vacuuming the the glass glass vial, vial, ( (b)) taking gas sample using the syringe, (c) transferring gasgas samplesample toto vacuumedvacuumed glassglass vial.vial.

2.4. Flow Rate Measurement To calculatecalculate thethe air air flow flow rate rate through through the the chamber, chambe ther, the wind wind speed speed profile profile of the of fanthe drawingfan drawing air into air ® theinto chamber the chamber was determined was determined using anusing airflow an airflow capture hoodcapture or balometerhood or balometer (Alnor Electronic(Alnor ® Electronic Balancing TM TM ToolBalancing EBT721, Tool TSI EBT721, Incorporated, TSI Incorporat Shoreview,ed, MN,Shoreview, USA and MN, AIRFLOW USA and AIRFLOWInstrumentTM ProHoodInstrument CaptureProHood HoodTM Capture PH721, Hood TSI PH721, Instruments TSI Instruments Ltd., London, Ltd., UK). London, The wind UK). speed The wind was speed recorded was across recorded the 3 surfaceacross the area surface of the area fan givingof the fan a flow giving rate a of flow 0.848 rate m of/s. 0.848 m3/s. 2.5. Gas Chromatography Analysis 2.5. Gas Chromatography Analysis To investigate the sources and emissions of major GHG (N2O, CH4), accurate concentration To investigate the sources and emissions of major GHG (N2O, CH4), accurate concentration analysis was made after sample collection. Gas concentration analysis was performed using a gas analysis was made after sample collection. Gas concentration analysis was performed using a gas chromatograph device to simultaneously analyze N2O and CH4. An electronic capture detector and a chromatograph device to simultaneously analyze N2O and CH4. An electronic capture detector and pulsed discharge detector (PDD) (VICI PDDs, Valco Instrument Co. Inc., Houston, TX, USA) were a pulsed discharge detector (PDD) (VICI PDDs, Valco Instrument Co. Inc., Houston, TX, USA) were equipped in gas chromatography (iGC7200A, DS Science, Gwangju, Korea). For gas analysis, Carboxen equipped in gas chromatography (iGC7200A, DS Science, Gwangju, Korea). For gas analysis, 1000 (80/100 mesh, 1.2 m 1/8 inch) column was used and helium gas with 99.999% purity was Carboxen 1000 (80/100 mesh,× 1.2 m × 1/8 inch) column was used and helium gas with 99.999% purity introduced as a carrier. Temperature set-up of injector, column, and oven were 50, 160, and 50 C, was introduced as a carrier. Temperature set-up of injector, column, and oven were 50, 160, and◦ 50 respectively. The concentrations of N2O and CH4 standard gas used in this study were 1 ppm and 100 °C, respectively. The concentrations of N2O and CH4 standard gas used in this study were 1 ppm and ppm, respectively. Before analysis of the samples, GC calibration was carried out to investigate the 100 ppm, respectively. Before analysis of the samples, GC calibration was carried out to investigate

Atmosphere 2020, 11, 845 5 of 12 precision and reproducibility of the repetition during analysis and each standard gas was analyzed 20 times.

2.6. Calculation of Emission Fluxes The samples (1 mL) were taken from the 8 mL glass-vials using a 1 mL SGE syringe (Trajan Scientific Australia Pty Ltd., Victoria, Australia) to calculate emission fluxes of CH4 and N2O. Each sample was injected three times to obtain N2O and CH4 average concentration. N2O and CH4 fluxes were calculated using the following equations,

Flux = FR ∆C/A (1) × where FR represents the air flow rate through the chamber (m3/s), A is the surface area of emitting materials in the chamber (m2), and ∆C indicates the difference in gas densities in the air inlet and outlet of the chamber (mg/m3).

∆C = (Cout C ) P M/T R (2) − in TGA × × × where (Cout C ) is the difference in concentration measured using gas chromatography (ppm), − in TGA p represents the atmospheric pressure (Pa), M indicates the molecular weight of methane or nitrous oxide (CH4 = 16.04 (g/mol); N2O = 44.01 (g/mol)), T is the average temperature of the analyzed air (K), and R shows the universal gas constant (8.314 J/mol K). To calculate the emission fluxes from litter in the barn, fluxes were measured after removing the litter from the cattle barn and later subtracted from the emission fluxes. In addition, while converting the annual GHG emissions from the Hanwoo cattle manure management systems to CO2 equivalent, global warming potential values for the 100-year time horizon mentioned in the IPCC Fourth Assessment Report were considered [24].

2.7. Statistical Analysis The graphs were prepared using Sigma plot (version 10, 2007) and statistical analysis was conducted using GraphPad Prism (version 8.4.2, 2020). Data obtained from the cattle barn and composting facility were analyzed with one-way analysis of variance (ANOVA). Multiple comparisons were performed using Tukey’s honest significant difference (HSD) post hoc test. A p-value of <0.05 was designated to determine statistical significance.

3. Results and Discussion

3.1. Greenhouse Gas Emissions from Litter in the Hanwoo Cattle Barn

3.1.1. Estimation of Methane Flux

Figure4 shows the variation in average CH 4 flux from the litter on the sampling days. The monthly average of CH flux was varied from 0.0 to 30.0 13.7 µg/m2 s during the whole measurement period 4 ± (November 2018 to October 2019). The CH flux in October (29.997 13.692 µg/m2 s) were higher over the values in the other 4 ± months, while very low flux was recorded in June (Figure4). Generally, the CH 4 flux is influenced by temperature which affects microbial activity; i.e., higher CH4 emission with high temperature [25,26]. Studies on litter reported that temperature ranges from of 35 to 50 ◦C was the best for microbial activity, which can be achieved with a litter height of 20 to 30 cm [27,28]. In this study, the shallow height of the litter (10 cm) and relatively low air temperature (below 35 ◦C) resulted in low CH4 flux during the summer (Figure4). Moreover, low CH 4 flux may also be caused by events such as litter mixing (red boxes) and change of bedding materials (green and blue boxes) since such events facilitate air-supply to the litter mixture. Another possible reason for low CH4 emission during the summer Atmosphere 2020, 11, 845 6 of 12 could be the low moisture content (approximately 12.9%) of the bedding material after replacing the litter and it requires some time to reach the optimal moisture level for CH4 production as moisture content can influence microbial activity [29]. Furthermore, compaction of the litter by cattle hoofs may prevent increasing the temperature of litter and ultimately results in low CH4 emission [30]. CH4 flux from the livestock manure also depends on the amount of manure produced and the part of amount anaerobically decomposes [31]. After replacing the litter (green box in March), CH4 flux was almost close to zero and then the flux was detected again in the middle of July. Furthermore, following litter mixing, the CH4 flux down temporarily for a few days and the emission was abruptly increased around 9.534 11.823 µg/m2 s in August with some fluctuations. Such phenomena might be happened due to ± the microbial degradation of organic materials for the last three months, which affects the CH4 flux through the acidification of organic materials [32,33]. Time-specific CH flux in a day was tended to be higher at 09:00 (7.107 13.526 µg/m2 s) and 4 ± showed comparatively lower fluxes at 12:00 and 15:00 (5.408 10.019 and 5.840 10.801 µg/m2 s, ± ± respectively) (Figure5a). However, daily variation of CH 4 flux did not show significant difference with each other as the time changes (p > 0.05). On the other hand, the average CH4 flux during the fall Atmosphere(18.538 202014.841, 11, xµ FORg/m 2PEERs) found REVIEW to be significantly higher than other seasonal fluxes (p < 0.05), while6 of 13 ± the spring season had the lowest average CH4 flux (Figure5b).

Figure 4. 4. VariationVariation in in average average CH CH44 fluxflux from from litter litter on on the the day day of of sampling sampling during during the the study study (error (error bars bars Atmosphere 2020, 11, x FOR PEER REVIEW 7 of 13 representrepresent the standard deviation of the average).

The CH4 flux in October (29.997 ± 13.692 μg/m2·s) were higher over the values in the other months, while very low flux was recorded in June (Figure 4). Generally, the CH4 flux is influenced by temperature which affects microbial activity; i.e., higher CH4 emission with high temperature [25,26]. Studies on litter reported that temperature ranges from of 35 to 50 °C was the best for microbial activity, which can be achieved with a litter height of 20 to 30 cm [27,28]. In this study, the shallow height of the litter (10 cm) and relatively low air temperature (below 35 °C) resulted in low CH4 flux during the summer (Figure 4). Moreover, low CH4 flux may also be caused by events such as litter mixing (red boxes) and change of bedding materials (green and blue boxes) since such events facilitate air-supply to the litter mixture. Another possible reason for low CH4 emission during the summer could be the low moisture content (approximately 12.9%) of the bedding material after replacing the litter and it requires some time to reach the optimal moisture level for CH4 production as moisture content can influence microbial activity [29]. Furthermore, compaction of the litter by cattle hoofs may prevent increasing the temperature of litter and ultimately results in low CH4 Figure 5. Average CH4 flux from litter by (a) time and (b) season (error bars represent the standard emissiondeviation [30]. ofCH the4 flux average). from Fluxthe livestock means with manure the same also letter depends are not on significantly the amount diff erentof manure (p > 0.05). produced and theFigure part 5. of Average amount CH anaerobically4 flux from litter decomposes by (a) time [ 31].and After(b) season replacing (error thebars litter represent (green the box standard in March), CH4 deviationflux was ofalmost the average). close Fluxto zero means and with then the thesame flux letter was are notdetected significantly again different in the (middlep > 0.05) .of July. Furthermore, following litter mixing, the CH4 flux down temporarily for a few days and the emission 3.1.2.was abruptly Estimation increased of Nitrous around Oxide 9.534 Flux ± 11.823 μg/m2·s in August with some fluctuations. Such phenomena might be happened due to the microbial degradation of organic materials for the last The variation in average N2O flux from litter in the barn on the sampling days are elucidated in three months, which affects the CH4 flux through the acidification of organic materials [32,33]. Figure 6. The monthly average of N2O flux was ranged from 0.896 ± 0.557 to 2.925 ± 2.853 μg/m2·s Time-specific CH4 flux in a day was tended to be higher at 09:00 (7.107 ± 13.526 μg/m2·s) and during the whole measurement period (November 2018 to October 2019). showed comparatively lower fluxes at 12:00 and 15:00 (5.408 ± 10.019 and 5.840 ± 10.801 μg/m2·s, respectively) (Figure 5a). However, daily variation of CH4 flux did not show significant difference with each other as the time changes (p > 0.05). On the other hand, the average CH4 flux during the fall (18.538 ± 14.841 μg/m2·s) found to be significantly higher than other seasonal fluxes (p < 0.05), while the spring season had the lowest average CH4 flux (Figure 5b).

Figure 6. Variation in average N2O flux from litter on the day of sampling during the study (error bars represent the standard deviation of the average).

N2O is well known as one of GHGs having high global warming potential with only a small amount. The highest average N2O flux was estimated in November as 2.925 ± 2.853 μg/m2·s, while the lowest was in January as 0.896 ± 0.557 μg/m2·s, respectively. However, the fluctuation of N2O flux was not very different as compared to CH4. The time-specific N2O flux showed the highest level of 1.263 ± 0.948 μg/m2·s at 12:00 but the fluxes in the morning at 09:00 and in the afternoon at 15:00 were slightly low with 1.249 ± 1.072 and 1.211 ± 1.353 μg/m2·s, respectively (Figure 7a). However, no significant difference in time-specific N2O flux was observed during the study period (p > 0.05).

Atmosphere 2020, 11, x FOR PEER REVIEW 7 of 13

AtmosphereFigure2020 5., Average11, 845 CH4 flux from litter by (a) time and (b) season (error bars represent the standard7 of 12 deviation of the average). Flux means with the same letter are not significantly different (p > 0.05).

3.1.2. Estimation Estimation of of Nitrous Oxide Flux

The variation in average N 2OO flux flux from from litter in the barn on the sampling days are elucidated in 2 Figure6. The monthly average of N O flux was ranged from 0.896 0.557 to 2.925 2.853 µg/m 2 s Figure 6. The monthly average of N2O flux was ranged from 0.896 ±± 0.557 to 2.925 ±± 2.853 μg/m ·s during the whole measurement period (November 2018 to October 2019).

Figure 6. Variation inin averageaverage N N2O2O flux flux from from litter litter on on the the day day of samplingof sampling during during the studythe study (error (error bars barsrepresent represent the standard the standard deviation deviation of the of average). the average).

N2OO is is well known known as as one of GHGs having high global warming potential with only a small µ 2 amount. The The highest highest average average N N2O2O flux flux was was estimated estimated in inNovember November as as2.925 2.925 ± 2.8532.853 μg/mg2/·s,m whiles, while the 2 ± the lowest was in January as 0.896 0.557 µ2g/m s, respectively. However, the fluctuation of N O lowest was in January as 0.896 ± 0.557± μg/m ·s, respectively. However, the fluctuation of N2O flux2 wasflux wasnot very not very different different as compared as compared to CH to CH4. The4. The time-specific time-specific N2O N flux2O flux showed showed the thehighest highest level level of 2 Atmosphere1.263of 1.263 ± 0.948 20200.948 ,μ 11g/m, µx gFOR2/·sm at PEER s12:00 at REVIEW 12:00 but the but fluxes the fluxes in the in morning the morning at 09:00 at 09:00 and in and the in afternoon the afternoon at 15:00 at 8 15:00were of 13 ± 2 were slightly low with 1.249 1.072 and 1.211 1.353 µg/m2 s, respectively (Figure7a). However, no slightly low with 1.249 ± 1.072± and 1.211 ± 1.353± μg/m ·s, respectively (Figure 7a). However, no significantsignificant difference difference in time-specifictime-specific NN22O fluxflux was observed during the study periodperiod ((pp >> 0.05).

Figure 7. Average N 2OO flux flux from from litter litter by by ( (aa)) time time and and ( (b)) season (error bars represent the standard deviation of the average). Flux Flux means means with th thee same letter are not significantly significantly different different (p > 0.05)0.05)..

The seasonal variationvariation ofof N N2O2O flux flux follows follows delineates delineates similar similar trend trend as as that that of CHof CH4 flux4 flux (Figure (Figure7b). 2 The average N O flux (1.870 1.990 µg/m s)2 during the fall season was significantly higher than 7b). The average2 N2O flux (1.870± ± 1.990 μg/m ·s) during the fall season was significantly higher than thethe other other seasonal seasonal fluxes fluxes (p (p << 0.050.05),), which which indicated indicated that that the the litter litter management management practices practices played played an importantan important role role in N in2O N emission2O emission rather rather than thanthe temperature. the temperature. Both aerobic Both aerobic and anaerobic and anaerobic status statusfavor Nfavor2O emission N2O emission from fromlivestock livestock manu manurere with with bedding bedding materials materials [31]. [31 ].When When organic organic nitrogen nitrogen and and ammonia nitrogen in urine is oxidized into hydroxylamine or nitrite under aerobic conditions, part of the N2O gas can be produced [34,35] or further N2O emission occurs when the oxidized form, nitrate, is reduced under anoxic condition by denitrifier [36]. According to the litter status, simultaneous nitrification and denitrification (SND) may occur under aerobic conditions, whereas events such as litter mixing and change of bedding materials shows influence on GHG emission rather than other environmental conditions.

3.2. Greenhouse Gas Emissions from Composting Lot The livestock production and manure management systems in Korea are very different to those of other parts of the world due to regional climate and limited land resources. For example, a pasture- based livestock farm will possibly focus on land spreading for manure management, whereas in barn- based farming system manure cannot be spread in the soil directly, rather the entire manure and bedding is transferred to the composting facility. Composting is done as a manure management strategy to minimize the impact of land spread manure to the environment. The Korean government recommends that prior to land application, cattle manure should stay in the composting lot for over 6 months. Accordingly, the GHG emission from composting lot need to be estimated after measuring from the cattle barn. Composting in general is an aerobic process. Gas emission under anaerobic condition would therefore be easily to be ignored. However, since manure contains 9–30% solids and 70–91% moisture, the inner space of solid fractions may form anaerobic conditions and favor CH4 and N2O production [37]. In addition, during composting if processes such as turning the composting pile and aeration not performed properly, the GHG emissions increase further [38,39]. Most cattle farms in Korea concentrate on livestock productivity without much consideration of the environmental issues related to manure management. Hence, to reflect the actual farm practices, in this study activities like turning the composting pile or aeration was not performed during composting. The measurement was carried out right after collecting the mixture of manure and bedding materials from the cattle barn to exchange the litter. The variation in average CH4 and N2O fluxes on the sampling days are shown in Figure 8.

Atmosphere 2020, 11, 845 8 of 12 ammonia nitrogen in urine is oxidized into hydroxylamine or nitrite under aerobic conditions, part of the N2O gas can be produced [34,35] or further N2O emission occurs when the oxidized form, nitrate, is reduced under anoxic condition by denitrifier [36]. According to the litter status, simultaneous nitrification and denitrification (SND) may occur under aerobic conditions, whereas events such as litter mixing and change of bedding materials shows influence on GHG emission rather than other environmental conditions.

3.2. Greenhouse Gas Emissions from Composting Lot The livestock production and manure management systems in Korea are very different to those of other parts of the world due to regional climate and limited land resources. For example, a pasture-based livestock farm will possibly focus on land spreading for manure management, whereas in barn-based farming system manure cannot be spread in the soil directly, rather the entire manure and bedding is transferred to the composting facility. Composting is done as a manure management strategy to minimize the impact of land spread manure to the environment. The Korean government recommends that prior to land application, cattle manure should stay in the composting lot for over 6 months. Accordingly, the GHG emission from composting lot need to be estimated after measuring from the cattle barn. Composting in general is an aerobic process. Gas emission under anaerobic condition would therefore be easily to be ignored. However, since manure contains 9–30% solids and 70–91% moisture, the inner space of solid fractions may form anaerobic conditions and favor CH4 and N2O production [37]. In addition, during composting if processes such as turning the composting pile and aeration not performed properly, the GHG emissions increase further [38,39]. Most cattle farms in Korea concentrate on livestock productivity without much consideration of the environmental issues related to manure management. Hence, to reflect the actual farm practices, in this study activities like turning the composting pile or aeration was not performed during composting. The measurement was carried out right after collecting the mixture of manure and bedding materials from the cattle barn to exchange the litter. The variation in average CH4 and N2O fluxes on the Atmospheresampling 2020 days, 11,are x FOR shown PEER inREVIEW Figure 8. 9 of 13

FigureFigure 8. Variation inin average average CH CH4 and4 and N2 ON2 fluxesO fluxes from from manure manure composting composting lot on thelot dayon the of sampling day of samplingduring the during study the (error study bars (error represent bars represen the standardt the standard deviation deviation of the average). of the average).

TheThe monthly monthly averages averages of of CH CH44 andand N N22OO fluxes fluxes ranged ranged from from 1.449 1.449 ± 0.7830.783 to to 86.930 86.930 ± 19.09219.092 and and 2 ± ± 0.511 0.410 to 2.629 1.105 µg/m2 s during the composting period. A different trend in CH emission 0.511 ±± 0.410 to 2.629 ±± 1.105 μg/m ·s during the composting period. A different trend in CH44 emission waswas observed whenwhen compared compared to theto emissionthe emission from litterfrom inlitter the cattlein the barn cattle with barn respect with to temperaturerespect to temperature(Figure9a). During (Figure the 9a). spring During season, the CHspring4 emission season, was CH abruptly4 emission increased was abruptly till May increased along with till gradual May alongincrement with ofgradual temperature, increment of which of temperature, emission was of causedwhich emission by microbial was activity caused and by showedmicrobial significant activity anddiff erenceshowed with significant other monthly difference average with other fluxes monthly (p < 0.05). average For N fluxes2O, significantly (p < 0.05). For higher N2O, emissionsignificantly was higher emission was also observed in May compared to the other months (p < 0.05) (Figure 9b). Gilroyed et al. explained the detail biological mechanisms of GHG production during the composting process [40]. They showed a typical GHG emission pattern over time with respect to microbial activity, temperature profile, and oxygen (O2) concentration. High CH4 emission was observed at the beginning of composting under thermophilic temperature, while N2O emission profile showed the opposite trend with CH4. This finding is in line with the results reported by Hao et al. [41]. Rapid consumption of O2 during composting due to microbial degradation of organic compounds results in a thermophilic condition, which produces CH4 via methanogenesis [42]. N2O can be emitted from the composting pile through both nitrification and denitrification processes [43,44]. In this study, the actual composting process performed in the Korean farms were considered, therefore, the majority of the N2O was emitted during composting through nitrification. As the time passes, the temperature of the composting pile reaches to mesophilic levels, and ultimately enables the growth of nitrifying bacteria which are responsible for N2O emission.

Figure 9. Monthly average emissions of (a) CH4 and (b) N2O from composting lot. Flux means with the same letter are not significantly different (p > 0.05).

Atmosphere 2020, 11, x FOR PEER REVIEW 9 of 13

Figure 8. Variation in average CH4 and N2O fluxes from manure composting lot on the day of sampling during the study (error bars represent the standard deviation of the average).

The monthly averages of CH4 and N2O fluxes ranged from 1.449 ± 0.783 to 86.930 ± 19.092 and 0.511 ± 0.410 to 2.629 ± 1.105 μg/m2·s during the composting period. A different trend in CH4 emission was observed when compared to the emission from litter in the cattle barn with respect to temperature (Figure 9a). During the spring season, CH4 emission was abruptly increased till May alongAtmosphere with2020 gradual, 11, 845 increment of temperature, of which emission was caused by microbial activity9 of 12 and showed significant difference with other monthly average fluxes (p < 0.05). For N2O, significantly higher emission was also observed in May compared to the other months (p < 0.05) (Figure 9b). Gilroyedalso observed et al. inexplained May compared the detail to thebiological other months mechanisms (p < 0.05) of GHG (Figure production9b). Gilroyed during et al. the explained composting the processdetail biological [40]. They mechanisms showed a oftypi GHGcal productionGHG emission during pattern the composting over time processwith respect [40]. Theyto microbial showed activity,a typical temperature GHG emission profile, pattern and oxygen over time (O2) with concentration. respect to High microbial CH4 emission activity, temperaturewas observed profile, at the beginningand oxygen of (Ocomposting2) concentration. under thermophilic High CH4 emission temperature, was observed while N2 atO theemission beginning profile of compostingshowed the oppositeunder thermophilic trend with temperature,CH4. This finding while is N in2O line emission with the profile results showed reported the oppositeby Hao et trend al. [41]. with Rapid CH4 . consumptionThis finding isof in O line2 during with composting the results reported due to microbial by Hao et degradation al. [41]. Rapid of organic consumption compounds of O2 duringresults incomposting a thermophilic due to condition, microbial which degradation produces of organicCH4 via compoundsmethanogenesis results [42]. in N a thermophilic2O can be emitted condition, from thewhich composting produces pile CH 4throughvia methanogenesis both nitrification [42]. and N2O de cannitrification be emitted processes from the [43,44]. composting In this pile study, through the actualboth nitrification composting and process denitrification performed processes in the Korean [43,44 farms]. In this were study, considered, the actual therefore, composting the majority process ofperformed the N2O was in the emitted Korean during farms werecomposting considered, through therefore, nitrification. the majority As the of time the Npasses,2O was the emitted temperature during ofcomposting the composting through pile nitrification. reaches to mesophilic As the time levels, passes, and the ultimately temperature enables of the the composting growth of pile nitrifying reaches bacteriato mesophilic which levels, are responsible and ultimately for N enables2O emission. the growth of nitrifying bacteria which are responsible for N2O emission.

Figure 9. Monthly average emissions of ( a) CH4 and ( b))N N2OO from from composting lot. Flux Flux means with thethe same same letter letter are are not significantly significantly different different (p > 0.05). 3.3. Greenhouse Gas Emissions from Manure Management Systems

By contrast with other countries, cattle in Korea are mostly raised in the barn due to lack of pasture. 2 The annual emissions of CH4 and N2O fluxes from litter in the barn were 6.192 and 1.242 µg/m 2 s, respectively, from 46 animals in 736 m of cattle barn (3.124 and 0.627 kg CH4 and N2O/animal year, respectively). Furthermore, CH4 and N2O fluxes from litter based on unit animal were 78.1 and 184.2 kg CO2eq/animal year, respectively when converted to CO2 equivalent. On the other hand, the average CH and N O fluxes from the composting lot were 28.037 39.848 and 1.514 1.051 µg/m2 4 2 ± ± s, respectively (2.235 and 0.098 kg CH4 and N2O/animal year, respectively). After converting to CO2 equivalent, CH4 and N2O fluxes from composting lot based on unit animal were calculated as 55.9 and 28.9 kg CO2eq/animal year, respectively. Therefore, in total a GHG of 347.1 kg CO2eq/animal year was emitted from the Hanwoo cattle manure management systems.

3.4. Comparison of Greenhouse Gas Emissions with Intergovernmental Panel on Climate Change (IPCC) Guidelines According to 2006 IPCC GL for National Greenhouse Gas Inventories [23], the Tier 1 values of manure management CH4 emission factor for in Asia, North America, Western Europe, and South America are 1, 1, 8, and 1 kg CH4/animal year, respectively. While for N2O, the value is 0.342 kg N2O/animal year, with consideration of the manure treatment facilities including liquid treatment (2.5%), solid storage (90.7%), and miscellaneous (6.8%). In this study, annual emissions of CH4 and N2O emission from the Hanwoo cattle manure management systems were almost 5.4 and 2.1 times, respectively higher than the values provided by IPCC. Jo et al. reported that such variation might be attributed to the differences in feeding systems and cattle breeds as the values mentioned Atmosphere 2020, 11, 845 10 of 12 by IPCC values were estimated based on the studies conducted mainly in western countries [21]. Country-specific emission factors are, therefore, needed rather than using the values of the 2006 IPCC GL to develop effective and efficient GHG emission reduction strategies for the livestock industries.

4. Conclusions This study was conducted to evaluate the GHG emission flux from Hanwoo cattle manure management systems using the dynamic chamber method. CH4 and N2O emission fluxes from litter in the cattle barn and composting lot were monitored and estimated. The monthly average CH4 and N2O emission fluxes from litter in the barn during the experimental period varied from 0.0 to 30.0 13.7 µg/m2 s and 0.896 0.557 to 2.925 2.853 µg/m2 s, respectively. The annual emissions of ± ± ± 2 CH4 and N2O fluxes from litter were estimated as 6.192 and 1.242 µg/m s, respectively (3.124 and 0.627 kg CH4 and N2O/animal year, respectively). The monthly averages of CH4 and N2O fluxes ranged from 1.449 0.783 to 86.930 19.092 and 0.511 0.410 to 2.629 1.105 µg/m2 s during the ± ± ± ± composting period and the calculated annual CH4 and N2O emissions from the composting lot were 2.235 and 0.098 kg CH4 and N2O/animal year, respectively. A comparison with the values for different continents in the world mentioned in 2006 IPCC GL for National Greenhouse Gas Inventories revealed that CH4 and N2O emissions from the Hanwoo cattle manure management systems were much higher than those reported. Hence, the results of this study highlight the significance and need to have country-specific emission factors as well as to encourage further studies to develop efficient and effective GHG reduction strategies for the livestock sector in Korea.

Author Contributions: Conceptualization, S.W., C.R. and K.-H.P; methodology, S.W. and K.-H.P; formal analysis, Y.Y., S.S., S.K. and E.N.; investigation, Y.Y., S.S., S.K. and E.N.; resources, K.-H.P.; data curation, S.W., Y.Y., A.R. and E.N.; writing—original draft preparation, M.M.A.H. and A.R.; writing—review and editing, A.R., S.W., C.R. and K.-H.P.; supervision, S.W. and K.-H.P.; project administration, K.-H.P.; funding acquisition, K.-H.P. All authors have read and agreed to the published version of the manuscript. Funding: This research was funded by Rural Development Administration of Korea, grant number PJ01359002. Conflicts of Interest: The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

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