Ammonia emissions from different pig production scales and their temporal variations in the North China Plain

ABSTRACT

Pig production systems in China are shifting from small to industrial scale. Significant variation in housing ammonia (NH₃) emissions can exist due to differences in diet, housing design, and management practices. However, there is a knowledge gap regarding the impacts of farm-scale in China, which may be critical in identifying hotspots and mitigation targets. Here, continuous in-situ NH₃ concentration measurements were made at pig farms of different scales for sows and fattening pigs over periods of 3–6 days during two different seasons (summer vs. winter). For the sow farms, NH₃ emission rates were greater at the small farm (summer: 0.52 g pig⁻¹ hr⁻¹; winter: 0.21 g pig⁻¹ hr⁻¹) than at the large farm (summer: 0.34 g pig⁻¹ hr⁻¹; winter: 0.12 g pig⁻¹ hr⁻¹). For the fattening pig farms, NH₃ emission rates were greater at the large farm (summer: 0.22 g pig⁻¹ hr⁻¹; winter: 0.16 g pig⁻¹ hr⁻¹) than at the small farm (summer: 0.19 g pig⁻¹ hr⁻¹; winter: 0.07 g pig⁻¹ hr⁻¹). Regardless of farm scale, the NH₃ emission rates measured in summer were greater than those in winter; the NH₃ emission rates were greater in the daytime than at the nighttime; a positive relationship (R² = 0.06–0.68) was established between temperature and NH₃ emission rate, whereas a negative relationship (R² = 0.10–0.47) was found between relative humidity and NH₃ emission rate. The effect of farm-scale on indoor NH₃ concentration could mostly be explained by the differences in ventilation rates between farms. The diurnal variation in NH₃ concentration could be partly explained by ventilation rate (R² = 0.48–0.78) in the small traditional farms and by emission rate (R² = 0.26–0.85) in the large industrial farms, except for the large fattening pig farm in summer. Overall, mitigation of NH₃ emissions from sow farms should be a top priority in the North China Plain.

Implications: The present study firstly examined the farm-scale effect of ammonia emissions in the North China Plain. Of all farms, the sow farm was identified as the greatest source of ammonia emission. Regardless of farm scale, ammonia emission rates were observed to be higher in summer. Ammonia concentrations were mostly higher in the large industrial farms partly due to lower ventilation rates than in the small traditional farms.

Introduction

China has experienced severe and persistent particulate pollution in recent years (Huang et al. 2014). A recent study indicated that severe haze in Northern China causes a loss in life expectancy of up to five years on average (Chen et al. 2013). Atmospheric ammonia (NH₃) contributes to aerosol formation through the secondary creation of fine particulate matter (PM2.5) after combining with other atmospheric pollutants, including nitrates and sulfates (Wu et al. 2016). Reducing NH₃ emissions is, therefore, an effective approach to decrease PM2.5 concentrations.

China is the largest source of NH₃ emissions (from 8.2 to 15.6 Tg N yr⁻¹) in the world (Kang et al. 2016; Zhang et al. 2017), with the North China Plain being the largest hotspot (Pan et al. 2018). Agricultural sources, with livestock housing and manure management in particular, are the most significant contributors to NH₃ emissions (Bai et al. 2017, 2016), with pig housing being an important component (Paulot et al. 2014). To accurately identify emission hotspots and devise effective NH₃ mitigation techniques applicable to pig housing, an accurate estimate of NH₃ emission rates is needed. However, current NH₃ emission factors proposed for pig housing in China are mainly based on European and American research. These emission factors may not accurately reflect emissions from China because substantial variation can exist between countries (Koerkamp et al. 1998) arising from differences in diet, housing, pig breed, and management practices (Lin et al. 2017; Paulot et al. 2014). Therefore, accurate NH₃ emission rates, reflecting local pig production systems and the environmental conditions in China must be obtained.

The structure of pig production is changing in China. Although the small traditional pig farms still represent a significant share of total pig production, the large industrial pig farms are accounting for a rapidly growing proportion (Bai et al. 2014). Pig farms of different scales differ in their diet, housing system design, indoor climate, and management, all of which will influence NH₃ emissions (Koerkamp et al. 1998). Published information suggests that: i) lowering dietary crude protein content decreases the excretion of urinary N, which is easily converted into NH₃ by the urease present in feces (Canh et al. 1998); ii) urine drains quickly from slatted floors via the openings, limiting the fouled area (Svennerstedt 1999) and thereby lowering NH₃ emissions (Hou, Velthof, and Oenema 2015); iii) greater emissions from mechanical-ventilated housing in comparison with natural-ventilated housing, can be partly explained by the higher temperature inside the former (Gallmann, Hartung, and Jungbluth 2003); iv) NH₃ emissions are positively related to temperature but negatively to relative humidity (Philippe, Cabaraux, and Nicks 2011). Therefore, NH₃ emissions are highly likely to vary depending on the farm scale. While several studies concerning NH₃ emissions and concentrations from pig housing have been reported for China (Dong et al. 2009; Wang et al. 2011; Xu et al. 2014; Zhu et al. 2006a, 2006b), to date these have not addressed potential impacts of farm scale and the underlying factors.

The primary objective of this study was to characterize the variability in NH₃ emissions with respect to sow and fattening pig farms of different scales and their temporal variations in the North China Plain. Potential reasons behind the effects of farm scale were also investigated, including feed intake and nitrogen content, ventilation, floor design, manure removal system, and microclimatic conditions. These data will contribute to the baseline information on farm-scale NH₃ emissions from pig farms in China, and such information is important for identifying emission hotspots and exploring effective mitigation techniques.

Materials and methods

Description of the experimental sites

Four pig farms, representative of the different-scale pig production facilities in the North China Plain, were selected for NH₃ emission measurements over two seasons (summer: August to September; winter: January to March). Two farms were large industrial pig farms (a total holding capacity of ~6000 sows and ~2,000 fattening pigs, respectively, from Cangzhou City, Hebei Province), and two were small traditional pig farms (a total holding capacity of ~30 sows and ~50 fattening pigs, respectively, from Shijiazhuang City, Hebei Province) (Figure 1). Basic information regarding pigs, feed, housing design, and manure removal system for each farm are given in Table 1 and Appendix A.

Table 1. Description of the pigs, feed, and housing system related to four pig farms; mean ± standard deviation

Farm	LS		SS		LF		SF
Season	Summer	Winter	Summer	Winter	Summer	Winter	Summer	Winter
Days of pregnancy (day)	75 ~ 112	40 ~ 80	80 ~ 107	75 ~ 103
Number (head house^−1)	460	500	12	7	969	980	25	28
Weight (kg)	210	220	250	250	60	45	77	75
Feed intake (kg day^−1 head^−1)	2.8	2.2	2.0	2.0	2.3	2.0	2.1	2.0
Feed Nitrogen content (%)	2.4 ± 0.2		2.7 ± 0.0		3.1 ± 0.0		2.3 ± 0.0
Ventilation	Mechanical		Natural		Mechanical		Natural
Floor	Partly slatted		Solid concrete		Partly slatted		Solid concrete
Manure removal	Flushing		Manual removal		Scraping		Manual removal

Figure 1. The location of the selected four pig farms in the North China plain

The large-scale sow farm (LS) had a total of 18 mechanically ventilated houses, grouped in three rows of six, with ~10 m separation distance between houses within each row. The house selected for measurement had dimensions 61 × 20 × 2.5 m (L × W × H) with an east-west orientation (Appendix A Figure A1). Each house had a total holding capacity of 504 sows, with 6 rows of pens and 84 pens (L × W × H: 2.2 × 0.7 × 1.1 m) in each row. Pens had partly slatted floors.

In summer, fresh air entered the house through water pads (for cooling) and exited through east-wall fans. In winter, fresh air entered the house through a heating system via the ridge vents and exited through sidewall fans. Fans could operate separately or together to achieve the target indoor temperature, which ranged from ~20°C in winter to ~23°C in summer. The sows were fed twice per day (summer: 8:00 and 17:00; winter: 7:00 and 14:00) before manure removal. Manure was collected in a gutter beneath the slatted floor and flushed daily.

The small-scale sow farm (SS) had a total of 6 naturally-ventilated houses in one row, with ~3 m separation distance between houses. The selected house had dimensions 18 × 7 × 3 m (L × W × H) with an east-west orientation (Appendix A Figure A2). The house had 10 ventilation windows (0.5 × 0.5 m) along the sidewalls, which were only opened in summer, and one door (W × H: 1.5 × 2 m). The house had a total holding capacity of 17 sows with 17 solid concrete floor pens (L × W × H: 3 × 2 × 1 m). The sows were fed three times per day (7:00, 11:30, and 17:00), and manure was removed manually by scraper daily at 10:00.

The large-scale fattening pig farm (LF) had a total of 2 mechanically ventilated houses with a ~10 m separation distance. The selected house had dimensions 74 × 16 × 2.5 m (L × W × H) with a north-south orientation (Appendix A Figure A3). The house had a total holding capacity of ~1,000 fattening pigs, with 2 rows of pens, each row comprising 13 partly-slatted-floor pens (L × W × H: 7 × 4 × 1.1).

In summer, fresh air entered the house through water pads and exited through south-wall fans. In winter, fresh air entered the house through a heating system via the ridge vents and exited the house through south-wall fans. Ventilation fans operated separately or together to achieve the target house temperature, which ranged from 22°C in winter to 23°C in summer. The fattening pigs were fed twice daily in summer (6:00–8:00 and 16:00–18:00) and once per day in winter (9:00–11:00). Manure was collected beneath the slatted floor and scraped daily at 17:00.

The small-scale fattening pig farm (SF) had a total of 2 naturally-ventilated houses with a ~5 m separation distance. The selected house had dimensions 25 × 11 × 3 m (L × W × H) with an east-west orientation (Appendix A Figure A4). The house had 12 ventilation windows (1 × 1 m) and one door (W × H: 1.2 × 2 m) and comprised of 6 solid-concrete-floor pens (L × W × H: 10 × 2 × 1 m). The fattening pigs were fed three times per day (7:00, 14:00, and 17:30), and manure was removed manually by scraper once per day (16:00).

Measurement

Ammonia and carbon dioxide (CO₂) concentrations were measured for 3–6 consecutive days at each farm during each season. Specific measurement dates were as follows: LS 2017/8/17–8/21 (summer) and 2017/1/5–1/11 (winter); SS 2017/9/26–9/30 (summer) and 2018/3/17–3/20 (winter); LF 2017/8/26-8/30 (summer) and 2018/1/18–1/22 (winter); SF 2017/9/21–9/25 (summer) and 2018/3/13–3/16 (winter). In the mechanically ventilated houses (LS and LF), the air was sampled at ventilation inlet and outlet points. An INNOVA 1409 Multipoint Sampler (LumaSense Technologies A/S, Ballerup, Demark) together with an INNOVA infrared 1412i Photoacoustic Field Multi-Gas Monitor (LumaSense Technologies A/S, Ballerup, Demark) were used to determine gas concentrations. For the naturally ventilated houses, the air was sampled inside and > 10 m outside of each house, also using the INNOVA Photoacoustic monitor with 12-point sampler. The INNOVA was calibrated prior to each measurement event using the appropriate standard calibration gases (ammonia and carbon dioxide) procured from the National Standard Material Center (Beijing, China). The air sampling period for each measurement point was 40 s, followed by 20 s flushing time before a new measurement commenced. Between 4 and 8 1-min measurements were made continuously for each sampling location in the large farms and 2–4 in the small farms, but only stable values were used for NH₃ and CO₂ concentrations for each sampling location. The temperature and relative humidity of outdoor and indoor air were continuously monitored at 1 min intervals using a combined sensor (ZDR-20, Hangzhou Zeda Instruments CO., Ltd, Hangzhou, China) at a height of 2.0 m. Feed was sampled at each farm and analyzed for total Kjeldahl nitrogen (TKN) (Lu 2000).

Flux calculation

The concentrations were measured as ppm (by volume) and converted to mg m⁻³ for emission calculations. The ventilation rate (VR, m³ hr⁻¹) was estimated using the CO₂ balance method (de Sousa and Pedersen 2004) according to Equation (1)(1) $\mathrm{V}R=\frac{\mathrm{C}\times \mathrm{A}\times \mathrm{\Phi }\times \mathrm{N}}{{\mathrm{C}\mathrm{O}}_2^L-{\mathrm{C}\mathrm{O}}_2^{\mathrm{E}}}\hspace{0.17em}$(1) :

(1) $\mathrm{V}R=\frac{\mathrm{C}\times \mathrm{A}\times \mathrm{\Phi }\times \mathrm{N}}{{\mathrm{C}\mathrm{O}}_2^L-{\mathrm{C}\mathrm{O}}_2^{\mathrm{E}}}\hspace{0.17em}$(1)

where:

• C: CO₂ production (0.185 m³ hr⁻¹ hpu⁻¹);

• A: Relative animal activity;

• Φ: Heat production of a pig at temperature t (hpu pig⁻¹);

• N: The number of pigs inside the house during the specific hour (head);

• ${\mathrm{C}\mathrm{O}}_2^L$: Average hourly CO₂ concentration for outlet or inside sampling points, mg m⁻³;

• ${\mathrm{C}\mathrm{O}}_2^{\mathrm{E}}$: Average hourly CO₂ concentration for inlet or outside sampling points, mg m⁻³.

Adjustment for diurnal variation in the relative animal activity (A) was carried out according to Equation (2)(2) $\mathrm{A}=1-\mathrm{a}\times sin\left[\left(2\times \frac{\pi }{24}\right)\times \left(\mathrm{h}+6-{\mathrm{h}}_{min}\right)\right]$(2) (Pedersen and Sällvik 2002):

(2) $\mathrm{A}=1-\mathrm{a}\times sin\left[\left(2\times \frac{\pi }{24}\right)\times \left(\mathrm{h}+6-{\mathrm{h}}_{min}\right)\right]$(2)

where:

• a: Constant (expressing the amplitude with respect to the constant 1);

• h: Time of the animal activity;

• h_min: Time of day with minimum activity (hours after midnight).

For fattening pigs and sows, the heat production (Φ) was calculated according to Pedersen and Sällvik (2002), based on the bodyweight of the pigs and the feed intake (Equations 3(3) ${\mathrm{\Phi }}_{\mathrm{f}\mathrm{a}\mathrm{t}\mathrm{t}\mathrm{e}\mathrm{n}\mathrm{i}\mathrm{n}\mathrm{g}\mathrm{p}\mathrm{i}\mathrm{g}}=\frac{5.09{\mathrm{m}}^{0.75}+\left[1-\left(0.47+0.003m\right)\right]\left[n\times 5.09m^{0.75}-5.09m^{0.75}\right]\hspace{0.17em}}{1000}\times \frac{1000+4\times \left(20-t\right)}{1000}$(3) ~5):

(3) ${\mathrm{\Phi }}_{\mathrm{f}\mathrm{a}\mathrm{t}\mathrm{t}\mathrm{e}\mathrm{n}\mathrm{i}\mathrm{n}\mathrm{g}\mathrm{p}\mathrm{i}\mathrm{g}}=\frac{5.09{\mathrm{m}}^{0.75}+\left[1-\left(0.47+0.003m\right)\right]\left[n\times 5.09m^{0.75}-5.09m^{0.75}\right]\hspace{0.17em}}{1000}\times \frac{1000+4\times \left(20-t\right)}{1000}$(3)

(4) $\hspace{0.17em}{\mathrm{\Phi }}_{\mathrm{p}\mathrm{r}\mathrm{e}\mathrm{g}\mathrm{n}\mathrm{a}\mathrm{n}\mathrm{t}\mathrm{s}\mathrm{o}\mathrm{w}}=\frac{4.85m^{0.75}+8\times {10}^{-5}{p}^3+76Y_1}{1000}\times \frac{1000+4\times \left(20-t\right)}{1000}$(4)

(5) ${\mathrm{\Phi }}_{nursing\hspace{0.17em}sow}=\frac{4.85m^{0.75}+28Y_2\hspace{0.17em}}{1000}\times \frac{1000+4\times \left(20-t\right)}{1000}$(5)

where:

• m: Body mass of the pig, kg;

• n: Daily feed energy intake in relation to maintenance, the default values vary according to body mass of the pig: 40 kg, 3.46; 50 kg, 3.52; 60 kg, 3.59; 70 kg, 3.20; 80 kg, 2.90;

• p: Days of pregnancy;

• Y₁: Daily gain, pregnant sow (assumed as 0.18 kg d⁻¹);

• Y₂: Milk production (assumed as 6 kg/d⁻¹).

The emission per pig unit (E, g pig⁻¹ hr⁻¹) was reported as in the following equation:

(6) $\mathrm{E}=\frac{\mathrm{V}\mathrm{R}\times \left({\mathrm{N}\mathrm{H}}_3^L-{\mathrm{N}\mathrm{H}}_3^{\mathrm{E}}\right)}{\mathrm{N}}$(6)

where:

${\mathrm{N}\mathrm{H}}_3^L$: Average hourly NH₃ concentration for the outlet or inside sampling points, mg m⁻³;

${\mathrm{N}\mathrm{H}}_3^{\mathrm{E}}$: Average hourly NH₃ concentration for the inlet or outside sampling points, mg m⁻³.

The pig live weight and productivity may differ from herd to herd. To make results comparable, the emission per livestock unit (E$\prime$, g LU⁻¹ hr⁻¹) where one LU is equivalent to 500 kg animal mass, was reported as follows:

(7) ${\mathrm{E}}^{\prime }=\mathrm{E}\times \frac{500}{\mathrm{m}}$(7)

Statistical analysis

The measured concentrations of NH₃ and CO₂ at each sampling point were averaged as mean hourly values and used with mean hourly ventilation estimates to calculate the emission rate. Daily means were used for statistical evaluation. The correlations between NH₃ concentrations or NH₃ emission rates and other parameters were investigated using Pearson’s analysis with the SPSS 20.0 IBM statistical analysis package.

Results and discussion

Microclimatic conditions

The recommended indoor temperature range for intensive pig farms in China is from 18 to 22°C for lactating sows and from 15 to 23°C for fattening pigs. The mean indoor temperature during the measurement periods ranged from 21.8 in winter to 25.1°C in summer (LS) and 22.7 in winter to 24.3°C in summer (LF) (Table 2). These results indicate that the seasonal indoor temperature patterns in the large industrial pig farms remained relatively steady as would be expected, given the temperature control features of these farms; the cooling effect of water pad-fan system in summer and the warming effect of the heating system in winter limited the fluctuation of indoor temperature. Additionally, the indoor temperature in the large industrial pig farms had a lower fluctuation (Figure 2a and b) compared with outdoor temperature. However, in the small traditional pig farms, the houses were designed with insufficient insulation and without supplemental heating or cooling. As expected, the indoor temperature followed the outside, being higher in summer (Table 2) and in the daytime (Figure 2a and b).

Table 2. Description of the indoor microclimatic conditions, NH₃ concentrations, and emission rates related to four pig farms: large-scale sow (LS), small-scale sow (SS), large-scale finishing pig (LF), and small-scale finishing pig (SF); mean ± standard deviation

Farm	LS		SS		LF		SF
Season	Summer	Winter	Summer	Winter	Summer	Winter	Summer	Winter
Indoor temperature (°C)	25.1 ± 0.14	21.8 ± 0.14	22.4 ± 0.54	13.0 ± 0.88	24.3 ± 0.08	22.7 ± 0.58	25.4 ± 0.43	12.6 ± 1.91
Indoor relative humidity (%)	94.5 ± 0.96	56.2 ± 0.89	61.5 ± 4.59	80.6 ± 5.13	82.3 ± 1.98	50.2 ± 2.66	67.6 ± 3.23	66.4 ± 3.21
Ventilation rate (m^3 pig^−1 hr^−1)	623 ± 38.1	17.5 ± 0.64	203 ± 14.0	47.2 ± 7.91	51.3 ± 6.72	15.3 ± 0.28	76.9 ± 9.69	96.6 ± 45.4
NH3 concentration (mg m^−3)	0.54 ± 0.07	7.25 ± 0.21	4.65 ± 0.26	4.89 ± 0.31	5.16 ± 0.20	10.2 ± 0.44	3.49 ± 0.72	1.08 ± 0.36
NH3 emission rate (g LU^−1hr^−1)	0.82 ± 0.13	0.31 ± 0.01	1.04 ± 0.04	0.42 ± 0.05	1.81 ± 0.08	1.74 ± 0.09	1.26 ± 0.14	0.46 ± 0.05
NH3 emission rate (g pig^−1hr^−1)	0.34 ± 0.05	0.12 ± 0.00	0.52 ± 0.02	0.21 ± 0.03	0.22 ± 0.01	0.16 ± 0.01	0.19 ± 0.02	0.07 ± 0.01

Figure 2. The seasonal and diurnal variation of temperature, relative humidity, and ventilation rate in different pig farms: a), c), and e): sow farms; b), d), and f): fattening pig farm

Irrespective of growth stage, the relative humidity was higher in summer than in winter in the large industrial pig farms (Table 2), because of the effect of the water pads. In the large industrial pig farms, there was little diurnal variation in relative humidity, especially in summer, suggesting that the outdoor relative humidity had no impact on that indoors. In summer, the relative humidity in the large industrial pig farms was higher than that in the small traditional farms because of the influence of the water pads on the incoming air. In the small traditional pig farms, the indoor relative humidity showed less seasonal variation (although was higher in winter in SS (Table 2), and was higher at nighttime (Figure 2c and d). This was as expected because the houses were ventilated by opening windows and/or doors, and hence the indoor relative humidity was subject to the impact of outdoor conditions. For the small farms, relative humidity (Figure 2c and d) was inversely related to the temperature (Figure 2a and b).

Pedersen et al. (1998) describe three methods for the estimation of the ventilation rate for insulated houses based on heat, moisture, and CO₂ balances, whereas for uninsulated housing only the CO₂ balance method is recommended. Hence, in this study, the ventilation rate for each farm was estimated using the CO₂ balance. In the large industrial pig farms, the fan operating system was temperature-dependent, and at higher temperatures, the ventilation requirement was higher. Therefore, ventilation rates were higher in the summer (Table 2) and higher during the daytime than the nighttime (Figure 2e and f). In the small traditional pig farms, the ventilation rates were higher during the daytime than nighttime. The ventilation rates obtained in the present study were comparable with those from Zhu et al. (2006a), who were making measurements from a natural-ventilated house from the same region as this study. The ventilation rates were mostly higher in the small fattening pig farm than those in the large fattening pig farm. The ventilation system may determine the difference between the farm scales. In many cases, ventilation rates are higher for naturally ventilated compared with mechanically ventilated housing (Kim et al. 2008) because of the smaller size and many openings.

Influence of farm scale on NH₃ emission

The ammonia emitted from pig housing derives from organic N in pig excreta. After deposition on the floor, the urea from urine is rapidly hydrolyzed to NH₃/NH₄⁺ (l) in solution by the fecal urease (Philippe et al. 2011). This will subsequently be emitted into the atmosphere as gaseous NH₃ (g) at a rate that depends on the concentration at the emitting surface and factors affecting the equilibrium between NH₃/NH₄⁺ in solution and between dissolved and gaseous NH₃ (Ivanova-Peneva, Aarnink, and Verstegen 2008):

(8) $\mathrm{C}\mathrm{O}(\mathrm{N}{\mathrm{H}}_2{)}_2+3{\mathrm{H}}_2\mathrm{O}\to 2{\mathrm{N}\mathrm{H}}_4^{+}\left(\mathrm{l}\right)+{\mathrm{H}\mathrm{C}\mathrm{O}}_3^{-}+\mathrm{O}{\mathrm{H}}^{-\hspace{0.17em}}$(8)

(9) ${\mathrm{N}\mathrm{H}}_4^{+}\left(\mathrm{l}\right)\leftrightarrow \mathrm{N}{\mathrm{H}}_3\left(\mathrm{l}\right)+{\mathrm{H}}^{+\hspace{0.17em}}$(9)

(10) $\mathrm{N}{\mathrm{H}}_3\left(\mathrm{l}\right)\leftrightarrow \mathrm{N}{\mathrm{H}}_3\left(\mathrm{g}\right)$(10)

Normalizing the NH₃ emission rate by dividing the total emission rate by the total live weight of pigs and then multiplying by 500 kg (1 livestock unit, LU) removes the total live weight as a variable and provides an effective means to compare emission rates between studies. Normalized NH₃ emission rates from different growing stages and farm scales are presented in Table 2. For LS, mean normalized NH₃ emission rates for summer and winter were slightly lower compared with values reported for Northern Europe, ranging from 0.50 to 1.28 g LU⁻¹ hr⁻¹ (Koerkamp et al. 1998; Philippe, Cabaraux, and Nicks 2011), possibly because of the daily manure removal for this house, rather than manure remaining in the below-slat slurry pit for a longer period as in the literature studies. As shown by Guarino et al. (2003), frequent manure removal can reduce NH₃ emission by 35% in comparison with the deep-pit system. Zhu et al. (2006a) observed seasonal variation in normalized NH₃ emission rates (summer: 0.46 ~ 1.21 g LU⁻¹ hr⁻¹; winter: 0.64 ~ 0.84 g LU⁻¹ hr⁻¹) from a naturally ventilated sow house with a slatted floor in China. Comparable values for summer were obtained in the present study, from the naturally ventilated small-scale sow house with a solid concrete floor. The lower normalized NH₃ emission rate we observed for winter may be because the inside temperature for this house was lower than that (~20°C) in the literature studies. For LF, mean normalized NH₃ emission rates were within the range of rates reported from previous studies for mechanically ventilated fattening pig housing with a partly-slatted floor, with rates ranging from 0.89 to 1.87 g LU⁻¹ hr⁻¹ (Zong, Li, and Zhang 2015) and 1.67 to 5.26 g LU⁻¹ hr⁻¹ (Wang et al. 2011). Zhu et al. (2006b) reported mean normalized NH₃ emission rates of 1.37 g LU⁻¹ hr⁻¹ in summer and 2.02 g LU⁻¹ hr⁻¹ in winter for a naturally ventilated fattening pig house with a fully slatted floor. Greater emission rates were reported for the “gan qing fen” system and deep bedding system by Xu et al. (2014) and Dong et al. (2009), who conducted experiments in the same region as in our study. Results from the small-scale finishing pig farm in the present study were lower, possibly because fattening pigs on the small farm were raised on a diet of cornflour and bran, with lower potential for NH₃ emission (Ivanova-Peneva, Aarnink, and Verstegen 2008). Griffing, Overcash, and Westerman (2007) reported emission factors, expressed as a percentage of the excreted total Kjeldahl nitrogen (TKN), for several national NH₃ emission inventories, to be in the range 4.8–40.6%. In the present study, lower values (ranging from 2.2 to 18.8%, see Appendix B, calculated from feed intake, feed N content, and the emission rate from this study) were obtained, which is expected considering the feed composition and manure collection/removal systems in North China.

As shown in Table 1 and Figure 2, pig farms of different scales differ in their feed N content, floor type, ventilation system, indoor climate, and manure removal system, all of which will influence NH₃ emission. However, few data are available to estimate the effects of farm scale, although the structure of pig production is changing in China. This study provides some of the first data comparing NH₃ emission between farm scales for China (Table 2). For the sow farms, NH₃ emission rates were greater for the small farm than for the large farm, which could be ascribed to the following factors: i) the slatted floor of the large farm enabled rapid draining of urine and hence limited fouled areas that are significant sources of NH₃ (Svennerstedt 1999), as evidenced by Hou, Velthof, and Oenema (2015) who reported 60% lower emissions from slatted floor housing compared with a solid concrete floor; ii) the sows were raised in individual compartments, which resulted in less floor contamination and therefore lowered NH₃ emission (Ni et al. 1999). For the fattening pig farms, NH₃ emission rates were greater for the large farm than for the small farm. The lower values for the SF farm were possibly related to the lower nitrogen content in the feed. This is supported by Canh et al. (1998), who found that NH₃ emissions were reduced by 10–12.5% for each percent decrease in dietary crude protein. On a per pig basis, NH₃ emission rates were mostly greater from the sow farms than the fattening pig farms. It is expected that NH₃ emissions increased with increasing animal weight (Ivanova-Peneva, Aarnink, and Verstegen 2008) because manure production is directly proportional to body weight (Hoeksma et al. 1992).

There is little data relating NH₃ emission rates to farm scale for China. Here, we provide the first estimates of NH₃ emission from different farm scales. However, it should be noted that the ventilation rate based on the CO₂ balance method provides only an approximation of the house ventilation rate, which will contribute to the appreciable variation in the emissions data (Bicudo et al. 2002), and thus more accurate measurement methods need to be applied in China. In addition, differences in manure collection/removal systems and animal diets adopted by the farms likely contributed to the variations in the observed emissions data.

Seasonal and diurnal variations in NH₃ emission rates

Figure 3 shows the diurnal variation in NH₃ emission rates for the different farms. Regardless of farm scale, NH₃ emission rates measured in summer were higher than those in winter. These results are explained by the greater indoor temperature and/or higher ventilation rate in summer (Table 2) which promote NH₃ emission. Ammonia emission rates were higher in the daytime than at nighttime due to higher indoor temperature and animal activity. In the large industrial farms, the indoor temperature remained relatively steady throughout the day, and temperature explained very little of the diurnal variation in NH₃ emission rate, but ventilation rate explained more (R² = 0.66–0.93, p < .001) (Figure 5); the higher NH₃ emission rates during the daytime were most likely due to the increased animal activity and their higher frequency of urination and defecation (Aarnink, Koetsier, and Van den Berg 1993). As reported by Jeppsson (2003), animal activity could be a larger factor because pigs lie on NH₃-emitting surfaces during the nighttime and are grubbing in the NH₃-emitting material during the daytime. Saha et al. (2014) observed that most pigs excreted 1–2 h after feeding, with consequent peaks in emissions. However, in the present study, feeding and manure removal showed no obvious impact on the NH₃ emission rate, possibly because other factors masked these impacts. Several microclimatic parameters can influence NH₃ emission, but a relationship between emission rate and a microclimatic parameter on one farm may be masked by other microclimatic parameters on another farm; thus, it is difficult to derive a consistent relationship between microclimatic parameters and NH₃ emission. Nevertheless, this study revealed a positive relationship between temperature and NH₃ emission rate, and a negative relationship between relative humidity and NH₃ emission rate, in agreement with the observations of Cortus et al. (2008).

Figure 3. Seasonal variation of NH₃ emission rates (mean ± standard deviation between days, day = 3–5) in different farms

Seasonal and diurnal variations in NH₃ concentrations

Indoor NH₃ concentrations measured at each pig farm (Table 2) were all below the threshold for indoor air quality in livestock housing (25 ppm and 19 mg m⁻³, for an 8 h working day) given by Koerkamp et al. (1998). This was probably due to the interaction between the low ammonia emission rates and high ventilation rates in the present study. Kim et al. (2008) measured NH₃ concentrations in different types of pig house and found that, irrespective of the type of manure collection system, the NH₃ concentrations in mechanically-ventilated pig houses were higher than those in the naturally ventilated pig house. Our findings are in agreement with this and can be explained by the so-called “dilution effect,” which varies depending on the ventilation rate (Elzing and Monteny 1997). The seasonal variation in the outlet or indoor NH₃ concentrations differed according to the farm scale. For the large industrial pig farms, outlet NH₃ concentrations in summer were lower compared with those in winter, although the ammonia emission rates were greater in summer. This suggests that the ventilation rate plays a more important role in the seasonal variation in NH₃ concentration. However, for the small traditional farms, seasonal differences were less evident, with none apparent for SS, but somewhat higher concentrations in summer than in winter for SF, which may have been related to the higher indoor temperature. This suggests that for small farms without mechanical ventilation, the NH₃ emission rate plays the more important role rather than the ventilation rate in indoor NH₃ concentration.

Figure 4 shows the diurnal variation in the outlet and indoor NH₃ concentrations for the different farms. The ventilation rate was a significant explanatory variable for NH₃ concentration (Elzing and Monteny 1997). In the small traditional pig farms, NH₃ concentrations were lower in the daytime than those at nighttime, which can be explained by the diurnal variation in the ventilation rate. When assessed on an hourly basis, a fairly strong negative correlation (R² = 0.48–0.78, p ≤ .001) was obtained between the ventilation rate and the NH₃ concentration (Figure 5c, d, g and h), showing that most of the diurnal variation in NH₃ concentration can be explained by the ventilation rate. The results show that increases in ventilation rate are required in the small farms to give a better indoor environment regarding NH₃ concentration. However, for the large industrial pig farms, this clear relationship (R² = 0.36 ~ 0.65, p ≤ .001) was only found in the summer, and emission rate rather than ventilation rate plays a more important role in explaining the diurnal variation of NH₃ concentration (Figure 5), possibly because at such low ventilation rates the effect of air dilution was being masked by other factors (Zong et al. 2014). A positive correlation was obtained between NH₃ concentration and ventilation rate in summer in the LS farm, suggesting that other factors (e.g., animal activity) were more important in explaining the diurnal variation for this farm. The inconsistent relationship between NH₃ concentration and ventilation rate also indicates that the ventilation rate may not be the primary cause of variation, but a secondary factor in the large industrial farms. However, few experiments consider only the ventilation rate effect because of the interlinked effect of temperature. There was no consistent relationship between temperature or relative humidity and NH₃ concentration. Neither did feeding or manure removal events show any obvious impact on the outlet or indoor NH₃ concentration.

Figure 4. Seasonal and diurnal variation of NH₃ concentrations (mean ± standard deviation between days, day = 3–5) in different pig farms

Figure 5. Pearson correlation matrix coefficients (R²) for NH₃ concentration and emission rate under different microclimatic conditions for the four pig farms: large-scale sow (LS), small-scale sow (SS), large-scale finishing pig (LF), and small-scale finishing pig (SF). The width of the arrows is proportionate to Pearson correlation matrix coefficients adjacent with values. Solid and dashed lines represent positive and negative correlations, respectively. The R² denotes the proportion of variance that could be explained by the corresponding variable. Significance levels are as follows: *: p < .05, **: p < .01, and ***: p < .001. a) LS (summer); b) LS (winter); c) SS (summer); d) SS (winter); e) LF (summer); f) LF (winter); g) SF (summer) and h) SF (winter)

Implications for NH₃ mitigation from pig farms

The data provided in this study will be helpful to establish mitigation targets and devise effective abatement techniques, and thus to promote the health of workers, improve the welfare of confined pigs, and protect the environment through the reduction of NH₃ emissions from pig housing. Accordingly, ammonia mitigation on sow farms (especially small-scale ones) should be a top priority in the North China Plain. In addition, mitigation techniques should be initially targeted to summer, particularly during the daytime. Although microclimatic parameters, to some extent influence indoor ammonia concentration and emission rate, using microclimatic parameters to modulate ammonia emission is rather impractical because the ambient parameters must primarily be set for the bioclimatic comfort of the animals. The results obtained in this study also indicated that the farm-scale effect on NH₃ emission could be ascribed to differences in i) feed composition for the fattening pig farms and ii) floor system and animal activity for the sow farms. Low-nitrogen feeding (targeted to meet pig requirement) is one of the most cost-effective and strategic ways of reducing NH₃ emissions (Bittman et al. 2014). Reduced N content diets containing synthetic amino acids have been shown to reduce N excretion, which leads to lower NH₃ emissions without any detrimental effect on pig performance. It has been shown that NH₃ emission can be decreased in this way by 24–65% (Hou, Velthof, and Oenema 2015). In this study, we also found that the farms using higher N content diets emit more NH₃ emission, such as the small-scale sow farm and the large-scale fattening pig farm; emission reductions on these farms could therefore be achieved by using lower protein feed. Furthermore, NH₃ mitigation techniques should be chosen based on the farm scale. For small farms, appropriate use of bedding can be an effective mitigation option (Wang et al. 2011), while for larger farms the use of air scrubbers or manure acidifying (both too expensive to implement on small-scale farms) can be effective in lowering NH₃ emissions (Liu et al. 2019).

Conclusion

Farms operating at different production scales differed in their feed N content, floor type, ventilation system, indoor climate, and manure removal system, all of which influence NH₃ emissions. This study investigated the farm-scale effect on NH₃ emissions and concentrations and their temporal variations in North China.

1. For sow farms, the NH₃ emission rate was greater from the small traditional farm, possibly due to raising sows on the slatted floor and in individual compartments in the large industrial farms. However, in fattening pig farms, NH₃ emission rates were greater in the industrial large farms, most likely due to dietary differences.

2. Regardless of the farm scale, NH₃ emission rates were higher in summer than in winter, attributed to a higher indoor temperature and high ventilation rate in summer. Emission rates were higher during daytime than at night, possibly due to high indoor daytime temperature and/or diurnal variation in animal activity.

3. NH₃ concentrations were mostly higher in the large industrial farms due to lower ventilation rates than in the small traditional farms; outlet NH₃ concentration in the large industrial farms was lower in summer than in winter; although the diurnal variation was inconsistent between farms, it could best be explained by the ventilation rate in the small traditional farms and the emission rate in the large industrial farms.

Disclosure statement

No potential conflict of interest was reported by the authors.

Additional information

Funding

This work was supported by the National Key Research and Development Program of China [2018YFC0213300]; the Research Equipment Developing Program of Chinese Academy of Sciences [YJKYYQ20170066]; Science and Technology Service Network Initiative [KFJ-STSZDTP-053 and KFJ-STS-QYZD-160]; Hebei Dairy Cattle Innovation Team of Modern Agroindustry Technology Research System [HBCT2018120206]; National Natural Science Foundation of China [31872403]; Hebei Poultry Innovation Team of Modern Agro-industry Technology Research System [HBCT2018150209]; the President’s International Fellowship Initiative (PIFI) of the Chinese Academy of Science [2016DE008 and 2016VBA073]; and the UK China Virtual Joint Centre for Improved Nitrogen Agronomy (CINAg) funded by the Newton Fund via UK BBSRC/NERC [BB/N013468/1].

Notes on contributors

Yubo Cao

Yubo Cao is a Ph.D. student at the Center for Agricultural Resources Research, IGDB, Chinese Academy of Science and the University of Chinese Academy of Science.

Zhaohai Bai

Zhaohai Bai and Xuan Wang are associate researchers at the Center for Agricultural Resources Research, IGDB, Chinese Academy of Science.

Tom Misselbrook

Tom Misselbrook is a principal research scientist at the Department of Sustainable Agriculture Sciences, Rothamsted Research, North Wyke, UK.

Lin Ma

Lin Ma is a research professor at the Center for Agricultural Resources Research, IGDB, Chinese Academy of Science.