Effects of biochar amendment on nitrogen mineralization in black soil with different moisture contents under freeze-thaw cycles

Geoderma 353 (2019) 459–467

Contents lists available at ScienceDirect

Geoderma journal homepage: www.elsevier.com/locate/geoderma

Effects of biochar amendment on nitrogen mineralization in black soil with different moisture contents under freeze-thaw cycles

T

Qiang Fua,b,c,d, Jiawen Yana,b,c, Heng Lia,b,c, , Tianxiao Lia,b,c,d, Renjie Houa,b,c, Dong Liua,b,c,d, Yi Jia,b ⁎

a

School of Water Conservancy and Civil Engineering, Northeast Agricultural University, Harbin, Heilongjiang 150030, China Key Laboratory of Effective Utilization of Agricultural Water Resources of Ministry of Agriculture, Northeast Agricultural University, Harbin, Heilongjiang 150030, China c Heilongjiang Provincial Key Laboratory of Water Resources and Water Conservancy Engineering in Cold Region, Northeast Agricultural University, Harbin, Heilongjiang 150030, China d Germplasm Innovation and Physiology-Ecology of Food Crop in Cold Region, Northeast Agricultural University, Harbin, Heilongjiang 150030, China b

ARTICLE INFO

ABSTRACT

Handling Editor: Junhong Bai

Freeze-thaw cycles (FTCs) affect the nitrogen cycling process in the non-growing season. To explore the effects of biochar application combined with soil moisture on nitrogen mineralization under FTCs, a laboratory FTC test of simulated soil columns was conducted. In this laboratory study, black soil from the Songnen Plain, China, was subjected to different biochar application rates (0%, 2% and 4%), moisture contents (15%, 20% and 25%) and numbers of FTCs (each FTC consisted of freezing at −20 °C for 48 h and thawing at 10 °C for 48 h). We explored the changes in soil moisture and aggregates as well as the effects of biochar application and different moisture contents on nitrogen availability under FTCs. The results showed that FTCs promoted the fragmentation and decomposition of soil aggregates, processes that are also related to the moisture content and biochar application rate. Moreover, the application of biochar increased the soil water holding capacity. The ammonium nitrogen and nitrate nitrogen contents in the soil first increased and then decreased during the FTCs and peaked after the third FTC. However, influenced by transfer and transformation processes, the inorganic nitrogen contents were higher than the initial levels after freezing and thawing. In addition, the content of ammonium nitrogen increased with increasing initial soil moisture content but decreased with increasing biochar application rate. However, the content of nitrate nitrogen increased with increasing initial soil moisture content and biochar application rate. Analysis of variance showed that FTCs and moisture content are the major driving factors that affect nitrogen mineralization (p < 0.05). This study provides guidance for the regulation of farmland soil nitrogen and the efficient utilization of agricultural resources in areas with seasonally frozen soil.

Keywords: Freeze-thaw cycle Biochar Black soil Soil aggregate Nitrogen mineralization

1. Introduction In boreal and temperate regions, freeze-thaw cycles (FTC) often occur at the soil surface and at certain depths below the surface, caused by seasonal or diurnal temperature variations. Against the background of global warming, FTCs occur frequently (Kreyling et al., 2010). Freezing and thawing can change the soil structure and the movement of water and heat (Fu et al., 2018) and can affect soil organic matter mineralization (Watanabe et al., 2019). Freezing and thawing can also cause the migration and transformation of soil nitrogen (Joseph and Henry, 2008; Jiang et al., 2018). Nitrogen is one of the most important nutrient elements in terrestrial ecosystems and is also the nutrient element that plants take up in the greatest amounts from the soil.

⁎

However, organic nitrogen is the main form of nitrogen in the nitrogen pool and must be transformed into inorganic nitrogen by mineralization so that it can be absorbed and utilized by plants. Mineralization is the decomposition of organic nitrogen into NH4+ and NO3− (Bruun et al., 2006) and is the primary means by which plants obtain available nitrogen from soil. Different initial soil moisture contents can affect soil physicochemical properties (Liu et al., 2017; Wei et al., 2019) and thereby affect soil nitrogen mineralization. Previous studies on the effect of freezing and thawing on soil nitrogen mineralization were mostly concentrated on alpine forests (Yang et al., 2016), wetlands (Song et al., 2017), and the polar tundra (Grogan et al., 2004; Choudhary et al., 2016), whereas research on farmland soil is relatively limited. Scholars have found significant differences in the

Corresponding author at: School of Water Conservancy and Civil Engineering, Northeast Agricultural University, Harbin, Heilongjiang 150030, China. E-mail addresses: [email protected] (H. Li), [email protected] (T. Li).

https://doi.org/10.1016/j.geoderma.2019.07.027 Received 23 February 2019; Received in revised form 9 July 2019; Accepted 11 July 2019 0016-7061/ © 2019 Elsevier B.V. All rights reserved.

Geoderma 353 (2019) 459–467

Q. Fu, et al.

effects of FTCs on soil nitrogen mineralization. For example, Song et al. (2017) found that FTCs destroy microbes and/or soil aggregates and that extra nutrient availability stimulates the activity of the remaining microorganisms, leading to an increase in nitrogen mineralization. Zhang et al. (2016) observed a similar phenomenon. By contrast, results indicating that FTCs have no significant effect on soil nitrogen mineralization have also been reported (Groffman et al., 2011). Sjursen et al. (2005) found that the soil inorganic nitrogen content decreased first and then increased with repeated FTCs. With the increase in the number of FTCs, soil nitrogen mineralization gradually decreased. Urakawa et al. (2014) proposed that the response to FTCs differed among different types of soil, and the effects of FTCs on nitrogen mineralization rates were also different. Biochar is a product of pyrolysis and carbonization under anaerobic or hypoxic conditions (Laird et al., 2010). In recent decades, biochar has emerged as a useful additive to farmland soil affected by FTCs. The application of biochar can reduce soil bulk density, increase the water holding capacity and change the abundance of soil biological communities (Jeffery et al., 2011; Fu et al., 2019). Biochar can effectively maintain the inorganic nitrogen content in the soil, affecting the nitrogen mineralization rate and ultimately plant growth (Song et al., 2006; Liu et al., 2018). Moreover, biochar pyrolyzed at high temperatures has a stronger nitrogen fixation ability than does biochar pyrolyzed at low temperatures (Singh et al., 2010). Previous studies have focused mostly on the effects of FTCs on soil nitrogen cycling or the effects of biochar on its regulation. However, studies on the effect of FTCs combined with biochar application on nitrogen mineralization are relatively insufficient. As stated, we made the following hypothesis: (1) FTCs could promote nitrogen mineralization in black soil, and the effects depend on the biochar application rates and initial moisture contents, and (2) a high biochar addition rate may lead to different changes in ammonium nitrogen and nitrate nitrogen contents. In this laboratory incubation study, we selected black soil as the research object because of its high content of organic, which can ensure a stable increase in grain production. The specific objectives of this study were the following: (1) to investigate the changes in soil aggregates and moisture contents during FTCs, (2) to explore the effects of different initial moisture contents and biochar rates under FTCs on nitrogen mineralization, and (3) to reveal the response factors of nitrogen transformation through variance analysis.

1

3

2

4

5 7 PC 400

6

Computer

8

Fig. 1. Freeze-thaw cycle device diagram. Note: 1- finned tube condenser, 2- soil sampling device, 3- controllable freezethaw cycle box, 4- methyl methacrylate cylinder, 5- temperature and moisture content sensor, 6- mariotte bottle, 7- data acquisition transmitter, 8- insulation materials.

chernozem, meadow soil, bog soil, sand soil, dark brown loam, brown coniferous forest soil, saline soil and alkaline soil—and the major soil type is black soil. The black soil area accounts for more than > 60% of the Songnen Plain. Soil samples (0–30 cm) were collected from the experimental farmland of Northeast Agricultural University of Songnen Plain in northeastern China (45.74°N, 126.64°E) (Fig. 2). The surface soils in this region usually experience seasonal freeze-thaw processes during early spring. The physicochemical properties of the soil are shown in Table 1. Soil organic carbon (SOC) was measured using the H2SO4-K2CrO7 oxidation method, while soil total nitrogen (TN) was detected using an automatic azotometer (Kjeltec 8400, FOSS, Denmark) according to the Kjeldahl method. Soil ammonium nitrogen (NH4+-N) and nitrate nitrogen (NO3−-N) were determined using a continuous flow analyser (AA3, SEAL Analytical, Germany) with 1 mol/L KCL extracts. Soil pH was measured using a pH meter (SevenEasy, MettlerToledo, Switzerland). The soil moisture content was determined gravimetrically after drying at 105 °C. The soil aggregate mass fraction was determined by the wet sieving method and was described by the soil mean weight diameter (MWD) according to the following formula (1):

2. Materials and methods 2.1. Test device The soil sampling device is a methyl methacrylate cylinder with a design specification of 40 cm in height and 30 cm in diameter (Fig. 1). The sealing effect of the cylinder is good, which can effectively prevent the loss of water and nutrients. To simulate the one-dimensional heat transfer of soil, insulation materials were wrapped around the barrel and bottom of the cylinder to ensure that the soil froze unilaterally from top to bottom and to avoid the influence of lateral frost heaving on the soil. The surface of the soil column remained naturally exposed throughout the process. In addition, the soil moisture and temperature sensors (Hydra CR800, Beijing, China) were placed at intervals of 10, 20, and 30 cm from the upper surface of the cylinder. The sensors monitored the soil temperature and moisture content in real time, which were automatically recorded by the data acquisition transmitter. The entire FTC simulation process was carried out in a controllable FTC box. The control temperature of the box ranged from −40 °C to 30 °C, and the control precision was ± 0.5 °C.

n

MWD =

x i wi i=1

(1)

where MWD is the mean weight diameter (mm), xi is the mean diameter of aggregates in any size range that were sieved out (mm), and wi is the total number of aggregates in any size range accounting for the dry weight of the soil samples. 2.3. Biochar analysis Biochar used for the experiment was produced by the Biochar Manufacturing Plant, Jinzhou, China. The raw material was straw, and the biochar was produced under a pyrolysis temperature of 500–600 °C. The biochar was ground to pass through a 2 mm nylon fibre sieve and was mixed thoroughly before experimental use. The total C, H, N and ash contents were characterized as described by Zheng et al. (2013). The pH, TN, NH4+-N and NO3−-N contents of biochar were determined using the previously mentioned methods. The physicochemical properties of the biochar are shown in Table 1.

2.2. Soil collection and analysis There are 9 soil types in the Songnen Plain, China—black soil, 460

Geoderma 353 (2019) 459–467

Q. Fu, et al.

Fig. 2. Sampling area.

the MWD values of the soil. The initial ammonium nitrogen contents under the B1, B2 and B3 treatments were 4.25 mg/kg, 3.78 mg/kg and 3.75 mg/kg, respectively. The initial nitrate nitrogen contents under the B1, B2 and B3 treatments were 12.47 mg/kg, 11.82 mg/kg and 11.45 mg/kg, respectively.

Table 1 The properties of the soil and biochar. Black soil

Biochar

pH

6.15 ± 0.24

pH

8.5 ± 0.1

TN(g N kg−1) NH4+-N(mg N kg−1) NO3−-N (mg N kg−1) Organic C(g C kg−1) Sand (%) Silt (%) Clay (%)

1.2 ± 0.1 3.1 ± 0.1 9.4 ± 0.1 25.7 ± 0.2 26.8 56.4 16.8

TN(g N kg−1) NH4+-N(mg N kg−1) NO3−-N (mg N kg−1) C (%) H (%) N (%) Ash (%)

1.0 ± 0.1 2.5 ± 0.2 1.7 ± 0.02 69.34 ± 3.12 2.13 ± 0.18 1.28 ± 0.13 29.7 ± 0.6

2.5. Statistical analysis Multiple-way ANOVA was used to examine the differences in the soil NH4+-N and NO3−-N contents and the nitrogen mineralization rate among the FTCs, biochar rates, moisture contents and soil layers. The Duncan method was used to test the significant difference in various soil nitrogen indexes after the FTCs. Data-sets were subjected to normality and heterogeneity tests and were log-transformed (base 10) when the variances were unequal before analyses. Pearson's correlation was employed to examine the correlations between the NH4+-N and NO3−-N contents. Differences and correlations were considered statistically significant if p < 0.05 and highly significant if p < 0.01.

Values are mean ± SEa (N = 3). astandard error.

2.4. Experimental design The collected soil samples were air-dried, homogenized and ground to pass through a 2 mm nylon fibre sieve before experimental use. All soils were pre-incubated at 10 °C (simulating the average soil temperature in early spring) in a constant-temperature incubator for 5 days. Soils were mixed with 0% (B1), 2% (B2) and 4% (B3) (w/w) biochar and were then wetted with deionized water to reach 15% (W1), 20% (W2) and 25% (W3) moisture contents (the actual moisture content error was ± 0.4%), resulting in a total of nine treatments. There were nine FTC events in total, and each FTC included freezing at −20 °C for 48 h and thawing at 10 °C for 48 h. After every FTC, triplicate samples of each treatment were randomly selected from the 10 cm (L1), 20 cm (L2) and 30 cm (L3) soil layers. Soils were used for determining the NH4+-N and NO3−-N contents together with the moisture content and

3. Results 3.1. Soil physical properties 3.1.1. Soil moisture characteristics The soil moisture contents of each soil layer under different treatment conditions during the FTCs are shown in Fig. 3. The moisture contents of the L1 and L2 soil layers increased throughout the FTCs, while that of the L3 soil layer gradually decreased 461

Geoderma 353 (2019) 459–467

Q. Fu, et al. 25

25 10cm 20cm 30cm

15

10

5

10

2

3

4

5

6

7

8

9

2

3

4

5

Freeze-thaw Cycle (time)

a

b

7

8

9

1

15 10 5

25 20 15 10

2

3

4

5

6

7

8

9

2

3

Freeze-thaw Cycle (time)

4

5

6

7

8

15 10

15 10

0 4

5

6

Freeze-thaw Cycle (time)

7

8

9

5

6

9

7

8

9

10cm 20cm 30cm

35

20

0 3

4

40

25

5

2

3

f

30

5

1

2

Freeze-thaw Cycle (time)

Soil Moisture Content (%)

Soil Moisture Content (%)

20

8

10

1

10cm 20cm 30cm

35

25

7

15

9

40

30

9

20

e

10cm 20cm 30cm

8

25

Freeze-thaw Cycle (time)

d

35

7

0 1

40

6

5

0 1

5

10cm 20cm 30cm

30

5

0

4

35

Soil Moisture Content (%)

Soil Moisture Content (%)

20

3

c

10cm 20cm 30cm

30

25

2

Freeze-thaw Cycle (time)

35

30

Soil Moisture Content (%)

6

Freeze-thaw Cycle (time)

10cm 20cm 30cm

10

0 1

35

15

5

0 1

Soil Moisture Content (%)

15

5

0

10cm 20cm 30cm

20 Soi l Moi sture Content (%)

20 Soi l Moi sture Content (%)

Soi l Moi sture Content (%)

20

25 10cm 20cm 30cm

30 25 20 15 10 5 0

1

2

3

4

5

6

Freeze-thaw Cycle (time)

g

h

7

8

9

1

2

3

4

5

6

Freeze-thaw Cycle (time)

i

Fig. 3. Changes in the moisture contents of W1 soil under the B1, B2 and B3 treatments (a, b, c, respectively), W2 soil under the B1, B2 and B3 treatments (d, e, f, respectively) and W3 soil under the B1, B2 and B3 treatment (g, h, i, respectively) during the freeze-thaw cycles.

(Fig. 3a). In the W1B1 soil column, the moisture content of the L1 soil layer increased by 1.41%–5.75% compared with the initial value. Similarly, as the number of FTCs increased, the moisture content of the L2 soil layer increased, but the overall extent of this increase was lower than that of the L1 soil layer. Due to the driving effect of the gradient in the soil water potential, the water in the L3 soil layer gradually migrated to the upper layer. The moisture content of the L3 soil layer decreased by 0.79%–4.77% compared with the initial value. As the biochar application rate increased, the variation trend of the soil moisture content remained the same, but the variation amplitude was gradually weakened (Fig. 3a, b, c). The moisture contents of the W1B2 and W1B3 soil columns decreased by 0.38%–1.16% and 0.6%–1.66%, respectively, compared with those of the W1B1 soil column of the L1 soil layer. As the biochar application rate increased, the water accumulation in the L2 soil layer also decreased. Although the moisture content of the L3 soil layer decreased, the application of biochar inhibited the transfer and diffusion of soil water. Therefore, the soil moisture content under the B2 and B3 treatments was higher than that under the B1 treatment. This indicated that biochar has a water immobilization effect.

In addition, the variation trends of the soil moisture content of the W2 and W3 soil columns were consistent with those of the W1 soil column. However, due to the increase in the initial value, the soil moisture content increased as a whole after various numbers of FTCs. Soil moisture migrated due to FTCs, resulting in uneven water distribution in the soil, which can affect the nutrient content and ultimately the nitrogen mineralization process. 3.1.2. Soil aggregate stability The initial soil MWD values under the B1, B2 and B3 treatments were 0.132 mm, 0.1312 mm and 0.1304 mm, respectively. The MWD values of each soil layer under different treatment conditions after each FTC are shown in Fig. 4. In the L1 soil layer, the MWD value under the W1B1, W2B1 and W3B1 soil columns decreased significantly after freezing and thawing and tended to stabilize between the 7th and 9th FTCs (Fig. 4a). The MWD value of the W1B1 soil column decreased by 3.41%–16.67% compared with the initial value during the whole FTC. With the increase in initial moisture content, the amplitude of 462

Geoderma 353 (2019) 459–467

Q. Fu, et al.

Fig. 4. Soil MWD during the freeze-thaw cycles in the 10 cm soil layer (a, d, g), 20 cm soil layer (b, e, h) and 30 cm soil layer (c, f, i). MWD mean weight diameter.

the variation in MWD values increased gradually. In addition, the MWD value decreased with increasing moisture content during the first to fifth FTCs, but the opposite trend was observed after the fifth FTC. As the biochar application rate increased, the initial soil MWD values under the B2 and B3 treatments decreased by 0.61% and 1.21%, respectively, compared with that under the B1 treatment (Fig. 4a, d, g). The soil MWD values under the B1 and B2 treatments tended to stabilize after the 7th to 9th FTCs, while those under the B3 treatment tended to stabilize after the 3rd to 5th FTCs. This finding indicated that as the biochar application rate increased, fewer FTCs were required for the soil aggregates to stabilize. The MWD values of the W1B2 and W1B3 soil columns increased by 0.55%–10.91% and 1.49%–17.18%, respectively, compared with those of the W1B1 soil column throughout the FTCs. As the biochar application rate increased, the amplitude of the variation in MWD values decreased gradually. In addition, the MWD values under the B2 treatment decreased with increasing moisture content from the first to the fifth FTCs, and the trend of W2 > W3 > W1 appeared after the fifth FTC. The MWD values under the B3 treatment consistently decreased with increasing moisture content throughout the FTC events. With increasing soil depth, the MWD value gradually increased during the FTC events, but the trend was the same as that in the L1 soil.

3.2. Effect of freeze-thaw cycles on nitrogen mineralization 3.2.1. Ammonium nitrogen content The variation characteristics of the soil NH4+-N content under different treatment conditions after all FTCs are shown in Fig. 5. For the W1B1 soil column, the NH4+-N content first increased and then decreased in the 10 cm layer during the FTCs and peaked after the third FTC. Moreover, the NH4+-N content was higher than the initial level at the end of the FTCs. In addition, as the biochar application rate increased, the NH4+-N contents of the W1B2 and W1B3 soil columns decreased by 3%–22% and 16%–26%, respectively, compared with that of the W1B1 soil column. As the initial moisture content increased, the NH4+-N content increased as a whole (Fig. 5a, b, c). However, the overall trend was consistent with that of the W1 moisture content level. Under the B2 and B3 treatments, the trends of the NH4+-N content under the W2 and W3 moisture content levels were the same as those under the B1 treatment. The NH4+-N content increased with increasing initial soil moisture content but decreased gradually with an increase in the biochar application rate. In addition, with increasing soil depth, the NH4+-N content decreased slightly. However, the trend during the FTCs was the same as that of the L1 soil layer, but the magnitudes of change were different.

463

Geoderma 353 (2019) 459–467

Q. Fu, et al.

20 a

15

a

b

b

a ab

a c

bc

c

a bb

b

10

a

b

c

ab c

a

a

b

bb

c

5

0

25 0% Biochar 2% Biochar 4% Biochar

20 a a

15 a ab

b

b

a c

bc

c b

10

2

3

4

5

6

7

8

9

b

b

b

a cb

a

a b

b

bb

2

3

4

5

6

7

8

a

c

bc

b

a

c

c

b

a bc

a bb

a bb a

a b

5

0 2

3

4

5

6

7

8

a

15 a aa

10

bc bc

ab c

b

ab

b

a

b

a

a

c c

a

b

bb

bb

5

2

3

4

5

6

7

8

b

c

b c

a bc

a

bc

a

b

a c

bb

a

ba

5

0 2

3

4

5

6

7

8

9

bb

a bb

3

4

5

6

7

8

9

0% Biochar 2% Biochar 4% Biochar

20 a

15

bc

a a

a b

bc

bb

c

a bb

a

a b

10

c

b

a

c

bb

7

8

a bb

5

2

3

4

5

6

9

f 25 0% Biochar 2% Biochar 4% Biochar

20

15 a

10

a

Cycle times

a b c

a bc

b

c

a

b

c

a

bb

a

bc

a

b

c

a

b

a b

b

5

0 1

2

1

b

+ Soil NH4 -N content/ mg*kg-1

b

10

bc

a bb

e + Soil NH4 -N content/ mg*kg-1

a

a a

bb

5

9

25 0% Biochar 2% Biochar 4% Biochar

a

0 1

d

a

c b

10

Cycle times

20

a

25

20

9

25

a

c

c 0% Biochar 2% Biochar 4% Biochar

Cycle times

15

b

Cycle times

0 1

b

c

c

1

+ Soil NH4 -N content/ mg*kg-1

b

a

+ Soil NH4 -N content/ mg*kg-1

20

bc

a

b bb

a

9

25

a

15

b 0% Biochar 2% Biochar 4% Biochar

a

a a

Cycle times

25

15

0% Biochar 2% Biochar 4% Biochar

20

0 1

a + Soil NH4 -N content/ mg*kg-1

a

5

Cycle times

+ Soil NH4 -N content/ mg*kg-1

b

0 1

10

a

+ Soil NH4 -N content/ mg*kg-1

25 0% Biochar 2% Biochar 4% Biochar

+ Soil NH4 -N content/ mg*kg-1

+ Soil NH4 -N content/ mg*kg-1

25

0% Biochar 2% Biochar 4% Biochar

20 a

15 a bc

a

b

a bb

c

b c

10

a

bc

a

bc

a

b

a c

bb

a

a b

5

0 1

2

3

Cycle times

4

5

6

Cycle times

g

h

7

8

9

1

2

3

4

5

6

7

8

9

Cycle times

i

Fig. 5. Changes in the ammonium nitrogen contents of W1, W2 and W3 soils in the 10 cm soil layer (a, b, c), W1, W2 and W3 soils in the 20 cm soil layer (d, e, f) and W1, W2 and W3 soils in the 30 cm soil layer (g, h, i). Values are means ± SE (N = 3). Different lower-case letters indicate significant differences at the 5% level. NH4+-N ammonium nitrogen.

NO3−-N content decreased slightly. However, the trend was the same as that of the L1 soil layer during all FTCs, but the magnitudes of change were different.

3.2.2. Nitrate nitrogen content The variation in the characteristics of the soil NO3−-N content under different treatments after all FTCs is shown in Fig. 6. For the W1B1 soil column, the NO3−-N content first increased and then decreased in the 10 cm layer during the FTCs and peaked after the third FTC. Moreover, the NO3−-N content was higher than the initial level at the end of the FTCs. In addition, as the biochar application rate increased, the NO3−-N content of the W1B2 and W1B3 soil columns increased by 1%–7% and 9%–18%, respectively, compared with that of the W1B1 soil column. As the initial moisture content increased, the NO3−-N content increased as a whole (Fig. 6a, b, c), but the overall trend was consistent. The NO3−-N content increased with increasing moisture content. However, in the initial freezing and thawing process, there was a trend of W2 > W3 > W1, which also showed that nitrogen mineralization is affected by many factors. Under the B2 and B3 treatments, the trends of the NO3−-N contents of W2 and W3 moisture contents were the same as those under the B1 treatment. The NO3−-N content increased with increasing biochar application rate. As the soil depth increased, the

3.2.3. Variation in the characteristics of inorganic nitrogen The significance level of the nitrogen index affected by different treatment conditions under FTCs is shown in Table 2 (p < 0.05). Analysis of variance showed that different treatments had significant effects on the soil ammonium and nitrate nitrogen contents, but the interaction among different treatments had no significant effect on the nitrate nitrogen content (p < 0.05). In addition, all the other treatments except the application of biochar had significant effects on the nitrogen mineralization rate. Comprehensive analysis showed that FTCs and the soil moisture content were the main driving factors that affected the nitrogen mineralization rate. Pearson correlation analysis showed that there was an extremely significant correlation between nitrate nitrogen and ammonium nitrogen under FTCs (Table 3).

464

Geoderma 353 (2019) 459–467

Q. Fu, et al.

30 25

a a a bb

cb

bb

a bb

a bb

a bc

15

a

bc

a

bc

a

10 5 0

30 25 20

a cb bba

a

ba

cb

c c

2

3

4

5

6

7

8

c

ba

aba c

a bb

10 5

1

2

3

4

5

6

7

8

a cb

a bb

a cb

15

a

a c b

bb

a

c

ba

a a a

10 5 0 2

3

4

5

6

7

8

0% Biochar 2% Biochar 4% Biochar

25

a

20 b

a

c

b

a

b

a cb

c

b

b

a b

c

aa c

ab

a c

b

a c

b

15 10 5

1

2

3

4

5

6

7

8

c

b

c

b

c

a b

a c

cb

a

a bb

a bb

a b a

10 5 0

Soil NO3--N content/ mg*kg-1

25

2

3

4

5

6

7

8

a c

b

a cb

ab c

7

8

a

a c

b

5

2

3

4

5

6

9

0% Biochar 2% Biochar 4% Biochar

30 25 20 b

a

c

bb

b

a ba b

bb

b

a cb

a

a c

a cb

b

15

b

a

b

10 5

2

3

4

5

6

7

8

9

Cycle times

f 35 0% Biochar 2% Biochar 4% Biochar

30 25 a

a

20 b

aa

cb

c

b

a c

b

a b c

b

a

c

b

aa

b

aa

aa

a

15 10 5

9

a

10

1

0 1

b

15

9

35

a

c

e 0% Biochar 2% Biochar 4% Biochar

20

c b

Cycle times

30

cb

b

0

9

35

a

c

c

30

d

b

a

b

35

Cycle times

a

c

Cycle times

0 1

ca

1

Soil NO3--N content/ mg*kg-1

25

Soil NO3--N content/ mg*kg-1

0% Biochar 2% Biochar 4% Biochar

b ab

20

a

b

30

cb

b

9

35

a

a

25

Cycle times

a

20

0% Biochar 2% Biochar 4% Biochar

30

0

9

35

Soil NO3--N content/ mg*kg-1

a

15

Cycle times

Soil NO3--N content/ mg*kg-1

cb

0

1

15

b

a

Soil NO3--N content/ mg*kg-1

20

c

b

35 0% Biochar 2% Biochar 4% Biochar

Soil NO3--N content/ mg*kg-1

35 0% Biochar 2% Biochar 4% Biochar

Soil NO3--N content/ mg*kg-1

Soil NO3--N content/ mg*kg-1

35

0% Biochar 2% Biochar 4% Biochar

30 25 a cb

20

a b

c

a c

b

a b

bba

a

cb

15

a

a bb

b

b

a

a c

b

10 5 0

1

2

Cycle times

3

4

5

6

7

8

9

1

2

3

Cycle times

g

4

5

6

7

8

9

Cycle times

h

i

Fig. 6. The changes in the nitrate nitrogen contents of W1, W2 and W3 soils in the 10 cm soil layer (a, b, c), W1, W2 and W3 soils in the 20 cm soil layer (d, e, f) and W1, W2 and W3 soils in the 30 cm soil layer (g, h, i). Values are means ± SE (N = 3). Different lower-case letters indicate significant differences at the 5% level. NO3−-N nitrate nitrogen.

Table 2 Results of ANOVAs testing the effects of FTCs, biochar rates, moisture contents and soil layers. Source

FTCs Moisture contents Biochar rates Soil layers FTCs* Moisture contents FTCs* Biochar rates FTCs* Soil layers Moisture contents* Biochar rates Moisture contents* Soil layers Biochar rates* Soil layers

NO3−-N

NH4+-N

Mean square

F-value

Sig.

221.861 71.073 251.470 40.297 3.654 4.601 1.816 5.287 7.441 2.009

44.795 14.350 50.773 8.136 0.738 0.929 0.367 1.068 1.502 0.406

0.000 0.000 0.000 0.000 0.756 0.535 0.989 0.372 0.200 0.805

Mean square 458.646 51.584 212.854 82.553 1.416 2.649 3.045 1.462 2.161 3.850

Bolded numbers indicated statistical significant at P < 0.05.

465

Mineralization rate F-value

Sig.

2091.893 235.276 970.833 376.527 6.458 12.082 13.887 6.668 9.855 17.559

0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000

Mean square

F-value

Sig.

55.929 1.391 0.165 1.797 0.109 0.030 0.199 0.039 0.077 0.029

875.739 21.788 2.576 28.134 1.700 0.470 3.113 0.613 1.201 0.455

0.000 0.000 0.077 0.000 0.042 0.961 0.000 0.654 0.309 0.769

Geoderma 353 (2019) 459–467

Q. Fu, et al.

increase in the biochar application rate (Fig. 3). Because of the large specific surface area and porous nature of biochar, the soil water holding capacity was improved (Laird et al., 2009; Zwieten et al., 2010). The application of biochar increased the nitrate nitrogen content, which was mainly reflected in the increased transformation of NH4+ to NO3− (Nelissen et al., 2012). We speculated that biochar application could promote nitrogen mineralization under FTCs. The reasons are as follows: (1) Biochar applied to soil could absorb phenolic compounds (inhibit nitrification) and indirectly promote nitrification (DeLuca et al., 2006). (2) Biochar indirectly promoted the catalytic oxidation of NH4+ to NO3− by increasing the abundance of elements of soil ammonia-oxidizing bacteria (Ball et al., 2010). (3) Biochar enhanced the activity of nitrifying bacteria in the soil and promoted the nitrification process (Kameyama et al., 2012). Therefore, the NH4+-N content decreased with an increase in the biochar application rate, while the NO3−-N content increased. As the biochar application rate increased, a greater influence was gradually exerted on the trend of the NO3−-N and NH4+-N contents. However, this effect will stabilize when biochar application reaches a certain level. Therefore, the trend was not the higher the biochar application rate was, the greater the effect on nitrogen mineralization.

Table 3 Pearson coefficients of the correlations among soil NO3−-N contents and NH4+N contents.

NO3−-N NH4+-N

Pearson correlation Significant (two-tailed) N Pearson correlation Significant (two-tailed) N

NO3−-N

NH4+-N

1

0.466 0.000 729 1

729 0.466 0.000 729

729

Bolded numbers indicated a significant correlation at the 0.01 level.

4. Discussion 4.1. Effect of freeze-thaw cycles on nitrogen content A key characteristic of FTCs is that temperature changes lead to phase changes in soil moisture and the redistribution of soil water and heat. The freezing and thawing process affects soil physical and chemical properties, thereby affecting the stability of aggregates and subsequently affecting soil nitrogen mineralization. The degree of influence is related mainly to factors such as the freeze-thaw pattern, soil moisture content (Hou et al., 2019) and soil properties (Hu et al., 2011). Moreover, the change rates of the NO3−-N and NH4+-N contents were different in different periods, but the change trends were basically the same, mainly as follows: The contents of NO3−-N and NH4+-N first increased and then decreased throughout the FTCs and peaked after the third FTC. However, the contents were still higher than the initial levels after the entire freeze-thaw process (Figs. 5, 6). Therefore, FTCs could promote nitrogen mineralization in this study. This result was consistent with the results of some previous studies (Fitzhugh et al., 2001; Prieme and Christensen, 2001). The main reason for this phenomenon was that soil macroaggregates are destroyed and broken into microaggregates by freezing and thawing, resulting in an increase in the specific surface area of the soil and facilitating the desorption of NH4+ and NO3−. At the same time, the water stored in the macroaggregates is released, which contains a certain amount of NH4+ and NO3−. Lehrsch et al. (1991) reported similar findings. The freezing and thawing process causes soil water to freeze, resulting in an ice expansion force that destroys the connection between soil particles. When the soil is exposed to a high moisture content, the force of ice expansion increases, resulting in greater damage to macroaggregates (Lehrsch, 1998). Therefore, the NO3−-N and NH4+-N contents increased with increasing moisture content, and the effect could accumulate under continuous FTCs (Oztas and Fayetorbay, 2003). In other words, the effects of FTCs on nitrogen mineralization were related to initial moisture contents. In addition, the increased NH4+-N content was due to the release of previously unavailable NH4+-N from soil organic or inorganic colloids under FTCs (Freppaz et al., 2007). It may also be that FTCs enhance soil denitrification. The increased NO3−-N content occurred because the FTC promoted soil nitrification and the mineralization of soil microbes. The reason for the decrease in NO3−-N and NH4+-N contents after the third FTC was the absence of plant absorption and nutrient accumulation and leaching. Soil nitrogen mineralization accumulation products inhibited mineralization. The amount of inorganic nitrogen released from soil aggregates gradually decreased under FTCs. The soil nitrification rate may also decrease with an increase in the number of FTCs (Christopher et al., 2008). Therefore, the destruction of soil structure and the change in physicochemical properties of soil under freezing and thawing were not continuous, as a certain trend was maintained within a certain range.

5. Conclusion Our results show that FTCs destroyed the soil structure and decreased the stability of soil aggregates. With an increasing number of FTCs, the soil MWD values decreased gradually. The application of biochar could promote the formation of macroaggregates. At the same time, FTCs promoted the upward migration of soil moisture, while the application of biochar improved the soil water immobilization capacity. Moreover, the NH4+-N and NO3−-N contents in the soil first increased and then decreased during the FTCs and reached their respective maximum values after the third FTC. The NH4+-N and NO3−-N contents increased with increasing initial soil moisture content. Biochar application inhibited soil water migration but improved soil nitrogen fixation ability during FTCs. The NO3−-N content increased with an increase in the biochar application rate, whereas the NH4+-N content decreased. Therefore, this study concluded that the best application of biochar is 2%. Acknowledgements This research has been supported by funds from the National Natural Science Foundation of China (51679039), the National Science Fund for Distinguished Young Scholars (51825901) and the Natural Science Foundation of the Heilongjiang Province of China (LC2016016). There are no conflicts of interest. The authors also thank the anonymous reviewers for their invaluable insight and helpful suggestions. References Ball, P.N., Mackenzie, M.D., Deluca, T.H., Holben, W.E., 2010. Wildfire and charcoal enhance nitrification and ammonium-oxidizing bacterial abundance in dry montane forest soils. J. Environ. Qual. 39, 1243–1253. Bruun, S., Luxhoi, J., Magid, J., Ade, N., Jensen, L.S., 2006. A nitrogen mineralization model based on relationships for gross mineralization and immobilization. Soil Biol. Biochem. 38, 2712–2721. Choudhary, S., Blaud, A., Osborn, A.M., Press, M.C., Phoenix, G.K., 2016. Nitrogen accumulation and partitioning in a high Arctic tundra ecosystem from extreme atmospheric N deposition events. Sci. Total Environ. 554, 303–310. Christopher, S.F., Shibata, H., Ozawa, M., Nakagawa, Y., Mitchell, M.J., 2008. The effect of soil freezing on N cycling: comparison of two headwater subcatchments with different vegetation and snowpack conditions in the northern Hokkaido Island of Japan. Biogeochemistry 88, 15–30. DeLuca, T.H., MacKenzie, M.D., Gundale, M.J., Holben, W.E., 2006. Wildfire-produced charcoal directly influences nitrogen cycling in Ponderosa Pine forests. Soil Sci. Soc. Am. J. 70, 448–453. Fitzhugh, R.D., Driscoll, C.T., Groffman, P.M., Tierney, G.L., Fahey, T.J., Hardy, J.P., 2001. Effects of soil freezing disturbance on soil solution nitrogen, phosphorus, and

4.2. Effect of biochar application on nitrogen content The application of biochar could inhibit the tendency of water to migrate upwards, and the inhibition capacity increased with an 466

Geoderma 353 (2019) 459–467

Q. Fu, et al. carbon chemistry in a northern hardwood ecosystem. Biogeochemistry 56, 215–238. Freppaz, M., Williams, B.L., Edwards, A.C., Scalenghe, R., Zanini, E., 2007. Simulating soil freeze/thaw cycles typical of winter alpine conditions: implications for N and P availability. Appl. Soil Ecol. 35, 247–255. Fu, Q., Hou, R.J., Li, T.X., Wang, M., Yan, J.W., 2018. The functions of soil water and heat transfer to the environment and associated response mechanisms under different snow cover conditions. Geoderma 325, 9–17. Fu, Q., Zhao, H., Li, T.X., Hou, R.J., Liu, D., Ji, Y., Zhou, Z.Q., Yang, L.Y., 2019. Effects of biochar addition on soil hydraulic properties before and after freezing-thawing. Catena 176, 112–124. Groffman, P.M., Hardy, J.P., Fashu-Kanu, S., Driscoll, C.T., Cleavitt, N.L., Fahey, T.J., Fisk, M.C., 2011. Snow depth, soil freezing and nitrogen cycling in a northern hardwood forest landscape. Biogeochemistry 102, 223–238. Grogan, P., Michelsen, A., Ambus, P., Jonasson, S., 2004. Freeze-thaw regime effects on carbon and nitrogen dynamics in sub-arctic health tundra mesocosms. Soil Biol. Biochem. 36, 641–654. Hou, R.J., Li, T.X., Fu, Q., Liu, D., Cui, S., Zhou, Z.Q., Yan, P.R., Yan, J.W., 2019. Effect of snow-straw collocation on the complexity of soil water and heat variation in the Songnen Plain, China. Catena 172, 190–202. Hu, K., Jiang, J.Q., Zhao, Q.L., Lee, D.J., Wang, K., Qiu, W., 2011. Conditioning of wastewater sludge using freezing and thawing: role of curing. Water Res. 45, 5969–5976. Jeffery, S., Fga, V., Van, D.V.M., Bastoset, A.C., 2011. A quantitative review of the effects of biochar application to soils on crop productivity using meta-analysis. Agric. Ecosyst. Environ. 144, 175–187. Jiang, N., Juan, Y.H., Tian, L.L., Chen, X.D., Sun, W.T., Chen, L.J., 2018. Modification of the composition of dissolved nitrogen forms, nitrogen transformation processes, and diversity of bacterial communities by freeze-thaw events in temperate soils. Pedobiologia 71, 41–49. Joseph, G., Henry, H.A.L., 2008. Soil nitrogen leaching losses in response to freeze-thaw cycles and pulsed warming in a temperate old field. Soil Biol. Biochem. 40, 1947–1953. Kameyama, K., Miyamoto, T., Shiono, T., Shinogi, Y., 2012. Influence of sugarcane bagasse-derived biochar application on nitrate leaching in calcaric dark red soil. J. Environ. Qual. 41, 1131. Kreyling, J., Beierkuhnlein, C., Pritsch, K., Schloter, M., Jentsch, A., 2010. Recurrent soil freeze-thaw cycles enhance grassland productivity. New Phytol. 177, 938–945. Laird, D.A., Brown, R.C., Amonette, J.E., Lehmann, J., 2009. Review of the pyrolysis platform for coproducing bio-oil and biochar. Biofuels Bioprod. Biorefin. 3, 547–562. Laird, D.A., Fleming, P., Davis, D.D., Horton, R., Wang, B.Q., Karlen, D.L., 2010. Impact of biochar amendments on the quality of a typical Midwestern agricultural soil. Geoderma 158, 443–449. Lehrsch, G.A., 1998. Freeze-thaw cycles increase near-surface aggregate stability. Soil Sci. 163, 63–70. Lehrsch, G.A., Sojka, R.E., Carter, D.L., Jolley, P.M., 1991. Freezing effects on aggregate stability affected by texture, mineralogy, and organic matter. Soil Sci. Soc. Am. J. 55, 1401–1406. Liu, H.Y., Yang, Y., Zhang, K.L., Sun, C.L., 2017. Soil erosion as affected by freeze-thaw

regime and initial soil moisture content. Soil Sci. Soc. Am. J. 81, 459–467. Liu, Y.X., Lonappan, L., Brar, S.K., Yang, S.M., 2018. Impact of biochar amendment in agricultural soils on the sorption, desorption, and degradation of pesticides: a review. Sci. Total Environ. 645, 60–70. Nelissen, V., Rutting, T., Huygens, D., Staelens, J., Ruysschaert, G., Boeckx, P., 2012. Maize biochars accelerate short-term soil nitrogen dynamics in a loamy sand soil. Soil Biol. Biochem. 55, 20–27. Oztas, T., Fayetorbay, F., 2003. Effect of freezing and thawing processes on soil aggregate stability. Catena 52, 1–8. Prieme, A., Christensen, S., 2001. Natural perturbations, drying-wetting and freezingthawing cycles, and the emission of nitrous oxide, carbon dioxide and methane from farmed organic soils. Soil Biol. Biochem. 33, 2083–2091. Singh, B.P., Hatton, B.J., Singh, B., Cowie, A.L., Kathuria, A., 2010. Influence of biochars on nitrous oxide emission and nitrogen leaching from two contrasting soils. J. Environ. Qual. 39, 1224–1235. Sjursen, H., Michelsen, A., Holmstrup, M., 2005. Effects of freeze-thaw cycles on microarthropods and nutrient availability in a sub-Arctic soil. Appl. Soil Ecol. 28, 79–93. Song, C., Zhang, J., Wang, Y., Wang, Y., Zhao, Z., 2006. Emission of CO2, CH4, and N2O from freshwater marsh during freeze-thaw period in Northeast of China. Atmos. Environ. 40, 6879–6885. Song, Y., Zou, Y.C., Wang, G.P., Yu, X.F., 2017. Stimulation of nitrogen turnover due to nutrients release from aggregates affected by freeze-thaw in wetland soils. Phys. Chem. Earth 97, 3–11. Urakawa, R., Shibata, H., Kuroiwa, M., Inagaki, Y., Tateno, R., Hishi, T., Fukuzawa, K., Hirai, K., Toda, H., Oyanagi, N., Nakata, M., Nakanishi, A., Fukushima, K., Enoki, T., Suwa, Y., 2014. Effects of freeze-thaw cycles resulting from winter climate change on soil nitrogen cycling in ten temperate forest ecosystems throughout the Japanese archipelago. Soil Biol. Biochem. 74, 82–94. Watanabe, T., Tateno, R., Imada, S., Fukuzawa, K., Isobe, K., Urakawa, R., Oda, T., Hosokawa, N., Sasai, T., Inagaki, Y., Hishi, T., Toda, H., Shibata, H., 2019. The effect of a freeze-thaw cycle on dissolved nitrogen dynamics and its relation to dissolved organic matter and soil microbial biomass in the soil of a northern hardwood forest. Biochemistry 142, 319–338. Wei, X., Huang, C.H., Wei, N., Zhao, H.C., He, Y., Wu, X.D., 2019. The impact of freezethaw cycles and soil moisture content at freezing on runoff and soil loss. Land Degrad. Dev. 30, 515–523. Yang, Z., Gao, J., Yang, M., Sun, Z.Z., 2016. Effects of freezing intensity on soil solution nitrogen and microbial biomass nitrogen in an alpine grassland ecosystem on the Tibetan Plateau, China. J. Arid Land 8, 749–759. Zhang, Z., Ma, W., Feng, W.J., Xiao, D.H., Hou, X., 2016. Reconstruction of soil particle composition during freeze-thaw cycling: a review. Pedosphere 26, 167–179. Zheng, H., Wang, Z., Deng, X., Zhao, J., Luo, Y., Novak, J., Herbert, S., Xing, B., 2013. Characteristics and nutrient values of biochars produced from giant reed at different temperatures. Bioresour. Technol. 130, 463–471. Zwieten, L.V., Kimber, S., Morris, S., Chan, K.Y., Downie, A., Rust, J., Joseph, S., Cowie, A., 2010. Effects of biochar from slow pyrolysis of papermill waste on agronomic performance and soil fertility. Plant Soil 327, 235–246.

467