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Soil nitrogen mineralization in a wind-disturbed area on Changbai Mountain after 30 years of vegetation restoration
Acta Ecologica Sinica 37 (2017) 265–271
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Soil nitrogen mineralization in a wind-disturbed area on Changbai Mountain after 30 years of vegetation restoration Fangfang Ma a,b, Xiang Jia a,b, Wangming Zhou a, Li Zhou a,⁎, Dapao Yu a, Yingying Meng c, Limin Dai a a b c
Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang 110016, China University of Chinese Academy of Sciences, Beijing 100049, China China Science Publishing & Media Ltd, Shenyang 110016, China
a r t i c l e
i n f o
Article history: Received 20 November 2015 Received in revised form 1 April 2016 Accepted 5 July 2016
Keywords: Wind disturbance Vegetation restoration Carbon and nitrogen content Nitrogen mineralization Changbai Mountain
a b s t r a c t Wind-disturbed (1986) and undisturbed primary forest areas (controls) on Changbai Mountain (China) were studied to compare levels of soil nitrogen mineralization. Soil samples were collected at 0–10 cm (topsoil) and 10–20 cm (subsoil) depths from the vegetation zones of a broadleaf Korean pine forest (BKPF), spruce-fir forest (SFF), and an Erman's birch forest (EBF) at different altitudes. Nitrogen status and mineralization characteristics were studied in the soil samples from a wind-disturbed area where vegetation cover has been restored after 30 years of regrowth. Soil organic carbon (SOC) and total nitrogen (TN) contents in the topsoil layer of the three vegetation types were significantly higher than in the subsoil layer. SOC and TN contents in the topsoil layer increased, and soil C/N ratio significantly decreased with increasing altitude. No significant differences in SOC, TN or pH were detected in the wind-disturbed and control area soils of BKPF and EBF. SOC and TN levels in the subsoil layer of SFF were significantly higher in wind-disturbed than in control areas. The topsoil C/N ratios of BKPF and SFF were significantly higher in the control area vs. the wind-disturbed area. After 21 d incubation, − inorganic nitrogen contents (ammonium nitrogen NH+ 4 -N and nitrate nitrogen NO3 -N) in the soils of BKPF, SFF and EBF increased in both the wind-disturbed and control areas. Ammonium nitrogen (NH+ 4 -N) was the primary inorganic form of nitrogen. The changes in the amount of NH+ 4 -N formed from ammonification contributed to the 57.1–76.2% total amount of nitrogen mineralized (net nitrogen mineralization) and the net nitrogen mineralization rate. The nitrogen mineralization process was mainly the result of net ammonification. Correlation analysis on the soil nitrogen mineralization rate and chemical properties showed that the ammonification rate had strong positive correlation with SOC and the C/N ratio. Nitrification rate was highly correlated with SOC and TN contents, as well as soil pH. Net nitrogen mineralization rate was significantly correlated with SOC and TN contents, C/N ratio, and soil pH. Multiple comparisons analysis of variance (ANOVA) demonstrated that soil nitrogen mineralization was greatly influenced by vegetation type, soil depth, and wind disturbance in the forest soils at different altitudes. Net ammonification and net nitrogen mineralization were significantly affected by wind disturbance. The vegetation cover has undergone restoration for nearly 30 years in the wind-disturbed area on Changbai Mountain, but our data demonstrate that differences in soil quality between primary forest and wind-disturbed areas remain significant due to the different vegetation types. © 2017 Published by Elsevier B.V. on behalf of Ecological Society of China.
Nitrogen is one of the most critical elements in the soils of terrestrial ecosystems affecting plant growth and net primary productivity [1–2]. The majority of available nitrogen for plant uptake is in the inorganic − forms (NH+ 4 -N and NO3 -N) [3]. However, 92–98% of nitrogen in the soil exists in organic forms. Thus, nitrogen mineralization, through which the soil organic nitrogen is converted to inorganic forms, directly impacts the ability of the soil to supply nitrogen for plant utilization [4– 6]. Organic nitrogen mineralization is primarily ammonification and nitrification. Mediated by soil microbes, nitrogen conversion from organic ⁎ Corresponding author. E-mail address: [email protected] (L. Zhou).
http://dx.doi.org/10.1016/j.chnaes.2017.02.011 1872-2032/© 2017 Published by Elsevier B.V. on behalf of Ecological Society of China.
matter to inorganic forms occurs in the nitrogen mineralization process [7]. Factors reflecting soil quality such as land use, physical and chemical properties of soil, soil pH, temperature and moisture, vegetation type, the amount and quality of vegetation litter, as well as natural and human disturbances, which affect microbial genera and activity, ultimately contribute to the soil nitrogen mineralization process [8–9]. In addition, the characteristics of nitrogen mineralization are a key indicator of soil quality. Wind is the most common disturbance agent in forest ecosystems. Many studies have reported detrimental impacts of wind in disturbed areas of forests. These include effects on tree growth and shape, forest regeneration, forest community structure and composition, and
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diversity of forest species [10–12]. Soil nutrient cycling can be affected by the changes in microclimate and the amount and quality of vegetation litter. Studies on the changes in soil nutrients and nitrogen mineralization rates in wind-disturbed areas with different forest types help us understand how to better maintain productivity and nutrient cycling in forest ecosystems [13]. In 1980s, a rare typhoon destroyed the plant communities within the nature reserve on the west and southwest slopes of Changbai Mountain, China. The forests in the wind-disturbed areas were almost completely gone after removal of the damaged trees. The vegetation in the wind-disturbed areas has recovered to great extent after nearly 30 years of regrowth [12,14]. However, the status and conversion characteristics of soil nutrients within the restored areas have not been studied. A wind-disturbed area in the Changbai Mountain nature reserve was selected as a soil investigation site to conduct comparative evaluations on the physical and chemical properties of different forest soils, and the soil characteristics of organic nitrogen mineralization. Our aim was to provide evidence for evaluating the restoration of the wind-disturbed area on Changbai Mountain.
1.2. Methods 1.2.1. Site selection and sample collection Three forest types (BKPF, SFF, and EBF) on Changbai Mountain were chosen along an altitudinal gradient as representatives of the vegetated areas. Investigation sites were located in the winddisturbed and undisturbed primary forest areas. A total of 3–5 replicates were prepared for each site. The distance between any two sites was N20 m. The dimensions of each site were 30 m × 30 m. At each site, 5 sampling locations were randomly selected. Soil samples were collected at 0–10 cm and 10–20 cm depths, respectively. Samples collected at the same depth from the same site were mixed into one large sample, placed into a reclosable bag, and immediately sent to laboratory for study. Each fresh soil sample obtained was divided into two parts. One part of the sample was air-dried and used for measuring soil organic carbon (SOC), total nitrogen (TN) content, and soil pH. The second portion of the soil sample was stored in a refrigerator at 4 °C prior to evaluation of soil mineralization content and use in an indoor incubation experiment.
1. Soil study site and methods 1.1. Site description The wind-disturbed area is located within nature reserves on the west and southwest slopes of Changbai Mountain (41°52′40″–42°01′ 10″ N, 127°53′37″–128°02′00″ E). The area is 15.75 km long (N-S) and 11.75 km wide (E-W). The wind-disturbed area is at altitudes ranging from 1050 to 1700 m, and spans three types of forest zones including broadleaf Korean pine forest (BKPF), spruce-fir forest (SFF), and Erman's birch forest (EBF) [15]. The main types of soil in these three forest zones are dark brown soil, brown coniferous soil, and subalpine meadow soil [16]. The average yearly temperature is 3.3 °C, the highest monthly temperature is 19.3 °C, and the lowest monthly temperature is −16.2 °C. Mean annual precipitation is 800 mm [17]. Significant changes have occurred in the vegetation communities of the wind-disturbed area after nearly 30 years of restoration growth. The original BKPF zone (1100–1300 m) that was comprised of Pinus koraiensis Sieb. Et Zucc. and broadleaf forest was replaced by a poplar forest, which includes Populus davidiana and Betula platyphylla. Few trees remained in the wind-disturbed coniferous forest zone (1300– 1500 m), which originally consisted of Picea jezoensis and Abies nephrolepis. The disturbed forest zone was replaced by herbaceous plants such as Cinnamomum camphora. The original SFF (1500– 1700 m) was replaced by a mixed forest with Larix olgensis and Betula ermanii (see Table 1) [12,14,16].
1.2.2. Analysis and measurement Soil pH was measured using a PHS-3C pH meter (Shanghai Leici). SOC was studied using the auto analyzer of a vario MICRO cube (Eelementar, Germany). To measure TN content, soil samples were first treated with the H2SO4-H2O2 Kjeldahl digestion method and then analyzed using a continuous flow analyzer (AutoAnalyzer III, Bran + Luebbe Gmbh, Germany). The level of soil nitrogen mineralization was determined using an indoor soil incubation method under an oxygen supply according to the following procedure: roots and stones in the soil samples were removed and the soils were sieved using a 4 mm opening size screen. Triplicate samples of sieved soil containing 20 g of air-dried material were then treated with water to adjust the soil moisture content to 60% of the water holding capacity. The resulting samples were then transferred to 150 ml flasks. The flasks were sealed with plastic wraps with a few pin holes on them to ensure a continuous supply of oxygen and minimal water evaporation. These samples were incubated at 20 °C for 21 d. At 21 d, the samples were removed from the incubator and 100 ml of a 2 mol/l KCl solution was added to each flask. The capped flasks were placed into a shaker after KCl treatment. The samples were then filtered − after shaken for 1 h. The NH+ 4 -N and NO3 -N contents in the extracted liquid were measured using a continuous flow AutoAnalyzer 3. Soil ammonification and nitrification rates were calculated based on − the differences in the concentration of NH+ 4 -N and NO3 -N in the incubated and initial soil samples. Net nitrogen mineralization rate is
Table 1 Investigation site overview. Forest types
Altitude/m
BKPF
1100–1300 Dark brown soil
SFF
EBF
Soil types
1300–1500 Brown coniferous soil
1500–1700 Subalpine meadow soil
Disturbance Slope Aspect types CA
7.8°
WDA
9.3°
CA
14.8°
WDA
13.6°
CA
4.5°
WDA
4.9°
WN 23.6° WN 18.9° WS 30.2° WS23.8° WS 17.9° WS 23.7°
Main vegetation type Tree layer
Shrub layer
Abies nephrolepis, Pinus koraiensis, Tilia amurensis, Quercus mongolica Betula platyphylla, Larix olgensis, Abies nephrolepis, Populus davidiana Abies nephrolepis, Larix olgensis, Picea jezoensis Abies nephrolepis, Betula ermanii, Picea jezoensis Betula ermanii, Larix olgensis
Acanthopanax senticosus, Acer tschonoskii, Acer ukurunduense, Lonicera chrysantha Acer ukurunduense, Actinidia kolomikta, Acer tegmentosum Vaccinium uliginosum, Lonicera edulis
Betula ermanii
Rubus matsumuranus, Rosa marretii, Lonicera edulis Lonicera edulis, Rubus matsumuranus Vaccinium uliginosum, Lonicera edulis, Rubus matsumuranus, Potentilla fruticosa
Notes: BKPF: broadleaved Korean pine forest; SFF: spruce-fir forest; EBF: Erman's birch forest; CA: control area; WDA: wind disturbed area.
F. Ma et al. / Acta Ecologica Sinica 37 (2017) 265–271 − defined as the change in inorganic nitrogen (NH+ 4 -N and NO3 -N) per time unit [3].
1.3. Statistical analysis Excel 2007 and SPSS 19.0 (SPSS Inc., 2004) were used for data processing and statistical analysis. t-Tests were used to determine the significance of differences between two variables. One-way analysis of variance (ANOVA) was used to compare the significance of differences between the means of three variables. Multiple comparisons analysis of variance (ANOVA) was used to detect the significance of differences among the factors such as wind disturbance, forest type, soil depth, as well as the effects of the interactions among the three factors on the amount of net nitrogen mineralization, net nitrification, and net ammonification (α = 0.05). Correlation analysis was used to measure the correlations between variables such as soil mineralization rate, soil nutrient contents, and soil pH. Origin 8.5 was used for plotting data. 2. Results 2.1. Physical and chemical properties of soil In the BKPF, SFF, and EBF, the SOC and TN contents were higher at the 0–10 cm soil depth than at the 10–20 cm depth in both the control and wind-disturbed areas (Table 2). At 0–10 cm, however, the SOC content of BKPF was significantly lower than that of EBF. The TN contents of both BKPF and SFF soils were significantly lower than that of EBF in the control area. The TN content increased with increasing altitude in the wind-disturbed area. Differences in TN content in the BKPF and EBF soils were significant. At 10–20 cm, no significant differences were found in SOC and TN contents among BKPF, SFF, and EBF with increasing altitude in the wind-disturbed area, but the soil TN content of SFF was lower than that of EBF in the control area. Among the three forest types, only the SOC and TN contents of SFF were significantly different between the control and wind-disturbed areas at 10–20 cm. C/N ratios declined with increasing altitude at both 0–10 cm and 10– 20 cm soil depths in the control and the wind-disturbed areas. The soil C/N ratios of BKPF and SFF were higher than that of EBF (Table 2). At 0– 10 cm, the C/N ratios of BKPF and SFF were considerably higher in the control area than that in the wind-disturbed area. At 10–20 cm, no significant differences in the C/N ratios were found among BKPF, SFF, and EBF in both the control and wind-disturbed areas. The soil pH values of the three forest types were significantly lower at 0–10 cm than those at 10–20 cm. However, the differences in the soil pH of BKPF, SFF, and EBF between the control and wind-disturbed areas were not significant.
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2.2. Characteristics of nitrogen mineralization in soil 2.2.1. Characteristics of inorganic nitrogen content in soil Inorganic nitrogen (ammonium nitrogen and nitrate nitrogen) contents in all BKPF, SFF, and EBF soils increased in both the control and wind-disturbed areas after 21 d incubation (Fig. 1). These results showed clear trends toward ammonium nitrogen (NH+ 4 -N) and nitrate nitrogen (NO− 3 -N) contents in the incubated soils of BKPF, SFF, and EBF at 0–10 cm soil depth in both the control and wind-disturbed areas. The soil NH+ 4 -N content of EBF was highest, BKPF was next, and SFF was lowest. The soil NO− 3 -N content of BKPF was highest, EBF was next, and SFF was lowest. The difference between any two of the three types of forest soils was significant. At 10–20 cm in the control area, − NH+ 4 -N and NO3 -N contents in the incubated soil of EBF were significantly higher than those of BKPF and SFF. In the wind-disturbed area, the differences in NH+ 4 -N content in the incubated soils of BKPF, SFF, and EBF were not significant. In comparison, the soil NO− 3 -N contents of BKPF and SFF were lower than those of EBF. Fig. 1 shows the differences in inorganic nitrogen content between the original and incubated soil samples at different soil depths in both the control and wind-disturbed areas. At 0–10 cm, the inorganic nitrogen content in the original soil of EBF was significantly higher in the control area than in the winddisturbed area, whereas the inorganic nitrogen content in the incubated soil of BKPF in the control area was significantly higher than in the wind-disturbed area. Similarly, at 10–20 cm, the inorganic nitrogen content in the initial soil of EBF was much higher in the control area than in the wind-damaged area, whereas the inorganic nitrogen contents in the incubated soils of BKPF, SFF, and EBF in the control area were significantly higher than in the wind-disturbed area. 2.2.2. Characteristics of nitrogen mineralization rate in soil The net ammonification rates of BKPF and EBF soils were significantly higher at 0–10 cm than at 10–20 cm, but the difference in the soil nitrogen mineralization rate of SFF between the two soil depths was minimal. At 0–10 cm in the control area, the soil net nitrification rates of the three types of forests were 0.73 ± 0.067 mg·kg−1·d−1 (SFF), 2.12 ± 0.29 mg·k− 1·d− 1 (EBF), and 2.53 ± 0.98 mg·kg− 1·d− 1 (BKPF), respectively. The results indicate that the soil net nitrogen mineralization rate of SFF was significantly lower than the rates of BKPF and EBF. In the wind-disturbed area, the soil net nitrogen mineralization rates of BKPF, SFF, and EBF ranged from 0.88 to 1.347 mg·kg−1·d−1 and the differences between them were not significant. At 10–20 cm, the soil net nitrogen mineralization rates of BKPF, SFF, and EBF ranged from 0.75 to 0.94 mg·kg−1·d−1. t-Test results revealed a significant difference in the soil nitrogen mineralization rate of BKPF between the control and wind-disturbed areas at 0–10 soil depth. The results also showed that the difference in the soil nitrogen mineralization rates of SFF and EBF between the two areas were not significant. The net
Table 2 Soil chemical properties. Forest types
Soil depth
Disturbance types
C content (g∙kg−1)a
N content (g∙kg−1)a
C:Na
pHa
BKPF
0–10 cm
CA WDA CA WDA CA WDA CA WDA CA WDA CA WDA
51.99 39.70 25.62 29.11 59.23 54.61 19.55 30.87 69.05 62.43 22.68 26.04
2.87 2.68 1.71 2.27 3.85 4.13 1.57 2.47 6.08 5.46 2.24 2.37
18.15 ± 1.12Aa 14.68 ± 1.20Ba 14.96 ± 0.32a 12.79 ± 0.58 15.36 ± 0.69Ab 13.22 ± 0.46Bb 12.45 ± 0.56b 12.47 ± 0.23 11.30 ± 0.48c 11.57 ± 0.31c 9.97 ± 0.48c 11.03 ± 0.40
5.09 4.92 5.42 5.57 4.54 4.92 5.11 5.42 4.66 4.53 5.32 5.30
10–20 cm SFF
0–10 cm 10–20 cm
EBF
0–10 cm 10–20 cm
± ± ± ± ± ± ± ± ± ± ± ±
6.03b 11.59b 1.22 3.55 8.37ab 2.37ab 4.30B 3.98A 2.48a 4.30a 2.81 1.98
± ± ± ± ± ± ± ± ± ± ± ±
0.29b 0.61b 0.06ab 0.18 0.43b 0.16ab 0.32Bb 0.30A 0.09a 0.42a 0.17a 0.17
± ± ± ± ± ± ± ± ± ± ± ±
0.10a 0.20a 0.03 0.14 0.34b 0.10a 0.29 0.08 0.01b 0.13b 0.04 0.21
Notes: different lowercase letters represent significant differences among BKPF, SFF, and EBF within the same area. Different capital letters represent significant differences between winddisturbed and control areas with same forest type. CA: control area; WDA: wind disturbed area. a Mean ± SE.
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Inorganic N content/(mg.kg -1)
240
180
EBF
*
120
* *
60
0 CA
WDA
WDA
CA
10-20 cm
0-10 cm
Fig. 1. Nitrogen mineralization of soil in control and wind-disturbed areas. Notes: broadleaved Korean pine forest (BKPF); spruce-fir forest (SFF); Erman's birch forest (EBF); * represents a significant (p b 0.05) difference between wind-disturbed and control areas. CA: control area; WDA: wind disturbed area.
ammonification process played a key role in the soil nitrogen mineralization process of the three forest types (Fig. 2).
nitrogen mineralization were significant and highly significant on the net nitrification. The analysis further indicated that the interaction effects between the wind disturbance and forest type and among the wind disturbance, forest type, as well as soil depth on the net ammonification, net nitrification, and net nitrogen mineralization were not significant. Among the factors analyzed, the influences of wind disturbance and soil depth on net ammonification and nitrogen mineralization were much greater than those of forest type. The soil depth, forest type, and the interaction between the two factors had greater effects on the net nitrification than the wind disturbance (see Table 3). Soil nutrients increased nitrogen conversion in the soils (Fig. 3). The ammonification rate was positively correlated with SOC and C/N ratios but not significantly correlated with TN content. The nitrification rate had highly significant correlations with SOC and TN contents but nonsignificant correlation with C/N ratios. The nitrogen mineralization rate was greatly influenced by SOC, TN content and C/N ratios. The ammonification, nitrification, and nitrogen mineralization rates were all negatively correlated with soil pH. The correlation between the nitrification rate and soil pH was significant as was the correlation between and the nitrogen mineralization rate and pH. 3. Discussion
2.3. Factors affecting soil nitrogen mineralization
3.1. Effects of restored vegetation on the physical and chemical properties of soil in the wind-disturbed area
Multiple comparisons ANOVA showed the highly significant influence of wind disturbance and soil depth on net ammonification and nitrogen mineralization. The analysis also demonstrated that soil depth and forest type had significant influences on net nitrification. The effects of the interaction between the wind disturbance and forest type on the net ammonification and nitrogen mineralization were significant but not significant on the net nitrification. The impacts of the interaction between the soil depth and forest type on the net ammonification and
After the destructive effects of typhoon exposure, significant changes in the vegetation types and community structure occurred in the wind-disturbed area on Changbai Mountain [12,14,16]. However, no significant differences in SOC and TN contents were observed between the control and wind-disturbed areas (Table 2), indicating that the SOC and TN contents in the wind-disturbed soil were essentially the same as in the undisturbed primary forest soil. Similar observations have been made by some researchers [18–21], but different findings
4 Nitrification rate Ammonification rate
BKPF 3
*
2
* 1
0 CA
0-10 cm
3
2
1
0
CA
WDA
SFF Nitrogen mineralization rate /(mg.kg-1.d-1)
Nitrogen mineralization rate (mg.kg-1.d-1)
4
WDA
CA
Nitrogen mineralization rate /(mg.kg-1.d-1)
4
WDA
0-10 cm
10-20 cm
CA
WDA
10-20 cm
EBF
3
2
1
0 CA
WDA
0-10 cm
CA
WDA
10-20 cm
Fig. 2. Net nitrogen mineralization rate of soil in control and wind-disturbed areas. Notes: broadleaved Korean pine forest (BKPF); spruce-fir forest (SFF); Erman's birch forest (EBF); * represents a significant (p b 0.05) difference between wind-disturbed and control areas. CA: control area; WDA: wind disturbed area.
F. Ma et al. / Acta Ecologica Sinica 37 (2017) 265–271
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Table 3 Multi comparisons ANOVA on net nitrogen, net ammonification, and net nitrification. Influence factors
Wind disturbance Soil depth Forest type Wind disturbance ∗ soil depth Wind disturbance ∗ forest type Soil depth ∗ forest type Wind disturbance ∗ soil depth ∗ forest type
Ammonification contents (Aamm)
Nitrification contents (Anit)
Net N mineralization contents (Amin)
F
P
F
P
F
P
14.004 13.160 2.736 0.959 5.116 3.523 1.431
0.001⁎⁎ 0.001⁎⁎
1.515 34.721 11.752 1.222 1.713 8.892 2.646
0.230 b0.001⁎⁎ b0.001⁎⁎ 0.280 0.202 0.001⁎⁎
14.838 27.014 3.323 1.567 5.762 5.606 1.215
0.001⁎⁎ b 0.001⁎⁎ 0.053 0.223 0.009⁎⁎ 0.01⁎
0.085 0.337 0.014⁎ 0.046⁎ 0.259
0.092
0.314
⁎ Significant at P ≤ 0.05 level. ⁎⁎ Significant at P ≤ 0.01 level.
have been reported by others. Carbon and nitrogen stocks in soil declined due to the conversion of primary forest to secondary forest and grassland after wind disturbance [22–25]. Discrepancy between observations could be related to the duration of forest restoration. Most studies on wind disturbance effects were conducted approximately 10 years after forest disturbance. This is a relatively short period for the restoration of disturbed vegetation. The present study showed that the soil nutrient levels in the typhoon-disturbed vegetation areas were essentially restored to those found in the undisturbed forest ecosystem on Changbai Mountain after 30 years of regrowth. The carbon-to-nitrogen ratio (C/N) is a key indicator used to identify soil quality change. Reduction in the C/N ratio is a gauge of accelerated organic matter decomposition [26]. The C/N ratios declined after wind disturbance, indicating more rapid soil nutrient decomposition in the wind-disturbed area than in the control area (Table 2). Increased soil temperatures caused by reduced vegetation cover in the wind-disturbed area may have facilitated organic matter decomposition in the soil with the consequent decrease in the C/N ratios [27]. At 0–10 cm soil depth, the soil C/N ratios of BKPF and SFF were significantly different
2 1 0 10
20
30
40
50
Fig. 1 illustrates that NH+ 4 -N stock in all the BKPF, SFF, and EBF soils was higher than NO− 3 -N stock in both the control and wind-disturbed areas. This suggests that NH+ 4 -N was the primary inorganic form of nitrogen in the forest soil of Changbai Mountain. These results are consistent with previous research [6,28]. The changes in the amount of NH+ 4 -N formed from ammonification, which contributed to the 57.1–76.2%
4
Ammonification rate P=0.012 Nitrification rate P=0.000 Mineralization rate P=0.001
3
3.2. Ammonium was the primary inorganic form of nitrogen in forest soil (NH+ 4 -N)
Mineralization rates/(mg.kg -1.d-1)
Mineralization rates/(mg.kg -1.d-1)
4
in both the control and wind-disturbed areas (Table 2), possibly related to the varying vegetation types. In the wind-disturbed area, primary BKPF was replaced by a secondary poplar forest, and the spruce-fir forest was mostly replaced by herbaceous plants such as Cinnamomum camphora. The vegetation litter in the area was mainly derived from broadleaf and herbaceous plants. The decreased C/N ratios of the soil litter layer primarily led to C/N ratio decreases in the disturbed soil. Compared to soil SOC and TN contents, C/N ratios appeared to more accurately reflect the effects of vegetation change on soil quality.
60
70
Ammonification rate P=0.087 Nitrification rate P=0.000 Mineralization P=0.003
3 2 1 0
80
1
3
4
5
6
7
·
·
4
4 Ammonification rate P =0.013 Nitrification rate P =0.753 Mineralization rate P =0.035
3
Mineralization rates/(mg.kg-1.d -1)
Mineralization rates/(mg.kg-1.d -1)
2
Nitrogen content/ (g.kg-1)
Carbon content/(g.kg-1)
2
1
0 8
10
12
14
C:N
16
18
20
Ammonification rate P =0.182 Nitrification rate P =0.000 Mineralization rate P =0.020
3
2
1
0 4.0
4.5
5.0
pH
Fig. 3. Correlation analysis between nitrogen mineralization rate and soil chemical properties.
5.5
6.0
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amount of nitrogen mineralized (nitrogen mineralization) and net nitrogen mineralization rate, primarily resulted in alterations in the nitrogen mineralization and net nitrogen mineralization rate in the three types of forest soils. Nitrogen mineralization was mainly the result of the ammonification process. The reasons that nitrification was not as dominant as ammonification were mostly due to the strong effect of forest soil pH. Table 2 shows that the soils in the vegetation zones of BKPF, SFF, and EBF were acidic. Generally, the optimal pH for soil nitrifying bacteria is near 8 and nitrification is inhibited by greater acidity. A low pH would reduce the solubility of soil organic matter and inhibit nitrifying bacteria growth. As a result, the nitrification process in the soil was − retarded and NH+ 4 -N content was higher than NO3 -N content [29]. Further, the nitrification process in the forest soil was usually limited by the amount of NH+ 4 -N formed from ammonification. The nitrification rate would therefore be lower than ammonification rate [30]. 3.3. Factors affecting soil nitrogen mineralization The forest types appeared to exert significant effects on the net nitrification, whereas they had no significant impact on net ammonification and TN mineralization. The interactions among the forest type, wind disturbance, and soil depth had great influences on net ammonification, net nitrification, and net TN mineralization. These results suggest that the differences in nitrogen mineralization in the BKPF, SFF, and EBF soils mainly resulted from the forest types, a finding consistent with other studies [31–33]. Table 2 shows that the differences in the net nitrogen mineralization between 0–10 cm and 10–20 cm depths were significant in both the control and wind-disturbed areas. At 0–20 cm, the net nitrogen mineralization rates of BKPF and EBF soils decreased as soil depth increased. Soil permeability may have slowly declined with increasing soil depth, resulting in aging of soil organic matter and reduced decomposition. The organic matter available for degradation and plant uptake would gradually decrease and microbial populations and their activity would have been reduced. These factors could lead to a decrease in the nitrogen mineralization rate [34–35]. In contrast, the soil mineralization rate of SFF was greater at 10–20 cm soil depth in the control area, possibly due to the higher SOC in the forest soil at the 10–20 cm depth. Comparative studies were performed on the nitrogen mineralization and net nitrogen mineralization rate in the three types of forest soils in both the control and wind-disturbed areas. The net ammonification, net nitrification, and net nitrogen mineralization rates of BKPF and EBF soils were higher in the control area than in the wind-disturbed area (Fig. 2). Correlation analysis indicated that SOC and TN contents, and C/N ratio had significant effects on soil ammonification, nitrification, and nitrogen mineralization rates (Fig. 3). The potential of fertile soil nitrogen mineralization may have been greater than that in infertile soil [36]. Multiple comparisons ANOVA showed that wind disturbance exerted a highly significant influence on the net ammonification and nitrogen mineralization. In addition, the effects of the interaction between the wind disturbance and forest type on the net ammonification were significant and highly significant, respectively, on the net nitrogen mineralization. The studies demonstrated, overall, that the nitrogen mineralization process in the forest soils remained affected by wind disturbance although the vegetation zones in the typhoon-disturbed area within the Changbai Mountain nature reserve have been undergoing restoration for 30 years. 4. Conclusions (1) SOC, TN, and pH in the BKPF and EBF soils were similar in both the control and wind-disturbed areas and this was also true for the SFF topsoil. However, the C/N ratios of BKPF and SFF topsoil in the control area were significantly higher than in the wind-disturbed area, indicating differences in the nutrient supply of available carbon and nitrogen to the forests, due to the changes in vegetation type in the wind-disturbed
area. Compared to SOC and TN contents, the C/N ratio is a more sensitive index of the effect of vegetation changes on soil quality. (2) NH+ 4 -N is the primary inorganic form of nitrogen in the forest soils. The changes in the amount of NH+ 4 -N formed from ammonification were used to characterize the 57.1%–76.2% range of the total variation in the nitrogen mineralization and net nitrogen mineralization rate. The nitrogen mineralization process was mainly the result of ammonification. The ammonification and nitrogen mineralization in the soils were regulated by pH and SOC and TN contents. (3) Forest type, soil depth, and alterations in vegetation type caused by wind disturbance exerted significant influences on organic nitrogen mineralization in the forest soils at different altitudes. Although vegetation cover in the wind-disturbed area of Changbai Mountain has largely been restored after 30 years of growth, we found significant differences in soil quality between the primary forest and wind-disturbed areas due to the varying vegetation types.
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Acta Ecologica Sinica journal homepage: www.elsevier.com/locate/chnaes
Soil nitrogen mineralization in a wind-disturbed area on Changbai Mountain after 30 years of vegetation restoration Fangfang Ma a,b, Xiang Jia a,b, Wangming Zhou a, Li Zhou a,⁎, Dapao Yu a, Yingying Meng c, Limin Dai a a b c
Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang 110016, China University of Chinese Academy of Sciences, Beijing 100049, China China Science Publishing & Media Ltd, Shenyang 110016, China
a r t i c l e
i n f o
Article history: Received 20 November 2015 Received in revised form 1 April 2016 Accepted 5 July 2016
Keywords: Wind disturbance Vegetation restoration Carbon and nitrogen content Nitrogen mineralization Changbai Mountain
a b s t r a c t Wind-disturbed (1986) and undisturbed primary forest areas (controls) on Changbai Mountain (China) were studied to compare levels of soil nitrogen mineralization. Soil samples were collected at 0–10 cm (topsoil) and 10–20 cm (subsoil) depths from the vegetation zones of a broadleaf Korean pine forest (BKPF), spruce-fir forest (SFF), and an Erman's birch forest (EBF) at different altitudes. Nitrogen status and mineralization characteristics were studied in the soil samples from a wind-disturbed area where vegetation cover has been restored after 30 years of regrowth. Soil organic carbon (SOC) and total nitrogen (TN) contents in the topsoil layer of the three vegetation types were significantly higher than in the subsoil layer. SOC and TN contents in the topsoil layer increased, and soil C/N ratio significantly decreased with increasing altitude. No significant differences in SOC, TN or pH were detected in the wind-disturbed and control area soils of BKPF and EBF. SOC and TN levels in the subsoil layer of SFF were significantly higher in wind-disturbed than in control areas. The topsoil C/N ratios of BKPF and SFF were significantly higher in the control area vs. the wind-disturbed area. After 21 d incubation, − inorganic nitrogen contents (ammonium nitrogen NH+ 4 -N and nitrate nitrogen NO3 -N) in the soils of BKPF, SFF and EBF increased in both the wind-disturbed and control areas. Ammonium nitrogen (NH+ 4 -N) was the primary inorganic form of nitrogen. The changes in the amount of NH+ 4 -N formed from ammonification contributed to the 57.1–76.2% total amount of nitrogen mineralized (net nitrogen mineralization) and the net nitrogen mineralization rate. The nitrogen mineralization process was mainly the result of net ammonification. Correlation analysis on the soil nitrogen mineralization rate and chemical properties showed that the ammonification rate had strong positive correlation with SOC and the C/N ratio. Nitrification rate was highly correlated with SOC and TN contents, as well as soil pH. Net nitrogen mineralization rate was significantly correlated with SOC and TN contents, C/N ratio, and soil pH. Multiple comparisons analysis of variance (ANOVA) demonstrated that soil nitrogen mineralization was greatly influenced by vegetation type, soil depth, and wind disturbance in the forest soils at different altitudes. Net ammonification and net nitrogen mineralization were significantly affected by wind disturbance. The vegetation cover has undergone restoration for nearly 30 years in the wind-disturbed area on Changbai Mountain, but our data demonstrate that differences in soil quality between primary forest and wind-disturbed areas remain significant due to the different vegetation types. © 2017 Published by Elsevier B.V. on behalf of Ecological Society of China.
Nitrogen is one of the most critical elements in the soils of terrestrial ecosystems affecting plant growth and net primary productivity [1–2]. The majority of available nitrogen for plant uptake is in the inorganic − forms (NH+ 4 -N and NO3 -N) [3]. However, 92–98% of nitrogen in the soil exists in organic forms. Thus, nitrogen mineralization, through which the soil organic nitrogen is converted to inorganic forms, directly impacts the ability of the soil to supply nitrogen for plant utilization [4– 6]. Organic nitrogen mineralization is primarily ammonification and nitrification. Mediated by soil microbes, nitrogen conversion from organic ⁎ Corresponding author. E-mail address: [email protected] (L. Zhou).
http://dx.doi.org/10.1016/j.chnaes.2017.02.011 1872-2032/© 2017 Published by Elsevier B.V. on behalf of Ecological Society of China.
matter to inorganic forms occurs in the nitrogen mineralization process [7]. Factors reflecting soil quality such as land use, physical and chemical properties of soil, soil pH, temperature and moisture, vegetation type, the amount and quality of vegetation litter, as well as natural and human disturbances, which affect microbial genera and activity, ultimately contribute to the soil nitrogen mineralization process [8–9]. In addition, the characteristics of nitrogen mineralization are a key indicator of soil quality. Wind is the most common disturbance agent in forest ecosystems. Many studies have reported detrimental impacts of wind in disturbed areas of forests. These include effects on tree growth and shape, forest regeneration, forest community structure and composition, and
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diversity of forest species [10–12]. Soil nutrient cycling can be affected by the changes in microclimate and the amount and quality of vegetation litter. Studies on the changes in soil nutrients and nitrogen mineralization rates in wind-disturbed areas with different forest types help us understand how to better maintain productivity and nutrient cycling in forest ecosystems [13]. In 1980s, a rare typhoon destroyed the plant communities within the nature reserve on the west and southwest slopes of Changbai Mountain, China. The forests in the wind-disturbed areas were almost completely gone after removal of the damaged trees. The vegetation in the wind-disturbed areas has recovered to great extent after nearly 30 years of regrowth [12,14]. However, the status and conversion characteristics of soil nutrients within the restored areas have not been studied. A wind-disturbed area in the Changbai Mountain nature reserve was selected as a soil investigation site to conduct comparative evaluations on the physical and chemical properties of different forest soils, and the soil characteristics of organic nitrogen mineralization. Our aim was to provide evidence for evaluating the restoration of the wind-disturbed area on Changbai Mountain.
1.2. Methods 1.2.1. Site selection and sample collection Three forest types (BKPF, SFF, and EBF) on Changbai Mountain were chosen along an altitudinal gradient as representatives of the vegetated areas. Investigation sites were located in the winddisturbed and undisturbed primary forest areas. A total of 3–5 replicates were prepared for each site. The distance between any two sites was N20 m. The dimensions of each site were 30 m × 30 m. At each site, 5 sampling locations were randomly selected. Soil samples were collected at 0–10 cm and 10–20 cm depths, respectively. Samples collected at the same depth from the same site were mixed into one large sample, placed into a reclosable bag, and immediately sent to laboratory for study. Each fresh soil sample obtained was divided into two parts. One part of the sample was air-dried and used for measuring soil organic carbon (SOC), total nitrogen (TN) content, and soil pH. The second portion of the soil sample was stored in a refrigerator at 4 °C prior to evaluation of soil mineralization content and use in an indoor incubation experiment.
1. Soil study site and methods 1.1. Site description The wind-disturbed area is located within nature reserves on the west and southwest slopes of Changbai Mountain (41°52′40″–42°01′ 10″ N, 127°53′37″–128°02′00″ E). The area is 15.75 km long (N-S) and 11.75 km wide (E-W). The wind-disturbed area is at altitudes ranging from 1050 to 1700 m, and spans three types of forest zones including broadleaf Korean pine forest (BKPF), spruce-fir forest (SFF), and Erman's birch forest (EBF) [15]. The main types of soil in these three forest zones are dark brown soil, brown coniferous soil, and subalpine meadow soil [16]. The average yearly temperature is 3.3 °C, the highest monthly temperature is 19.3 °C, and the lowest monthly temperature is −16.2 °C. Mean annual precipitation is 800 mm [17]. Significant changes have occurred in the vegetation communities of the wind-disturbed area after nearly 30 years of restoration growth. The original BKPF zone (1100–1300 m) that was comprised of Pinus koraiensis Sieb. Et Zucc. and broadleaf forest was replaced by a poplar forest, which includes Populus davidiana and Betula platyphylla. Few trees remained in the wind-disturbed coniferous forest zone (1300– 1500 m), which originally consisted of Picea jezoensis and Abies nephrolepis. The disturbed forest zone was replaced by herbaceous plants such as Cinnamomum camphora. The original SFF (1500– 1700 m) was replaced by a mixed forest with Larix olgensis and Betula ermanii (see Table 1) [12,14,16].
1.2.2. Analysis and measurement Soil pH was measured using a PHS-3C pH meter (Shanghai Leici). SOC was studied using the auto analyzer of a vario MICRO cube (Eelementar, Germany). To measure TN content, soil samples were first treated with the H2SO4-H2O2 Kjeldahl digestion method and then analyzed using a continuous flow analyzer (AutoAnalyzer III, Bran + Luebbe Gmbh, Germany). The level of soil nitrogen mineralization was determined using an indoor soil incubation method under an oxygen supply according to the following procedure: roots and stones in the soil samples were removed and the soils were sieved using a 4 mm opening size screen. Triplicate samples of sieved soil containing 20 g of air-dried material were then treated with water to adjust the soil moisture content to 60% of the water holding capacity. The resulting samples were then transferred to 150 ml flasks. The flasks were sealed with plastic wraps with a few pin holes on them to ensure a continuous supply of oxygen and minimal water evaporation. These samples were incubated at 20 °C for 21 d. At 21 d, the samples were removed from the incubator and 100 ml of a 2 mol/l KCl solution was added to each flask. The capped flasks were placed into a shaker after KCl treatment. The samples were then filtered − after shaken for 1 h. The NH+ 4 -N and NO3 -N contents in the extracted liquid were measured using a continuous flow AutoAnalyzer 3. Soil ammonification and nitrification rates were calculated based on − the differences in the concentration of NH+ 4 -N and NO3 -N in the incubated and initial soil samples. Net nitrogen mineralization rate is
Table 1 Investigation site overview. Forest types
Altitude/m
BKPF
1100–1300 Dark brown soil
SFF
EBF
Soil types
1300–1500 Brown coniferous soil
1500–1700 Subalpine meadow soil
Disturbance Slope Aspect types CA
7.8°
WDA
9.3°
CA
14.8°
WDA
13.6°
CA
4.5°
WDA
4.9°
WN 23.6° WN 18.9° WS 30.2° WS23.8° WS 17.9° WS 23.7°
Main vegetation type Tree layer
Shrub layer
Abies nephrolepis, Pinus koraiensis, Tilia amurensis, Quercus mongolica Betula platyphylla, Larix olgensis, Abies nephrolepis, Populus davidiana Abies nephrolepis, Larix olgensis, Picea jezoensis Abies nephrolepis, Betula ermanii, Picea jezoensis Betula ermanii, Larix olgensis
Acanthopanax senticosus, Acer tschonoskii, Acer ukurunduense, Lonicera chrysantha Acer ukurunduense, Actinidia kolomikta, Acer tegmentosum Vaccinium uliginosum, Lonicera edulis
Betula ermanii
Rubus matsumuranus, Rosa marretii, Lonicera edulis Lonicera edulis, Rubus matsumuranus Vaccinium uliginosum, Lonicera edulis, Rubus matsumuranus, Potentilla fruticosa
Notes: BKPF: broadleaved Korean pine forest; SFF: spruce-fir forest; EBF: Erman's birch forest; CA: control area; WDA: wind disturbed area.
F. Ma et al. / Acta Ecologica Sinica 37 (2017) 265–271 − defined as the change in inorganic nitrogen (NH+ 4 -N and NO3 -N) per time unit [3].
1.3. Statistical analysis Excel 2007 and SPSS 19.0 (SPSS Inc., 2004) were used for data processing and statistical analysis. t-Tests were used to determine the significance of differences between two variables. One-way analysis of variance (ANOVA) was used to compare the significance of differences between the means of three variables. Multiple comparisons analysis of variance (ANOVA) was used to detect the significance of differences among the factors such as wind disturbance, forest type, soil depth, as well as the effects of the interactions among the three factors on the amount of net nitrogen mineralization, net nitrification, and net ammonification (α = 0.05). Correlation analysis was used to measure the correlations between variables such as soil mineralization rate, soil nutrient contents, and soil pH. Origin 8.5 was used for plotting data. 2. Results 2.1. Physical and chemical properties of soil In the BKPF, SFF, and EBF, the SOC and TN contents were higher at the 0–10 cm soil depth than at the 10–20 cm depth in both the control and wind-disturbed areas (Table 2). At 0–10 cm, however, the SOC content of BKPF was significantly lower than that of EBF. The TN contents of both BKPF and SFF soils were significantly lower than that of EBF in the control area. The TN content increased with increasing altitude in the wind-disturbed area. Differences in TN content in the BKPF and EBF soils were significant. At 10–20 cm, no significant differences were found in SOC and TN contents among BKPF, SFF, and EBF with increasing altitude in the wind-disturbed area, but the soil TN content of SFF was lower than that of EBF in the control area. Among the three forest types, only the SOC and TN contents of SFF were significantly different between the control and wind-disturbed areas at 10–20 cm. C/N ratios declined with increasing altitude at both 0–10 cm and 10– 20 cm soil depths in the control and the wind-disturbed areas. The soil C/N ratios of BKPF and SFF were higher than that of EBF (Table 2). At 0– 10 cm, the C/N ratios of BKPF and SFF were considerably higher in the control area than that in the wind-disturbed area. At 10–20 cm, no significant differences in the C/N ratios were found among BKPF, SFF, and EBF in both the control and wind-disturbed areas. The soil pH values of the three forest types were significantly lower at 0–10 cm than those at 10–20 cm. However, the differences in the soil pH of BKPF, SFF, and EBF between the control and wind-disturbed areas were not significant.
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2.2. Characteristics of nitrogen mineralization in soil 2.2.1. Characteristics of inorganic nitrogen content in soil Inorganic nitrogen (ammonium nitrogen and nitrate nitrogen) contents in all BKPF, SFF, and EBF soils increased in both the control and wind-disturbed areas after 21 d incubation (Fig. 1). These results showed clear trends toward ammonium nitrogen (NH+ 4 -N) and nitrate nitrogen (NO− 3 -N) contents in the incubated soils of BKPF, SFF, and EBF at 0–10 cm soil depth in both the control and wind-disturbed areas. The soil NH+ 4 -N content of EBF was highest, BKPF was next, and SFF was lowest. The soil NO− 3 -N content of BKPF was highest, EBF was next, and SFF was lowest. The difference between any two of the three types of forest soils was significant. At 10–20 cm in the control area, − NH+ 4 -N and NO3 -N contents in the incubated soil of EBF were significantly higher than those of BKPF and SFF. In the wind-disturbed area, the differences in NH+ 4 -N content in the incubated soils of BKPF, SFF, and EBF were not significant. In comparison, the soil NO− 3 -N contents of BKPF and SFF were lower than those of EBF. Fig. 1 shows the differences in inorganic nitrogen content between the original and incubated soil samples at different soil depths in both the control and wind-disturbed areas. At 0–10 cm, the inorganic nitrogen content in the original soil of EBF was significantly higher in the control area than in the winddisturbed area, whereas the inorganic nitrogen content in the incubated soil of BKPF in the control area was significantly higher than in the wind-disturbed area. Similarly, at 10–20 cm, the inorganic nitrogen content in the initial soil of EBF was much higher in the control area than in the wind-damaged area, whereas the inorganic nitrogen contents in the incubated soils of BKPF, SFF, and EBF in the control area were significantly higher than in the wind-disturbed area. 2.2.2. Characteristics of nitrogen mineralization rate in soil The net ammonification rates of BKPF and EBF soils were significantly higher at 0–10 cm than at 10–20 cm, but the difference in the soil nitrogen mineralization rate of SFF between the two soil depths was minimal. At 0–10 cm in the control area, the soil net nitrification rates of the three types of forests were 0.73 ± 0.067 mg·kg−1·d−1 (SFF), 2.12 ± 0.29 mg·k− 1·d− 1 (EBF), and 2.53 ± 0.98 mg·kg− 1·d− 1 (BKPF), respectively. The results indicate that the soil net nitrogen mineralization rate of SFF was significantly lower than the rates of BKPF and EBF. In the wind-disturbed area, the soil net nitrogen mineralization rates of BKPF, SFF, and EBF ranged from 0.88 to 1.347 mg·kg−1·d−1 and the differences between them were not significant. At 10–20 cm, the soil net nitrogen mineralization rates of BKPF, SFF, and EBF ranged from 0.75 to 0.94 mg·kg−1·d−1. t-Test results revealed a significant difference in the soil nitrogen mineralization rate of BKPF between the control and wind-disturbed areas at 0–10 soil depth. The results also showed that the difference in the soil nitrogen mineralization rates of SFF and EBF between the two areas were not significant. The net
Table 2 Soil chemical properties. Forest types
Soil depth
Disturbance types
C content (g∙kg−1)a
N content (g∙kg−1)a
C:Na
pHa
BKPF
0–10 cm
CA WDA CA WDA CA WDA CA WDA CA WDA CA WDA
51.99 39.70 25.62 29.11 59.23 54.61 19.55 30.87 69.05 62.43 22.68 26.04
2.87 2.68 1.71 2.27 3.85 4.13 1.57 2.47 6.08 5.46 2.24 2.37
18.15 ± 1.12Aa 14.68 ± 1.20Ba 14.96 ± 0.32a 12.79 ± 0.58 15.36 ± 0.69Ab 13.22 ± 0.46Bb 12.45 ± 0.56b 12.47 ± 0.23 11.30 ± 0.48c 11.57 ± 0.31c 9.97 ± 0.48c 11.03 ± 0.40
5.09 4.92 5.42 5.57 4.54 4.92 5.11 5.42 4.66 4.53 5.32 5.30
10–20 cm SFF
0–10 cm 10–20 cm
EBF
0–10 cm 10–20 cm
± ± ± ± ± ± ± ± ± ± ± ±
6.03b 11.59b 1.22 3.55 8.37ab 2.37ab 4.30B 3.98A 2.48a 4.30a 2.81 1.98
± ± ± ± ± ± ± ± ± ± ± ±
0.29b 0.61b 0.06ab 0.18 0.43b 0.16ab 0.32Bb 0.30A 0.09a 0.42a 0.17a 0.17
± ± ± ± ± ± ± ± ± ± ± ±
0.10a 0.20a 0.03 0.14 0.34b 0.10a 0.29 0.08 0.01b 0.13b 0.04 0.21
Notes: different lowercase letters represent significant differences among BKPF, SFF, and EBF within the same area. Different capital letters represent significant differences between winddisturbed and control areas with same forest type. CA: control area; WDA: wind disturbed area. a Mean ± SE.
268
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Inorganic N content/(mg.kg -1)
240
180
EBF
*
120
* *
60
0 CA
WDA
WDA
CA
10-20 cm
0-10 cm
Fig. 1. Nitrogen mineralization of soil in control and wind-disturbed areas. Notes: broadleaved Korean pine forest (BKPF); spruce-fir forest (SFF); Erman's birch forest (EBF); * represents a significant (p b 0.05) difference between wind-disturbed and control areas. CA: control area; WDA: wind disturbed area.
ammonification process played a key role in the soil nitrogen mineralization process of the three forest types (Fig. 2).
nitrogen mineralization were significant and highly significant on the net nitrification. The analysis further indicated that the interaction effects between the wind disturbance and forest type and among the wind disturbance, forest type, as well as soil depth on the net ammonification, net nitrification, and net nitrogen mineralization were not significant. Among the factors analyzed, the influences of wind disturbance and soil depth on net ammonification and nitrogen mineralization were much greater than those of forest type. The soil depth, forest type, and the interaction between the two factors had greater effects on the net nitrification than the wind disturbance (see Table 3). Soil nutrients increased nitrogen conversion in the soils (Fig. 3). The ammonification rate was positively correlated with SOC and C/N ratios but not significantly correlated with TN content. The nitrification rate had highly significant correlations with SOC and TN contents but nonsignificant correlation with C/N ratios. The nitrogen mineralization rate was greatly influenced by SOC, TN content and C/N ratios. The ammonification, nitrification, and nitrogen mineralization rates were all negatively correlated with soil pH. The correlation between the nitrification rate and soil pH was significant as was the correlation between and the nitrogen mineralization rate and pH. 3. Discussion
2.3. Factors affecting soil nitrogen mineralization
3.1. Effects of restored vegetation on the physical and chemical properties of soil in the wind-disturbed area
Multiple comparisons ANOVA showed the highly significant influence of wind disturbance and soil depth on net ammonification and nitrogen mineralization. The analysis also demonstrated that soil depth and forest type had significant influences on net nitrification. The effects of the interaction between the wind disturbance and forest type on the net ammonification and nitrogen mineralization were significant but not significant on the net nitrification. The impacts of the interaction between the soil depth and forest type on the net ammonification and
After the destructive effects of typhoon exposure, significant changes in the vegetation types and community structure occurred in the wind-disturbed area on Changbai Mountain [12,14,16]. However, no significant differences in SOC and TN contents were observed between the control and wind-disturbed areas (Table 2), indicating that the SOC and TN contents in the wind-disturbed soil were essentially the same as in the undisturbed primary forest soil. Similar observations have been made by some researchers [18–21], but different findings
4 Nitrification rate Ammonification rate
BKPF 3
*
2
* 1
0 CA
0-10 cm
3
2
1
0
CA
WDA
SFF Nitrogen mineralization rate /(mg.kg-1.d-1)
Nitrogen mineralization rate (mg.kg-1.d-1)
4
WDA
CA
Nitrogen mineralization rate /(mg.kg-1.d-1)
4
WDA
0-10 cm
10-20 cm
CA
WDA
10-20 cm
EBF
3
2
1
0 CA
WDA
0-10 cm
CA
WDA
10-20 cm
Fig. 2. Net nitrogen mineralization rate of soil in control and wind-disturbed areas. Notes: broadleaved Korean pine forest (BKPF); spruce-fir forest (SFF); Erman's birch forest (EBF); * represents a significant (p b 0.05) difference between wind-disturbed and control areas. CA: control area; WDA: wind disturbed area.
F. Ma et al. / Acta Ecologica Sinica 37 (2017) 265–271
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Table 3 Multi comparisons ANOVA on net nitrogen, net ammonification, and net nitrification. Influence factors
Wind disturbance Soil depth Forest type Wind disturbance ∗ soil depth Wind disturbance ∗ forest type Soil depth ∗ forest type Wind disturbance ∗ soil depth ∗ forest type
Ammonification contents (Aamm)
Nitrification contents (Anit)
Net N mineralization contents (Amin)
F
P
F
P
F
P
14.004 13.160 2.736 0.959 5.116 3.523 1.431
0.001⁎⁎ 0.001⁎⁎
1.515 34.721 11.752 1.222 1.713 8.892 2.646
0.230 b0.001⁎⁎ b0.001⁎⁎ 0.280 0.202 0.001⁎⁎
14.838 27.014 3.323 1.567 5.762 5.606 1.215
0.001⁎⁎ b 0.001⁎⁎ 0.053 0.223 0.009⁎⁎ 0.01⁎
0.085 0.337 0.014⁎ 0.046⁎ 0.259
0.092
0.314
⁎ Significant at P ≤ 0.05 level. ⁎⁎ Significant at P ≤ 0.01 level.
have been reported by others. Carbon and nitrogen stocks in soil declined due to the conversion of primary forest to secondary forest and grassland after wind disturbance [22–25]. Discrepancy between observations could be related to the duration of forest restoration. Most studies on wind disturbance effects were conducted approximately 10 years after forest disturbance. This is a relatively short period for the restoration of disturbed vegetation. The present study showed that the soil nutrient levels in the typhoon-disturbed vegetation areas were essentially restored to those found in the undisturbed forest ecosystem on Changbai Mountain after 30 years of regrowth. The carbon-to-nitrogen ratio (C/N) is a key indicator used to identify soil quality change. Reduction in the C/N ratio is a gauge of accelerated organic matter decomposition [26]. The C/N ratios declined after wind disturbance, indicating more rapid soil nutrient decomposition in the wind-disturbed area than in the control area (Table 2). Increased soil temperatures caused by reduced vegetation cover in the wind-disturbed area may have facilitated organic matter decomposition in the soil with the consequent decrease in the C/N ratios [27]. At 0–10 cm soil depth, the soil C/N ratios of BKPF and SFF were significantly different
2 1 0 10
20
30
40
50
Fig. 1 illustrates that NH+ 4 -N stock in all the BKPF, SFF, and EBF soils was higher than NO− 3 -N stock in both the control and wind-disturbed areas. This suggests that NH+ 4 -N was the primary inorganic form of nitrogen in the forest soil of Changbai Mountain. These results are consistent with previous research [6,28]. The changes in the amount of NH+ 4 -N formed from ammonification, which contributed to the 57.1–76.2%
4
Ammonification rate P=0.012 Nitrification rate P=0.000 Mineralization rate P=0.001
3
3.2. Ammonium was the primary inorganic form of nitrogen in forest soil (NH+ 4 -N)
Mineralization rates/(mg.kg -1.d-1)
Mineralization rates/(mg.kg -1.d-1)
4
in both the control and wind-disturbed areas (Table 2), possibly related to the varying vegetation types. In the wind-disturbed area, primary BKPF was replaced by a secondary poplar forest, and the spruce-fir forest was mostly replaced by herbaceous plants such as Cinnamomum camphora. The vegetation litter in the area was mainly derived from broadleaf and herbaceous plants. The decreased C/N ratios of the soil litter layer primarily led to C/N ratio decreases in the disturbed soil. Compared to soil SOC and TN contents, C/N ratios appeared to more accurately reflect the effects of vegetation change on soil quality.
60
70
Ammonification rate P=0.087 Nitrification rate P=0.000 Mineralization P=0.003
3 2 1 0
80
1
3
4
5
6
7
·
·
4
4 Ammonification rate P =0.013 Nitrification rate P =0.753 Mineralization rate P =0.035
3
Mineralization rates/(mg.kg-1.d -1)
Mineralization rates/(mg.kg-1.d -1)
2
Nitrogen content/ (g.kg-1)
Carbon content/(g.kg-1)
2
1
0 8
10
12
14
C:N
16
18
20
Ammonification rate P =0.182 Nitrification rate P =0.000 Mineralization rate P =0.020
3
2
1
0 4.0
4.5
5.0
pH
Fig. 3. Correlation analysis between nitrogen mineralization rate and soil chemical properties.
5.5
6.0
270
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amount of nitrogen mineralized (nitrogen mineralization) and net nitrogen mineralization rate, primarily resulted in alterations in the nitrogen mineralization and net nitrogen mineralization rate in the three types of forest soils. Nitrogen mineralization was mainly the result of the ammonification process. The reasons that nitrification was not as dominant as ammonification were mostly due to the strong effect of forest soil pH. Table 2 shows that the soils in the vegetation zones of BKPF, SFF, and EBF were acidic. Generally, the optimal pH for soil nitrifying bacteria is near 8 and nitrification is inhibited by greater acidity. A low pH would reduce the solubility of soil organic matter and inhibit nitrifying bacteria growth. As a result, the nitrification process in the soil was − retarded and NH+ 4 -N content was higher than NO3 -N content [29]. Further, the nitrification process in the forest soil was usually limited by the amount of NH+ 4 -N formed from ammonification. The nitrification rate would therefore be lower than ammonification rate [30]. 3.3. Factors affecting soil nitrogen mineralization The forest types appeared to exert significant effects on the net nitrification, whereas they had no significant impact on net ammonification and TN mineralization. The interactions among the forest type, wind disturbance, and soil depth had great influences on net ammonification, net nitrification, and net TN mineralization. These results suggest that the differences in nitrogen mineralization in the BKPF, SFF, and EBF soils mainly resulted from the forest types, a finding consistent with other studies [31–33]. Table 2 shows that the differences in the net nitrogen mineralization between 0–10 cm and 10–20 cm depths were significant in both the control and wind-disturbed areas. At 0–20 cm, the net nitrogen mineralization rates of BKPF and EBF soils decreased as soil depth increased. Soil permeability may have slowly declined with increasing soil depth, resulting in aging of soil organic matter and reduced decomposition. The organic matter available for degradation and plant uptake would gradually decrease and microbial populations and their activity would have been reduced. These factors could lead to a decrease in the nitrogen mineralization rate [34–35]. In contrast, the soil mineralization rate of SFF was greater at 10–20 cm soil depth in the control area, possibly due to the higher SOC in the forest soil at the 10–20 cm depth. Comparative studies were performed on the nitrogen mineralization and net nitrogen mineralization rate in the three types of forest soils in both the control and wind-disturbed areas. The net ammonification, net nitrification, and net nitrogen mineralization rates of BKPF and EBF soils were higher in the control area than in the wind-disturbed area (Fig. 2). Correlation analysis indicated that SOC and TN contents, and C/N ratio had significant effects on soil ammonification, nitrification, and nitrogen mineralization rates (Fig. 3). The potential of fertile soil nitrogen mineralization may have been greater than that in infertile soil [36]. Multiple comparisons ANOVA showed that wind disturbance exerted a highly significant influence on the net ammonification and nitrogen mineralization. In addition, the effects of the interaction between the wind disturbance and forest type on the net ammonification were significant and highly significant, respectively, on the net nitrogen mineralization. The studies demonstrated, overall, that the nitrogen mineralization process in the forest soils remained affected by wind disturbance although the vegetation zones in the typhoon-disturbed area within the Changbai Mountain nature reserve have been undergoing restoration for 30 years. 4. Conclusions (1) SOC, TN, and pH in the BKPF and EBF soils were similar in both the control and wind-disturbed areas and this was also true for the SFF topsoil. However, the C/N ratios of BKPF and SFF topsoil in the control area were significantly higher than in the wind-disturbed area, indicating differences in the nutrient supply of available carbon and nitrogen to the forests, due to the changes in vegetation type in the wind-disturbed
area. Compared to SOC and TN contents, the C/N ratio is a more sensitive index of the effect of vegetation changes on soil quality. (2) NH+ 4 -N is the primary inorganic form of nitrogen in the forest soils. The changes in the amount of NH+ 4 -N formed from ammonification were used to characterize the 57.1%–76.2% range of the total variation in the nitrogen mineralization and net nitrogen mineralization rate. The nitrogen mineralization process was mainly the result of ammonification. The ammonification and nitrogen mineralization in the soils were regulated by pH and SOC and TN contents. (3) Forest type, soil depth, and alterations in vegetation type caused by wind disturbance exerted significant influences on organic nitrogen mineralization in the forest soils at different altitudes. Although vegetation cover in the wind-disturbed area of Changbai Mountain has largely been restored after 30 years of growth, we found significant differences in soil quality between the primary forest and wind-disturbed areas due to the varying vegetation types.
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