Revegetation impacts soil nitrogen dynamics in the water level fluctuation zone of the Three Gorges Reservoir, China

Science of the Total Environment 517 (2015) 76–85

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Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv

Revegetation impacts soil nitrogen dynamics in the water level fluctuation zone of the Three Gorges Reservoir, China Chen Ye, Xiaoli Cheng ⁎, Wenzhi Liu, Quanfa Zhang Key Laboratory of Aquatic Botany and Watershed Ecology, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan 430074, China

H I G H L I G H T S • • • • •

Tree plantations decreased soil inorganic N concentration and N leaching. Tree plantations decreased soil net N mineralization and ammonification rates. Tree plantations increased soil net N nitrification and denitrification rates. Soil net N nitrification rate was positively related with C:N ratios. C inputs are important in determining the soil N dynamics.

a r t i c l e

i n f o

Article history: Received 23 January 2015 Received in revised form 19 February 2015 Accepted 19 February 2015 Available online 24 February 2015 Editor: C.E.W. Steinberg Keywords: Vegetation type Soil N transformation Leaching of N Plant N uptake N dynamics Water level fluctuation zone

a b s t r a c t Revegetations in riparian ecosystem are important in regulating soil nitrogen (N) dynamics. However, impacts of revegetation on soil N cycling and thereby on ecosystem functioning are not fully understood. We conducted an in situ incubation in the water level fluctuation zone (WLFZ) of the Three Gorges Reservoir region to evaluate soil N transformation including net N mineralization rate, net ammonification rate, net nitrification rate, net denitri− fication rate, N leaching and plant N uptake as well as the soil inorganic N (NH+ 4 -N and NO3 -N) concentration in the top soils (0–20 cm) following revegetations (implementing tree, shrub and herb plantations) over two years. The soil inorganic N concentration and N leaching were lower in the tree soils than in herb and shrub soils. Tree plantations decreased net N mineralization rate and net ammonification rate compared to herb and shrub soils, possibly due to lower soil organic carbon (SOC) input and soil temperatures. Whereas tree plantations increased soil net denitrification rate compared to herb and shrub soils because of higher tree NO− 3 -N uptake together with higher net nitrification rate. The inorganic N in the tree and shrub soils were lower in fall and summer, respectively, which was dependent on the seasonal variations in plant N uptake, soil N transformation, and N leaching. Thus, our results suggest that tree plantations could decrease soil inorganic N concentration and N leaching by altering both the quantity and quality of SOC and thereby potentially improve water quality in the riparian zone. © 2015 Elsevier B.V. All rights reserved.

1. Introduction Riparian zones provide important services for buffering nitrogen (N) pollution from agricultural upland and regulating eutrophication in aquatic ecosystems (DeSimone et al., 2010; Liu et al., 2011; Jacobs and Harrison, 2014). The recognition of the regulatory role of riparian zones primarily focuses on the relationship between riparian vegetation and soil N dynamics (Knops et al., 2002; Tall et al., 2011; Ye et al., 2012; Audet et al., 2014). For example, riparian vegetation is thought to uptake N by roots and regulate N leaching from ecosystems as well (Knops et al., 2002; Zhang et al., 2012). Meanwhile, plant carbon (C) substrate can affect soil N transformation (e.g., mineralization, nitrification and denitrification) by influencing microbial activity (Booth ⁎ Corresponding author. E-mail address: [email protected] (X. Cheng).

http://dx.doi.org/10.1016/j.scitotenv.2015.02.068 0048-9697/© 2015 Elsevier B.V. All rights reserved.

et al., 2005; Cheng et al., 2010, 2011). Thus, changes in vegetation following revegetation could substantially alter soil N dynamics in riparian zones. Vegetation can influence soil N dynamics primarily by altering soil organic C (SOC) input, root uptake, and soil N availability (Bardgett and Wardle, 2003; Knoepp and Vose, 2007; Kreiling et al., 2011; do Carmo et al., 2012). Revegetation usually alters soil C inputs into soils through plant root exudation and litter production, and hence potentially changes soil N dynamics (Knops et al., 2002; Liu et al., 2011). However, consequences of revegetation for soil N dynamics remain controversial due to diverse plant species and soil properties (Clément et al., 2002; Dhondt et al., 2004; Vargas et al., 2006; Zhang et al., 2012). For instance, some studies have reported that revegetation exerts an important control on N cycling by changing the quantity and quality of litter inputs (Vargas et al., 2006; Papini et al., 2011; Zhang et al., 2012). Other studies, however, have indicated that revegetation

C. Ye et al. / Science of the Total Environment 517 (2015) 76–85

3.86 ± 0.16b 6.12 ± 0.18b 0.49 ± 0.02b 12.38 ± 0.33a 20.39 ± 0.52b 22.37 ± 0.60b 7.08 ± 0.03a

Values are mean ± SE. Different letters a and b in the same row indicate statistical significance at P b 0.05 between vegetation types.

has a negligible effect on soil N dynamics because of N cycling regulated by multiple factors such as ecosystem types and climatic factors (Clément et al., 2002; Dhondt et al., 2004; Booth et al., 2005). Indeed, soil microclimates (e.g. soil temperature, moisture and pH) play a key role in controlling both spatial and temporal variations in soil N cycling processes except for vegetation (Dijkstra et al., 2008; Cheng et al., 2011). For example, previous studies have reported that elevated temperature can stimulate the soil net N mineralization in various ecosystems worldwide (Melillo et al., 2002; Wan et al., 2005; Wang et al., 2006). Soil moisture can also impact the soil net N mineralization and nitrification by controlling the soil microbial activity (Paul et al., 2003; Knoepp and Vose, 2007; Brookshire et al., 2011). Furthermore, Li et al. (2014) have demonstrated that an increased pH stimulated soil net N nitrification, because a high soil pH increases the dissolubility of SOC and then promotes the activity of nitrobacteria and soil net nitrification (Curtin et al., 1998). Yet the influence of vegetation on soil N dynamics can differently interact with microclimate among different ecosystems (Booth et al., 2005; Knoepp and Vose, 2007; Zhang et al., 2012). Therefore, more field studies on the response of soil N dynamics to vegetation types and changing environments are necessary, particularly regarding soil N dynamics in the riparian zone. With the full functioning of the Three Gorges Dam in 2010, the water level of the reservoir fluctuates from 145 m a.s.l in summer (May to September) to 175 m in winter (October to April), creating a new water-level-fluctuation zone (WLFZ) with a total area of 350 km2 in the Three Gorges Reservoir (Zhong and Qi, 2008). Due to the reversal of submergence time and prolonged duration of flooding, the new WLFZ dramatically alters the environmental conditions of the riparian zone, resulting in various ecological problems such as loss of pre-dam terrestrial vegetation and erosion of sedimentation (New and Xie, 2008). Revegetation is one of the effective measures to restore and protect the riparian ecosystem. Previous researches in the WLFZ of the Three Gorges Reservoir have demonstrated that species including herb (Cynodon dactylon, Hemarthria sibirica); shrub (Hibiscus syriacus, Morus alba, and Salix variegate); and tree (Salix chaenomeloides, and Taxodium distichum) with a high tolerance to summer exposure and winter inundation were selected for WLFZ revegetation of the reservoir (Lu et al., 2010). The soil inorganic N in the WLFZ declined following the revegetation and flooding (Ye et al., 2012). However, little information is available about the impacts of different vegetation types on soil N dynamics including soil N transformation, N leaching and plant uptake N following the revegetation in the WLFZ. In this study, we investigated root biomass, root N, soil properties, inorganic N concentration, in situ net N mineralization, ammonification, nitrification, and denitrification rates, and N leaching in different vegetation types (herb, shrub and tree) in the WLFZ of the Three Gorges Reservoir. We hypothesized that revegetation would significantly affect soil N dynamics due to changes in SOC supply and soil environmental factors in the WLFZ of the Three Gorges Reservoir. To test this hypothesis, we specifically focused on (1) how different vegetation types have potentially impacted soil inorganic N concentrations, N transformation rate, plant N uptake and N leaching; and (2) how the associated changes

2. Materials and methods 2.1. Site description The study was conducted at Zhongxian (30°26′ N 108°11′ E), Chongqing, China (Ye et al., 2012). The Three Gorges Reservoir lies within the northern subtropical zone and climate in this region belongs to subtropical monsoon, with a mean annual temperature of 16.5–19 °C and monthly average temperature of 3.4–7.2 °C in January and 28–30 °C in July. The annual mean precipitation ranges from 886 to 1614 mm, 80% of which falls between April and October (Ye et al., 2011). The soil is purple soil consisting of 29% sand, 49% silt and 22% clay in the top 20 cm. The water level of the study region fluctuates from 145 m in summer to 175 m in winter. Before submergence, vegetation in the water level fluctuation zone of the Three Gorges Reservoir was dominated by annuals, e.g., Setaria viridis, Digitaria ciliaris, and Leptochloa chinensis, perennials including C. dactylon, Hemarthria altissima, and Capillipedium assimile, and woody plants such as Ficus tikoua, Pterocarya stenoptera, and Vitex negundo (Lu et al., 2010; Ye et al., 2013). After the prolonged submergence since 2008, annual plants such as Echinochloa crusgalli and Bidens tripartita, and perennials including C. dactylon are dominant species, and a few alien invasive plants, such as Eupatorium adenophorum and Alternanthera philoxeroides, are present in the areas (Zhong and Qi, 2008). To restore the riparian ecosystem, revegetation in Zhongxian has been carried out along the elevation from 155 m to 175 m since March 2008. Herbs including C. dactylon and H. sibirica were planted between the elevations of 155 and 165 m, with the 95% mean coverage. Shrubs were planted between the elevations of 165 and 172 m with a density of eight stems per square meters and the dominant species were H. syriacus, M. alba and S. variegate. 600

(a)

-2

Tree (n = 56)

6.42 ± 0.15a 7.74 ± 0.14a 0.77 ± 0.02a 10.76 ± 0.18b 20.50 ± 0.63b 30.66 ± 5.53ab 6.97 ± 0.03b

Root biomass (g m )

Shrub (n = 56)

6.22 ± 0.14a 8.04 ± 0.18a 0.77 ± 0.02a 10.82 ± 0.20b 25.79 ± 1.02a 25.68 ± 0.31a 7.20 ± 0.04a

a

450

300

b

b 150

0

(b) 3

a

-2

Herb (n = 32)

Soil organic C (g kg−1) Total C (g kg−1) Total N (g kg−1) Soil C:N ratio Soil moisture (%) Soil temperature (°C) pH

Root N (g m )

Soil properties

in soil properties (e.g. SOC, soil C:N ratio, soil temperature and moisture, and pH) and plant traits (e.g. root biomass and root C:N ratio) determine soil N dynamics.

2

b

b

1

0 100

Root C:N ratio

Table 1 Soil properties of top soil (0–20 cm) under different vegetation types in Zhongxian revegetation area of the Three Gorges Reservoir, PR China.

77

80

a

(c) b

b

60 40 20 0

Herb

Shrub

Tree

Fig. 1. Biomass, N and C:N ratio of roots under different vegetation types. Values are mean ± SE, and different letters over the bars indicate statistically significant differences between the vegetation types.

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C. Ye et al. / Science of the Total Environment 517 (2015) 76–85

Trees including S. chaenomeloides and T. distichum were planted between the elevations of 172 and 175 m with the mean planting density of four stems per square meters (Ye et al., 2012, 2013). 2.2. Field measurements

Inorganic N concentration (mg kg-1)

NO3--N concentration (mg kg-1)

NH4+-N concentration (mg kg-1)

Field surveys were conducted in spring, summer and fall of 2011 and 2012. According to the hydrological change in the Three Gorges Reservoir, trees and shrubs are exposed in spring, summer and fall (from March to September), but herbs exposed in summer and early fall (from May to August) and they are all submerged in winter (from October to February). Three stands of each vegetation type (50 m × 1000 m), including trees, shrubs, and herbs were delimited in this study. Within each stand, we randomly placed 4 sub-plots (1 m × 1 m each) for each vegetation type. Soil net N mineralization, nitrification and ammonification rates, soil N leaching and plant N uptake were measured seven times per year during March–September of 2011 and 2012 using the in situ core technique over two years (Raison et al., 1987). In each sub-plot, three of 5 cm-diameter and 30 cm-height PVC tubes, with one of which was covered-top by polyethylene film allowing for gas exchange and the others were opened, were driven 20 cm into the ground soil at the beginning of each incubation period. One opened-top tube was immediately removed for de− termination of the initial NH+ 4 -N and NO3 -N concentrations and soil properties. The other two tubes were left in the field for one month to undergo incubation before being retrieved. The net N mineralization, ammonification and nitrification are calculated by the changes in the NH+ 4 -N, NO− 3 -N and inorganic-N contents in covered-cores after 30 days of

incubation (Rhoades and Coleman, 1999). The N leaching can be assessed by comparing the quantity of mineral-N present in covered (no leaching) and open cores at the end of incubation. The deficit in mineral-N in open cores represents an upper limit (because of the absence of uptake of water and N by roots inside cores) for leaching losses. The plant N uptake can be estimated by comparing the quantity of mineral-N present in open cores and bulk (unconfined) soil at the end of incubation. The change in mineral-N in bulk soil indicates the amount of mineral-N (because of the absence of uptake N by roots inside cores) for plant uptake (Raison et al., 1987). The in situ net denitrification rates under different vegetation types were measured using the acetylene blocking technique (Tiedje et al., 1989). Although this technique might inhibit gross nitrification and potentially underestimate denitrification when coupled to nitrification, it was very appropriate for the experimental design (Groffman et al., 2006). PVC tubes, 5 cm in diameter and 100 cm in height, were inserted 20 cm deep into ground at each sub-plot. Acetylene gas was injected into the chambers until 10% (v/v) of the headspace of the chamber was occupied by the gas. Then, headspace gas samples were collected every 20 min for 2 h. Accumulated nitrous oxide concentrations in the gas samples were analyzed using a gas chromatograph (Hewlett Packard 5890). For calculating the denitrification flux, only the slope which showed a linear increase in nitrous oxide concentrations with time was selected (Song et al., 2010). The roots were collected using a root corer with a diameter of 16 cm and length of 20 cm. Roots were washed by hand over a 0.5 mm sieve (Hefting et al., 2005). All of the collected soil samples were sealed in plastic bags and temporarily stored in a refrigerator at 4 °C prior to analysis.

16

(a)

Herb Shrub Tree

a

12

b a a a

8

a a

4

(d) ab

a b

b

0

(b)

a

15

(e)

a

b a

a 10

b

ab

a

a

a

a

a

b 5 0

(c) 27

(f)

a b

a

a b b

18

b

b c

9 0

Spring

Summer

Fall

Herb

Shrub

Tree

− Fig. 2. Seasonal variations and annual averages of soil NH+ 4 -N, NO3 -N and inorganic N concentrations under different vegetation types. Values are mean ± SE, and different letters over the bars indicate statistically significant differences between the vegetation types in each season (a–c) and annual (d–f), respectively.

C. Ye et al. / Science of the Total Environment 517 (2015) 76–85

79

Table 2 − Significance of the effects of vegetation type, season and their interactions on soil NH+ 4 -N, NO3 -N and inorganic N concentrations, net N mineralization (MR), net ammonification rate (AR), net nitrification rate (NR) and net denitrification rate (DR) based on repeated measure ANOVA; numbers are F-values. Source of variation

NH+ 4 -N

NO− 3 -N

Inorganic N

MR

AR

NR

DR

Vegetation type Season Vegetation type × season

12.5⁎⁎⁎ 27.6⁎⁎⁎ 10.8⁎⁎⁎

20.8⁎⁎⁎ 48.0⁎⁎⁎ 14.7⁎⁎⁎

33.5⁎⁎⁎ 57.8⁎⁎⁎ 20.4⁎⁎⁎

0.8⁎ 103.3⁎⁎⁎ 6.6⁎⁎

145.1⁎⁎⁎ 104.9⁎⁎⁎ 82.9⁎⁎⁎

600.5⁎⁎⁎ 552.9⁎⁎⁎ 451.2⁎⁎⁎

20.9⁎⁎⁎ 81.9⁎⁎⁎ 40.6⁎⁎⁎

⁎ P b 0.05. ⁎⁎ P b 0.01. ⁎⁎⁎ P b 0.001.

2.3. Sample analysis Total C, SOC, total N, and the total C and N concentrations of root were analyzed by C/N Analyzer (Flash, EA, 1112 Series, Italy). Soil samples were air-dried and sieved (b2 mm) before analysis. A 15-g sample of soil was extracted by shaking with 100 ml of 2 M KCl for 1 h. − Exchangeable NH+ 4 -N and NO3 -N were determined with spectrophotometer using the Indophenol blue colorimetric method and Phenol disulfonic acid colorimetry, respectively. Soil moisture and bulk density were measured by dried intact soil cores at 105 °C for 24 h. Soil pH

MR (mg kg-1 d-1)

0.6 (a)

a

2.4. Calculations The soil net N mineralization rate (MR), net ammonification rate (AR) and net nitrification rate (NR) during the incubation period were

Herb Shrub Tree

a

0.4 0.2

b

AR (mg kg-1 d-1)

0.4 b

a a

0.6 (b) 0.2

0.6

a ab

0.0

0.4

(e)

a

-0.2 a

0.2 0.0

a

(f) a

0.6 0.4

a b

b

a a

b

0.0

c

-0.4 0.75 (c) 0.60 0.45 0.30 0.15 0.00 -0.15 72 (d) 54 36

0.2 0.0

-0.2

DR (ug N2O-N m-2 h-1)

NR (mg kg-1 d-1)

a

was measured in a 2:1 (by weight) soil to water solution using Fisher Scientific AR15 (Waltham, MA) pH probe. Within the 0–20 cm layer, soil temperature was measured with a temperature probe. The root biomass was determined gravimetrically after drying the fresh roots at 70 °C for 48 h (Ye et al., 2012).

-0.2

a

a

(g)

0.3 0.2

b

a

0.1

b b a b

b

b 0.0 -0.1

a a

(h)

ab

a 30

a a

18

a b

a b

b

15

0 -18

0 Spring

Summer

Fall

Herb Shrub Tree

Fig. 3. Seasonal variations and annual averages of soil net N mineralization rate (MR), net ammonification rate (AR), net nitrification rate (NR), net denitrification rate (DR) under different vegetation types. Values are mean ± SE, and different letters over the bars indicate statistically significant differences between the vegetation types in each season (a–d) and annual (e–h), respectively.

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C. Ye et al. / Science of the Total Environment 517 (2015) 76–85

Table 3 Significance of the effects of vegetation type, season and their interactions on plant N uptake and N leaching based on repeated measure ANOVA; numbers are F-values. Source of variation

NH+ 4 -N

NO− 3 -N

Inorganic N

Plant N uptake Vegetation type Season Vegetation type × season

1.9 36.0⁎⁎⁎ 0.1

6.5⁎⁎⁎ 19.9⁎⁎⁎ 18.6⁎⁎⁎

6.6⁎⁎ 27.2⁎⁎⁎ 0.6

N leaching Vegetation type Season Vegetation type × season

43.9⁎⁎⁎ 29.2⁎⁎⁎ 15.5⁎⁎⁎

1.5 5.9⁎⁎ 18.5⁎⁎⁎

11.3⁎⁎⁎ 6.6⁎⁎ 4.1⁎

− + − where NH+ 4 -Nbi and NO3 -Nbi are NH4 -N and NO3 -N concentrations of bulk (b, unconfined) soil at the beginning (time i) of the incubation − + − period; NH+ 4 -Nc(i + 1) and NO3 -Nc(i + 1) are NH4 -N and NO3 -N concentrations of incubated and covered (c) soil at the end (time i + 1) of the incubation period. − The N leaching (NH+ 4 -Nl, NO3 -Nl and inorganic Nl) and plant N − uptake (NH+ 4 -Nu, NO3 -Nu and inorganic Nu) during incubation period can be assessed by the following equations:

þ

þ

þ

þ

þ

−

−

−

NH4 ‐Nu ¼ NH4 ‐Noðiþ1Þ −NH4 ‐Nbðiþ1Þ

⁎ P b 0.05. ⁎⁎ P b 0.01. ⁎⁎⁎ P b 0.001.

NO3 ‐Nl ¼ NO3 ‐Ncðiþ1Þ −NO3 ‐Noðiþ1Þ −

− − calculated as the changes in total mineral N (NH+ 4 -N + NO3 -N), NO3 -N + and NH4 -N using the following equations:

þ

MR ¼

AR ¼

−

þ

−

þ

−

Inorganic N1 ¼ NH4 ‐Nl þ NO3 ‐Nl þ

−

Inorganic Nu ¼ NH4 ‐Nu þ NO3 ‐Nu + + + where NH+ 4 -Nc(i + 1), NH4 -No(i + 1) and NH4 -Nb(i + 1) are NH4 -N concentrations of covered (c) and opened (o) cores, and bulk soil at the end − (time i + 1) of the incubation period, respectively; NH− 3 -Nc(i + 1), NH3 − − No(i + 1) and NH3 -Nb(i + 1) are NO3 -N concentrations of covered (c) and opened (o) cores, and bulk soil at the end (time i + 1) of the incubation period, respectively (Raison et al., 1987).

þ NHþ 4 ‐Ncðiþ1Þ −NH4 ‐Nbi

t iþ1 −t i − NO− 3 ‐Ncðiþ1Þ −NO3 ‐Nbi

t iþ1 −t i

12 (a)

a

Herbs Shrubs Trees

a

a

(d)

8

6

b

b b

4

b

c a a

0 NO3--N leaching (mg kg-1)

−

NO3 ‐Nu ¼ NO3 ‐Noðiþ1Þ −NO3 ‐Nbðiþ1Þ

−

NH4 ‐Ncðiþ1Þ þ NO3 ‐Ncðiþ1Þ −NH4 ‐Nbi −NO3 ‐Nbi t iþ1 −t i

NH4+-N leaching (mg kg-1)

NR ¼

þ

NH4 ‐Nl ¼ NH4 ‐Ncðiþ1Þ −NH4 ‐Noðiþ1Þ

a

a

(b) a

a

(e)

a

a

a

a

4 b

2

Inorganic N leaching (mg kg-1)

b 0 20 15 10

a

a

(c) a

ab

a b

(f) b

b a

c

5 b 0 Spring

Summer

Fall

Herbs Shrubs

Trees

− Fig. 4. Seasonal variations and annual averages of leaching of NH+ 4 -N, NO3 -N and inorganic N concentrations under different vegetation types. Values are mean ± SE, and different letters over the bars indicate statistically significant differences between the vegetation types in each season (a–c) and annual (d–f), respectively.

Plant NH4+-N uptake (mg kg-1)

C. Ye et al. / Science of the Total Environment 517 (2015) 76–85

(a)

a

6

Herbs Shrubs Trees

a

a 4

81

(d) a ab

a a

b

2 a a

Plant NO3--N uptake (mg kg-1)

0 a

(b)

(e)

8 a

a

a

a

a

4 b

Plant inorganic N uptake (mg kg-1)

0 ab

15 (c) 12 9

b

a b

a

(f) a

a b

a

b

6 3

b

a b

0

Summer

Spring

Herbs

Fall

Shrubs Trees

Fig. 5. Seasonal variations and annual averages of plant N uptake under different vegetation types. Values are mean ± SE, different letters over the bars indicate statistically significant differences between the vegetation types in each season (a–c) and annual (d–f), respectively.

2.5. Statistical analyses The normality of all data was checked via Kolmogorov–Smirnov's test prior to analysis of variance. Repeated measures ANOVA was performed to test the statistical significance of the vegetation type and

season and their interactive effects on soil properties, inorganic N concentrations, soil N transformation rates, N leaching and plant N uptake. Duncan's multiple comparison test was further employed to test for differences at the P = 0.05 level. Pearson correlation and regression analyses were performed to correlate the soil inorganic N concentration,

Table 4 Pearson correlation coefficients (r) of net N mineralization rate (MR), net ammonification rate (AR), net nitrification rate (NR), net denitrification rate (DR), and N leaching and plant N uptake on soil properties, root biomass and root C:N ratio across vegetation types. − NH+ 4 -N NO3 -N Inorganic N MR

Total C 0.15 SOC 0.29 Total N 0.26 Soil C:N ratio −0.42 pH −0.44 Soil moisture 0.46 Soil temperature −0.29 NH+ 0.36 4 -N leaching 0.22 NO− 3 -N leaching Inorganic N leaching 0.45 + 0.23 Plant NH4 -N uptake 0.38 Plant NO− 3 -N uptake Plant inorganic N uptake 0.17 Root biomass 0.34 Root N 0.35 Root C:N ratio 0.16

0.21 0.32 0.32 −0.50 −0.37 0.57 −0.51 0.33 0.09 0.39 −0.11 0.29 0.01 0.56 0.33 0.10

0.25 0.32 0.32 −0.48 −0.45 0.57 −0.34 0.34 0.28 0.46 0.09 0.32 0.13 0.50 0.34 0.14

AR

NR

0.21 0.76⁎ −0.58 0.05 0.67 −0.55 0.06 0.69 −0.70 0.16 −0.50 0.87⁎⁎ 0.33 0.37 −0.12 −0.25 0.06 −0.41 0.68 0.73⁎ 0.08 0.40 0.65 −0.19 0.48 −0.09 0.55 0.48 0.65 −0.05 0.88⁎⁎ 0.60 0.39 0.36 −0.01 0.62 0.80⁎ 0.70 0.17 −0.70 −0.33 −0.32 −0.19 0.31 −0.46 −0.24 −0.76⁎ 0.49

Bold-faced values represent the significant correlations (Pb0.05) between the two parameters. ⁎ P b 0.05. ⁎⁎ P b 0.01.

DR

NH+ 4 -N leaching

−0.38 0.58 −0.28 0.54 −0.39 0.53 0.48 −0.44 −0.24 0.48 −0.30 0.48 0.51 0.05 −0.03 1.00 0.29 −0.11 0.02 0.95⁎⁎ 0.78⁎ 0.50 0.35 0.57 0.31 0.85⁎⁎ −0.56 −0.10 0.34

−0.27 −0.03 −0.57

− NO− Inorganic N Plant NH+ 3 -N 4 -N Plant NO3 -N Plant leaching leaching uptake uptake inorganic N uptake

−0.17 −0.31 −0.27 0.34 −0.18 −0.29 0.10 −0.11 1.00 0.14 0.43 0.40 0.28 −0.13 −0.20 0.37

0.65 0.60 0.57 −0.43 0.33 0.37 0.16 0.95⁎⁎ 0.14 1.00 0.58 0.61 0.87⁎⁎ −0.14 0.09 −0.55

0.11 0.09 0.03 0.12 0.06 −0.06 0.57 0.50 0.43 0.58 1.00 0.56 0.81⁎ −0.61 −0.08 −0.06

−0.19 −0.18 −0.27 0.36 0.20 0.20 −0.23 0.57 0.40 0.61 0.56 1.00 0.68 −0.38 −0.50 0.18

0.38 0.27 0.27 −0.09 0.50 0.17 0.30 0.85⁎⁎ 0.28 0.87⁎⁎ 0.81⁎ 0.68 1.00 −0.58 −0.24 −0.40

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C. Ye et al. / Science of the Total Environment 517 (2015) 76–85

Table 5 − Regression analysis of net N mineralization rate (MR), net ammonification rate (AR), net nitrification rate (NR), net denitrification rate (DR), N leaching (NH+ 4 -Nl, NO3 -Nl and inorganic Nl) − and plant N uptake (NH+ 4 -Nu, NO3 -Nu and inorganic Nu) against soil properties, root biomass, root N and root C:N ratio across vegetation types.

MR (mg kg−1 day−1) AR (mg kg−1 day−1) NR (mg kg−1 day−1) DR (μg N2O m−2 h−1) −1 NH+ ) 4 -Nl (mg kg −1 NO− ) 3 -Nl (mg kg Inorganic Nl (mg kg−1) −1 NH+ ) 4 -Nu (mg kg Inorganic Nu (mg kg−1)

Regression equations

R2

P

+ Y = 0.171 + 0.144 NH+ 4 -Nu − 0.039 NH4 -N Y = 4.720 + 3.352 total C − 0.002 root biomass − 0.918 pH Y = −2.737 + 0.250 soil C:N ratio Y = 6.517 + 16.393 NH+ 4 -Nu − 2.570 inorganic Nl − Y = 0.837 − 1.414 NH+ 4 -Nu − 0.021 NO3 -Nu + 1.071 inorganic Nu 2 − Y = −13.913 − 0.173 (NO− 3 -N) + 3.672 NO3 -N Y = −4.839 + 0.966 inorganic Nu + 0.774 NO3−-N Y = −0.940 + 6.329 MR + 0.258 NH+ 4 -N Y = 2.887 + 0.643 inorganic Nl − 0.008 root biomass + 6.424 MR − 1.067 root N

0.911 0.977 0.749 0.898 0.825 0.791 0.907 0.913 0.999

0.002 0.001 0.005 0.003 0.054 0.020 0.003 0.002 0.000

soil N transformation rates, N leaching and plant N uptake with soil microclimate, root biomass, root N and root C:N ratio across vegetation types. Linear regression analysis was further conducted to correlate soil N with root N, soil organic C with root biomass, soil C:N ratios with root C:N ratios. All the processes were performed using SPSS 16.0 for windows.

(a)

0.08

-1

Total N (g kg )

0.10

0.06 0.04 0.02

9

-1

Soil organic C (g kg )

0.00

R2 = 0.843 P = 0.010 0.6

0.9

1.2

1.5

1.8

2.1

-2

2.4

2.7

Root N (g m )

(b)

3

R2 = 0.155 P = 0.334 100

200

300

400

3.1. Soil properties, microclimates and plant biological traits The soil organic C, total C and total N were the lowest in the tree soils with no significant difference between the herb and shrub soils (Table 1), whereas soil C:N ratio was higher in the tree soils than that in the herb and shrub soils (Table 1). Soil pH was lower in the shrub soils compared to other soils (Table 1). Seasonal soil temperature and moisture were altered by different vegetation types. Overall, the average soil temperature and moisture significantly differed between the herb and tree soils during the incubation periods, with higher values in the herb soils and lower values in the tree soils (Table 1). The root biomass and root N content were higher in the shrub community compared to herb and tree communities, while root C:N ratio was the highest in the tree soils among vegetation types (Fig. 1).

3.2. Soil inorganic N concentrations, net mineralization, ammonification, nitrification and denitrification rates In general, soil inorganic N concentrations were higher in spring − compared to summer and fall (Fig. 2). The soil NH+ 4 -N, NO3 -N and inorganic-N concentrations in the tree soils decreased from spring to summer to fall (Fig. 2a to c). There was significant difference in soil + NO− 3 -N between vegetation types, whereas NH4 -N and inorganic-N concentrations were lower in tree soils compared to herb and shrub soils (Fig. 2). Similarly, the MR, AR and DR in the shrub and tree soils showed comparable patterns associated with the seasons, with higher values in summer (Table 2 and Fig. 3a, b and d). Soil N transformation significantly differed between the herb and tree soils, with higher values of MR and AR in herb soils and higher NR and DR in tree soils (Fig. 2e to h).

6

0

3. Results

500

-2

Soil C:N ratio

14

Root biomass (g m )

(c)

3.3. N leaching and plant N uptake

12

10

8 50

R2 = 0.410 P = 0.087 60

70

80

90

100

110

Root C:N ratio Fig. 6. The relationship of total N with root N (a), the relationship of soil organic C with root biomass (b), and the relationship of soil C:N ratio with root C:N ratio (c) across the vegetation types and seasons.

− The patterns observed for NH+ 4 -N, NO3 -N and inorganic-N leaching associated with seasons were comparable across vegetation types, with higher values in spring and summer than fall, except for the NO− 3 -N leached in shrub soils (Table 3 and Fig. 4a to c). The vegetation types significantly affected N leaching, except NO− 3 -N, with the highest values in herb soils, intermediate in shrub soils and lowest in tree soils (Fig. 4d to f). Plant N uptake exhibited clear seasonal variations across vegetation types, with higher values in spring and summer than fall (Table 3 and Fig. 5a to c). There were significant differences in plant NO− 3 -N and inorganic-N uptakes between vegetation types (Table 3 and Fig. 5e and f). The plant NO− 3 -N uptake concentration was the lowest in the shrub, but did not differ between the herb and tree (Fig. 5e). The herb absorbed the maximum amount of inorganic-N, but those for shrub and tree were similar (Fig. 5f).

C. Ye et al. / Science of the Total Environment 517 (2015) 76–85

3.4. Controls on soil N dynamics + The MR was positively related to plant NH+ 4 -N uptake and soil NH4 N concentration (Tables 4 and 5). The AR was positively correlated with total C and soil temperature but negatively related with root C:N ratio (Table 4). However, after combining all the factors in the multiple regression analysis, AR was correlated with total C, root biomass and pH (Table 5). The NR was strongly dependent on soil C:N ratio, which explained 75% of the variation in NR (Tables 4 and 5). DR was correlated + with N leaching and plant NH+ 4 -N uptake (Tables 4 and 5). The NH4 N leaching was related to the plant N uptake (Tables 4 and 5). Soil − NO− 3 -N concentration accounted for 79% of the variation in the NO3 -N + leaching (Table 5). Plant N uptake was related to the MR, soil NH4 -N content, leaching of inorganic-N, root biomass and root N (Table 5). The root N significantly accounted for 84% of the variation in soil total N (P = 0.010), and root C:N ratio explained 41% of the variation in soil C:N ratio with marginal significance (P = 0.087) (Fig. 6a and c). Root biomass did not show significant relationship with soil organic C concentration (Fig. 6b).

4. Discussion This study showed that vegetation types (implementing tree, shrub and herb plantations) strongly affected soil N dynamics in the WLFZ of the Three Gorges Reservoir. Tree plantation significantly decreased soil inorganic N concentration, MR and AR, while increased soil NR and DR compared to herb and shrub soils (Table 2 and Figs. 2 and 3). These patterns may be due to interactions of plant N uptake, SOC input, N leaching and soil microclimate in regulating soil N dynamics (DeLaune et al., 2005; Cheng et al., 2011). Alterations in root N uptake in response to vegetation type can greatly affect soil N dynamics (Table 3 and Fig. 5; Hefting et al., 2005). This evidence was supported by our results that root N uptake was correlated with soil NH+ 4 -N loading, MR, root biomass and root N content (Table 5). Higher MR and AR in the herb soils could increase soil inorganic N concentration, leading to higher root N uptake in herb soil than shrub and tree soils (Figs. 3 and 5). Moreover, tree with lower root biomass in the top (0–20 cm) soil absorbed higher NO− 3 -N but similar amount of NH+ 4 -N in comparison to the shrub (Figs. 1 and 5). The results were inconsistent with Hefting et al. (2005) who reported that shrub could remove more nitrate due to the higher root biomass. The discrepancy may be attributed to the selective uptake of nutrients in plants, and different plant N use efficiency between vegetation types (Knops et al., 2002). Furthermore, the relationship between root N and soil total N (Fig. 6) indicated that most of the plant N was incorporated into the soil organic matter, which primarily determined MR and thereby soil N dynamics and primary productivity (Knops et al., 2002; Booth et al., 2005). Different vegetation type can impact soil N dynamics directly by root N uptake and indirectly by regulating the quantity and quality of carbon supplies to the soil (Potthast et al., 2010; Li et al., 2014). In this study, the positive relationship between the AR and total C as well as the relationship between the NR and soil C:N ratio across all the vegetation types (Table 4) suggested that the AR and NR were controlled by soil carbon quality (Booth et al., 2005; Cheng et al., 2013; Li et al., 2014). Changes in the quantity and quality of soil carbon due to vegetation type (Table 1 and Fig. 6) can determine the MR, and in turn can influence the total amount of soil inorganic N produced (Knops et al., 2002; Li et al., 2014). Being inconsistent with Greenan et al. (2006) and Leppelt et al. (2014), who presented that lower soil C:N ratio increased denitrification, we found that higher soil C:N ratio in tree soils were associated with higher DR, probably due to higher NR in tree soils leading to increased denitrification (Table 1 and Fig. 3). Overall, higher plant NO− 3 -N uptake and lower MR and AR, together with higher NR and DR could cause lower inorganic N pools in the tree soils in comparison with the herb and shrub soils (Figs. 2, 3 and 5).

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Vegetation types also strongly affected the N leaching in the WLFZ (Table 3 and Fig. 4). Herb plantations significantly increased the NH+ 4 N and inorganic N leaching, while tree significantly decreased the NH+ 4 -N and inorganic N leaching compared to shrub soils (Fig. 4d and f). These results were probably related to plant N uptake, SOC supplied − by plants and soil inorganic N (NH+ 4 -N and NO3 -N) concentrations (Table 5; Knops et al., 2002; Booth et al., 2005). This evidence was supported by our results that plant NH+ 4 -N and inorganic N uptakes explained most of the variations in the NH+ 4 -N and inorganic N leaching (Table 5). Meanwhile, Hruška et al. (2012) have demonstrated that the timing and degree of plant N uptake control the rates of N loss from ecosystems. We found that the different vegetation types could regulate the quality and quantity of root C inputs (Fig. 6), which could determine the soil MR and NR and therefore influenced the total amount of inorganic N produced as well as leached from the ecosystem (Hefting et al., 2005; Li et al., 2014). In the present study, lower MR and AR in tree soils caused by lower amount of SOC inputs (Table 1 and Fig. 3), together with higher DR and plant NO− 3 -N uptake (Figs. 3 and 5) compared to shrub soils led to lower soil inorganic N concentration and leaching (Figs. 2 and 4). However, in herb soils, higher plant N uptake and then faster incorporation into the SOC, could promote soil MR and AR and thereby increase soil inorganic N produced and leached from the ecosystem (Figs. 2 to 5; Knops et al., 2002). Interestingly, different vegetation types did not significantly impact the NO− 3 -N leaching from ecosystems (Fig. 4e). Our stepwise regression analysis also showed that the soil NO− 3 -N loading can explain 79% variation in the leaching of − NO− 3 -N (Table 5). The similar concentrations of NO3 -N under the three vegetation types contributed to the non-significant differences in the NO− 3 -N leaching (Figs. 2e and 4e). The results indicated that any factors − impacting the soil NO− 3 -N loading could regulate the soil NO3 -N leaching. Soil N dynamics can also be regulated by soil microclimates (e.g. soil moisture, soil temperature and soil pH) (Tables 4 and 5). Our results indicated that the soil AR was significantly correlated with soil temperature, but not with soil moisture (Table 4). Soil temperature regulated soil N transformation by altering microbial activity (Wang et al., 2006). Increase in AR at the higher temperature was in agreement with the results of previous studies (Nicolardot et al., 2001; Dalias et al., 2002; Wang et al., 2006). The soil moistures were all within the optimum moisture range (20–35%) across the vegetation types examined in the present study (Table 1). Thus, the soil AR was found to be more sensitive to soil temperature than soil moisture. Moreover, soil biotic factors (e.g. soil organic C and root biomass) can interact with soil microclimate to impact soil N transformation (Knoepp and Vose, 2007). In the present study, the relationship between soil pH and AR was not significant (Table 4), whereas the stepwise regression analysis showed that the interactive effects of soil total C and root biomass together with soil pH explained 98% variation in soil AR (Table 5). These results suggested that changes in plant C substrate supply represented as soil total C and root biomass is more important in determining the soil N dynamics than soil microclimate (Cheng et al., 2011). Soil N transformations including MR, AR and DR were higher in summer (rain season) for the shrub and tree soils compared to other seasons (Fig. 3), possibly attributed to higher temperature and moisture stimulating microbial activity and accelerating soil N transformation. Other studies also found similar seasonal variations in soil N transformation in other ecosystems (Eviner et al., 2006; Tripathi and Singh, 2009; Li et al., 2014). However, the NR in shrub soils was lower in spring and summer compared to the fall, possibly due to higher DR (Fig. 3c and d). Meanwhile, the plant N uptake also showed significantly seasonal variations, with higher N uptake in summer for growth under the three vegetation types, except plant NO− 3 -N uptake in shrub soils (Fig. 5), which is consistent with previous studies demonstrating that the plant traits including plant N uptake, plant C substrate input and root turnover, varied seasonally and thereby caused the seasonal variations on soil N dynamics (Eviner et al., 2006). The lower plant NO− 3 -N uptake in summer under the

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shrub soils was probably related to the selective uptake of nutrients in plants (Knops et al., 2002). Additionally, similar seasonal variations was observed in the N leaching with higher N leaching in spring and summer seasons than fall under the three vegetation types, except for the NO− 3 -N leached in shrub soils (Fig. 4). The results were directly related to the higher precipitation in summer accelerating the N leaching (Li et al., 2014). Meanwhile, higher MR and AR in summer increased the soil inorganic N concentration and then promoted leaching process (Fig. 3; Knops et al., 2002). However, higher NO− 3 -N leaching in shrub soils in fall (Fig. 4) was probably due to less plant NO− 3 -N uptake (Fig. 5 and Eviner et al., 2006) and lower DR in fall than other seasons (Fig. 3). Higher NO− 3 -N leaching in tree soils during spring was probably related to the higher NR in tree soils at that time compared to shrub soils (Figs. 3 and 4). Thus, the seasonal variations in plant N uptake, soil N transformation, and N leaching interactively regulated the seasonal dynamics in soil N (DeLaune et al., 2005; Eviner et al., 2006; Cheng et al., 2013). In summary, soil N dynamics following revegetation (implementing tree, shrub and herb plantations) in the WLFZ of the Three Gorges Reservoir can be indicators of the interactions between the biotic (e.g. plant N uptake, SOC input, soil C:N ratio) and abiotic factors (e.g. soil temperature and pH) in different ecosystems. The low soil inorganic N concentration and lower N leaching in tree soils were mainly associated with low MR and AR and high DR and plant NO− 3 -N uptake. This provided evidence that riparian ecosystems respond differently to the type of vegetation established (e.g. Hefting et al., 2005; Liu et al., 2011), which in turn provides strategies for government and policy makers to revegetation and water quality protection. Acknowledgments This research is supported by the Executive Office of the State Council Three Gorges Construction Committee (SX2013-022) and the National Natural Science Foundation of China (No. 31300441). We would like to thank Ming Li, Xunzhang Tong, and Chuan Wu for their assistance during fieldwork, Pingcai Yan for the assistance on the laboratory analyses, and Yole Debellis for editing the manuscript. We also thank Professor Christian EW Steinberg and anonymous reviewers for their constructive suggestions and comments on early draft of this manuscript. References Audet, J., Hoffmann, C.C., Andersen, P.M., Baattrup-Pedersen, A., Johansen, J.R., Larsen, S.E., Kjaergaard, C., Elsgaard, L., 2014. Nitrous oxide fluxes in undisturbed riparian wetlands located in agricultural catchments: emission, uptake and controlling factors. Soil Biol. Biochem. 68, 291–299. Bardgett, R.D., Wardle, A.D., 2003. Herbivore-mediated linkages between aboveground and belowground communities. Ecology 84, 2258–2268. Booth, M.S., Stark, J.M., Rastetter, E., 2005. Controls on nitrogen cycling in terrestrial ecosystems: a synthetic analysis of literature data. Ecol. Monogr. 75, 139–157. Brookshire, E.N.J., Gerber, S., Webster, J.R., Vose, J.M., Swank, W.T., 2011. Direct effects of temperature on forest nitrogen cycling revealed through analysis of long-term watershed records. Glob. Chang. Biol. 17, 297–308. Cheng, X., Luo, Y., Su, B., Zhou, X., Niu, S., Sherry, B., Weng, E., Zhang, Q., 2010. Experimental warming and clipping altered litter carbon and nitrogen dynamics in a tallgrass prairie. Agric. Ecosyst. Environ. 138, 206–213. Cheng, X.L., Luo, Y., Su, B., Wan, S.Q., Hui, D.F., Zhang, Q.F., 2011. Plant carbon substrate supply regulated soil nitrogen dynamics in a tallgrass prairie in the Great Plains, USA: results of a clipping and shading experiment. J. Plant Ecol. 4, 228–235. Cheng, X.L., Yang, Y.H., Li, M., Dou, X.L., Zhang, Q.F., 2013. The impact of agricultural land use changes on soil organic carbon dynamics in the Danjiangkou Reservoir area of China. Plant Soil 366, 415–424. Clément, J.C., Pinay, G., Marmonier, P., 2002. Seasonal dynamics of denitrification along topohydrosequences in three different riparian wetlands. J. Environ. Qual. 31, 1025–1037. Curtin, D., Campbell, C., Jalil, A., 1998. Effects of acidity on mineralization: pH-dependence of organic matter mineralization in weakly acidic soils. Soil Biol. Biochem. 30, 57–64. Dalias, P., Anderson, J.M., Bottner, P., Couteaux, M.M., 2002. Temperature responses of net N mineralization and nitrification in conifer forest soils incubated under standard laboratory conditions. Soil Biol. Biochem. 34, 691–701. DeLaune, R.D., Jugsujinda, A., West, J.L., Johnson, C.B., Kongchum, M., 2005. A screening of the capacity of Louisiana freshwater wetlands to process nitrate in diverted Mississippi River water. Ecol. Eng. 25, 315–321.

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