Responses of peat carbon at different depths to

Science of the Total Environment 548–549 (2016) 429–440

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

Responses of peat carbon at different depths to simulated warming and oxidizing Liangfeng Liu a,c, Huai Chen a,b,c,⁎, Qiuan Zhu a,c, Gang Yang c,d, Erxiong Zhu a,c, Ji Hu a,c, Changhui Peng a,e, Lin Jiang a,c, Wei Zhan a,c, Tianli Ma a,c, Yixin He b,c,f, Dan Zhu b,c a

State Key Laboratory of Soil Erosion and Dry land Farming on the Loess Plateau, College of Forestry, Northwest A&F University, Yangling 712100, China Key Laboratory of Mountain Ecological Restoration and Bioresource Utilization & Ecological Restoration Biodiversity Conservation Key Laboratory of Sichuan Province, Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu 610041, China c Zoige Peatland and Global Change Research Station, Chinese Academy of Sciences, Hongyuan, 624400, China d School of Life Science and Engineering, Southwest University of Science and Technology, Mianyang 621010, China e Center of CEF/ESCER, Department of Biology Science, University of Quebec at Montreal, Montreal, Canada f Key Laboratory of Physical Geography and Environment Process of Qinghai Province, Qinghai, Normal University, Xining 810008, China b

H I G H L I G H T S

G R A P H I C A L

A B S T R A C T

• Advanced temperature and O2 increased soil respiration much with different increments. • Old soil accounted for a larger proportion of soil respiration and increased increments. • Much difference was observed between our peatlands and others of higher latitudes.

a r t i c l e

i n f o

Article history: Received 24 July 2015 Received in revised form 16 November 2015 Accepted 27 November 2015 Available online xxxx Editor: CASAR Keywords: Zoige plateau peatlands

a b s t r a c t Warming and water table drawdown greatly reshape peatland carbon cycle, especially when considering the old carbon stored under the peatland subsurface. However, little is known about the effects of warming, oxidizing by drying or their combination on carbon decomposition at different depths (0–100 cm) of peat. In this research, soil of different depths from Zoige Plateau was incubated in four scenarios (8 °C-anaerobic, 8 °C-aerobic, 18 °C-anaerobic and 18 °C-aerobic) to detect the exported carbon. Our result showed that soil respiration (Rs) increased obviously with enhanced temperature and oxygen. The total CO2 fluxes of 2400.22 ± 57.69 mg m-2 d-1 under 8 °C-anaerobic condition increased by 73.6%, 40.7% and 176.5% with warming, oxidizing and their combined effect, respectively. The average dissolved organic carbon (DOC) concentration was 74.90 ± 8.09 mg kg-1 under 8 °C-anaerobic condition, but increased by 53.5%, 44% and 159.4%, respectively under the condition of warming, oxidizing and their combination. Rs and its variation under warming and oxidization differed significantly among

⁎ Corresponding author at: Key Laboratory of Mountain Ecological Restoration and Bioresource Utilization & Ecological Restoration Biodiversity Conservation Key Laboratory of Sichuan Province, Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu 610041, China. E-mail address: [email protected] (H. Chen).

http://dx.doi.org/10.1016/j.scitotenv.2015.11.149 0048-9697/© 2016 Elsevier B.V. All rights reserved.

430 incubaiton aerobic environment anaerobic environment

L. Liu et al. / Science of the Total Environment 548–549 (2016) 429–440

different depths, probably caused by the differences of soil substrate, especially the variation in distribution of soil microbes and enzymes among depths of peatlands. By classifying the source of Rs as young soil (YS: 0–20 cm) and old soil (OS: 21–100 cm), this reseaerch found that OS accounted for a huge part of total Rs under 8 °C-anaerobic condition (CO2: 74.2%; DOC: 60.7%). Such relative contribution of OS to total Rs did not change obviously with warming or oxidizing. Though YS and OS responded equally to warming and oxidizing, OS was responsible for a larger proportion of total increase in Rs. Compared with other studies, we concluded that peatlands soil in our field of mid-latitude and high altitude is less sensitive to warming and oxidizing than peatlands of higher latitude, but that OS of this peatlands is more critical in predicting regional carbon cycle. © 2016 Elsevier B.V. All rights reserved.

1. Introduction With 15–30% of total world soil carbon, peatlands, mainly distribute in the northern high latitude areas, are an important carbon sink for the atmosphere (Gorham, 1991; Knoblauch et al., 2013; Lee et al., 2012). Large quantity of carbon deposits in peatlands is a result of the imbalance between production and decomposition (Knoblauch et al., 2013; Laiho, 2006). The decomposition was much lower than production for water saturated condition in peatlands and the consequent anaerobic environment accompanied with low temperature (Bubier et al., 2003; Griffis et al., 2000). In the changing environment, the fate of carbon in peatlands will depend on the response of soil substrate to the changes of water regime, O2 abundance and temperature (Avis et al., 2011; Chen et al., 2014). Just like soil characters that are determined by vegetation and vary markedly with climate (Chu et al., 2010; Zak and Kling, 2006), peat as the remains of vegetation may also differ among the whole depth profile as a result of climate change during peat development (Moore and Dalva, 1997) and cryoturbation (O’Donnell et al., 2012; Rinkes et al., 2013; Treat et al., 2014; Wickings et al., 2012). Under a warm and humid climate, peat mainly derives from Cyperaceae and Equisetaceae; under a cool and dry climate, however, it mainly consists of Picea remains (Guo et al., 2013). Cryoturbation can redistribute carbon among the whole depth profile (Schuur et al., 2008). With comparatively high water table, low oxygen diffusion and low temperature in peatlands, carbon is protected from decomposition and seldom participates in carbon cycle since its formation (McCallister and Del Giorgio, 2012; Singer et al., 2012). Global warming have increased air temperature by 0.88 °C from 1988 to 2012, and even more at the end of the 21 century (IPCC, 2013). Climate warming, land use changes and hydrologic redistribution have changed local, regional and global carbon cycle (Hicks Pries and Schuur, 2013) and have the potential to shift peatlands from a carbon sink to a carbon source (Dorrepaal et al., 2009; Knoblauch et al., 2013; Schuur et al., 2009; Wang et al., 2013; Yan et al., 2014). High altitude areas where climate is sensitive to warming are experiencing a “much larger than average” increase in temperature (Knoblauch et al., 2013; Lee et al., 2012; Liu and Chen, 2000; Peng et al., 2014). Besides warming, water table drawdown is the other very important cause for the degradation of peatlands in recent decades on Zoige Plateau peatlands - one of the largest alpine peatlands in the world (Bai et al., 2013; Chen et al., 2010; Gao, 2006; Li et al., 2010). Water table drawdown may destroy the stable environment in peatlands, exposing the preserved carbon to aerobic (AE) environment (Oechel et al., 1998), and together with the optimum soil moisture creating an available environment for microbes (Serreze et al., 2000; Yan et al., 2014; Zimov et al., 2006). Water table drawdown also shifts soil respiration (Rs) pathway from anaerobic (AN) to aerobic environment, which responds to climate change differently (Knoblauch et al., 2013; Lee et al., 2012; Schuur et al., 2008; Treat et al., 2014; Yang et al., 2014). Studies showed that the stored old carbon in deep soil of degraded peatlands had participated in modern carbon cycle (McCallister and Del Giorgio, 2012; Schuur et al., 2009; Singer et al., 2012). However, the responses of peat of different depths to the changing environment remains poorly understood. The main factors in Rs include soil microbial communities, enzyme diversity and nutrient condition (Lawrence et al., 2009; Moorhead and

Sinsabaugh, 2006) which all vary with temperature and O2 conditions (Kim et al., 2012). Most microbes and enzymes are sensitive to temperature and O2 change, and so is soil nutrient determined by vegetation that varies with climate (Mikan et al., 2002). Warming leads to an earlier spring thawing in peatlands (Briones et al., 2014) with an advanced increase in microbial activity, as well as Rs. O2 can activate most oxygen enzyme activities which could be a proximate control of soil organic matter (SOM) dynamics, especially in plateau peatlands (Laiho, 2006; Sinsabaugh et al., 2008; Tian and Shi, 2014). O2 also relieves the inhibition effect of polyphenolic on soil hydrolase and microbial activity (Freeman et al., 1997; Freeman et al., 2001a). Therefore, understanding the response of soil microbes, enzymes and nutrient condition to the changes of temperature and O2 is important to predict peatland carbon cycle. The main objective of this study was to detect the response of peat at different depths to warming and oxidizing. The specific objectives were to: 1) determine the changes of peat Rs under warming and oxidizing conditions; 2) quantify the Rs increase increment of each layer in warming and oxidizing conditions, the contribution of young soil (YS: 0–20 cm) and old soil (OS: 21–100 cm) to total Rs and their contribution to the increased Rs in warming and oxidizing conditions; 3) detect the roles of microbes, enzymes and nutrient conditions in soil carbon decomposition. 2. Materials and methods 2.1. Sampling sites Samples were collected from the Zoige Peatland and Global Change Research Station, Chinese Academy of Sciences (33°06′25′′ N, 102°38′ 33′′ E), located at the Riganqiao Provincial Wetland Reserve (av. 3400 m a.s.l.) in the northeastern Qinghai-Tibetan Plateau (Fig. 1). Zoige peatlands cover an area of about 4605 km2, with about 3179 km2 intact peatlands and 1426 km2 degraded peatlands. The basal age of carbon ranges from 1635 to 14095 cal yr BP (Chen et al., 2014). In an orbicular shape, Zoige plateau is surrounded by a series of alpine mountainsand affected by the southwest monsoon and southeast monsoon, it belongs to the cold Qinghai-Tibetan climatic zone with an annual average temperature of 1.5 °C and precipitation of 720 mm. The warmest monthly temperature (10.9 °C) is recorded in July and the coolest in January (-10 °C) (Yang et al., 2014). The peatland on Zoige plateau has a peat depth of 0.2–6.0 m (mean depth about 1.39 m), an average pH of 6.6–7.0 (Tian et al., 2012), and a mean peat accumulation rate of 0.39 mm yr-1 (from 0.12 to 0.85 mm yr-1) (Chen et al., 2014). The water table, though fluctuating seasonally, was approximately 0 cm during our sampling in October 2013. So the sampled soil was in water saturated condition. The dominant vegetation at Riganqiao is herbaceous plants including Carex muliensis, Trollius farreri, Gentiana formosa, and Caltha palustris (Yang et al., 2014). 2.2. Experiment design Soils of each depth (0–100 cm, with intervals of 10 cm) were incubated under four scenarios: (1) anaerobic at 8 °C (8 °C-AN); (2) aerobic at 8 °C (8 °C-AE); (3) anaerobic at 18 °C (18 °C-AN); (4) aerobic at 18 °C (18 °C-AE). Rs of each depth and each condition were monitored during


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Fig. 1. Map of Zoige Plateau, located on the northeast of Qinghai-Tibet Plateau, showing the location of sample sites.

the 35-day incubation. The presumption was that warming and oxidizing function on soil from the surface to the depth in a gradual pattern (Fig. S1). Such gradual effect was measured for each 10 cm depth throughout the whole 100 cm depth profile. We recorded the total Rs (the sum of Rs in all ten depths), the increased Rs at each depth and the contribution to the total Rs increment under 8 °C-AE, 18 °C-AN and 18 °C-AE in comparison to that under 8 °C-AN. The source of Rs was classified as YS and OS. We detected the proportion of YS and OS to the total Rs under each condition, and the relative contribution of OS to the total Rs increment in response to warming and oxidizing. 8 °C was chosen as the incubation temperature because it was the mean temperature of vegetation period in 1970; after that the Zoige Plateau was involved in the significant and universal warming, with an increase of 0.4 °C per decade (Yang et al., 2014). At our experiment time, the surface soil had been under warming for 4 decades, but the deeper soil was scarcely affected. We thus assumed the temperature of 8 °C as the original condition of soil not influenced by the climate change. On the other hand, 18 °C was chosen as the warming temperature to get a soil sensitive data (Q10) of incubation condition.

2.3. Soil sampling and incubation Peat samples (0–100 cm) were collected randomly in October 2013 by a gasoline drill before soil freezing. Soil samples of every 10 cm as a depth were wrapped with foil paper in low temperature and transported to the laboratory. Sample for each depth was divided into two parts, one for incubation and the other for soil chemical analysis. Before incubation, roots (N1 mm in diameter) were cautiously removed by hand in case of disturbance on origin soil structure. Soil for chemical analysis was sieved through 2 mm mesh to remove visible roots or stones and stored at 4 °C. The incubation experiment was done under four conditions with triplicate sampling for soil of all ten depths, so altogether there were 120 samples (4 conditions × 3 samples × 10 depths). For each sampling, 60 g soil was cut from the origin soil and placed in a 500 ml glass jar with rubber stopper. The jars were flushed with N2 for 5–10 min to keep an anaerobic headspace for AN conditions, and with CO2-free air for AE conditions. All jars were kept sealed and dark during incubation. Every 24 h after incubation, 10 ml headspace gas was sampled with a syringe equipped with three way valve to measure the CO2 concentration by gas

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chromatography (Agilent 7890A, Agilent Co., USA) equipped with a flame ionization detector (FID) operating at 250 °C. The headspace was again flushed with N2 or CO2-free air to remove the cumulated CO2 after each sampling. The CO2 emission rate was calculated as: T0 P V0 1 0 F ¼ PPM:M 22:4 T P 0 A d

where F (mg CO2.m-2.d-1) is the rate of CO2 emission; M0: the molar mass of CO2; T and P: the temperature and atmosphere pressure of jar headspace; T0 and P0: the atmosphere pressure and absolute temperature under standard conditions; V0: the bottle volume that is 500 × 10-6 m3; d: the incubation time that was 1 d. A: the effective area of soil surface in emission CO2 calculated based on soil density (m-2). (In the experiment, the incubated soil was cut from soil core in cubic shape that theoretically had six surfaces releasing CO2; but one surface was connected with the jar bottom that impeded gas release, so the effective area of soil surface is the sum of other five surfaces.) The increased percentage was calculated with the equation of %= (F in -F non )/ Fnon ⁎ 100%, where F in is the carbon export rate at warming, oxidizing or co-function conditions, and Fnon that under the 8 °C-AN condition. Q10 is defined as the ratio of CO2 emission at temperature T + 10 (°C) relative to that at temperature T (°C). After 35-day incubation, soil of each condition was taken out for analyses of enzyme activity, microbial biomass carbon (MBC) and dissolved organic carbon (DOC) concentration. Considering the possible influences of moisture loss to the incubation results, we did one affiliated experiment beforehand to predict the moisture loss, where we found that soil moisture decreased but not much during incubation, from 220.8% to 204.8%. During incubation the jars were completely sealed, permitting only 5–10 minutes of gas exchange time. Therefore, the short incubation period (35 days) did not cause much moisture loss, similar to other short incubation experiments (Wang et al., 2013; Szafranek-Nakonieczna and Stêpniewska, 2014).

2.4. Soil character analysis Origin soil characters including total carbon (TC), total nitrogen (TN), DOC, MBC and the activity of three enzymes (phenol oxidase, peroxidase and cellulase) were detected in triplicates of 3 soil samples (3 samples × 3 analyses × 10 depths) before incubation. TC and TN were determined by total organic carbon analyzer (LIQUIL TOCII, Elementar, Germany) and automatic azotometer (KjeltecTM8400 Analyzer UnitUnitU nit, Foss, Sweden). DOC was extracted with 2 M KCL solution for 60 min on a shaker at 250 rpm; the extracted solution was filtered through 0.45 μm filter membrane and detected with continuous flow analyzer (SKALAR San ++, SKALAR Co., Netherlands). MBC was detected by chloroform fumigation (Vance et al., 1987). Both fumigated and non-fumigated soils were extracted with K2SO4 solution, and the extraction was analyzed on total organic carbon analyzer (LIQUIL TOCII, Elementar, Germany). The difference between fumigated and non-fumigated soils was used to calculate MBC concentration with an extractability of 0.45 (Jenkinson and Ladd, 1981). Activities of three enzymes were determined with methods of Pind et al. (1994) and Guan et al. (1986) (Guan et al., 1986; Pind et al., 1994; Saiya-Cork et al., 2002). All three enzymes were measured spectrophotometrically. Phenol oxidase and peroxidase were measured using L-3,4-dihydroxyphenylalanine (L-DOPA) as substrate with the activity calculated by the equation of Jared L. DeForest (DeForest, 2009; Saiya-Cork et al., 2002). Cellulase was measured using carboxymethylcellulose as substrate with the activity calculated by the equation in Guan et al. (1986). DOC, MBC and activity of the three enzymes were also detected after incubation, with the differences before and after incubation as the DOC exported during incubation and the variations of MBC and enzyme activity, respectively. Soil age of different depths also was calculated. For absence of more direct age data of the experiment area, we supposed that carbon accumulation rate kept stable in the whole depth profile. The known data were about the 8 cm depth detected by 137Cs in Wang et al., 2015 and

the 91–100 depth detected by 14C in Chen et al., 2014. Thus the 10– 20 cm soil age was calculated based on the recent carbon accumulate rate in Wang et al., 2015, and the 21–90 cm soil age was calculated based on an average accumulate rate (Table 1) 2.5. Statistical analysis Carbon export rate, Q10 values and variation of soil characteristics with the depth were assessed with one way analysis of variance (ANOVA). One way ANOVA was also used to assess the effect of four incubation conditions on soil carbon export, enzyme activity and MBC concentration changes with depth (Duncan test was used in the ANOVA analysis). Linear regression was used to examine the effect of soil microbes and enzymes on soil carbon export, and to examine the influence of origin soil characters on the soil carbon export. All data were checked and confirmed to be normally distributed before ANOVA analysis (K-S test). SPSS 20.0 for Windows (SPSS Inc., Chicago, IL, USA) was used for all statistical analysis. 3. Results 3.1. Soil characteristics Soil TC in this study showed a wide range from 171 ± 21.51 g.kg-1 to 551.37 ± 24.62 g.kg-1 (mean ± SE; P b 0.05; Table 1). The highest carbon content was not at the surface but at 80–90 cm depth, and the lowest was at 30–40 cm. The C/N of different depths ranged from 12.36 to 35.39 and changed significantly throughout the whole depth (P b 0.05; Table 1). Different from C/N, DOC concentration changed little with depth (P N 0.05; Table 1). MBC concentration and the activities of phenol oxidase, peroxidase and cellulase decreased substantially with the depth (P b 0.05, Table 1). Calculated from the assumption of stable accumulation rate and the age of soil carbon of 4340 Cal BP at 90–100 cm as detected by 14C in Chen et al. (2014) and 137Cs in Wang et al. (2015), the peat age of each 10 cm interval was found to be 52 4340 yr BP (Table 1). 3.2. Soil carbon emission during incubation 3.2.1. Soil carbon emission under different conditions During the 35-day incubation, CO2 emission rate began low, reached an emission peak at about eighth to twelfth day, and then kept a relative lower state in the remaining days (Fig. S2). We observed that CO2 emission was significantly related to the temperature and O2 (P b 0.01 for both; Fig. 2A). Mean CO2 emission of the whole depth was 2400.22 ± 57.69 mg CO2-C m-2 d-1 under the condition of 8 °C-AN, 3377.13 ± 100.51 mg CO2-C m-2 d-1 under 8 °C-AE, 4166.40 ± 135.17 mg CO2-C m-2 d-1 under 18 °C-AN, and 6637.67 ± 307.22 mg CO2-C m-2 d-1 under 18 °C-AE. Compared with that in 8 °C-AN, CO2 emission increased by 40.7% with O2 and 73.6% with 10 °C temperature increase. The CO2 emission at 18 °C-AE was 176.5% higher than that at 8 °C-AN. The exported DOC during incubation was also significantly related to the temperature and O2 (P b 0.01 for both; Fig. 2B). The highest DOC concentration was 194.3 ± 11.86 mg.kg-1 at 18 °C-AE and the lowest was 74.9 ± 8.1 mg.kg-1 at 8 °C-AN. Under 8 °C-AE and 18 °C-AN conditions, DOC concentration was 44% and 53.5% higher than that at 8 °C-AN, respectively. 3.2.2. Soil carbon emission varied with depth For all four conditions, both produced CO2 and DOC showed significant variations among all depths (P b 0.01 for all; Fig. 3). Both CO2 emission and DOC concentration at 0–20 cm was higher than those of deeper layers, but the variation pattern during deeper depths was different among four conditions. For example, CO2 emission rate at 8 °C-AN showed no much difference among depths, but much difference was observed under other three conditions, with the highest rate at 60–


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Table 1 Origin of soil properties of different depths in sampling site. Depth (cm)

TC (g kg-1)

C/N

DOC mg kg-1

MBC g kg-1

Phenol oxidase nmol gdw-1h-1

Peroxidase nmol gdw-1h-1

Cellulase mg gdw-1 d-1

Calibrated age (cal year BP) mean

0–10 10–20 20–30 30–40 40–50 50–60 60–70 70–80 80–90 90–100

491.93 ± 4.74b 400.4 ± 46.44c 211.85 ±7.4f 171.49 ± 21.54g 297.59 ± 5.82e 259.68 ± 8.85e 476.63 ± 1.35b 347.73 ± 18.60d 551.37 ± 24.62a 268.83 ± 31.61e

26.35 ± 0.95b 24.44 ±1.70bc 14.14 ± 0.36e 12.36 ±1.00e 22.48 ± 0.35c 17.06 ± 0.62d 33.43 ±0.25a 27.81 ± 1.39b 35.39 ± 0.72a 21.29 ± 1.20c

337.93 ±8.02a 261.80 ±26.09b 197.63 ±1.76def 162.03 ± 5.5f 178.83 ±4.15ef 174.90 ±6.82f 231.63 ±8.38bcd 242.9 ± 7.64bc 236.97 ±2.37bc 215.6 ± 5.78cde

2.67 ± 0.10a 2.68 ± 0.13a 2.08 ± 0.08c 1.70 ± 0.04d 2.06 ± 0.17c 1.74 ±0.06d 2.35 ± 0.01b 1.68 ± 0.05d 1.55 ± 0.03d 2.54 ±0.01ab

283.49 ± 28.74a 164.82 ± 2.8bc 147.24 ± 4.90bcd 142.84 ± 2.73bcd 206.58 ±3.80b 156.03 ± 2.19bcd 92.30 ± 4.15cde 74.72 ± 3.23de 92.30 ± 11.41cde 35.16 ± 4.39e

573.03 ± 5.95a 461.50 ± 5.08b 466.99 ± 3.73b 368.10 ± 3.74 c 224.71 ±3.27d 361.51 ± 7.92c 482.38 ± 3.55b 250.80 ±1.91d 189.54 ± 2.28d 178.56 ± 1.50d

477.08 ± 5.17a 490.41 ± 10.78a 359.58 ± 8.23b 137.5 ± 2.31d 166.68 ± 14.38 cd 174.58 ± 4.39cd 170.42 ± 3.00cd 203.33 ± 4.39cd 172.92 ± 11.54cd 223.33 ± 3.21c

52$ 185& 704# 1223# 1742# 2261# 2780# 3299# 3818# 4340⁎

Values are means ± standard error. Different letters among depths indicate significant differences (Duncan test; P b 0.05 for lowercase and P b 0.01 for uppercase). $ : data from (Wang et al., 2015), with soil collected at the same field at Riganqiao. & : data calculated based on peat accumulation rate as 0.9 mm/yr at 10–20 cm in (Wang et al., 2015). ⁎ : data from (Chen et al., 2014), with soil collected at the same field at Riganqiao. # : data calculated based on the stable peat accumulation rate from 21 to 100 cm at Riganqiao.

80 cm of deeper depths. Contrary to CO2, DOC concentration showed much difference in all four conditions. The variation was also the highest at 60–80 cm under 18 °C-AN and 18 °C-AE conditions. By classifying the peat into YS and OS, we found that OS was the major carbon contributor to total Rs under all four conditions, accounting for 74.2%, 70.3%, 71.4% and 65.9%, respectively, to total CO2 emissions under 8 °C-AN, 8 °C-AE, 18 °C-AN and 18 °C-AE conditions, and 60.7%, 64%, 64.8% and 70.6%, respectively, to the total DOC under these conditions (Fig. 4). Rs showed substantial increase under 8 °C-AE, 18 °C-AN and 18 °C-AE conditions, but in different degrees at each depth (Fig. S3). The highest CO2 increase was at 0–10 cm, about 9.2% in 8 °C-AE, 18.7% in 18 °C-AN and 36.7% in 18 °C-AE. In deeper peat, the increase was lower, except for 60–80 cm where the total CO2 emission increased by

11.4% in 8 °C-AE, 23.1% in 18 °C-AN, and 49.4% in 18 °C-AE, accounting for 28.1%, 31.4% and 28% of the total increase under these conditions. The top two depths (0–20 cm) also contributed much to the total increase of CO2 emissions (Fig. S3 A, C and E). The highest DOC increase appeared at 0–10 cm under 8 °C-AE and 18 °C-AE conditions and at 70– 80 cm under 18 °C-AN condition. Similar with CO2 emission increase, DOC increase was also higher at 0–20 cm and 60–80 cm depths. The increase at 0–20 cm accounted for 28.3%, 27.3% and 23.1% of the total DOC increases under the conditions of 8 °C-AE, 18 °C-AN and 18 °C-AE, respectively; the DOC increase at 60–80 cm accounted for 29.6%, 43.8% and 34.7% of the total increase under the three conditions respectively (Fig. S3 B, D and F). In the whole depth profile, the relative contribution of OS to the total increased CO2 emission was 60.6%, 67.5% and 59.6% under 8 °C-AE, 18 °C-AN and 18 °C-AE conditions, respectively. DOC export from OS was responsible for 71.7%, 72.4% and 76.9% of the total increase under 8 °C-AE, 18 °C-AN and 18 °C-AE conditions, respectively.

3.3. Temperature sensitivity It was obvious that Q10 value was higher under AE condition than under AN condition (Fig. 5). With the increase of depth, Q10 values showed significant difference under both conditions (P b 0.01 for both). In the whole depth profile, Q10 was higher at 0–20 cm and 60– 80 cm than other depths under both two conditions.

3.4. Variations of MBC concentration and enzyme activity during incubation

Fig. 2. Difference of soil respiration rate (A: CO2; B: DOC) under four conditions. Different letters and the color indicate significant difference (P b 0.05).

Compared with that after incubation under 8 °C-AN condition, the increase of MBC concentration was substantially higher under other three conditions (Fig. 6; P b 0.01; Table 2). The highest MBC concentration was under 18 °C-AE condition, followed by 18 °C-AN and 8 °C-AE, and the lowest under 8 °C-AN condition. MBC concentration showed little difference among the whole depth in four conditions (P N 0.05). Compared with those in original soil, the activities of phenol oxidase, peroxidase and cellulase changed in different patterns after incubation (Fig. 7). O2 increased phenol oxidase activities much (P b 0.05) but had little effect on peroxidase and cellulase (P N 0.05; Table 2). Temperature had much effect on peroxidase (P b 0.01) but no influence on phenol oxidase or cellulase (P N 0.05; Table 2). Both phenol oxidase and peroxidase had great changes under 18 °C-AE (P b 0.01), but cellulase had none (P N 0.05; Table 2). Among the whole depth, the activities of all three enzymes had significant differences (P b 0.01 for all; Table 2). Corresponding with Rs in the whole depth, a big peak was observed at 60–80 cm in activities of phenol oxidase and peroxidase.

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Fig. 3. Difference of soil respiration rate among the whole depth profile under four conditions. Different letters and color indicate significant difference (P b 0.05).

Fig. 4. Total soil respiration and the proportion of YS (0-20 cm) and OS (21-100 cm) to total soil respiration (A: CO2; B: DOC). Datum above the bar are the proportion of YS and OS respiration to total respiration. Error bars represent standard errors of the means (n = 3).

Fig. 5. Q10 value variations among whole depths under aerobic and anaerobic conditions. Different letters indicate significant difference (P b 0.05).


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Fig. 6. Soil MBC concentration variations during four incubation conditions. Error bars represent standard errors of the means (n = 3).

3.5. Relationship between carbon emission and influencing factors Cumulative carbon emission over 35-day incubation was expressed in CO2 and DOC. No linear relationship was found among CO2 emission rate, DOC concentration and TC, or between CO2 emission and C/N, between DOC and C/N (P N 0.05 for all; Fig. S4). Phenol oxidase, peroxidase and MBC concentration of the original soil showed no linear relationship with CO2 emission rate or DOC concentration (P N 0.05 for all; Figs. S5 and S6). But cellulase activity was found to be of linear related with CO2 and DOC export rate (R2 = 0.31 for CO2; R2 = 0.37 for DOC; P b 0.05; Fig. S5). The MBC concentration was linearly correlated with DOC and CO2 export under all four conditions (R2 = 0.66 for CO2; R2 = 0.54 for DOC; P b 0.01; Fig. 8). During incubation, three enzymes had different effect on CO2 and DOC export (Fig. 9). CO2 emission and DOC concentration were positively correlated with phenol oxidase activity under 18 °C-AE and 8 °C-AE conditions (R2 = 0.40, R2 = 0.38 for CO2; R2 = 0.24, R2 = 0.26 for DOC; P b 0.01 for all), and were positively correlated with peroxidase activity under 18 °C-AE and 18 °C-AN conditions (R2 = 0.74, R2 = 0.27 for CO2; R2 = 0.35, R2 = 0.20 for DOC, respectively; P b 0.01 for all). Under all four conditions, neither DOC nor CO2 emission rate was correlated to cellulase activity (P N 0.05 for all).

Fig. 7. Soil enzyme activity variations during four incubation conditions. Error bars represent standard errors of the means (n = 3).

4. Discussion 4.1. Comparisons with other studies Since soil samples were kept intact during incubation in this study to better simulate field condition, we had expected the result of CO2 emission rate would be higher than those measured at other sites across the peatlands, because CO2 flux in our study was the respiration of 0–100 cm soil and the results of others were CO2 at soil surface. But contrary to our expectation, the CO2 emission rate of 2400.22±57.69 mg m-2 d-1 under 8 °C-AN condition was much lower than most studies,

Table 2 Significance of Pearson’s rank correlation between carbon emission rate and enzyme activity changes under different incubation conditions.

CO2 DOC MBC Phenol Oxidase Peroxidase Cellulase

Warming × oxidizing

Oxidizing

Warming

Depth

** ** ** ** ** ns

** ** ** * ns ns

** ** ** ns * ns

** ** ns ** ** **

“ns” indicates no significant correlation; “*” indicates significant correlation at P b 0.05; “**” indicates highly significant correlation at P b 0.01.

Fig. 8. Relationship between soil respiration and MBC concentration after incubation (A: CO2; B: DOC).

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Fig. 9. Relationship between soil respiration and enzyme activities under four incubation conditions (PhenO: phenol oxidase; PerO: peroxidase; Cellu: cellulase).

including peatlands (4941.6–7528.8 mg m-2 d-1) (Berglund and Berglund, 2011; Dorrepaal et al., 2009; Mäkiranta et al., 2008; Peng et al., 2014), forest (6272.64–6697 mg m-2 d-1) (Yan et al., 2014; Zeng et al., 2014) and grassland (5772.3–6538.75 mg m-2 d-1) (Cao et al., 2001; Liu et al., 2009) (Table 3). The main reason probably was that other studies were done in the field and the results represented ecosystem respiration (Reco) containing autotrophic respiration (Ra) and heterotrophic respiration (Rh). In our study, however, fresh root (N 1 mm in diameter) were removed carefully before incubation and thus our result only represented Rh. Compared with the study which only detected

Rh at soil surface (1044.44–1430.56 mg m-2 d-1) (Minkkinen et al., 2007), our result was obviously higher. With about 40.4–56.5% more carbon lost from deeper soil, our result demonstrated that the subsurface carbon in peatlands had huge potential in increasing Rs. Giardina and Ryan (2000) found that soil substrate quality had controlled effect on deeper soil decomposition. Contrary to the idea that deeper soil carbon was older and more recalcitrant to environment changes (Liski et al., 1999; Giardina and Ryan, 2000), we found deeper soil being sensitive to environment changes (Knorr et al., 2005) and increasing carbon loss. Such results should be very useful for modeling scientists to


calibrate their models. Since the current carbon models for peatlands do not include into consideration the carbon loss from subsurface and deep soils, therefore probably under-estimating the real carbon loss from peatlands (Bond-Lamberty and Thomson, 2010; Davidson and Janssens, 2006; Fan et al., 2014; McGuire et al., 2012; Rowson et al., 2013; Todd-Brown et al., 2013; Watts et al., 2014). 4.2. Effects of temperature and oxygen It is widely accepted that temperature determines SOM decomposition, especially in peatlands for the special climates (Hobbie et al., 2000). The direct result of water table drawdown in peatlands is O2 participating in peatland Rs. Therefore, with degradation of peatlands, increased temperature and O2, as well as their combination, may have important effect on peatlands Rs. We found that temperature increased CO2 and DOC export rate by an average of 73.6% and 53.5%, respectively, and O2 increased CO2 and DOC export rate by an average of 40.7% and 44.0%, respectively. The effect of temperature on Rs has been illustrated in a wide range of studies (Eliasson et al., 2005; Fierer et al., 2005; Lloyd and Taylor, 1994; Tucker et al., 2013). Biasi et al. (2005) reported that temperature could influence the utilization of carbon source by microbes or microbial metabolism leading to Rs rate changes. Treat et al. (2014) found that warmer and drier climate could result in substantial increase in carbon loss (Biasi et al., 2005; Dutta et al., 2006; Treat et al., 2014). DOC also was driven by temperature rising (Freeman et al., 2001b). O2 deficiency inhibited Rs (Freeman et al., 2001a; Mettrop et al., 2014) and O2 could accelerate SOM decomposition (Blodau and Moore, 2003; Fenner and Freeman, 2011; Kane et al., 2013; Moore and Knowles, 1989; Oechel et al., 1998). In saturated peatlands, water not only displaces air from soil pores, but also hinders gas exchange between soil and atmosphere (Minkkinen et al., 2007). Water table drawdown, however, supplies soil porosity for gas diffusion, permitting O2 to increase Rs by being the terminal electron acceptor during Rs (Kane et al., 2013; Keller and Takagi, 2013; Kristensen and Holmer, 2001). At the same time, the difference of Q10 values under AE and AN conditions also demonstrated that soil

437

carbon became more liable to microbes under O2 abundant environment (Lee et al., 2012; Wang et al., 2013). Though the effect of temperature and O2 on Rs had been well studied in other peatlands (Knoblauch et al., 2013; Moore and Dalva, 1997; Szafranek-Nakonieczna and Stêpniewska, 2014; Treat et al., 2014; Wang et al., 2013), our results from an area of midlatitude and high altitude were different from others. Rs increase with oxidizing or 10 °C warming was much lower in our study than in other incubation studies (85.8–226.1% and 128.9–200%) (Table S1), indicating the lower sensitivity of peat in this area to warming and oxidizing, which can be explained by the different climate (temperature and precipitation) and vegetation in our study area from those of the others (Table S1). Under the combined effect of warming and oxidizing, CO2 and DOC export rate in 18 °C-AE were 176.5% and 159.4% higher than that in 8 °C-AN. Such combination condition represented the degenerating peatlands, where substantial carbon was released as CO2 to the atmosphere (Zhu et al., 2012) and as DOC to the nearby waters (Chen et al., 2014; Singer et al., 2012). On one hand, in a warmer and O2 richer environment, SOM becomes more available for microbes that accelerate Rs (Guntiñas et al., 2013). On the other hand, warming may dry up peatlands, which in turn accelerates SOM decomposition (Dorrepaal et al., 2009; Fenner and Freeman, 2011; Munir et al., 2015). 4.3. Variations among the whole depth profile The results showed that Rs differed significantly among the whole profile, but with different patterns in four conditions. Both CO2 and DOC export rates were higher in 0–20 cm than in deeper layers. This result was consistent with other studies (Biasi et al., 2014; Wang et al., 2013) and in agreement with the idea that older soil found in deeper layers contains higher proportions of “recalcitrant” carbon than younger soil at surface (Bosatta and Agren, 1999; Hogg et al., 1992; Knorr et al., 2005; Nadelhoffer et al., 1991). Under the condition of restricted temperature and O2 (8 °C-AN), Rs did not differ much among soils of different depths; under other three conditions where temperature and O2 were not so restricted, however, CO2 and DOC export rates were all substantially higher than those of the same depth in 8 °C-AN condition. But

Table 3 Comparisons of CO2 emission from peatlands under different incubation conditions Type

Country

Location

Depth (cm)

CO2(mg m-2.d-1)

Reference

Peatlands

China

Zoige Plateau, 33°06′N,102°38′E Abisko, in north Sweden 68°21′N,18°49′E Örke, in central Sweden 60.03°N,17.45°E Majnegården, in southern Sweden 58.13°N,13.54°E Yangtze River source 34°49′N,92°56′E Kannus municipality 65°55′N,23°51′E Seida 67°03′N,62°57′E Kicalo 58°59′N,25°27′E Väätsa 66°21′N,26°37′E Taihang mount 37°53′N, 114°16′E Dinghushan 23°09′-23°12′N, 112°31′-112°3′E Haibei station 37°37′N,101°19′E Inner Mongolia 42°02′N,116°17′E

100 cm

2400.22±57.69

This study

Surface

4941.6#⁎

Dorrepaal et al. (2009)

Surface

6373.2±448.8⁎ 5797.2±496.8⁎ 8548.8±448.8⁎ 7528.8±484.1⁎

Berglund and Berglund (2011)

Surface

5702#$

Peng et al. (2014)

surface

6980.82±564%

Mäkiranta et al. (2008)

surface

2755±133.7⁎

Biasi et al. (2014)

Sweden Sweden

China Finland Russia Finland Estonia Forest

China China

Grassland

China China

# data collected from figures with GETDATA. ⁎ : data directly collected from paper and transformed from “mg CO2 m-2 h-1”. $ : data directly collected from paper and transformed from “μmol CO2 m-2 s-1”. % : data directly collected from paper and transformed from “g CO2 m-2 a-1”.

Surface

1430.56

%

Minkkinen et al. (2007)

1044.44% Surface Surface

6272.64$ 6697#

Zeng et al. (2014) Yan et al. (2014)

Surface

5772.295±516.48%

Cao et al. (2001)

Surface

6538.75#$

Liu et al. (2009)

438


the increment at each depth was unequable and differed much with depth, which may reflect the variation of soil substrate among all profiles (Treat et al., 2014). The fact that the increments at 0–20 cm and 60–80 cm were higher than other layers may demonstrate that the carbon at these two layers is intrinsically labile and has higher potential decomposability (Oechel et al., 1998). Q10 values also were higher at these two depths under both AN and AE conditions. This was probably because plenty of new carbon (fresh litters) participated in surface soil at the late growing season, resulting in a higher Rs at surface soil (Keller and Takagi, 2013). In addition, soil invertebrates, including enchytraeids that mainly distribute at surface soil, also could increase Rs by comminuting and mixing soil substrate. Another reason was probably related to the formation condition of peat at these depths. The speculated age of peat at 60–80 cm was about 2780–3299 Cal. BP (Table 1). We found that during this period the climate of Riganqiao was warmer and slightly humid (Guo et al., 2013), which could lead to deposition of more plant debris and carbon. The deposited carbon was stored away from atmosphere and was sensitive to warming and oxidizing (Bosatta and Agren, 1999; Dorrepaal et al., 2009; Knorr et al., 2005). It would be decomposed when enough energy was supplied (Biasi et al., 2005). CO2 emission from deeper depths (21–100 cm) kept stable under 8 °C-AN condition but had unequal increases under warming and oxidizing conditions. It was probably because in a restricted environment, environment factors like temperature and O2 restricted Rs; but in a looser environment with higher temperature and more O2, soil substrate character was the main factor controlling Rs. Different from CO2, DOC concentration from deeper depths was not stable under 8 °C-AN condition. This was probably because soil DOC concentration is dependent on a balance between production from vegetation and SOM and consumption by soil organisms (Dalva and Moore, 1991; Jones et al., 2003; Van den Berg et al., 2012). The difference in organisms may lead to different consumption, and therefore instable DOC. By classifying the source of Rs into YS and OS, we found that YS (CO2: 25.8%; DOC: 39.3%) contributed less to total Rs than OS (CO2: 74.2%; DOC: 60.7%). We further found that the relative contribution of OS to total Rs was of very little, if any, change with warming and/or oxidizing. YS and OS responded equally to warming and oxidizing, with OS still responsible for a large part (70.3%, 71.4% and 65.9% respectively for CO2 in condition of 8 °C-AE, 18 °C-AN and 18 °C-AE; 64%, 64.8% and 70.6% for DOC at the same condition) of the total increase in Rs. With climate warming and oxidizing, most peatland carbon pools may become destabilized, releasing their stored carbon to the atmosphere in CO2 or to rivers in DOC (Freeman et al., 2001a; Freeman et al., 2004; Moore and Basiliko, 2006; Pastor et al., 2003). Aged carbon exporting DOC to rivers is receiving increasing attentions (Butman et al., 2015; Marwick et al., 2015). The contribution of OS to total Rs was much higher in our study than that in other studies (6–18% in Hicks Pries and Schuur, 2013; 7–41% in Schuur et al., 2009), suggesting that OS was probably more critical in peatlands of mid-latitude and high altitude than others in predicting regional carbon cycle in a warming world. This difference may be determined by the peat type, climate and carbon cycle patterns which are greatly different among the studied peatlands. 4.4. Roles of microbes, soil enzyme and soil substrate The effect of increased temperature and O2 as well as their combination on Rs is mainly through acting on soil microbes and enzymes. In our study, MBC concentration increased substantially during incubation, with strong correlation between MBC concentration and Rs after incubation. Enhanced temperature and O2 not only increased microbial quantity but also enriched the structure of soil microorganism community (Lee et al., 2012; Mikan et al., 2002). Bacteria, fungus and Actinomyce are the main decomposers in peatlands carbon dynamic (Briones et al., 2014; Laiho, 2006; Tveit et al., 2013), all involved in both AN and AE respiration (Szafranek-Nakonieczna and

Stêpniewska, 2014). The increase of aerobic bacteria in O2 abundant environment may lead to higher Rs. Fungi are more efficient than bacterial in producing extracellular enzymes and in decomposing high molecular weight compound (Tveit et al., 2013). The inhibition effect of polyphenol compound on fungi was relieved in O2 abundant environment. Soil enzymes, mainly produced by microorganisms, respond to the changes of soil environment rapidly (Kandeler et al., 1999) and are widely used as an indicator of specific biochemical reactions in soil (Kujur and Patel, 2014; Dick et al., 1994). Phenol oxidase, peroxidase and cellulase are indicators of complex compound metabolism. Phenol oxidase is a “latch” in peatlands carbon decomposition (Freeman et al., 2001a). The majority of phenolic substance accumulated in peatlands due to low activity of phenol oxidase and inhibited hydrolase activities, leading to lower Rs (Freeman et al., 2001b; Mettrop et al., 2014; Tveit et al., 2013). The strict inhibition mechanism is relieved under AE condition (Freeman et al., 2001b). Increased temperature also enhanced peroxidase activity much. The important role of enzyme in Rs was demonstrated by the fact that correlations between carbon emission and activity of the three enzymes were found not in the origin soil but only after incubation. The variation of soil microbial and enzyme activity distribution among the whole depth profile could be a main cause of Rs variation among the whole profile. In addition, soil nutrient characteristics (C/N ratio) govern the accessibility of SOM to soil microorganism (Briones et al., 2014; Fierer et al., 2005; Hartley and Ineson, 2008; Kirschbaum, 2004; Treat et al., 2014). Carbon cycle is faster with larger quantity of labile C and N, or lower C/N ratio (Aerts, 1997; Lee et al., 2012). In our study we failed to find any linear correlation between carbon export rate and soil characteristics like TC or C/N ratio. Lower quantity of soil N and higher soil C/N ratio could constrain soil microbial metabolism and carbon decomposition (Bragazza et al., 2006; Cleveland and Liptzin, 2007). The C/N ratio in our study was in the range of 12.36 to 35.39 among the whole depth. It was shown that soil N could meet soil microbial requirements when C/N ratio was above 25 (Cleveland and Liptzin, 2007). In our research, Rs was limited by N at a few depths but not at others, therefore there was no apparently significant relationship in the whole profile. Enzyme activities were activated by temperature and oxygen during incubation, increasing carbon mineralization, which in turn may supply more available N to soil microbes. Our results also confirmed that the high quantity of soil C is not a conclusive factor in peat carbon decomposition; carbon diversity and microorganism availability are also critical in soil carbon decomposition (Hartley and Ineson, 2008; Kirschbaum, 2004; Tucker et al., 2013). 5. Conclusions This study showed that enhanced temperature and O2 substantially increased Rs, and with different increment among all layers of peatlands at mid-latitude and high altitude, suggesting that soil substrate character varies among the whole profile of peat. Soil microbes and enzymes had critical effect on soil carbon decomposition. The variation of soil microbial activity and enzyme distribution among the whole depth was one of the main causes that Rs differed significantly among the depth profile. By dividing the source of Rs into YS and OS, we found that OS contributed a huge part to total Rs (CO2:74.2%; DOC: 60.7%) and was responsible for a large proportion of the total increase in Rs. Compared with other peatlands studies, this research got lower increased Rs with 10 °C warming or oxidizing, but higher contribution of OS to total Rs. We can conclude that peatlands soil in our field is less sensitive to warming and oxidizing than other peatlands and that OS in this peatlands is more critical in predicting regional peatland carbon cycle. Our results could be very useful for modeling scientists to calibrate their models. Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.scitotenv.2015.11.149.


Acknowledgments This study was supported by 100 Talents Program of The Chinese Academy of Sciences, the External Cooperation Program of BIC, Chinese Academy of Sciences (No.151751KYSB20130027), 1000 Talents Program of Sichuan Province of China, National Natural Science Foundation of China (No. 31570480 and 41201205) and Open Project from Key Laboratory of Physical Geography and Environment Process of Qinghai Province, Qinghai Normal University. The authors give special thanks to Ms. Wan Xiong for her editing and valuable comments on the manuscript.

References Aerts, R., 1997. Climate, leaf litter chemistry and leaf litter decomposition in terrestrial ecosystems: a triangular relationship. Oikos 79, 439–449. Avis, C.A., Weaver, A.J., JM, K., 2011. Reduction in areal extent of high-latitude wetlands in response to permafrost thaw. Nat. Geosci. 4, 444–448. Bai, J., Lu, Q., Zhao, Q., Wang, J., Ouyang, H., 2013. Effects of Alpine Wetland Landscapes on Regional Climate on the Zoige Plateau of China. Adv. Meteorol. 2013, 1–7. Berglund, Ö., Berglund, K., 2011. Influence of water table level and soil properties on emissions of greenhouse gases from cultivated peat soil. Soil Biol. Biochem. 43, 923–931. Biasi, C., Jokinen, S., Marushchak, M.E., Hämäläinen, K., Trubnikova, T., Oinonen, M., et al., 2014. Microbial Respiration in Arctic Upland and Peat Soils as a Source of Atmospheric Carbon Dioxide. Ecosystems 17, 112–126. Biasi, C., Rusalimova, O., Meyer, H., Kaiser, C., Wanek, W., Barsukov, P., et al., 2005. Temperature-dependent shift from labile to recalcitrant carbon sources of arctic heterotrophs. Rapid Commun. Mass Spectrom. 19, 1401–1408. Blodau, C., Moore, T.R., 2003. Experimental response of peatland carbon dynamics to a water table fluctuation. Aquat. Sci. 65, 47–62. Bond-Lamberty, B., Thomson, A., 2010. Temperature-associated increases in the global soil respiration record. Nature 464, 579–582. Bosatta, E., Agren, G.I., 1999. Soil organic matter quality interpreted thermodynamically. Soil Biol. Biochem. 31, 1889–1891. Bragazza, L., Freeman, C., Jones, T., Rydin, H., Limpens, J., Fenner, N., et al., 2006. Atmospheric nitrogen deposition promotes carbon loss from peat bogs. Proc. Natl. Acad. Sci. U. S. A. 103, 19386–19389. Briones, M.J., McNamara, N.P., Poskitt, J., Crow, S.E., Ostle, N.J., 2014. Interactive biotic and abiotic regulators of soil carbon cycling: evidence from controlled climate experiments on peatland and boreal soils. Glob. Chang. Biol. 20, 2971–2982. Bubier, J.L., Bhatia, G., Moore, T.R., Roulet, N.T., Lafleu, P.M., 2003. Spatial and Temporal Variability in Growing-Season Net Ecosystem Carbon Dioxide Exchange at a Large Peatland in Ontario, Canada. Ecosystems 6, 353–367. Butman, D.E., Wilson, H.F., Barnes, R.T., Xenopoulos, M.A., Raymond, P.A., 2015. Increased mobilization of aged carbon to rivers by human disturbance. Nat. Geosci. 8, 112–116. Cao, G., Yingnian, L., Jinxia, Z., Xinquan, Z., 2001. Values of Carbon Dioxide Emission from Different Land2use Patterns of Alpine Meadow. Environ. Sci. 22, 14–19. Chen, H., Wu, N., Wang, Y., Gao, Y., Peng, C., 2010. Methane Fluxes from Alpine Wetlands of Zoige Plateau in Relation to Water Regime and Vegetation under Two Scales. Water Air Soil Pollut. 217, 173–183. Chen, H., Yang, G., Peng, C., Zhang, Y., Zhu, D., Zhu, Q., et al., 2014. The carbon stock of alpine peatlands on the Qinghai–Tibetan Plateau during the Holocene and their future fate. Quat. Sci. Rev. 95, 151–158. Chu, H., Fierer, N., Lauber, C.L., Caporaso, J.G., Knight, R., Grogan, P., 2010. Soil bacterial diversity in the Arctic is not fundamentally different from that found in other biomes. Environ. Microbiol. 12, 2998–3006. Cleveland, C.C., Liptzin, D., 2007. C:N:P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass? Biogeochemistry 85, 235–252. Dalva, M., Moore, T.R., 1991. Source and sinks of dissolved organci carbon a forested swamp catchment. Biogeochemistry 15, 1–19. Davidson, E.A., Janssens, I.A., 2006. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440, 165–173. DeForest, J.L., 2009. The influence of time, storage temperature, and substrate age on potential soil enzyme activity in acidic forest soils using MUB-linked substrates and LDOPA. Soil Biol. Biochem. 41, 1180–1186. Dick, R.P., Sandor, J.A., Eash, N.S., 1994. Soil enzyme activities after 1500 years of terrace agriculture in the Colca Valley, Peru. Agric. Ecosyst. Environ. 50, 123–131. Dorrepaal, E., Toet, S., van Logtestijn, R.S.P., Swart, E., Swart, E., van de Weg, M.J., Callaghan, T.V., et al., 2009. Carbon respiration from subsurface peat accelerated by climate warming in the subarctic. Nature 460, 616–619. Dutta, K., Schuur, E.A.G., Neff, J.C., 2006. Potential carbon release from permafrost soils of Northeastern Siberia. Glob. Chang. Biol. 12, 2336–2351. Eliasson, P.E., McMurtrie, R.E., Pepper, D.A., Stromgren, M., Linder, S., Agren, G.I., 2005. The response of heterotrophic CO2 flux to soil warming. Glob. Chang. Biol. 11, 167–181. Fan, Z., Neff, J.C., Waldrop, M.P., Ballantyne, A.P., Turetsky, M.R., 2014. Transport of oxygen in soil pore-water systems: implications for modeling emissions of carbon dioxide and methane from peatlands. Biogeochemistry 121, 455–470. Fenner, N., Freeman, C., 2011. Drought-induced carbon loss in peatlands. Nat. Geosci. 4, 895–910. Fierer, N., Craine, J.M., McLauchlan, K., Schimel, J.P., 2005. Litter quality and the temperature sensitivity of decomposition. Ecology 86, 320–326.

439

Freeman, C., Evans, C., Monteith, D.T., 2001a. An enzymic ‘latch’ on a global carbon store-a shortage of oxygen lacks up carbon in peatlands by restraining a singe enzyme. Nature 409, 149–150. Freeman, C., Evans, C., Monteith, D.T., 2001b. Export of organic carbon from peat soils. Nature 421, 785–786. Freeman, C., Fenner, N., Ostle, N.J., Kang, H., Dowrick, D.J., Reynolds, B., et al., 2004. Export of dissolved organic carbon from peatlands under elevated carbon dioxide levels. Nature 430, 195–198. Freeman, C., Liska, G., Ostle, N.J., 1997. Enzymes and biogeochemical cycling in wetlands during a stimulated drought. Biogeochemistry 39, 177–187. Gao, J., 2006. Degradation factor analysis and solutions of Ruoergai wetland in Sichuan. Sichuan Environ. 25, 48–53. Giardina, C.P., Ryan, M.G., 2000. Evidence that decomposition rates of organic carbon in mineral soil do not vary with temperature. Nature 404, 858–861. Gorham, E., 1991. Northern Peatlands: Role in the Carbon Cycle and Probable Responses to Climatic Warming. Ecol. Appl. 2, 182–195. Griffis, T.J., Rouse, W.R., Waddington, J.M., 2000. Interannual variability of net ecosystem CO2 exchange at a subarctic fen. Glob. Biogeochem. Cycles 14, 1109–1121. Guan, S., Zhang, D., Zhang, Z., 1986. Soil Enzyme and Its Research Method. Agricultural Press, Beijing, China (in Chinese). Guntiñas, M.E., Gil-Sotres, F., Leirós, M.C., Trasar-Cepeda, C., 2013. Sensitivity of soil respiration to moisture and temperature. J. Soil Sci. Plant Nutr. 2, 445–461. Guo, C., Luo, F., Ding, X., Luo, Q., Luo, C.-x., Cai, Y., et al., 2013. Palaeoclimate reconstruction based on pollen records from the Tangke and Riganqiao peat sections in the Zoige Plateau, China. Quat. Int. 286, 19–28. Hartley, I.P., Ineson, P., 2008. Substrate quality and the temperature sensitivity of soil organic matter decomposition. Soil Biol. Biochem. 40, 1567–1574. Hicks Pries, C.E., Schuur, E.A.G., 2013. Thawing permafrost increases old soil and autotrophic respiration in tundra: Partitioning ecosystem respiration using δ13C and Δ14C. Glob. Chang. Biol. 19, 649–661. Hobbie, S.E., Schimel, J.P., Trumbore, S.E., Randeron, J.P., 2000. Controls ocer carbon storage and tureover in high-latitude soils. Glob. Chang. Biol. 6, 196–210. Hogg, E.H., Lieffers, V.J., Wein, R.W., 1992. Potential carbon losses from peat profiles: effects of temperature, drought cycles, and fire. Ecol. Appl. 2, 298–306. IPCC, 2013. Climate Change 2013: the Physical Science Basis. Cambridge University Press, Cambridge. Jenkinson, D.S., Ladd, J.N., Ladd, J.N., 1981. Microbial biomass in soil: measurement and turnover. In: Paul, E.A. (Ed.), Soil Bichemistry New York. Marcel Dekker, pp. 415–471. Jones, D.L., Dennis, P.G., Owen, A.G., PAWv, H., 2003. Organic acid behavior in soils - misconceptions and knowledge gaps. Plant Soil 248, 31–41. Kandeler, E., Palli, S., Stemmer, M., Gerzabek, M.H., 1999. Tillage changes microbial biomass and enzymes activities in particle size fractionsof a Haplic Chernozem. Soil Biol. Biochem. 31, 1253–1264. Kane, E.S., Chivers, M.R., Turetsky, M.R., Treat, C.C., Petersen, D.G., Waldrop, M., et al., 2013. Response of anaerobic carbon cycling to water table manipulation in an Alaskan rich fen. Soil Biol. Biochem. 58, 50–60. Keller, J.K., Takagi, K.K., 2013. Solid-phase organic matter reduction regulates anaerobic decomposition in bog soil. Ecosphere 4. Kim, S.Y., Freeman, C., Fenner, N., Kang, H., 2012. Functional and structural responses of bacterial and methanogen communities to 3-year warming incubation in different depths of peat mire. Appl. Soil Ecol. 57, 23–30. Kirschbaum, M.F., 2004. Soil respiration under prolonged soil warming: are rate reductions caused by acclimation or substrate loss? Glob. Chang. Biol. 10, 1870–1877. Knoblauch, C., Beer, C., Sosnin, A., Wagner, D., Pfeiffer, E.M., 2013. Predicting long-term carbon mineralization and trace gas production from thawing permafrost of Northeast Siberia. Glob. Chang. Biol. 19, 1160–1172. Knorr, W., Prentice, C., House JI, Holland, E.A., 2005. Long-term sensitivity of soil carbon turnover to warming. Nature 433, 298–301. Kristensen, E., Holmer, M., 2001. Decomposition of plant materials in marine sediment -2 exposed to different electron acceptors (O2, NO-1 3 ,and SO4 ), with emphasis on substrate origin, degradation kinetics, and the role of bioturbation. Geochim. Cosmochim. Acta 65, 419–433. Kujur, M., Patel, A.K., 2014. Kinetics of soil enzyme activities under different ecosystems: An index of soil quality. Chil. J. Agric. Res. 74, 96–104. Laiho, R., 2006. Decomposition in peatlands: Reconciling seemingly contrasting results on the impacts of lowered water levels. Soil Biol. Biochem. 38, 2011–2024. Lawrence, C.R., Neff, J.C., Schimel, J.P., 2009. Does adding microbial mechanisms of decomposition improve soil organic matter models? A comparison of four models using data from a pulsed rewetting experiment. Soil Biol. Biochem. 41, 1923–1934. Lee, H., Schuur, E.A.G., Inglett, K.S., Lavoie, M., Chanton, J.P., 2012. The rate of permafrost carbon release under aerobic and anaerobic conditions and its potential effects on climate. Glob. Chang. Biol. 18, 515–527. Li, J., Wang, W., Hu, G., Wei, Z., 2010. Changes in ecosystem service values in Zoige Plateau, China. Agric. Ecosyst. Environ. 139, 766–770. Liski, J., Ilvesniemi, H., Makela, A., Westman, C.J., 1999. CO2 emissions from soil in response to climatic warming are overestimated - the decomposition of old soil organic matter is tolerant of temperature. Ambio 28, 171–174. Liu, X., Chen, B., 2000. Climate warming in the Tibetan Plateau during recent decades. Int. J. Climatol. 20, 1729–1742. Liu, W., Zhang, Z., Wan, S., 2009. Predominant role of water in regulating soil and microbial respiration and their responses to climate change in a semiarid grassland. Glob. Chang. Biol. 15, 184–195. Lloyd, J., Taylor, J.A., 1994. On the temperature dependence of soil respiration. Funct. Ecol. 8, 315–323.

440


Mäkiranta, P., Minkkinen, K., Hytönen, J., Laine, J., 2008. Factors causing temporal and spatial variation in heterotrophic and rhizospheric components of soil respiration in afforested organic soil croplands in Finland. Soil Biol. Biochem. 40, 1592–1600. Marwick, T.R., Tamooh, F., Teodoru, C.R., Borges, A.V., Darchambeau, F., Bouillon, S., 2015. The age of river-transported carbon: a global perspective. Glob. Biogeochem. Cycles http://dx.doi.org/10.1002/2014GB004911. McCallister, S.L., Del Giorgio, P.A., 2012. Evidence for the respiration of ancient terrestrial organic C in northern temperate lakes and streams. Proc. Natl. Acad. Sci. 109, 16963–16968. McGuire, A.D., Christensen, T.R., Hayes, D., Heroult, A., Euskirchen, E., Kimball, J.S., et al., 2012. An assessment of the carbon balance of Arctic tundra: comparisons among observations, process models, and atmospheric inversions. Biogeosciences 9, 3185–3204. Mettrop, I.S., Cusell, C., Kooijman, A.M., Lamers, L.P.M., 2014. Nutrient and carbon dynamics in peat from rich fens and Sphagnum-fens during different gradations of drought. Soil Biol. Biochem. 68, 317–328. Mikan, C.J., Schimel, J.P., Doyle, A.P., 2002. Temperature controls of microbial respiration in arctic tundra soils above and below freezing. Soil Biol. Biochem. 34, 1785–1795. Minkkinen, K., Laine, J., Shurpali, N.J., Mäkiranta, P., Alm, J., Penttilä, T., 2007. Heterotrophic soil respiration in forestry-drained peatlands. Boreal Environ. Res. 12, 115–126. Moore, T., Basiliko, N., 2006. Decomposition in boreal peatlands. Boreal peatland ecosystems. Springer, pp. 125–143. Moore, T.R., Dalva, M., 1997. Methane and carbon dioxide exchange potentials of peat soils in aerobic and anaerobic labroatory incubations. Soil Biol. Biochem. 29, 1157–1164. Moore, T.R., Knowles, R., 1989. The influence of water table levels on methane and carbon dioxide emissions from peatland soils. Can. J. Soil Sci. 69, 33–38. Moorhead, D.L., Sinsabaugh, R.L., 2006. A theoretical model of litter decay and microbial interaction. Ecol. Monogr. 2, 151–174. Munir, T.M., Perkins, M., Kaing, E., Strack, M., 2015. Carbon dioxide flux and net primary production of a boreal treed bog: Responses to warming and water-table-lowering simulations of climate change. Biogeosciences 12, 1091–1111. Nadelhoffer, K., Giblin, A., Shaver, G., Laundre, J., 1991. Effects of temperature and substrate quality on element mineralization in six arctic soils. Ecology 72, 242–253. O’Donnell, J.A., Jorgenson, M.T., Harden, J.W., McGuire, A.D., Kanevskiy, M.Z., Wickland, K.P., 2012. The Effects of Permafrost Thaw on Soil Hydrologic, Thermal, and Carbon Dynamics in an Alaskan Peatland. Ecosystems 15, 213–229. Oechel, W.C., L.Vourlitis, G., Hastngs, S.J., 1998. The effects of water tale manipulation and elevated temperature on the net CO2 flux of wet sedge tundra ecosystem. Glob. Chang. Biol. 4, 77–90. Pastor, J., Solin, J., Bridgham, S.D., Updegraff, K., Harth, C., Weishampel, P., et al., 2003. Global warming and the export of dissolved organic carbon from boreal peatlands. Oikos 100, 380–386. Peng, F., Xue, X., You, Q., Zhou, X., Wang, T., 2014. Warming effects on carbon release in a permafrost area of Qinghai-Tibet Plateau. Environ. Earth Sci. 73, 57–63. Pind, A., Freeman, C., Lock, M.A., 1994. Enzymic degradation of phenolic materials in peatlands- measurement of phenol oxidase activity. Plant and Soil 159, 227–231. Rinkes, Z.L., DeForest, J.L., Grandy, A.S., Moorhead, D.L., Weintraub, M.N., 2013. Interactions between leaf litter quality, particle size, and microbial community during the earliest stage of decay. Biogeochemistry 117, 153–168. Rowson, J.G., Worrall, F., Evans, M.G., Dixon, S.D., 2013. Predicting soil respiration from peatlands. Sci. Total Environ. 442, 397–404. Saiya-Cork, K., Sinsabaugh, R.L., Zak, D.R., 2002. The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol. Biochem. 34, 1309–1315. Schuur, E.A.G., Bockheim, J., Canadell, J.G., 2008. Vulnerability of Permafrost Carbon to Climate Change:Implications for the Global Carbon Cycle. Bioscience 58, 701–714. Schuur, E.A.G., Vogel, J.G., Crummer, K.G., Lee, H., Sickman, J.O., Osterkamp, T.E., 2009. The effect of permafrost thaw on old carbon release and net carbon exchange from tundra. Nature 459, 556–559.

Serreze, M., Walsh, J., Chapin III, F., Osterkamp, T., Dyurgerov, M., Romanovsky, V., et al., 2000. Observational evidence of recent change in the northern high-latitude environment. Clim. Chang. 46, 159–207. Singer, G.A., Fasching, C., Wilhelm, L., Niggemann, J., Steier, P., Dittmar, T., et al., 2012. Biogeochemically diverse organic matter in Alpine glaciers and its downstream fate. Nat. Geosci. 5, 710–714. Sinsabaugh, R.L., Lauber, C.L., Weintraub, M.N., Ahmed, B., Allison, S.D., Crenshaw, C., et al., 2008. Stoichiometry of soil enzyme activity at global scale. Ecol. Lett. 11, 1252–1264. Szafranek-Nakonieczna, A., Stêpniewska, Z., 2014. Aerobic and Anaerobic Respiration in Profiles of Polesie Lubelskie Peatlands. Int. Agrophys. 28, 219–229. Tian, J., Zhu, Y., Kang, X., Dong, X., Li, W., Chen, H., et al., 2012. Effects of drought on the archaeal community in soil of the Zoige wetlands of the Qinghai–Tibetan plateau. European Journal of Soil Biology 52, 84–90. Tian, L., Shi, W., 2014. Soil peroxidase regulates organic matter decomposition through improving the accessibility of reducing sugars and amino acids. Biol. Fertil. Soils 50, 785–794. Todd-Brown, K.E.O., Randerson, J.T., Post, W.M., Hoffman, F.M., Tarnocai, C., Schuur, E.A.G., et al., 2013. Causes of variation in soil carbon simulations from CMIP5 Earth system models and comparison with observations. Biogeosciences 10, 1717–1736. Treat, C.C., Wollheim, W.M., Varner, R.K., Grandy, A.S., Talbot, J., Frolking, S., 2014. Temperature and peat type control CO2 and CH4 production in Alaskan permafrost peats. Glob. Chang. Biol. 20, 2674–2686. Tucker, C.L., Bell, J., Pendall, E., Ogle, K., 2013. Does declining carbon-use efficiency explain thermal acclimation of soil respiration with warming? Glob. Chang. Biol. 19, 252–263. Tveit, A., Schwacke, R., Svenning, M.M., Urich, T., 2013. Organic carbon transformations in high-Arctic peat soils: key functions and microorganisms. ISME J. 7, 299–311. Van den Berg, L.J., Shotbolt, L., Ashmore, M.R., 2012. Dissolved organic carbon (DOC) concentrations in UK soils and the influence of soil, vegetation type and seasonality. Sci. Total Environ. 427-428, 269–276. Vance, E., Brookes, P., Jenkinson, D., 1987. An extraction method for measuring soil microbial biomass C. Soil Biol. Biochem. 19, 703–707. Wang, X., Song, C., Wang, J., Miao, Y., Mao, R., Song, Y., 2013. Carbon release from Sphagnum peat during thawing in a montane area in China. Atmos. Environ. 75, 77–82. Wang, M., Yang, G., Gao, Y., Chen, H., Wu, N., Peng, C., et al., 2015. Higher recent peat C accumulation than that during the Holocene on the Zoige Plateau. Quaternary Science Reviews 114, 116–125. Watts, J.D., Kimball, J.S., Parmentier, F.J.W., Sachs, T., Rinne, J., Zona, D., et al., 2014. A satellite data driven biophysical modeling approach for estimating northern peatland and tundra CO2 and CH4 fluxes. Biogeosciences 11, 1961–1980. Wickings, K., Grandy, A.S., Reed, S.C., Cleveland, C.C., 2012. The origin of litter chemical complexity during decomposition. Ecol. Lett. 15, 1180–1188. Yan, J., Zhang, W., Wang, K., Qin, F., Wang, W., Dai, H., et al., 2014. Responses of CO2, N2O and CH4 fluxes between atmosphere and forest soil to changes in multiple environmental conditions. Glob. Chang. Biol. 20, 300–312. Yang, G., Chen, H., Wu, N., Tian, J., Peng, C., Zhu, Q., et al., 2014. Effects of soil warming, rainfall reduction and water table level on CH4 emissions from the Zoige peatland in China. Soil Biol. Biochem. 78, 83–89. Zak, D.R., Kling, G.W., 2006. Microbial Community Composition and function across an arctic tundra landscape. Ecology 7, 1659–1670. Zeng, X., Zhang, W., Shen, H., Cao, J., Zhao, X., 2014. Soil respiration response in different vegetation types at Mount Taihang, China. Catena 116, 78–85. Zhu, D., Chen, H., Zhu, Q., Wu, Y., Wu, N., 2012. High Carbon Dioxide Evasion from an Alpine Peatland Lake: The Central Role of Terrestrial Dissolved Organic Carbon Input. Water Air Soil Pollut. 223, 2563–2569. Zimov, S.A., Schuur, E.A., Chapin III, F.S., 2006. Permafrost and the global carbon budget. Science (Washington) 312, 1612–1613.