Emissions of CO2, CH4 and N2O from Southern European peatlands

Soil Biology & Biochemistry 42 (2010) 1437e1446

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Emissions of CO2, CH4 and N2O from Southern European peatlands Tjasa Danev ci c, Ines Mandic-Mulec*, Bla z Stres 1, David Stopar, Janez Hacin University of Ljubljana, Biotechnical Faculty, Department of Food Science and Technology, Vecna pot 111, 1000 Ljubljana, Slovenia

a r t i c l e i n f o

a b s t r a c t

Article history: Received 14 October 2009 Received in revised form 23 April 2010 Accepted 4 May 2010 Available online 21 May 2010

Peatlands play an important role in emissions of the greenhouse gases CO2, CH4 and N2O, which are produced during mineralization of the peat organic matter. To examine the influence of soil type (fen, bog soil) and environmental factors (temperature, groundwater level), emission of CO2, CH4 and N2O and soil temperature and groundwater level were measured weekly or biweekly in loco over a one-year period at four sites located in Ljubljana Marsh, Slovenia using the static chamber technique. The study involved two fen and two bog soils differing in organic carbon and nitrogen content, pH, bulk density, water holding capacity and groundwater level. The lowest CO2 fluxes occurred during the winter, fluxes of N2O were highest during summer and early spring (February, March) and fluxes of CH4 were highest during autumn. The temporal variation in CO2 fluxes could be explained by seasonal temperature variations, whereas CH4 and N2O fluxes could be correlated to groundwater level and soil carbon content. The experimental sites were net sources of measured greenhouse gases except for the drained bog site, which was a net sink of CH4. The mean fluxes of CO2 ranged between 139 mg m2 h1 in the undrained bog and 206 mg m2 h1 in the drained fen; mean fluxes of CH4 were between 0.04 mg m2 h1 in the drained bog and 0.05 mg m2 h1 in the drained fen; and mean fluxes of N2O were between 0.43 mg m2 h1 in the drained fen and 1.03 mg m2 h1 in the drained bog. These results indicate that the examined peatlands emit similar amounts of CO2 and CH4 to peatlands in Central and Northern Europe and significantly higher amounts of N2O. Ó 2010 Elsevier Ltd. All rights reserved.

Keywords: Greenhouse gas emissions Peatland Drainage Bog Fen Groundwater level Carbon dioxide Methane Nitrous oxide

1. Introduction Peatlands cover only approximately 3% of the Earth’s surface but store about 26% of soil organic carbon (Smith et al., 2004). Although these soils have acted for millennia as sinks for C and N through accumulation of organic C (Gorham, 1991) and N (Driesen, 1978), there is global concern that they may become an important source of greenhouse gases (GHG), due to enhanced mineralization of soil organic matter (SOM) caused by drainage, agricultural use and other anthropogenic disturbances leading to climate change. The type and magnitude of individual GHG loss is strongly dependent on environmental factors such as groundwater level, temperature and soil organic matter content (Aerts and Ludwig, 1997; Chimner and Cooper, 2003; Smith et al., 2003). Soil moisture is the main determinant of the type of C and N gaseous losses, whereas temperature affects the magnitude of GHG emissions both seasonally and regionally (reviewed in Jungkunst and Fiedler, 2007). A latitudinal trend in the relative reduction of CO2

* Corresponding author. Tel.: þ386 1 423 33 88; fax: þ386 1 257 33 90. E-mail address: [email protected] (I. Mandic-Mulec). 1 Present address: University of Ljubljana, Biotechnical Faculty, Zootechnical Department, Groblje 3, 1230 Dom zale, Slovenia. 0038-0717/$ e see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.soilbio.2010.05.004

emissions by 10e20% and 30e60% with rising groundwater was found for tropical and temperate zone conditions, respectively, whereas these values were over 60% for boreal zones (Jungkunst and Fiedler, 2007). In the latter a strong dependence of GHG emissions on seasonal variations in temperature and groundwater level could be observed with the highest emissions of CO2, CH4 and N2O during summer, when the groundwater was below 10e20 cm (Von Arnold et al., 2005a, 2005b). Methane emissions did not exhibit temperature dependent responses to rising groundwater but did increase above a threshold groundwater depth of 10 cm below the soil surface (Jungkunst and Fiedler, 2007). Methane emissions decrease with decreasing soil water content and peat soils may eventually become a net sink for methane (reviewed in Laiho, 2006). Temperature, however, may affect methanogenic pathways (Schulz and Conrad, 1996; Avery et al., 1999; Hines et al., 2001; Duddleston et al., 2002,). The highest N2O emissions are found at intermediate groundwater levels, which allow their aerobic and anaerobic production (Martikainen et al., 1993). Aerobic production of N2O via nitrification may be substantial (up to 80% of total N2O emissions) (Webster and Hopkins, 1996; Pihlatie et al., 2004), and another product of nitrification is nitrate, which is the rate controlling factor for anaerobic N2O production via denitrification (Conrad, 1996; Davidson et al., 2000; Öquist et al., 2007).

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T. Danevcic et al. / Soil Biology & Biochemistry 42 (2010) 1437e1446

Very few studies have compared the effects of groundwater level and temperature on GHG emissions in ombrotrophic acid bogs and minerotrophic neutral to alkaline fens (Martikainen et al., 1995; Laine et al., 1996; Silvola et al., 1996; Nykänen et al., 1998). These two main types of peatlands differ in peat composition (sedge peat in the former and sphagnum peat in the latter), total organic carbon content and bulk density, which affects the soil water holding capacity and moisture regime at fluctuating groundwater level (Ausec et al., 2009). In fen and bog peatlands drainage increased CO2 emissions (Fiedler et al., 1998; Von Arnold et al., 2005a, 2005b) and decreased CH4 emissions by one to several orders of magnitude (Laine et al., 1996; Von Arnold et al., 2005a, 2005b). At similar groundwater levels fens emitted more CH4 than bogs (Laine et al., 1996). N2O emissions from fen and bog sites were variable. In the fen area, drainage substantially increased annual N2O fluxes (Martikainen et al., 1995; Laine et al., 1996), but had less pronounced or negligible effects in the bog areas (Laine et al., 1996; Von Arnold et al., 2005a, 2005b). However, at similar groundwater levels annual N2O fluxes were higher in fens than in bogs (Laine et al., 1996). GHG emissions have been studied most extensively in Northern peatlands, due to their largest area and potential global importance (Martikainen et al., 1993, 1995; Nykänen et al., 1998; Von Arnold et al., 2005a, 2005b). Despite their smaller size, however, peatlands in Central and South Europe may be important for regional inventories of GHG emissions (Lokupitiya and Paustian, 2006). The Ljubljana Marsh is in a large drained peatland covering 160 km2 in central Slovenia that is dominated by fens with isolated bog fragments not exceeding 200,000 m2 each. The drainage system in the Ljubljana Marsh was established in the early 19th century but in spite of peat excavation, drainage and agriculture, the area still provides unique habitats for wetland fauna and flora. Conservation and restoration efforts have been initiated, including attempts to raise the groundwater level in some areas. This indicated the need to obtain data on GHG fluxes in the field before the start of restoration efforts and compare the data to microcosm experiments simulating the situation after rewetting (Stres et al., 2008). Microcosm studies with fen soil indicated that CO2 fluxes were affected most by temperature, whereas N2O fluxes correlated positively with nitrate availability and waterlogged conditions (Stres et al., 2008). Methane was produced in fen soil only after a lag of two months and at elevated temperature (Jerman et al., 2009). Another reason to study GHG emissions locally is a need for country specific emission factors (Lokupitiya and Paustian, 2006), which are used in national GHG inventory reports, according to UNFCCC (UN Framework Convention on Climate Change). Despite its relatively small area, the diversity of habitats in the Ljubljana Marsh offers a unique opportunity to study the effect of physico-chemical properties of peat soils on GHG emissions under the same climatic conditions. Two fen and two bog sites differing significantly in organic matter content, C/N ratio, pH, bulk density, water holding capacity and groundwater level were selected for this study with the following objectives: (i) to determine the fluxes of CO2, CH4 and N2O in relation to physico-chemical properties of peat soils, (ii) to quantify the influence of seasonal changes in temperature and groundwater level on fluxes of CO2, CH4 and N2O and (iii) to compare GHG fluxes in a South European peatland to those in Northern peatlands in Germany, Sweden and Finland. 2. Materials and methods 2.1. Study sites All study sites were located within Ljubljana Marsh, south of Ljubljana, Slovenia, where two drained fen grassland soils

(45 580 N, 14 280 E) and two bog forest soils (drained and undrained) (45 590 N, 14 300 E) were investigated. The fen site is grassland cut once or twice annually and classified as Arrhenatherion, according to botanical composition of the grass community (Cop et al., 2004). Dominating species on the fen site are Arrhenatherum elatius, Dactylis glomerata, Festuca rubra, Equsetum palustre and Galium mollugo, followed by Ranunculus repens, Achillea millefolium, Leucanthemum ircutianum and Centaurea jacea. A region of the meadow proximal to the main drainage ditch is characterized by fluvial clay deposits, lower content of organic carbon (LC) and lower groundwater level, whereas the region distal from the main drainage ditch has no clay deposits, higher organic carbon (HC) and higher groundwater level. These two fen sites were classified as Rheic Fibric Histosol (HC) and Humic Gleysol (LC) (Hacin et al., 2001). The bog site is a forested area representing a natural succession with Betula sp., Frangula alnus, Salix sp., Quercus robur and Pinus sylvestris as dominating tree species in the undrained and drained regions (Martincic, 1987). In contrast, the bottom vegetation in the undrained region (KG1) is dominated by Sphagnum sp. and other mosses, Caluna vulgaris and some herbaceous species, whereas the bottom vegetation in the drained region (KG2) consists exclusively of Pteridium aquilinum (Hacin, unpublished data). The undrained bog soil was classified under World reference base for soil resources (2006) as the Rheic Fibric Histosol (Dystric), while the drained bog soil (KG2) was classified as Rheic Hemic Histosol (Dystric). 2.2. Physical and chemical analysis of the soils To determine soil chemical properties soil organic carbon (Corg) and soil organic nitrogen content (Norg), pH and water holding capacity (WHC), nine soil cores were collected from a depth of 0e20 cm on 3 5 m plots on three separate occasions (spring (March), summer (August) and autumn (November)) and homogenized through an 8-mm sieve to account for spatial heterogeneity as described by Robertson et al. (1999). Fresh homogenized samples were used for pH and WHC determination, while dried (60 C), ground (2 mm sieve) samples were used to determine Corg and Norg. For bulk density determination, three series of cores (0e5e10e15e20 cm) were taken from three locations approximately 1 m apart at each study site. Soil pH was measured with a glass electrode in a 1:5 (v/v) suspension of soil in distilled water or in 1 M KCl according to ISO 10390 standard. WHC was determined as described by Stres et al. (2008). Soil bulk density was determined in soil sampling rings (100 cm3, Eijkelkamp, NL) according to Forster (1995). Corg was measured according to ISO 10694 standard, after combustion in a LECO CNS-2000 analyzer (LECO, USA) and subtraction of CaCO3, determined by a Scheibler’s calcimeter. Norg was determined by standard Kjeldahl analysis (Bundy and Meisinger, 1994), using a Tecator 2012 digestion apparatus (Tecator AB, Sweden) and micro Kjeldahl distillation apparatus. Soil Nmin (NHþ 4 eN and NO3 þ NO2 eN) was determined following 2 M KCl extraction (Bundy and Meisinger, 1994), using a continuous flow analyzer (FlowSys, Alliance Instruments, Austria). 2.3. Gas flux determination Gas fluxes were determined by the static chamber technique (Martikainen et al., 1993; Nykänen et al., 1995; Alm et al., 1999). Gas concentrations were measured using dark, static, manually sampled, polyvinyl chloride (PVC) chambers (diameter 16 cm and height 9 cm) equipped with butyl rubber septa for gas sampling. The chambers were placed on PVC rings covering an area of 0.02 m2 inserted into the soil to allow repeated measurements to be made at the same place. The three rings were installed in June 2005


approximately 1e1.5 m apart on a 3 5 m plot, representative for each study site. Gas emissions were measured in all chambers at approximately weekly intervals, from June 2005 to August 2006. All gas flux measurements were made between 10:00 am and 2:00 pm. To minimize plant respiration (Nykänen et al., 1995; Merino et al., 2004; Maljanen et al., 2004; Mäkiranta et al., 2007) the surface plant cover inside the rings was routinely removed. The remaining extent of plant cover was thus comparable between the sites. Before placing the chambers on the rings, the grass was cut to the ground on the fen sites, whereas at the bog sites there was no surface vegetation, other than surface litter which was left intact. For winter measurements, the snow cover was removed from the rings. Chambers were covered with plastic containers wrapped in aluminium foil to prevent exposure to direct sunlight and overheating. The gas samples were taken from the chamber headspace 0, 30 and 60 min after closure and were collected in 2mL vials sealed by butyl rubber septa, previously flushed with 8 mL of sample. CO2, CH4 and N2O concentrations were determined in the laboratory on the same day by network GC System 6890 N (Agilent Technologies, USA) gas chromatograph equipped with a GS-CarbonPLOT capillary column (30 m 0.53 mm ID 3 mm film) (Agilent Technologies, USA), methaniser, flame ionization (FID) and electron capture detectors (mECD). The carrier gas throughout the column was N2 with flow 5.6 mL min1. The temperatures of the injector, oven, methaniser, FID and mECD were 100 C, 50 C, 375 C, 300 C and 300 C, respectively. 2.4. Abiotic variables Air temperature, soil temperature and groundwater level were measured at the same time as gas fluxes. Air temperature was measured at the soil surface, and soil temperature was measured 5, 30, 60 and 90 cm below the soil surface next to the chambers using a portable digital thermometer (Hanna, USA). Groundwater level was monitored in piezometers installed at each study site. 2.5. Data analysis Gas fluxes were calculated from the linear increase or decrease in gas concentration in each chamber with time, using a linear regression equation (Christensen et al., 1995), and were corrected for air temperature according to the ideal-gas equation. Only regressions with coefficients r2 > 0.7 for CO2 and N2O and r2 > 0.5 for CH4 were used in further calculations. Mean hourly gas fluxes and standard errors were calculated for the three chambers at each experimental site. Annual gas emissions were calculated from the integrated weekly fluxes of the three chambers, assuming a constant flux rate between gas samplings (Merino et al., 2004). Statistical analyses were carried out using SPSS version 10.1 software (SPSS, Inc., Chicago). The significance of differences in gas flux between experimental sites over time was tested using the nonparametric ManneWhitney U-test. The threshold for accepting significance was p ¼ 0.05. Correlations between gas concentrations and environmental parameters were tested using the Pearson correlation coefficient. Differences in environmental parameters and mean gas fluxes between the sites were tested with the Student’s t-test at p ¼ 0.05. 3. Results 3.1. Climate and physico-chemical characteristics of fen and bog soils Fen and bog soils differed significantly in their physical and chemical characteristics (Table 1). Organic carbon content was

1439

approximately three times higher in bog than in fen sites. It was similar in the undrained (KG1) and drained (KG2) bog site (45.4 and 40.4%) but significantly lower in drained LC fen (9.73%) than in drained HC fen (16.3%) site. The same pattern was observed in the organic nitrogen content. The C/N ratio was highest (19.3) in the drained bog site (KG2) and lowest (11.1) in the drained LC fen site. There was no difference in pH within fen or bog sites (p ¼ 0.18 and 0.3 for fen and bog soils, respectively), but pH was approximately three units higher in fen sites (p < 0.05) compared to bog sites. The bulk density in the two bog soils was approximately 3.5 times lower than in the fen soils. In addition, WHC in the bog soils was several times higher than in the fen soils (p < 0.05). The groundwater level throughout the sampling period was significantly higher at the drained HC fen site (from 15 to 115 cm below the surface) than at the drained LC fen site (between 70 and 135 cm below the surface). At the drained bog site (KG2) the groundwater level was between 30 and 100 cm, and was significantly higher at the undrained bog site (KG1), varying between 10 and 70 cm (Fig. 1). The air temperature ranged from 5 to 40 C (data not shown), while the soil temperature measured 5 cm below the surface ranged from 1 to 24 C. Soil temperature measured 30, 60 and 90 cm below the surface ranged from 0 to 21 C, 2 to 19 C and 3.5 to 17.5 C, respectively (data not shown). The soil temperature profile was similar at all experimental sites (Fig. 1). 3.2. Greenhouse gases fluxes GHG emitted from the experimental sites varied significantly (p < 0.05) during the year (Fig. 1). The mean fluxes of CO2, representing total soil respiration, were significantly lower (139 mg CO2 m2 h1) at the undrained bog site (KG1) (p < 0.05), but were not significantly (p > 0.05) different (200e206 mg CO2 m2 h1) between the other three study sites (HC, LC and KG2) (Table 2). Total soil respiration was positively correlated with soil temperature, r2 ¼ 0.7e0.8, for all study sites and negatively correlated with groundwater level (r2 ¼ 0.4e0.65). Highest correlations between total soil respiration and temperature were obtained for the soil temperature measured 5 cm below the surface. The lowest CO2 fluxes occurred during the winter, when temperature was low and groundwater level was high. There were no significant (p > 0.05) differences in temporal variation in CO2 fluxes at the four study sites (Fig. 1). The mean fluxes of CH4 were close to zero for all study sites and often within the standard error (Table 2). However, both negative (i. e. uptake) and positive (i.e. emission) CH4 fluxes were detected at all experimental sites during the year and the highest CH4 fluxes were measured during autumn (Fig. 1). The CH4 data did not show any correlation with soil temperature or groundwater level. Despite the low hourly CH4 fluxes, variation was high on many sampling dates, due to high variability within sampling sites. Temporal

Table 1 The main physico-chemical characteristics of the soils (0e20 cm depth) from two fen grassland and two bog forest sites in Ljubljana Marsh, Slovenia. Values represent the mean and the standard deviation (n ¼ 3). Experimental sites

Corg content (%) Norg content (%) pH (in water) pH (in 1 M KCl) WHC e 100% (g H2O g1 soil) Bulk density (g cm3)

Fen e grassland

Bog e forest

HC e drained

KG1 e undrained

16.3 1.4 7.55 7.02 1.65

0.21 0 0.02 0.02 0.21

0.59 0.05

LC e drained 9.73 0.88 7.63 6.99 1.41

0.14 0.01 0.01 0.01 0

0.74 0.04

45.4 2.75 4.58 3.24 8.14

0.21 0.01 0.16 0.06 0.29

0.16 0.05

KG2 e drained 40.4 2.09 4.28 2.99 4.77

0.78 0 0.14 0.12 0.41

0.21 0.01


1440

Drained HC fen grassland

Drained LC fen grassland

900

900

750

750

600

600

450

450

300

300

150

150

0

0

2

-2

-1

C O f lu x ( mg m h )

A

0 ,6

0 ,6

0 ,4

0 ,4

0 ,2

0 ,2

CH4 flux (mg m h )

-1

J J A S O N D J F M A M J J A

-2


0 ,0

0 ,0

-0 ,2

-0 ,2

-0 ,4

-0 ,4

2

-2

-1

N O flux (mg m h )

J J A S O N D J F M A M J J A 7 6 5 4 3 2 1 0 -1

J J A S O N D J F M A M J J A 7 6 5 4 3 2 1 0 -1 J

groundwater level (cm)


0

0

-2 0

-2 0

-4 0

-4 0

-6 0

-6 0

-8 0

-8 0

-1 0 0

-1 0 0

-1 2 0

-1 2 0

-1 4 0

J

F M A M J

J A

-1 4 0 J J A S O N D J F M A M J J A

soil temperature (°C)

J A S O N D


25

25

20

20

15

15

10

10

5

5

0

0

-5

-5

J J A S O N D J F M A M J J A 2

1


Fig. 1. Annual variations in greenhouse gas fluxes (mg m h ), groundwater level (cm below surface) and soil temperature ( C) measured 5 cm below the soil surface at (A) the drained HC fen site and the drained LC fen site and (B) the undrained bog (KG1) site and the drained bog (KG2) site. Data points for gas fluxes represent means of the three chambers installed at each study site and error bars indicate standard error of the mean.


B

-2

-1

CO 2 flux (mg m h )

Undrained bog KG1 forest

Drained bog KG2 forest

900

900

750

750

600

600

450

450

300

300

150

150

0

0 J

-2

-1

CH4 flux (mg m h )


0.6

0,6

0.4

0,4

0.2

0,2

0.0

0,0

-0.2

-0,2

-0.4

-0,4

-2

-1

N2O flux (mg m h )

J J A S O N D J F M A M J J A 7 6 5 4 3 2 1 0 -1

groundwater level (cm)

J A S O N D

J

F M A M J J A

J J A S O N D J F M A M J J A 7 6 5 4 3 2 1 0 -1 J

J J A S O N D J F M A M J J A 0

0

-20

-20

-40

-40

-60

-60

-80

-80

-100

-100

-120

-120

J

A S O N D

J

F M A M

J

J

A

-140

-140



soil temperature (°C)

1441

25

25

20

20

15

15

10

10

5

5

0

0

-5

-5 J J A S O N D J F M A M J J A

J

Fig. 1. (continued).

J A S O N D

J

F M A M

J

J A

Location and latitude

Soil type

Mean annual air temperature ( C)

Mean annual precipitation (mm)

Mean C/N ratio annual groundwater level (cm)

Mean CO2 flux Mean N2O flux Mean CH4 flux (mg m2 h1) (mg m2 h1) (mg m2 h1)

Annual N2O emissions (g m2 y1)

Annual CH4 emissions (g m2 y1)

Reference

Slovenia 45 580 N, 14 280 E Slovenia 45 580 N, 14 280 E Slovenia 45 590 N, 14 300 E Slovenia 45 590 N, 14 300 E Southern Germany 47 200 N, 12 250 E Southern Germany 47 200 N, 12 250 E Southern Germany 47 200 N, 12 250 E Southern Germany 47 200 N, 12 250 E Southern Germany 48 410 N, 11 090 E Southern Germany 48 400 N, 11 120 E SW Germany 47 520 N, 10 520 E SW Germany 47 520 N, 10 520 E Southern Sweden 57 080 N, 14 450 E Southern Sweden 57 080 N, 14 450 E Southern Sweden 57 080 N, 14 450 E Southern Sweden 57 080 N, 14 450 E Southern Sweden 57 080 N, 14 450 E Southern Sweden 57 080 N, 14 450 E Southern Sweden 57 080 N, 14 450 E Finland 61 480 N, 24 190 E Finland 61 480 N, 24 190 E Finland 61 480 N, 24 190 E Finland 61 480 N, 24 190 E Finland 61 480 N, 24 190 E Finland 61 480 N, 24 190 E Finland 61 480 N, 24 190 E Finland 61 480 N, 24 190 E Finland 62 450 N, 31 030 E

Drained fen HC, grassland Drained fen LC, grassland Undrained bog KG1, forest Drained bog KG2, forest Undrained bog

10

1400

53.2 22

11.7 0.2

200 29

0.56 0.15

0.04 0.03

5.83 0.03

0.31 0.01

This study

10

1400

96.7 14.4

11.1 0.25 206 28

0.43 0.12

0.05 0.02

4.21 0.02

0.3 0.01

This study

10

1400

24.4 13.8

16.5 0.01 139 26

0.61 0.18

0.03 0.06

5.77 0.03

0.31 0.01

This study

10

1400

54.7 16.4

19.3 0.37 204 34

1.03 0.4

0.04 0.05

9.52 0.1 3

0.28 0.01 This study 3

1483

8.4

nd

163

nd

0.83

3$10

Undrained bog

8.5

1483

6.3

nd

141

nd

1.54

4$103 3$103

Undrained bog

8.5

1483

9.5

nd

125

nd

4.21

4$103 2$103

Undrained bog

8.5

1483

0

nd

80

nd

5.83

3$103 2$103

Drained fen,

7.6

700

46

13.5

nd

0.52 0.2

0.018 0.003

0.031

M. Drösler e data from Jungkunst and Fiedler (2007) 13.47 3.07 M. Drösler e data from Jungkunst and Fiedler (2007) 36.93 2.8 M. Drösler e data from Jungkunst and Fiedler (2007) 50.93 2.93 M. Drösler e data from Jungkunst and Fiedler (2007) 1.39$103 Flessa et al., 1998

Drained fen,

7.6

700

71

14.8

nd

1.2 0.24

3.1$103 7$104

0.089

2.8$104

Flessa et al., 1998

Drained fen

6.5

1200

19

nd

541.7

nd

0.25

nd

nd

Fiedler et al., 1998

Undrained fen

6.5

1200

9

nd

333.3

nd

2

nd

nd

Fiedler et al., 1998

Drained bog

5.6

662

15 4

22 2

264 24.6

0.023 0.004

0.106 0.041

0.2 0.11

0.9 0.51

Von Arnold et al., 2005a

Drained bog

5.6

662

18 5

16 0

277 23.8

0.13 0.04

0.078 0.058

0.9 0.35

0.9 0.47


Undrained bog

5.6

662

1 3

21 1

168 20.75

0.0125 0.004 1.118 0.202

0.1 0.05

7.6 3.1


0.08 0.05

0.0 0.13

Von Arnold et al., 2005b

3

3

7.2 0.67

Drained bog

5.6

662

27 1.7

28 1.4

215 17.7

0.012 0.003

5.5$10

Drained bog

5.6

662

22 2.1

26 1.2

180 18.9

0.009 0.004

0.079 0.029

0.05 0.03

0.3 0.22


Drained bog

5.6

662

17 1.0

40 1.9

195 20.1

0.004 0.0014 0.150 0.022

0.04 0.05

1.1 0.45


Undrained bog

5.6

662

7 1.0

47 2.6

155 15.3

0.004 0.002

1.45 0.184

0.03 0.04

11.4 3.87


Undrained fen Drained fen Undrained fen Drained fen Undrained bog Drained bog Undrained bog Drained bog Undrained fen

3 3 3 3 3 3 3 3 1.9

700 700 700 700 700 700 700 700 650

4 33 10 33 19 31 11 24 10

26.1 24.6 34.4 21.8 52.6 52.6 89.4 90.8 nd

nd nd nd nd nd nd nd nd nd



5.7$103 0.1485 0.0147 0.0469 3.35$103 0.0124 6.96$103 4.87$103 3$104

30.13 0 9.69 0.07 2.41 0.81 5.52 2.77 0.272

Laine et al., 1996 Laine et al., 1996 Laine et al., 1996 Laine et al., 1996 Laine et al., 1996 Laine et al., 1996 Laine et al., 1996 Laine et al., 1996 Nykänen et al., 1995

Values represent mean standard error. nd e not determined.

8.5$10


8.5

3$10

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Table 2 Comparison of climate, soil parameters, mean hourly fluxes from measured day time values and annual emissions of greenhouse gases from Northern and Southern peatlands. Annual gas emissions were calculated from the integrated weekly fluxes of the three replicates, assuming a constant flux rate between gas samplings.


variation in CH4 fluxes at the drained bog site (KG2) differed from those at the other three sites, where the patterns were generally similar (p < 0.05). The proportion of negative CH4 fluxes (63.2%) was highest at the drained bog (KG2) site, while positive CH4 fluxes (73e93%) predominated at the other study sites. The mean hourly N2O fluxes at the four experimental sites ranged from 0.4 to 1 mg N2O m2 h1, but were not significantly (p > 0.05) different between fen and bog sites (Table 2). Fluxes of N2O were highest during early spring (February, March) and during summer at all study sites (Fig. 1). No correlation was observed between N2O fluxes and soil temperature or groundwater level (r2 < 0.05). The temporal variation in N2O fluxes from the drained bog site (KG2) differed significantly (p < 0.05) from that in the drained fen sites (HC and LC), but not from the undrained bog site (KG1), which differed only from the drained LC fen site, with the lowest organic carbon content (Fig. 1). 3.3. Annual emissions of greenhouse gases Annual gas emissions were calculated from mean hourly fluxes for CH4 and N2O only. The two drained fen sites (HC and LC) and the undrained bog site (KG1) did not differ significantly (p > 0.05), in annual CH4 emissions, while the drained bog site (KG2) was a net CH4 sink (Table 2). Annual emissions of N2O (Table 2) were highest (9.52 g m2 y1) in the drained bog site (KG2), similar (p < 0.05) in the drained HC fen and the undrained bog (KG1) (5.83 g m2 y1 and 5.77 g m2 y1) and lowest in the drained LC fen (4.21 g m2 y1). GHG emissions and physico-chemical properties of soil at our experimental sites were then compared to those from fens or bogs in Southern Germany (Fiedler et al., 1998; Flessa et al., 1998; Jungkunst and Fiedler, 2007), Southern Sweden (Von Arnold et al., 2005a, 2005b) and Finland (Nykänen et al., 1995; Laine et al., 1996). Annual emissions of CH4 in our sites were in the same range as in other peatlands, but annual emissions of N2O from our sites were much greater (Table 2), and were significantly higher (p < 0.05) than from soils with similar C/N ratio (Fig. 2, Table 2). 4. Discussion Greenhouse gas emissions from peatlands have been studied most extensively in fens and bogs in the northern hemisphere

Fig. 2. Relationship between soil C/N ratio and annual N2O emissions. The squares represent the data from Klemedtsson et al. (2005) and the triangles represent the data from our experimental sites.

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under cold and temperate climates. This study provides data on hourly fluxes of CO2, CH4 and N2O and annual emissions of CH4 and N2O from the fen and bog sites of the Ljubljana Marsh, which is a peatland in Southern Europe with warmer and more humid climate than northern peatlands. The four different study sites are exposed to the same climatic conditions but differ significantly in soil properties and groundwater levels. Despite abundant literature on GHG emissions, there is surprisingly little overlap or consistency in investigations of variables affecting GHG, in terms of frequency, duration, environmental parameters, calculations and land use. This makes it extremely difficult to compare data from different studies and comparison was only possible with the few studies that contained similar sets of environmental parameters in association with GHG emissions mean annual temperature and precipitation and groundwater level. The mean annual temperature increases across the latitudinal gradient from Finland to Slovenia. Fen and bog sites in Southern Germany with the lowest mean annual precipitation are comparable to Southern Sweden or Finland, whereas those with the highest mean annual precipitation are comparable to sites in Slovenia. Groundwater levels in our fen and bog sites are the lowest compared to Northern European peatlands. The role of plants in regulating greenhouse gas emissions is not well understood. Peatland vegetation potentially controls CO2 and CH4 fluxes (Drösler et al., 2008), while plant residues increase the availability of organic carbon for denitrification and consequently N2O fluxes (McCarty and Bremner, 1993). Natural mires take up CO2 by photosynthesis and release CO2 and CH4 to the atmosphere during microbial decomposition but they are neutral with respect to N2O. In contrast, drainage of peatlands increases release of CO2 and sometimes N2O, while CH4 emissions are decrease or even CH4 is taken up. Von Arnold et al. (2005a) report that the forest type (deciduous, coniferous forest) influences N2O emissions, whereas CO2 and CH4 emissions did not differ significantly. They also cited an earlier report by Menyailo and Huwe (1999) that N2O emissions from similar soils with different vegetation increase in the following order: grassland < coniferous forest < deciduous forest. It has been also shown that the N2O emissions from the soils without plants were higher compared to those from cultivated soil (Nykänen et al., 1995; Maljanen et al., 2007), because plants uptake nitrate and limits denitrification. 4.1. Carbon dioxide fluxes Total soil respiration from fen and bog sites in the Ljubljana Marsh correlated positively with temperature and negatively with groundwater level, in agreement with published data for north European regions (reviewed in Smith et al., 2003). The positive correlation of total soil respiration with soil temperature is generally observed (Curiel Yuste et al., 2007) as long as soil water content is optimal for microbial activity (Smith et al., 2003). In Slovenia, mean hourly CO2 fluxes were similar in the drained bog (KG2) and the drained fen (HC and LC) sites, but significantly lower in the undrained bog site (KG1) (Table 2). This would imply that groundwater level is the principal factor controlling total soil respiration in fens and bogs, whereas differences in Corg content, which also affect microbial activity (Kraigher et al., 2006), and differences in surface plant residues (cut grass in fen vs. surface litter in bog) are less important. Drainage increases oxygen penetration in peat above the groundwater level, where increased CO2 release may be a consequence of enhanced aerobic peat mineralization by heterotrophs (Silvola et al., 1996). Despite differences in geographic location, climate and vegetation, the mean hourly fluxes of CO2 from the four experimental sites in Slovenia (Table 2) were in the same range as those from the bog

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sites (80e277 mg CO2 m2 y1) in Southern Germany (reviewed in Jungkunst and Fiedler, 2007) and Southern Sweden (Von Arnold et al., 2005a, 2005b). However, fluxes were significantly lower than those from the fen sites (333 and 542 mg CO2 m2 y1) in Southern Germany (reviewed in Jungkunst and Fiedler, 2007), possibly through differences in the amount or quality of organic matter, due to differences in land use rather than groundwater level (cf. Table 2). 4.2. Methane fluxes CH4 emissions at all study sites in the Ljubljana Marsh were also affected by soil water content and consequent oxygen availability, but not by soil temperature. The observed very low emissions, which were very often close to the ambient concentration or the detection limit, suggest that the Ljubljana Marsh peatlands do not contribute significantly to the regional, much less global CH4 emissions (Table 2). Low to negligible CH4 emissions are not surprising since groundwater level at all our sites is well below the critical threshold for CH4 release (Jungkunst and Fiedler, 2007). Annual CH4 emissions from Slovenian experimental sites (0.28 and 0.3 g CH4 m2 y1) were much lower than those reported for Finnish drained and undrained fens and bogs (Nykänen et al., 1998; Huttunen et al., 2003), German undrained bog (Fiedler et al., 1998) and Swedish undrained bog sites (Von Arnold et al., 2005a, 2005b). The same trend was observed for mean hourly CH4 fluxes. However, mean hourly CH4 fluxes from Slovenian drained fen (HC and LC) sites were similar to those from Swedish drained bog sites (Von Arnold et al., 2005a, 2005b) despite much higher groundwater levels in the latter (Table 2). These results confirm the validity of the critical threshold groundwater of 10 cm for CH4 release. At lower groundwater levels higher oxygen availability in deeper layers of the peat profile reduces CH4 production and favours CH4 oxidation (Whalen and Reeburgh, 1990). In our study net CH4 uptake occurred only in the drained bog site (KG2), but CH4 uptake rates were almost half of those reported for Finnish boreal forest soils (Maljanen et al., 2003; Saari et al., 2004) and comparable to those from agricultural soils in Spain (Merino et al., 2004). Drained or aerated soils are generally considered to contribute to the removal of CH4 from the atmosphere (Smith et al., 2000). Several studies have shown that drained forest and agricultural soils act as methane sinks (Martikainen et al., 1995; Flessa et al., 1998; Le Mer and Roger, 2001), although the magnitude of the sink depends on groundwater level and weather conditions in the season (Nykänen et al., 1995; Maljanen et al., 2003). 4.3. Nitrous oxide fluxes As in other studies (reviewed in Smith et al., 2003), N2O emissions at all study sites in the Ljubljana Marsh were affected by soil temperature, groundwater level and organic carbon and nitrogen availability. Drainage, and consequent better aeration, increase organic C and N availability, due to increased mineralization, which also affects gas emissions (Martikainen et al., 1993; Silvola et al., 1996). Increased N2O emissions with drainage were reported for Finnish peat soils (Martikainen et al., 1995; Nykänen et al., 1995) and organic agricultural soils in Germany (Flessa et al., 1998). Much higher N2O emissions at our sites than at Swedish (Von Arnold et al., 2005a, 2005b), German (Flessa et al., 1998) and Finnish (Nykänen et al., 1995; Laine et al., 1996) sites could therefore be associated with much lower annual groundwater level (Table 2). In addition, higher mean annual temperatures and significantly higher mean annual precipitation rates in Slovenia compared to Northern Europe may favour mineralization of organic matter and

nitrification and denitrification, which both contribute to N2O emissions (Gödde and Conrad, 1999). The mean hourly N2O fluxes at all our study sites were comparable to N2O fluxes from drained fen sites in Southern Germany (Flessa et al., 1998) and were 2e8 times higher than N2O fluxes from bog sites in Southern Sweden (Von Arnold et al., 2005a, 2005b). Lowest N2O emissions were observed during the winter, when the temperatures close to or below zero may have decreased nitrification and denitrification rates (Öquist et al., 2004; Mørkved et al., 2006). Interestingly N2O fluxes were highest during early spring, when temperatures were only few (1e3) degrees above zero, but microbial processes may have been stimulated by higher availability of organic carbon and nitrogen due to thawing of the frozen soil (Christensen and Tiedje, 1990). N2O fluxes from the drained bog site (KG2) were approximately twice those from the drained HC fen site, despite similar groundwater levels, and this difference could be due >2-fold greater organic carbon content in the drained bog site (KG2) (Table 1). Annual N2O emissions from the Slovenian fen and bog sites (4e10 g N2O m2 y1, Table 2) were 40to 100-fold higher than those reported for Swedish bogs (0.1e1.1 g N2O m2 y1, Von Arnold et al., 2005a, 2005b), Finnish fens and bogs (0e0.2 g N2O m2 y1, Martikainen et al., 1993; Nykänen et al., 1995; Laine et al., 1996) and German fens and bogs (0e0.1 g N2O m2 y1, reviewed in Jungkunst and Fiedler, 2007). However, as indicated by previous studies on our HC and LC fens with similar C/N ratio and bogs with higher C/N ratio (Hacin et al., 2001; Kraigher et al., 2006; Ausec et al., 2009) microbial activity increases with soil carbon content, implying greater carbon availability and higher N2O emissions are usually observed at lower groundwater level (Table 2; Martikainen et al., 1995). Dramatic N2O fluxes evident at the Ljubljana Marsh sites suggest that even greater care should be taken to prevent rapid mineralization of high organic soils in environments with mild temperatures and high annual precipitation. Klemedtsson et al. (2005) demonstrated an exponential relationship between soil C/N ratio and annual N2O emissions from drained organic forest soils. The model, which was further developed by Ernfors et al. (2007), was not confirmed at all sites in our study, where annual N2O emissions were highest at the drained bog site (KG2) and lowest at the drained LC fen site. The two sites differ significantly in organic C and N content and hence the C/N ratio (Tables 1 and 2). Although the drained fen sites with similar C/N ratio (HC and LC) fitted the model of Ernfors et al. (2007), N2O emissions from undrained and drained bog sites (KG1 and KG2) were 9-fold and 25-fold greater, than predicted by the model. Our results therefore suggest that groundwater level and carbon availability influenced N2O emissions in bog soil independently of the C/ N ratio. As already speculated by Klemedtsson et al. (2005) other environmental parameters, such as temperature, pH, groundwater level and substrate availability, may influence N2O emissions when the soil C/N ratio is between 15 and 20, as in our undrained (KG1) and drained (KG2) bog sites (Table 2). 5. Conclusions Comparison of greenhouse gas emissions from fens and bogs in Southern Europe demonstrates that fen and bog sites in Slovenia have similar mean hourly CO2 fluxes and up to 300-fold higher annual N2O emissions than peatlands in Northern Europe, but are not a significant source of CH4. CO2 emissions, but not CH4 and N2O emissions, correlated with soil temperature and groundwater level. The relationship between the soil C/N ratio and N2O emissions was confirmed for fens but was less clear for bogs. This suggests that other factors, including lower mean annual groundwater level, higher mean annual temperature and precipitation in Southern


peatlands, contribute to considerably higher annual emissions of N2O compared to Northern peatlands. Acknowledgements This work was supported by the Slovenian Research Agency grants J4-6149-0481-04 and P4-0116 and by the Centre of Excellence Environmental Technology Grant. We would like to thank Simona Leskovec for technical assistance and Prof. J.I. Prosser for helpful discussions. References Aerts, R., Ludwig, F., 1997. Water-table changes and nutritional status affect trace gas emissions from laboratory columns of peatland soils. Soil Biology & Biochemistry 29, 1691e1698. Alm, J., Saarnio, S., Nykänen, H., Silvola, J., Martikainen, P.J., 1999. Winter CO2, CH4 and N2O fluxes on some natural and drained boreal peatlands. Biogeochemistry 44, 163e186. Ausec, L., Kraigher, B., Mandic-Mulec, I., 2009. Differences in the activity and bacterial community structure of drained grassland and forest peat soils. Soil Biology & Biochemistry 41, 1874e1881. Avery, G.B., Shannon, R.D., White, J.R., Martens, C.S., Alperin, M.J., 1999. Effect of seasonal changes in the pathways of methanogenesis on the d13C values of pore water methane in a Michigan peatland. Global Biogeochemical Cycles 13, 475e484. Bundy, L.G., Meisinger, J.J., 1994. Nitrogen availability indices. In: Weaver, R.W., Angle, S., Bottomley, P., Bezdicek, D., Smith, S., Tabatabai, A., Wollum, A. (Eds.), Methods of Soil Analysis, Part 2: Microbiological and Biochemical Properties. SSSA Book Series, No.5. SSSA, Madison, Wisconsin, USA, pp. 951e983. Chimner, R.A., Cooper, D.J., 2003. Influence of water table levels on CO2 emissions in a Colorado subalpine fen: an in situ microcosm study. Soil Biology & Biochemistry 35, 345e351. Christensen, T.R., Jonasson, S., Callaghan, T.V., Hvstrom, M., 1995. Spatial variation in high-latitude CH4 flux along a transect across Siberian and European tundra environments. Journal of Geophysical Research 100, 21035e21045. Christensen, S., Tiedje, J.M., 1990. Brief and vigorous N2O production by soil at spring thaw. Journal of Soil Science 41, 1e4. Conrad, R., 1996. Soil microorganisms as controllers of atmospheric trace gases (H2, CO, CH4, OCS, N2O, and NO). Microbiological Reviews 60, 609e640. Cop, J., Sinkovi c, T., Vidrih, M., Hacin, J., 2004. Vpliv kosnje in gnojenja na botani cno sestavo dveh razli cnih travnikov na Ljubljanskem barju. (Influence of cutting and fertilising management on the botanical composition of Ljubljana marsh grasslands). Acta Agriculturae Slovenica 83, 157e169. Curiel Yuste, J., Baldocchi, D.D., Gershenson, A., Goldstein, A., Misson, L., Wong, S., 2007. Microbial soil respiration and its dependency on carbon inputs, soil temperature and moisture. Global Change Biology 13, 1e18. Davidson, E.A., Keller, M., Erickson, H.E., Verchot, L.V., Veldkam, E., 2000. Testing a conceptual model of soil emissions of nitrous and nitric oxides. Bioscience 50, 667e680. Driesen, P.M., 1978. Peat soil. In: Soil and Rice. IRRI, Los Banos, Philippines, pp. 763e779. Drösler, M., Freibauer, A., Christensen, T.R., Friborg, T., 2008. Observations and status of peatland greenhouse gas emissions in Europe. In: Dolman, H., Valentini, R., Freibauer, A. (Eds.), The Continental-scale Greenhouse Gas Balance of Europe. Ecological Studies, vol. 203. Springer, New York, pp. 243e261. Duddleston, K.N., Kinney, M.A., Kiene, R.P., Hines, M.E., 2002. Anaerobic microbial biogeochemistry in a northern bog: acetate as a dominant metabolic end product. Global Biogeochemical Cycles 16, 1063e1071. Ernfors, M., von Arnold, K., Stendahl, J., Olsson, M., Klemedtsson, L., 2007. Nitrous oxide emissions from drained organic forest soilseean up-scaling based on C:N ratios. Biogeochemistry 84, 219e231. Fiedler, S., Adam, K., Sommer, M., Stahr, K., 1998. CO2 und CH4 emissionen aus böden entlang eines Feuchtegradienten im südwestdeutschen Alpenvorland. Mitteilungen Deutsche Bodenkundliche Gesellschaft 88, 15e18. Flessa, H., Wild, U., Klemisch, M., Pfadenhauer, J., 1998. Nitrous oxide and methane fluxes from organic soils under agriculture. European Journal of Soil Science 49, 327e335. Forster, J.C., 1995. Soil physical analysis. In: Alef, K., Nannipieri, P. (Eds.), Methods in Applied Soil Microbiology and Biochemistry. Academic Press Inc., San Diego, pp. 105e121. Gödde, M., Conrad, R., 1999. Immediate and adaptational temperature effects on nitric oxide production and nitrous oxide release from nitrification and denitrification in two soils. Biology and Fertility of Soils 30, 33e40. Gorham, E., 1991. Northern peatlands: role in the carbon cycle and probable response to climatic warming. Ecological Applications 1, 182e195. Hacin, J., Cop, J., Mahne, I., 2001. Nitrogen mineralization in marsh meadows in relation to soil organic matter content and watertable level. Journal of Plant Nutrition and Soil Science 164, 503e509. Hines, M.E., Duddlestn, K.N., Kiene, R.P., 2001. Carbon flow to acetate and C1 compounds in northern wetlands. Geophysical Research Letters 28, 4251e4254.

1445

Huttunen, J.T., Nykänen, H., Turunen, J., Martikainen, P.J., 2003. Methane emissions from natural peatlands in the northern boreal zone in Finland, Fennoscandia. Atmospheric Environment 37, 147e151. Jerman, V., Metje, M., Mandi c Mulec, I., Frenzel, P., 2009. Wetland restoration and methanogenesis: the activity of microbial populations and competition for substrates at different temperatures. Biogeosciences 6, 1127e1138. Jungkunst, H.F., Fiedler, S., 2007. Latitudinal differentiated water table control of carbon dioxide, methane and nitrous oxide fluxes from hydromorphic soils: feedbacks to climate change. Global Change Biology 13, 2668e2683. Klemedtsson, L., von Arnold, K., Weslien, P., Gundersen, P., 2005. Soil CN ratio as a scalar parameter to predict nitrous oxide emissions. Global Change Biology 11, 1142e1147. Kraigher, B., Stres, B., Hacin, J., Ausec, L., Mahne, I., van Elsas, J.D., Mandic-Mulec, I., 2006. Microbial activity and community structure in two drained fen soils in the Ljubljana Marsh. Soil Biology & Biochemistry 38, 2762e2771. Laiho, R., 2006. Decomposition in peatlands: reconciling seemingly contrasting results on the impacts of lowered water levels. Soil Biology & Biochemistry 38, 2011e2024. Laine, J., Silvola, J., Tolonen, K., Alm, J., Nykänen, H., Vasander, H., Sallantaus, T., Savolainen, I., Sinisalo, J., Martikainen, P.J., 1996. Effect of water-level drawdown on global climatic warming: northern peatlands. Ambio 25, 179e184. Le Mer, J., Roger, P., 2001. Production, oxidation, emission and consumption of methane by soils: a review. European Journal of Soil Biology 37, 25e50. Lokupitiya, E., Paustian, K., 2006. Agricultural soil greenhouse gas emissions: a review of national inventory methods. Journal of Environmental Quality 35, 1413e1427. Mäkiranta, P., Hytönen, J., Aro, L., Maljanen, M., Pihlatie, M., Potila, H., Shurpali, N., Laine, J., Martikainen, P.J., Minkkinen, K., 2007. Soil greenhouse gas emissions from afforested organic soil croplands and cutaway peatlands. Boreal Environment Research 12, 159e175. Maljanen, M., Liikanen, A., Silvola, J., Martikainen, P.J., 2003. Methane fluxes on agricultural and forested boreal organic soils. Soil Use and Management 19, 73e79. Maljanen, M., Komulainen, V.M., Hytönen, J., Martikainen, P.J., Laine, J., 2004. Carbon dioxide and methane dynamics in boreal organic agricultural soils with different soil characteristics. Soil Biology & Biochemistry 36, 1801e1808. Maljanen, M., Hytönen, J., Mäkiranta, P., Alm, J., Minkkinen, K., Laine, J., Martikainen, P.J., 2007. Greenhouse gas emissions from cultivated and abandoned organic croplands in Finland. Boreal Environment Research 12, 133e140. Martikainen, P.J., Nykänen, H., Crill, P., Silvola, J., 1993. Effect of lowered water table on nitrous oxide fluxes from northern peatlands. Nature 366, 51e53. Martikainen, P.J., Nykänen, H., Alm, J., Silvola, J., 1995. Change in fluxes of carbon dioxide, methane and nitrous oxide due to forest drainage of mire sites of different trophy. Plant and Soil 168e169, 571e577. Martin ci c, A., 1987. Fragmenti visokega barja na Ljubljanskem barju. Scopolia 14, 1e53. McCarty, G.W., Bremner, J.M., 1993. Factors affecting the availability of organic carbon for denitrification of nitrate in subsoils. Biology and Fertility of Soils 15, 132e136. Menyailo, O.V., Huwe, B., 1999. Activity of denitrification and dynamics of N2O release in soils under six tree species and grassland in central Siberia. Journal of Plant Nutrition and Soil Science 162, 533e538. Merino, A., Pérez-Batallón, P., Macías, F., 2004. Responses of soil organic matter and greenhouse gas fluxes to soil management and land use changes in a humid temperate region of southern Europe. Soil Biology & Biochemistry 36, 917e925. Mørkved, P.T., Dörsch, P., Henriksen, T.M., Bakker, L.R., 2006. N2O emissions and product ratios of nitrification and denitrification as affected by freezing and thawing. Soil Biology & Biochemistry 38, 3411e3420. Nykänen, H., Alm, J., Lång, K., Silvola, J., Martikainen, P.J., 1995. Emissions of CH4, N2O and CO2 from a virgin fen and a fen drained for grassland in Finland. Journal of Biogeography 22, 351e357. Nykänen, H., Alm, J., Silvola, J., Tolonen, K., Martikainen, P.J., 1998. Methane fluxes on boreal peatlands of different fertility and the effect long-term experimental lowering of the water table on flux rates. Global Biogeochemical Cycles 12, 53e69. Öquist, M.G., Nilsson, M., Sörensson, F., Kasimir-Klemedtsson, A., Persson, T., Weslien, P., Klemedtsson, L., 2004. Nitrous oxide production in a forest soil at low temperatures e processes and environmental controls. FEMS Microbiology Ecology 49, 371e378. Öquist, M.G., Petrone, K., Nilsson, M., Klemedtsson, L., 2007. Nitrification controls N2O production rates in a frozen boreal forest soil. Soil Biology & Biochemistry 39, 1809e1811. Pihlatie, M., Syväsalo, E., Simojoki, A., Esala, M., Regina, K., 2004. Contribution of nitrification and denitrification to N2O production in peat, clay and loamy sand soils under different soil moisture conditions. Nutrient Cycling in Agroecosystems 70, 135e141. Robertson, G.P., Coleman, D.C., Bledsoe, C.S., Sollins, P., 1999. Standard Soil Methods for Long-term Ecological Research. Oxford University Press, New York. Saari, A., Smolander, A., Martikainen, P.J., 2004. Methane consumption in a repeatedly nitrogen-fertilised and limed spruce forest soil after clear-cutting. Soil Use and Management 20, 65e73. Schulz, S., Conrad, R., 1996. Influence of temperature on pathways to methane production in the permanently cold profundal sediment of Lake Constance. FEMS Microbiology Ecology 20, 1e14.

1446


Silvola, J., Alm, J., Ahlholm, U., Nykänen, H., Martikainen, P.J., 1996. CO2 fluxes from peat in boreal mires under varying temperature and moisture conditions. Journal of Ecology 84, 219e228. Smith, K.A., Dobbie, K.E., Ball, B.C., Bakken, L.R., Sitaula, B.K., Hansen, S., Brumme, R., Borken, W., Christensen, S., Prieme, A., Fowler, D., Macdonald, J.A., Skiba, U., Klemedtsson, L., Kasimir-Klemedtsson, Å., Degórska, A., Orlanski, P., 2000. Oxidation of atmospheric methane in northern European soils, comparison with other ecosystems, and uncertainties in the global terrestrial sink. Global Change Biology 6, 791e803. Smith, K.A., Ball, T., Conen, F., Dobbie, K.E., Massheder, J., Rey, A., 2003. Exchange of greenhouse gases between soil and atmosphere: interactions of soil physical factors and biological processes. European Journal of Soil Science 54, 779e791. Smith, L.C., MacDonald, G.M., Velichko, A.A., Beilman, D.W., Borisova, O.K., Frey, K.E., Kremenetski, K.V., Sheng, Y., 2004. Siberian peatlands a net carbon sink and global methane source since the early Holocene. Science 303, 353e356. Stres, B., Danev ci c, T., Pal, L., Mrkonji c Fuka, M., Resman, L., Leskovec, S., Hacin, J., Stopar, D., Mahne, I., Mandic-Mulec, I., 2008. Influence of temperature and soil

water content on bacterial, archaeal and denitrifying microbial communities in drained fen grassland soil microcosms. FEMS Microbiology Ecology 66, 110e122. Von Arnold, K., Nilsson, M., Hånell, B., Weslien, P., Klemedtsson, L., 2005a. Fluxes of CO2, CH4 and N2O from drained organic soils in deciduous forests. Soil Biology & Biochemistry 37, 1059e1071. Von Arnold, K., Weslien, P., Nilsson, M., Svensson, B.H., Klemedtsson, L., 2005b. Fluxes of CO2, CH4 and N2O from drained coniferous forests on organic soils. Forest Ecology and Management 210, 239e254. Webster, E.A., Hopkins, D.W., 1996. Contributions from different microbial processes to N2O emission from soil under different moisture regimes. Biology and Fertility of Soils 22, 326e330. Whalen, S.C., Reeburgh, W.S., 1990. Consumption of atmospheric methane by tundra soils. Nature 346, 160e162. World Reference Base for Soil Resources, 2006. World Soil Resources Reports. A Framework for International Classification, Correlation and Communication, vol. 103. FAO, Rome, 128 pp.