Relationships were determined between methane (CH4) production and in situ conditions within the permafrost active layer during a single melt season at Stordalen, Sweden, with a specific emphasis on temperature sensitivity of methanogenesis. In situ temperature, moisture, pH, dissolved organic carbon, and CH4 concentration data were measured at three contrasting active layer sites (sedge mire, Sphagnum mire, and ombrotrophic bog), and laboratory incubations of active layer material were subsequently employed to determine the sensitivity of CH4 production to temperature. Q10 values, describing the CH4 production response of peat to a temperature change of 10 °C, ranged from 1.9 to 3.5 and 2.4 to 5.8 for the sedge and Sphagnum mire sites, respectively. A wider review of the literature on Q10 responses of methanogenesis in northern peatlands shows similar features to the temperature response of CH4 production in the active layer at Stordalen. In general, Q10 values are not significantly different in Arctic permafrost wetlands than non-Arctic northern wetlands; however, Sphagnum sites display Q10 responses (mean Q10 = 8) that are notably greater than that of wetter minerotrophic-sedge environments (mean Q10 = 4.3). This finding has implications for the parameterization of Q10 factors in numerical carbon cycling models, and suggests that the use of spatially variable Q10 values could be a useful approach for more accurate modeling of CH4 fluxes from northern wetlands under different climatic change scenarios.
Mean annual Arctic air temperatures have increased at almost twice the rate of the global average during the past 100 years (IPCC, 2007). Future climatic projections suggest that the mean annual air temperature will increase by 2.2 to 3.2 °C in the 60 to 90°N latitudinal zone by 2050, with the potential for significant effects on terrestrial ecosystem processes and carbon cycling. Of particular concern is the impact of such temperature increases on Arctic tundra carbon reserves (Callaghan et al., 2005; Chapin et al., 2005).
Since the last glaciation, organic soils (peatlands) and cryoturbated permafrost-affected mineral soils in the northern permafrost region have accumulated 1600 Pg of C (1015 g) due to the sequestration of organic matter (Tarnocai et al., 2009). The fate of these carbon reserves in Arctic tundra regions depends upon rates of aerobic and anaerobic microbial decomposition of organic matter (OM) in the seasonally thawed “active layer.” Rates of decomposition are critically dependent on both hydrology and temperature (Christensen, 1991; Gorham, 1991; Hargreaves and Fowler, 1998); whereas dry conditions lead to predominantly aerobic decomposition producing CO2, waterlogged conditions promote slower decomposition yielding the more potent greenhouse gas CH4 (as well as CO2) (Callaghan et al., 2005). Soil temperature is known to have an effect on rates of these microbial processes (Anderson, 1992; Schimel et al., 1993). Although CH4 budget estimates change year to year, the most recent models of Wania et al. (2010) and Petrescu et al. (2010) for northern peatlands (45–90°N), account for 40–74 Tg CH4 yr-1 and for 37.7–157.4 Tg CH4 yr-1, respectively, of the total 190–220 Tg CH4 yr-1 from natural sources (IPCC, 2007).
Methane production results from the interaction of different biological and physical processes in the soil (Hogan, 1993; Schimel et al., 1993; Conrad, 1989; Bouwman, 1990; Wang et al., 1996) where decomposition of organic matter takes place under anaerobic conditions. The final step in the process of anoxic decomposition of complex organic matter is methanogenesis (Conrad, 1999) where the main substrates are hydrogen (Equation 1) or acetate (Equation 2).
Major process-level controls upon CH4 production in wetland ecosystems are: pH, temperature (Valentine et al., 1994), and substrate quantity and quality (Bridgham and Richardson, 1992; Valentine et al., 1994). Ecosystem-level controls include the presence of water, and the position of the water table (Harriss et al., 1982), and plant composition (Waddington et al., 1996; Bellisario et al., 1999). Controls on CH4 production in temperate and northern peatlands are well documented (Bergman et al., 2000; Dunfield et al., 1993; Le Mer and Roger, 2001; Segers, 1998; Svensson, 1984), but there is disproportionately less information on the spatial and temporal variation of these controls (especially with respect to soil temperature) in Arctic permafrost environments (Christensen et al., 2003, 2004; Valentine et al., 1994). In addition, most studies derive associations between temperature and CH4 production from seasonal field data sets where many other environmental variables also were changing. Few attempts have been made to conduct controlled laboratory experiments to determine the sensitivity of CH4 production in permafrost wetlands to changing soil temperature (Brouchkov and Fukuda, 2000; Metje and Frenzel, 2005, 2007; Rivkina et al., 2007; Svensson, 1984; Wagner et al., 2003, 2005, 2007), and no studies have compared the sensitivity for methanogenesis in the permafrost active layer to the range of Q10 in northern peatlands more generally. This paper aims to assess the variation in the controls of the CH4 concentration and production in the permafrost active layer of three contrasting peatlands located in a low Arctic discontinuous permafrost environment in northern Sweden. Through a comparison of our own experimental incubations data and those derived from previous studies, we investigate in detail the potential effect of temperature increase on CH4 production rates in the organic matter rich soils of permafrost and non-permafrost northern wetlands.
Materials and Methods
Fieldwork was conducted in Stordalen mire, 10 km southeast of Abisko (68°21′N, 18°49′E) in northern Sweden. The site is 25 ha in area and situated ∼200 km north of the Arctic Circle and 385 m a.s.l. on the south shore of Lake Torneträsk (Fig. 1). It is characterized by discontinuous permafrost with small (∼2 m) variations in topography. The small-scale topography gives rise to three types of peatland environments that differ in their nutrient and moisture conditions (Rosswall et al., 1975; Sonesson, 1969; Johansson et al., 2006). These three environments formed the focus for this study and are:
(a) Minerotrophic-sedge mire in which water and ion inputs derive from precipitation, surface water, and groundwater sources, leading to a relatively high soil pH and nutrient status. The dominant plant species in this wet mire is Eriophorum angustifolium Hock., but with considerable areas of Sphagnum riparium Ångst. The mire was not underlain by permafrost at the time of sampling, but the ground surface freezes and thaws seasonally. Fully thawed conditions usually prevail by mid-June.
(b) Minerotrophic-Sphagnum mire, which is dominated by Sphagnum, spp. It is underlain by permafrost, with a variable summer active layer depth. The active layer depth in summer 2006 was 22 cm (June) and ∼90 cm in August and September.
(c) Ombrotrophic bog, which receives water and associated ions solely from the atmosphere, usually because the accumulation of soil organic matter has caused hydrologic isolation from groundwater inputs, resulting in low soil pH and low nutrient status. The vegetation is dominated by ericaceous and other woody species such as Rubus chamaemorus L., Empetrum hermaphroditum Hagerup., and Andromeda polifolia L. (Johansson et al., 2006). The upper part of the permafrost thaws during summer forming an active layer of variable thickness. Average active layer depths recorded in summer 2006 were 22 cm (June), 32 cm (August), and 53 cm (September).
These three sub-habitats are hereafter designated as sedge (or Eriophorum) mire, Sphagnum mire, and ombrotrophic sites.
SAMPLING AND IN SITU MEASUREMENTS
Field sampling was conducted at the sedge, Sphagnum, and ombrotrophic sites during the summer thaw period in 2006 (from 12 to 21 June, 1 to 8 August, and 18 to 25 September). The coring sites were located within a 50 m2 area that represented the three typical vegetation covers of the area: Eriophorum angustifolium dominated at the minerotrophic sedge site, Sphagnum for the other minerotrophic site, and ericaceous and other woody species for the ombrotrophic bog. Two cores (A and B) were collected at each site using a 60 cm (length) × 15 cm (diameter) cm metal manual peat corer. Water table level and active layer depth were recorded prior to coring using a graduated metal rod. Immediately following core extraction, the temperature of the peat was measured in the soil profile using a Hanna Check Temperature probe (resolution = 0.1 °C; accuracy = ±0.3 °C), and soil moisture was measured using a delta T HH2 Theta Probe (accuracy = 1 to 5%). Once collected, cores were wrapped in pre-combusted (450 °C for 4.5 h) aluminum foil.
Core Subsampling and Analysis
Cores A and B from each site were subsampled at six depths. The subsampling interval depended on the core length, which was between 22 to 50 cm. Each core section was ∼10 cm in diameter and 4 cm long.
Core A was retained for analysis in Abisko and was subsampled in the laboratory within a few hours of collection for (a) pore water nutrient analysis, (b) pH measurement, (c) dissolved CH4 concentration, and (d) subsequent CH4 production rate incubations. Pore water pH was measured in the laboratory on core subsample slurries using an Orion 250 A pH meter (resolution: 0.01/0.1 pH; accuracy: ±0.02). A ∼2 cm diameter core was removed from each section using a metal mini-corer. Each mini-core (including 3 replicate samples for each depth) was placed in a 35 mL serum vial for CH4 concentration and production analyses. Our aim was to minimally disturb the peat to avoid outgassing of CH4 or entry of O2 that might impact methanogen populations. We did not attempt to remove living roots that were present in the mini-cores, with the exception of the largest ones that could be eliminated without damage to the peat structure. The presence of severed roots in the peat may have provided labile carbon to support methanogenesis; however, under in situ conditions these roots also would have been releasing exudates that are readily metabolized by methanogens. Consequently, minimizing CH4 outgassing and entry of O2 were given priority because their impact on the incubation results was deemed to be potentially more detrimental.
Pore water was extracted from soil subsamples by centrifugation (2000 rpm) using ∼75 cm3 of peat in Fisher Vectaspin 20 centrifuge tubes. The water supernatant was filtered immediately through Whatman glass microfibre GF/F filters (pore size = 0.7 µm). The filtrate was subsequently frozen until analysis in the U.K.
Each core B was wrapped in combusted Al foil and stored at - 15 °C immediately after collection. Samples were transported to the U.K. encased in plastic pipes and then stored at -20 °C prior to analysis.
Analytical Laboratory Methods
Elemental Analysis. The elemental compositions (C, H, and N) of freeze-dried subsamples from core B were measured using a Carlo Erba EA1108 Elemental Analyser (accuracy ±0.3%). Each analysis was conducted in triplicate.
Pore Water Chemistry Analyses. Pore water filtrate was thawed at room temperature and nutrients (NH4+, NO3-, NO2-, and Soluble Reactive Phosphorus [SRP]) and Si were determined colorimetrically using a Bran and Luebbe Auto Analyser 3. Detection limits were 0.6 g L-1 for NH4+, 0.2 g L-1 for NO3-, 0.04 g L-1 for NO2-, 0.5 g L-1 for SRP, and 0.8 g L-1 for Si. Non-Purgeable Organic Carbon (NPOC) and Total Dissolved Nitrogen (TDN) in the samples were determined using a Shimadzu TOC-VCSN/TNM-1 analyzer. NPOC was measured as the carbon remaining after acidification with 2M HCl and sparging with He for 2 min. Six replicate injections were made per sample. Acidified and sparged deionized water samples were used as blanks. Detection limits were 1.2 mg L-1 for DOC and 0.1 mg L-1 for TDN. Dissolved Organic Nitrogen (DON) was calculated as [TDN] -[DIN], where [DIN] = [NH4+] + [NO3-] + [NO2-]. Data are not available for June samples due to vial breakage during transport.
Dissolved CH4 Concentrations and CH4 Production
Dissolved CH4 Concentrations. Core subsamples, including fragments of small plant roots, collected from 6 depths (3 replicates each) from the three sites were placed in 35 mL serum vials with 20 mL of a 10% KCl solution acidified with HCl to pH 1. Vials were stored at 4 °C at the Abisko research station before departure to the U.K. and were kept cold during transport. The vial headspace gas, representing the dissolved CH4 in sediment porewater, was analyzed in the U.K. using a CarloErba HRGC 5300 Mega Series Gas-Chromatograph (GC) fitted with a flame ionization detector (FID). The GC was equipped with a 2 m Porapak QS (80/100 mesh) column at oven temperature of 35 °C. The carrier gas was helium (flow rate = 35 mL min-1) and the support gases (H2 and zero air) were set at flow rates of 35 and 350 mL min-1, respectively.
Methane Production. Core subsamples were placed in 35 mL serum vials within a few hours of core collection and flushed with oxygen-free nitrogen. Large root fragments were removed during the subsampling. Vials were stored in the dark at 4 °C in Abisko for a few days and kept refrigerated with ice during transportation to the U.K. Once in Bristol the samples were stored in an incubator at 4 °C. Samples from the 3 different sites (6 depths each) were subsequently incubated sequentially at 4, 14, and 24 °C. In the choice of this specific methodology we assume that the effect of the incubation sequence does not affect the reliability of CH4 production rates because the predominant substrate for methanogenesis should be the labile fraction of organic matter. It has been shown elsewhere that in short duration sequential incubations of peat, the age of respired carbon does not change with time and temperature (Dioumaeva et al., 2002).
The headspace gas was sampled (50 µL) by syringe after 1, 2, and 3 days, respectively, for the three different temperatures. CH4 concentration was determined by gas chromatography as described already. June samples were incubated only at 4 °C due to instrumentation problems.
Data Analysis: Q10 Values and Other Biological Coefficients
Methane production data were corrected for peat moisture content after having calculated the natural water content of the samples. Values are reported as µg CH4 per gram (g-1) of dry peat per day (d-1). Linear regression analyses of the change in CH4 concentration with time were performed to determine differences in the methanogenic production potential of the peat at different depths.
Biological coefficients were subsequently calculated as follows. The Q10 value (Equation 3) is a temperature coefficient that measures the rate of change of a biological or chemical system as a consequence of increasing a temperature change of 10 °C.
where R1 and R2 are the rates of methane production µg g-1 d-1) at temperatures T1 and T2, respectively, where T is the temperature in °C or Kelvins. An R0 value is the extrapolated production rate at 0 °C (R0 = R/Q10T/10) and does not take into account the possibility of ‘on’ vs. ‘off’ in the metabolism of microorganisms. Calculation of the parameter assumes a gradual decrease in metabolic rate at low temperature.
The apparent Activation Energy (Ea; kJ mol-1) is the minimum energy necessary for a specific chemical reaction to occur (Equation 4) and is calculated as:
where Q10 is the temperature coefficient (described above), R is the production rate µg g-1 d-1), and T1 and T2 are the temperatures in °C.
During the three-month study period both the minerotrophic sites were waterlogged, and the water table level in each was close to the surface (∼2 cm depth). In contrast, the ombrotrophic bog was relatively dry [moisture = 20 (top 20 cm) to 50 (40–50 cm)%] with no obvious water table within the upper 50 cm. In June, only the upper 20 cm of soil was thawed at all three sites. In August and September, the sedge and Sphagnum sites were permafrost free and the ombrotrophic bog active layer depths were 32 and 53 cm, respectively. Mean soil temperatures along the soil profile for all sites on the days of core collection were 3.4 ± 1.4 °C, 11.3 ± 3.2 °C, and 5.7 ± 2.8 °C in June, August, and September, respectively (Table 1). The difference between the surface and deeper temperatures was more evident in August where the variation was ∼7 °C over 45 cm depth range (e.g. Sphagnum site). Pore water pH was relatively constant (within 0.2 units) with depth at each site (Table 1). The pH of pore water at the minerotrophic Sphagnum mire (mean 4.2 ± 0.1) and ombrotrophic bog (mean pH = 4.1 ± 0.2) were lower than that of the sedge mire (mean pH = 5.6 ± 0.2).
pH and temperature values for the three different sites and months.
ELEMENTAL ANALYSIS AND NUTRIENT CHARACTERIZATION
The sedge (Fig. 2, part a) and Sphagnum mires (Fig. 2, part b) displayed relatively constant soil Total Organic Carbon (TOC) contents with depth (240 ± 14 to 590 ± 22 mg g-1) and exhibited little variation between sampling periods. The ombrotrophic bog displayed similar values for TOC concentration in the upper soil profile (<25 cm) for June and August but below 25 cm there was a decrease in percent TOC with depth (Fig. 2, part c). The September samples showed a sharp decrease in percent TOC at 15 cm of depth. Total Nitrogen (TN) concentrations at all sites ranged from 9 ± 4 to 25 ± 4 mg g-1. There are few well-defined trends in TN, but soil TN concentrations in the Sphagnum and Eriophorum mires tended to be higher in June and September. In the ombrotrophic bog (Fig. 2, part c), TN generally increased in concentration with depth and through the thaw season.
Pore Water Samples
Non-Purgeable Organic Carbon (NPOC), Total Nitrogen (TN), and Total Organic Nitrogen (TON) exhibited high down-profile variability in the sedge and Sphagnum spp. sites (Fig. 2, parts a and b). Concentrations of TN and NPOC were generally higher in June (1.2 ± 0.2 to 3.7 ± 0.2 mg L-1 for TN and 21 ± 3 to 200 ± 13 mg L-1 for NPOC) than in August (1.0 ± 0.1 to 2.5 ± 0.1 mg L-1 for TN and 19 ± 3 to 164 ± 13 mg L-1 for NPOC) and September (1.0 ± 0.2 to 2.6 ± 0.1 mg L-1 for TN and 23 ± 12 to 122 ± 14 mg L-1 for NPOC).
There was comparatively little variation in dissolved species with depth and between sampling periods in the ombrotrophic bog (Fig. 2, part c) other than an increase in NPOC in the upper 10 cm of the core in all three sampling periods (mean NPOC at 5 cm = 137 ± 24 mg L-1).
The highest concentrations of CH4 were recorded in the sedge (Fig. 3, part a) and Sphagnum sites (Fig. 3, part b) with mean values ranging from 13 ± 5 to 153 ± 69 µmol L-1 and 13 ± 16 to 160 ± 103 µmol L-1, respectively. The pore water concentrations of CH4 decreased from June to August and then increased in September. Methane concentrations generally increased with depth (Fig. 3, parts a and b) during each sampling period, and the position of the CH4 concentration maxima tended to shift down the soil profile as the size of the active layer increased at both these sites. The ombrotrophic bog (Fig. 3, part c) displayed much lower CH4 concentrations (<6 µmol L-1) during all sampling periods and at all depths. The deepest sample (30–35 cm) contained a slightly higher CH4 concentration (∼14 µmol L-1) in August and September.
The temperature sensitivities of CH4 production at the three main sites and at different depths in the soil profile are shown in Figures 4 and 5. Incubation of peat subsamples in the absence of oxygen demonstrated that CH4 production rates vary with temperature, peatland type, and soil depth. In general, the response of CH4 production to an increase in temperature was strongest in the sedge mire, followed by the Sphagnum site. In the former, the average CH4 production rate at 14 °C was 27 ± 22 µg d-1 g-1 compared with 48 ± 44 µg d-1 g-1 at 24 °C (Fig. 5, parts a and b). Incubations of ombrotrophic bog samples produced only a few µg d -1 g-1 of CH4 and there was no significant change in CH4 production rate with an increase in temperature (Fig. 5, parts e and f).
These site-dependant temperature responses of CH4 production varied with soil profile depth and time of sampling. For example, rates of CH4 production in the sedge site, with their high temperature sensitivity, decreased with increasing soil depth for all sampling months and at the three temperatures (Fig. 4, except June; Fig. 5, parts a and b). By comparison, the Sphagnum site displayed much smaller variations in rate with depth (Fig. 5, parts c and d). Comparison of CH4 production rates in the two minerotrophic sites at a single temperature (4 °C) but for different sampling times show highest rates of methane production for the September soil samples (Fig. 4, parts a and b). In the Sphagnum mire, rates of CH4 production in June and August samples were negligible at 4 °C compared to September samples incubated at the same temperature. Sedge site rates of CH4 production showed a progressive increase from June to September in the top 20 cm of the active layer when incubated at 4 °C.
In order to better understand the CH4 production trends described above and therefore how the consortium of microorganisms responsible for soil methanogenesis responds to temperature change, we calculated R0 and Q10 values (Table 2; Fig. 6). A true Q10 response should fit the relationship R = R0Q10(T/10) and most of the data sets exhibit a high R2 value (Table 2) albeit it is based upon CH4 production rates determined at three temperatures (4, 14 and 24 °C; Fig. 6). In general, Q10 values in the sedge site are within the same range for the two sampling months (2.4 to 3.5 and 1.9 to 2.8, in August and September, respectively; Table 2). Q10 values are higher in the Sphagnum site (3.2–5.8 and 2.5–4.2, in August and September, respectively) relative to the sedge mire (2.4–3.5 and 1.9–2.8, in August and September, respectively). The difference in the means of the Q10 values for the two sites is significant at the 95% confidence interval using a 2-tailed Student's t-test (p = 0.012). Q10 values also vary by depth with deeper samples exhibiting slightly higher values.
Extrapolated production rates at 0 °C (R0) also are shown in Table 2. The sedge mire displayed higher values (e.g., August mean = 5.6 ± 6.3) than the Sphagnum site (e.g., August mean = 0.5 ± 0.3) at all depths and during August and September. R0 values in the sedge mire also tended to decrease with depth, exhibiting particularly high values (R0 = 18) in the upper 2 cm of soil. The apparent Activation Energy (Ea) showed slightly higher values in the Sphagnum site with a mean of 115 and 91 kJ mol-1 in August and September, respectively. In the same months, the sedge site had values of 83 and 68 kJ mol-1. This difference between the Ea at the two minerotrophic sites was statistically significant at the 95% confidence level (p = 0.003; 2-tailed t-test).
Main biological coefficients for the sedge and Sphagnum mire in August and September (the numbers in parentheses indicate the standard deviation).
ENVIRONMENTAL CONTROLS ON CH4 CONCENTRATIONS AND PRODUCTION
Methane concentration profiles reflect the interaction of several processes (e.g., CH4 production and oxidation rates, transport of CH4 by plants), while the CH4 production rates termed via incubation of peat indicate the potential for methanogenesis over short-time intervals under anoxic conditions and with a fixed organic carbon pool. Plant-mediated effects on CH4 production (e.g., gas transport and root exudation) are absent in the production potentials.
The highest CH4 production potentials and extrapolated production rates at 0 °C (R0; Table 1) always occurred in surface peat and declined with depth (for both mire sites and months). High CH4 production potentials in surface soil have been reported elsewhere (Segers, 1998; Valentine et al., 1994; Sundh et al., 1994; Yavitt et al., 1987) and reflect the accumulation of above-ground litter inputs, in addition to inputs of fresh organic matter from root turnover and exudation in these layers (Joabsson and Christensen, 2001). The low CH4 concentrations and production rates in the ombrotrophic bog reflect the unsuitable conditions of this environment for methanogenesis. The absence of a high water table and, consequently, the presence of a deep oxic zone coupled with low temperature during a large part of the year (annual mean = -0.7 °C), and the dominance of recalcitrant organic matter (due to a dominance of feather mosses, ericaceous and other woody species), are not conducive to the development of a significant and active community of anaerobic microorganisms (Valentine et al., 1994). Despite the common conception that ombrotrophic bogs have a low nutrient status, our results indicate solid phase and dissolved nutrient and organic carbon levels that are comparable to the sedge and Sphagnum sites (Fig. 2), suggesting that the lower CH4 production potentials arise primarily from the presence of a deep oxic zone. These findings are consistent with the low total hydrocarbon emissions [CH4 + non-methane volatile organic compounds (NMVOCs)] from these sites in Stordalen of 2.2 ± 0.3 mg C m-2 d-1 (mean 2003 to 2006) as reported in Bäckstrand et al. (2008).
The high water tables in the sedge and Sphagnum sites throughout the summer promote anoxic conditions and high concentrations of CH4 and potential rates of CH4 production (Figs. 3 and 5). The slightly higher concentrations of CH4 in the sedge mire relative to the Sphagnum-dominated mire during August and September are supported by the CH4 production experiments (discussed below), which show higher potential rates of CH4 production in the sedge soil compared to the Sphagnum peat (Fig. 5). Total hydrocarbon emission data are consistent with this observation and show higher average rates of CH4 flux from the sedge site (120 ± 1.4 mg C m-2 d-1) compared to 28 ± 0.3 mg C m-2 d-1 for the Sphagnum site during 2003–2006 (Bäckstrand et al., 2008).
These data can be explained by the different hydrological conditions and associated contrasts in plant species composition between the two sites. The sedge site is dominated by Eriophorum angustifolium and the other minerotrophic mire by Sphagnum spp. Plant species composition determines the quality of peat that develops at the respective sites and several studies have recognized the importance of vegetation as a predicator of CH4 production and emission because it integrates several ecological variables (Bubier et al., 1995). In the Sphagnum-dominated mire, the lack of a well-developed rhizoid system results in little labile organic carbon being released to anaerobic peat layers (Galand et al., 2005). The presence of recalcitrant carbon compounds leads to slow bacterial decomposition rates beneath the Sphagnum spp. groundcover (Karunen and Ekman, 1982; Chapin et al., 1986; Johnson and Damman, 1991).
Pore water CH4 concentrations are similar in the sedge and Sphagnum mires, but CH4 production rates are as much as 40-fold greater in the former site. This difference likely reflects the greater potential for methanogenesis in the sedge peat resulting from the release of root exudates but also the higher capacity for plantmediated export of CH4 through Eriophorum angustifolium. Moreover, the high concentrations of CH4 in soil at the sedge site in June may also reflect lower rates of loss via plant-mediated transport early in the thaw season. This observation is consistent with the low CH4 fluxes measured from the sedge site at Stordalen in early summer by Bäckstrand et al. (2010) and Jackowicz-Korczynski et al. (2010). It is also supported by the findings of Heyer et al. (2002) who reported low early summer CH4 emissions from peatlands in Siberia.
By August at Stordalen, the soil had been thawed for ∼2 months, soil temperatures were higher (9 to 17 °C), and vegetation growth was well established. Lower pore water concentrations of CH4 in August and September in the sedge-dominated mire compared with June likely reflect a more highly developed plant root system in the later summer months (Shaver and Billings, 1975), resulting in higher rates of plant-mediated gas transport to the atmosphere (Fig. 5) (Joabsson and Christensen, 2001; King et al., 1998; Frenzel and Karofeld, 2000) and less CH4 in soil pore water.
SENSITIVITY OF CH4 PRODUCTION TO TEMPERATURE
Our results suggest that temperature has a variable influence on CH4 production rates in sedge and Sphagnum mires as indicated by Q10 values, ranging from 1.9 to 5.8 (overall mean = 3.2). The reported values compare well with published Q10 values for temperate peatlands (Bridgham and Richardson, 1992; Frenzel and Karofeld, 2000; Priemé, 1994; Updegraff et al., 1995) and other anoxic habitats (e.g. paddy soils, lake sediment, or swamp) reported in Segers et al. (1998) and Dunfield et al. (1993). The apparent activation energies determined in this study (50–140 kJ mol-1, mean 90 kJ mol-1) are slightly lower than those for northern peatlands (123–271 kJ mol-1, Dunfield et al., 1993) but within the range reported for other anoxic environments such as paddy soils (53–132 kJ mol-1, Shültz et al., 1990; 68–91 kJ mol-1, Conrad et al., 1987) and alder swamp (92–117 kJ mol-1, Westermann and Ahring, 1987), suggesting that the energy necessary for methanogenesis in permafrost areas is broadly similar to that in other anoxic freshwater wetlands.
Figure 7 compares Q10 values measured in this study with published values for northern (non-permafrost sites) (Fig. 7, parts a and c) and permafrost wetlands (Fig. 7, parts b and c) that have been determined using laboratory-based incubations and field-based relationships between soil or air temperatures and CH4 fluxes. Our results (1.9–5.8) are similar to those of Heyer et al. (2002) who reported Q10 values ranging from 1.3 to 5.6 for a permafrost site in northern Siberia. In general, the Q10 values determined for peatlands at Stordalen lie at the low end of the range of published values for northern wetlands and do not display any unusually high values, which have been reported in other studies. Those high values typically are derived from Sphagnum-dominated peatlands, for example the values reported by Bergman et al. (1998) (Q10 = 2.5 to 35), Bergman et al. (2000) (Q10 = 4.4 to 13), and Dunfield et al. (1993) (Q10 = 6 to 16). Field-based determinations of Q10 for northern wetlands (including permafrost peatlands) as a whole do not yield dramatically different average Q10 values compared to laboratory studies (Fig. 7, parts a–c).
Differences in Q10 values reported in Table 2 and CH4 production rates at different temperatures (Fig. 5; 4–14 °C and 14–24 °C; 95% confidence interval, p < 0.001, for the sedge site and 95% confidence interval, p < 0.0012 for the Sphagnum site using a t-test) between the two minerotrophic sites likely also reflect differences in temperature sensitivity of microbial processes that generate CH4-precursors in the anaerobic chain of decay.
The higher mean Q10 values and apparent activation energy (Ea) in the Sphagnum mire (Q10 = 4.5; Ea = 110 kJ mol-1) versus the sedge site (Q10 = 2.7; Ea = 78 kJ mol-1) at Stordalen are consistent with the presence of more recalcitrant organic matter, possibly due to a greater predominance of Sphagnum spp. in the former mire (Verhoeven and Toth, 1995). Such a difference is consistent with fundamental principles of enzyme kinetics associated with the Arrehenius equation, and the carbon quality temperature (CQT) hypothesis (Davidson and Janssens, 2006; Bosatta and Ågren, 1999) predicts that the temperature sensitivity of microbial decomposition should increase with increasing Ea of a reaction. A similar pattern is evident in Figure 7 based upon published data in which the highest Q10 values (>8) derive primarily from Sphagnum-dominated mires and the lower values from sedge-rich mires. Notably the mean Q10 values for these two peatland types differ significantly (Q10 = 7 for Sphagnum mires and 4.2 for sedge mire; 99% confidence interval using a 2-tailed Student's t-test, p = 0.002).
The intra-site differences in Q10 values suggest subtle contrasts in the temperature response of methanogenesis between peatland types. In general, areas containing more recalcitrant organic matter typically are characterized by lower rates of organic carbon decomposition (Craine et al., 2010; Davidson and Janssens, 2006) and hence, contribute less to total CH4 emissions than sites where vascular plants are present. However, in most northern peatlands recalcitrant compounds are more abundant than labile compounds, with Sphagnum-dominated mires globally covering a greater area than sedge-dominated peatlands (Charman, 2002), in particular in the Arctic where mesic (with a moderate supply of moisture) and drier ecosystems cover 44 to 58% of ice-free areas (Bliss and Matveyeva, 1992). At Stordalen, Sphagnum mires account for 36% of the total area of the 16.5 ha mire complex (versus 49% ombrotrophic bog and 12% sedge mire) (Johansson et al., 2006). Hence, differences in temperature sensitivity between these two peatland types may be significant for the future response of northern wetlands to climate change. While CH4 emissions are significantly less from the Sphagnum mire than the wetter sedge-dominated areas at Stordalen (Bäckstrand et al., 2008) and other Arctic sites, the significantly higher Q10 values for methanogenesis in the Sphagnum-rich areas could yield proportionally larger changes in CH4 flux for changes in temperature. Whether such an effect would be sustained will depend upon the longer term ecosystem response to climate forcing, and how other factors that impact methanogenesis (e.g., changes in hydrology) are altered (e.g., Oechel et al., 2000; Christensen et al., 2004). At Stordalen, the ombrotrophic palsa area has already decreased in size yielding larger areas of wetter minerotrophic peatland during the period 1970 to 2000 and an associated increase in CH4 emissions from the new sedge-dominated mires (Christensen et al., 2004, Johansson et al., 2006). However, a future shift towards drier conditions would deepen the oxic zone and most likely lower CH4 production potentials and enhance methanotrophy, limiting the flux of CH4 from these areas of former Sphagnum mire.
Our findings have implications for the parameterization of methanogenesis in numerical models of the global and regional carbon cycles as discussed recently by Craine et al. (2010). Some models rely on a single Q10 function to determine the potential impact of climate warming on CH4 fluxes from wetlands (e.g., Frolking et al., 2001; Gedney et al., 2004). The assumed Q10 values typically are similar to the median of published values summarized in Figure 7, indicating a generally good parameterization given the uncertainty and potential range of Q10 values. There is considerable variability in the temperature sensitivity of methanogenesis in northern and Arctic wetlands (Fig. 7, parts a–c), in particular, within mesic bogs versus minerotrophic mires. Hence, employing a single parameterization of Q10 may lead to inaccurate prediction of future CH4 flux from these environments, especially in models that are able to incorporate changes in ecosystem type and organic matter decomposition as a function of climate (e.g., where surface hydrology, and hence the spatial extent of mire type changes with climate). Recent soil carbon models that employ spatially variable values for Q10 to predict response to climate change support this viewpoint (e.g., Zhuang et al., 2003). In this context, Craine et al. (2010) suggested that in order to predict how the present-day soil organic carbon pool will respond to climate change we need to determine the generality of the carbon quality—temperature correlation and hence, the use of a single value of Q10 to describe decomposition response to temperature is likely to be inadequate. Craine et al. (2010) implied that the kinetic theory underlying temperature sensitivity of decomposition at a molecular level could also be employed at the soil scale, suggesting that large-scale models using temperature sensitivity of organic matter decomposition within their parameters might be based accurately on soil incubations or possibly through the creation of a global system of soil-incubation experiments (Janssens and Vicca, 2010).
Investigation of the temperature sensitivity of methanogenesis in peatland soil from Stordalen, northern Sweden, indicates that CH4 production is controlled by a complex suite of interrelated factors, including water table level, plant composition, and temperature. Temperature has a clear and direct effect on CH4 production rates, although its influence is moderated by the site-specific factors of vegetation composition and hence, organic matter quality. The Q10 values determined for sedge and Sphagnum mires are similar to published values for northern peatlands. Permafrost wetlands, including Stordalen, do not display a significantly different response of CH4 production to temperature forcing in comparison to northern, non-permafrost wetlands. However, our results from Stordalen exhibit intra-sites differences that demonstrate stronger temperature sensitivity of methanogenesis based upon presumably more recalcitrant soil organic matter in the Sphagnum mire versus the sedge-dominated site. This contrasting response in CH4 production has been reported in other studies of northern wetlands and in general, methanogenesis in Sphagnum-dominated wetlands responds more strongly to temperature forcing than within wetter, sedge-rich peatlands. This finding is significant given that Sphagnum sites constitute a significant proportion of the northern peatland area. Our results provide potentially useful data to inform parameterization of Q10 values in models of carbon cycling in northern wetlands, in particular, for anaerobic decomposition in the active layer of permafrost peatlands. The data indicate the importance of using spatially variable Q10 values in such models to reflect differences in temperature response of CH4 production in key biotypes in high-resolution, coupled climate-ecosystem models.
This work was supported by a Marie Curie PhD Fellowship to M. Lupascu via the EU Early Stage Training Programme “Biotransformations of trace elements in aquatic systems.” We thank Professor Torben Christensen for his input in relation to sampling at Abisko and for providing access to the field site. We thank the staff at the Abisko Research Station and at the University of Bristol for assistance during fieldwork and laboratory analysis. The UK Joint Higher Education Funding Council for England and Office of Science and Technology Science Research Investment Fund (SRIF) are thanked for infrastructure funding. Work was conducted in the Low Temperature Experimental and BIOGAS Facilities in Bristol.