Methane Production and Bubble Emissions from Arctic Lakes: Isotopic Implications for Source Pathways and Ages

JOURNAL OF GEOPHYSICAL RESEARCH, VOL 113, G00A08, doi: 10.1029/2007JG000569, 2008

Methane production and bubble emissions from arctic lakes: Isotopic implications for source pathways and ages

K. M. Walter,1 J. P.Chanton,2 F. S. Chapin III,3 E. A.G. Schuur,4 and S. A.Zimov5 Received 9 August 2007: revised 19 March 2008: accepted 11 April 2008; published 2 August 2008.

[1] This study reports an atmospheric methane (CH4) source term previously uncharacterized regarding strength and isotopic composition. Methane emissions from 14 Siberian lakes and 9 Alaskan lakes were characterized using stable isotopes (13C and D) and radiocarbon ( 4C) analyses. We classified ebullition (bubbling) into three categories (background, point sources, and hot spots) on the basis of fluxes, major gas concentrations, and isotopic composition. Point sources and hot spots had a strong association with thermokarst (thaw) erosion because permafrost degradation along lake margins releases ancient organic matter into anaerobic lake bottoms, fueling methanogenesis. With increasing ebullition rate, we observed increasing CH4 13 concentration of greater radiocarbon age, depletion of CCH4, and decreasing bubble N2 content. Microbial oxidation of methane was observed in bubbles that became trapped below and later within winter lake ice; however, oxidation appeared insignificant in bubbles sampled immediately after release from sediments. Methanogenic pathways differed among the bubble sources: CO2 reduction supported point source and hot spot ebullition to a large degree, while acetate fermentation appeared to contribute to background bubbling. To provide annual whole-lake and regional CH4 isofluxes for the Siberian lakes, we combined maps of bubble source distributions with long-term, continuous flux measurements and isotopic composition. In contrast to ty~ical values used 1 in inverse models of atmospheric CH4 for northern wetland sources ? CCH4 = -58%o, 14C age modern), which have not included northern lake ebullition as a source, we show that this large, new source of high-latitude CH4 from lakes is isotopically distinct 13 14 (? CCH4 = -70%o C age 16,500 years, for North Siberian lakes).

Citation: Walter, K. M., 1. P. Chanton, F. S. Chapin III, E. A. G. Schuur, and S. A. Zimov (2008), Methane production and bubble emissions from arctic lakes: Isotopic implications for source pathways and ages, J Geophys. Res., 113, G00A08, doi: 1 0.1029/2007JG000569.

1. Introduction et al., 2004a]. Wetlands playa major role in global atmospheric CH4 dynamics, representing ~ 10-30% (50-150 Tg -l [2] Atmospheric methane (CH4) is a potent greenhouse CH4 a ) of known sources [Matthews and Fung, 1987; gas responsible for ~20% of the direct radiative forcing from Fung et al., 1991], with northern wetlands contributing a-1 all long-lived greenhouse gases [intergovernmental Panel on substantially to the total (<6 to 40 Tg CH4 ) [Roulet et Climate Change (IPCC), 2007). Its concentration in the al., 1994; Reeburgh et al., 1998; Worthy et al., 2000; IPCC, atmosphere results from a balance between sources and sinks. 2001; Zhuang et al., 2006]. This wide range in wetland While potential new, large sources are still being identified emission estimates results primarily from uncertainties in [Keppler et al., 2006], some known sources are poorly the areal extent of wetlands and from the large spatial and quantitied because of difficulties in assessing high variability temporal variability of short-term local CH4 emission meas- in emission rates [Fung et al., 1991; Intergovernmental urements [Reeburgh et al., 1998; Mikaloff Fletcher et al., Panel on Climate Change (lPCC), 2001, Mikaloff Fletcher 2004a, 2004b]. [3] Local CH4 emissions from most lakes and wetlands 1 Institute of Northern Engineering and International Arctic Research can vary by several orders of magnitude on the scale of a Center, University of Alaska Fairbanks. Fairbanks, Alaska, USA. 2 few meters or over several hours. Heterogeneity in ebulli- Department of Oceanography, Florida State University, Tallahassee, Florida. USA. tion (bubbling) is a major contributor to this variability, and 3Institute of Arctic Biology, University of Alaska Fairbanks, Fairbanks. the spatial and temporal patchiness of ebullition challenges Alaska. USA. efforts to quantity this mode of emission.As a result, many 4Department of Botany, University of Florida, Gainesville, Florida, studies of CH4 emissions from lakes and wetlands report USA 5Northeast Science Station, Cherskii, Republic of Sakha, Russia. only emissions via molecular diffusion and aquatic plant transport [Kling et al., 1992; K. M. Walter et al., A new Copyright 2008 by the American Geophysical Union. method to evaluate methane emissions from northern lakes: 014H-0227JG000569$09.00

G00A08 1 of 16 G00A08 WALTER ET AL.: ISOTOPES OF ARCTIC LAKE BUBBLING C00A08

[6] The purpose of this study is to characterize CH4 Surveying bubbles in lake ice, submitted to Bio Science, production and emission from a variety of arctic and boreal 2008, hereinafter referred to as K. M. Walter et a\., submit- 14 lakes in Siberia and Alaska using 13C, D and C isotopic ted manuscript, 2008]. Studies that aimed to assess ebulli- ratios to help elucidate the role of lake ebullition, particu- tion with greater accuracy showed that ebullition .in lakes is larly that associated with thermokarst erosion (ground a dominant, yet inadequately quantified mode of CH 4 subsidence resulting from the thawing of ground ice), in emission leading to a systematic underestimation from lakes global atmospheric CH dynamics. Specific objectives globally [Casper et al., 2000; Bastviken et al., 2004; Walter 4 include (1) characterizing the isotopic composition of dif- et a ., 2006; K. M. Walter et al., submitted manuscript, l ferent types of CH bubble sources including background 2008]. 4 bubbling, point sources and hot spots; (2) identifying factors [4] Model estimates of northern wetland emissions have that influence these signatures such as CH production yet to include ebullition from lakes [Zhaung et a ., 2004; 4 l pathways and environmental water- sources, (3) exploring Mikaloff Fletcher et al., 2004a, 2004b; Bousquet et al., the potential for CH oxidation in lake bubbles; and 2006; Chen and Prinn, 2006]. Recent studies that quantified 4 (4) combining careful measurements of ebullition patchi- the patchiness of ebullition showed that adding emission ness with isotopic signatures of bubbles and measured estimates of CH from N Siberian the okarst lakes 4 orth rm fluxes to determine whether whole-lake and regional CH increased current estimates of total northern wetland emis- 4 isofluxes (flux-weighted average isotopic signatures) differ sion by 10-63% [Walter et al., 2006]. Thermokarst (thaw) from previous estimates based on methods that ignored erosion resulting from permafrost degradation along lake point source and hot spot ebullition. margins drives CH4 emissions from North Siberian lakes by depositing thawed Pleistocene-aged organic matter into anaerobic lake bottoms, fueling methanogenesis. Expansion 2. Methods of thermokarst lakes in continuous permafrost regions of 2.1. Location of Study Lakes Siberia during recent decades constitutes a positive feed- [7] Most isotopic studies in northern lakes have been back to climate warming [Smith et al., 2005; Walter et al., conducted in North America and Europe [Wahlen et al., 2006]. Global circulation models predict that greatest warm- 1989, Quay et al., 1988, Martens et al., 1986], with little ing will occur at high latitudes [IPCC, 2001, 2007] with attention to Russian lakes [Nakagawa et al., 2002], which significant permafrost degradation during the 21st century comprise ~ 70% of arctic lakes [Holmes and Lammers, [Sazonova et al., 2004; Lawrence and Slater, 2005], raising 2006]. We studied a variety of lakes in the boreal forest concerns about the increase of CH4 emissions from northern and tundra of the Kolyma River Basin in Siberia and in lakes and wetlands to future climate change. Alaska situated on permafrost substrates of various types [5] Isotopic signatures of atmospheric CH4 and its sources can be used in isotope mass balance models to define including: (l) Pleistocene-aged, organic-rich, silty ice-com- the magnitudes of different sources and sinks [Hein et al., plex "yedoma" near Cherskii in northeast Siberia (68°45'N, 1997; Houweling et al., 1999; Mikaloff Fletcher et al., 161°20'E) [Zimov et al., 1997, 2006]; (2) Holocene organic 2004a, 2004b; Bousquet et al., 2006]. For instance, inverse soil on top of organic-rich, Pleistocene-aged retransported modeling of high-resolution spatiotemporal atmospheric silt near Fairbanks in Interior Alaska (64°49'N, 147°52'W), l3 and (3) organic-poor glacial deposits near Toolik Lake in CH4 concentrations and its C isotope ratio was used to determine the relative contributions of northern wetland northern Alaska (68°28'N, 149°34'W) (Table 1 and emissions and biomass burning in the tropics [Lowe et al., Figure 1). Siberian and Interior Alaskan lakes that we 1994; Mikaloff Fletcher et al., 2004a, 2004b; Bousquet et studied were formed by thermokarst activity. Study lakes 14 in northern Alaska arc kettle lakes that formed upon thaw of al., 2006]. Similarly, the C isotope ratio of CH4 has been used to estimate the contribution of fossil carbon (14 Cfree) ice blocks deposited in glacial drift and outwash plains of attributed to natural gas seepage and coal mining [Lowe et late Pleistocene glaciation [Hamilton, 2003]. These types of al., 1994; Wahlen et al., 1989]. Stable hydrogen isotopes lakes are occasionally influenced by thermokarst along can be combined with stable carbon isotopes and used to margins today. distinguish sources of CH4 including bacterial formation, 2.2. Sample Collection and CH4 Flux Measurements thermogenic formation and biomass burning [Whiticar et al., 1986], as well as to detennine the effect of microbial [8] We collected gas from several different types of lake oxidation in lake and wetland environments [Coleman et bubbling events in Siberia and Alaska from 2001 to 2004. In 200 we stirred surface sediments in a variety of tundra al., 1981; Happell et al., 1994]. In aquatic environments, 1 13 and boreal thermokarst lakes in Siberia and collected variations in the ? C of CH4 and carbon dioxide (CO2) can reveal the importance of different biochemical pathways of bubbles through a handheld funnel into glass serum vials methanogenesis including CO reduction and acetate fer- that we sealed with butyl rubber stoppers. Samples were 2 stored in a refrigerator at 4°C in the dark. We did not mentation [Whiticar et al., 1986; Chasar et al., 2000a, measure flux in conjunction with bubble samples collected 2000b; Chanton et al., 2005], particularly as these pathways by stirring lake sediments. In 2003-2004 in Siberia all vary spatially in thennokarst-influenced ecosystems [Prater bubble samples werc collected from natural ebullition et al., 2007]. Differences in ?DcH4 are also useful for events into floating traps without disturbing sediments. determining CH4 sources, but are primarily linked to ?D Bubble traps (~ -m diameter), placed permanently under of the source water [Sugimoto and Wada, 1995; Waldron et 1 the surface of lakes and beneath winter ice, were either al., 1999a; Chanton et al., 2006]. Careful bottom-up studies freely floating to capture the average "background" ebul- of processes driving CH emissions and isotope signatures 4 lition, or they were fixed in place over discrete points of are necessary to help define source estimates in models.

2 of 16 ~;;;. o ee

~ ~ rn ;:<:l r.l -l » r en o d-0 rn

C1 o »o ee<= G00A08 . WALTER ET AL.: ISOTOPES OFARCTIC LAKE BUBBLING G00A08

avoiding air bubbles. Vials were capped and stored at 4°C in the dark until analysis in August 2005. 2.3. Gas Concentration and Isotope Procedures

[12] Concentrations of CO2, O2, N2 and CH4 in lake bubble samples were measured by gas chromatography using a thermal conductivity detector (TCD Shimadzu 8A).O2 values presented in this paper were corrected for argon (Ar) on the basis of atmospheric molar ratios of N2/ Ar. Argon coeluted with O2 and comprised 0.01 to 1% of 13 I2 peak area. We measured C/ Cof CH4 by direct syringe injection using gas chromatography/mass spectrometry (Hewlett-Packard 5890 Series II GC coupled to a Finnigan MAT Delta S). Subsamples of gas were combusted to CO2, purified, and catalytically reduced to graphite [Stuhler and Polach, 1977], and the 14C/12C isotopic ratios were measured by accelerator mass spectrometry at the Keck Carbon bubbling, called "point sources" and "hot spots." Units of Cycle AMS Facility at the University of California, Irvine. flux differ for the discrete types of bubbling. Background We determined D/H of CH4 on a Finnigan MAT delta +XP ebullition, captured by randomly placed traps, is a function using a Trace GC with a poroplot column and the reduction -2 -1 of trap area and expressed as mg CH4 m d , whereas column set at 1450°C. Lake water samples were analyzed units for point source and hot spot bubbling are mg CH4 for ?DH2O by the zinc reduction method [Coleman et al., spot -1 d-1 because emissions from discrete, small holes in 1982]. lake sediments (<2 cm diameter) were independent of [13] Stable isotope compositions are expressed in ? (%o)= bubble trap area. Walter et al. [2006] showed that point 103 ((Rsample/Rstnndard)-I)w, here R is 13C/12C or D/H and source and hot spot bubbling, which had a probability of standards refer to the Vienna Pee Dee Belemnite (VPDB) ~,0.001% of being captured by randomly placed bubble and Vienna Standard Mean Ocean Water (VSMOW), traps and which accounted for ~70% of emissions from respectively. The analytical errors of the stable isotopic 13 lakes, were distinctly different from background ebullition analyses are ±0.l%o ? C and ±l.0%o ?D. We express with regards to ebullition rates. Bubble samples collected radiocarbon data as percent modem carbon, pmC (%) = 14 12 14 12 into serum vials within ~2 h of release from the lake bottom (C C/ C)sample/( C/ C)stand a rd ) x 100, which is the per- 14 12 13 are labeled as "fresh" hereafter. Samples collected from centage of C/ C ratio normalized to ? C = -25%o and background traps accumulated slowly and therefore sat up decay corrected relative to that of an oxalic standard in 1950 to a few days in the traps before collection; these are labeled [Stuiver and Polach, 1977]. "not fresh." [9] In the spring of 2003, we collected bubbles trapped 2.4. Methane Production Pathway in lake ice by carefully tapping into frozen gas pockets [14] Methanogenesis is an ancient process that relies on from the ice surface and capturing trapped gases into relatively simple substrates, for example carbon monoxide, serum vials as the bubbles streamed up from inside the carbon dioxide, acetate, formate, methy lamine, methanol, ice. These samples, which represented wintertime point and dimethylsufide, that are produced by other metabolic source bubbling (described by Walter et al. [2006]), are processes [Conrad, 1989]. The two main pathways of here referred to as "ice koshkas" (i.e., the Russian term bacterial methane production in anaerobic sediments arc for pockets of CH4-rich gas bubbles trapped in lake ice). CO2 reduction and acetate fermentation: In autumn 2005, ice-koshka samples were collected from tundra lakes in northern Alaska, and fresh bubbling from hot spots was captured from two boreal thermokarst lakes near Fairbanks. [10] Year-round flux dynamics for background, point source, and hot spot bubbling from Siberian lakes were presented in detail by Walter et al. [2006; K. M. Walter et al., submitted manuscript, 2008]. To show the relationship between CH4 isotope values and bubbling rates in this study, we used the 10-day average ebullition flux surround- ing each sample date for the bubbles collected for isotopic analyses in our regressions. To calculate the whole-lake and regional isofluxes, we applied seasonal rates of ebullition to the range of isotope values determined for CH4 bubbling from these arctic lakes. [11] Lake water samples in Siberian lakes were collected with a Van Dorn bottle from 14 June 2003 through 11 August 2003 just above the sediment surface for deter- mination of D Water was poured into glass vials ? H2O.

4 of 16

G00A08 WALTER ET AL.: ISOTOPES OF ARCTIC LAKE BUBBLING G00A08

13 ? CH4(ace) is the isotope ratio of CH4 produced by the acetate fermentation pathway, and assumed to be -43%o when acetate fermentation occurs in sediments with a sufficient supply of fresh organic material (Case 1), and -27%o when sediments are extremely depleted in fresh organic material (Case 2) [Nakagawa et al., 2002].

3. Results 3.1. Concentrations of Gases in Bubbles [17] Concentrations of the major gas constituents of bubbles varied by lake and bubble sourec (Table 2). Methane was the predominant constituent of point source and hot spot bubbling (range 67-94%; mean ± std. dev. 82 ± 7%, n = 55). Methane was less concentrated and more variable in bubbles collected by stirring surface sediments and in background bubble traps (range 0-77%, mean ± std. dev. 39 ± 25%, n = 39). We found a negative linear relationship between the concentration of CH4 and N2 in bubbles and a negative curvilinear relationship between ebullition rate and %N (Figure 2). Oxygcn (02) concentration in gas bubbles ranged from 0.4% to 29%, depended on the source of bubbling (Table 2), and was negatively related to CH4 concentration ([02] = -0.08[CH4] + 10.0, F = 29.05(1146) P < 0.0001). The concentration of CO2 was low (0-2%) in samples collected from fresh bubbling in Siberia and Alaska in 2003-2004 (Table 2). 3.2. Stable Isotopes in Bubbles and Lake Water 13 13 [18] The stable isotope signatures ? CC02, h CCH4, ?DcH4) of bubbles and ?D of Siberian and Alaskan lake CH4 in bubbles respectively. This estimation of ac is water varied by lake and bubble source (Table 2). Siberian approximate because CH4 and CO2 are not related in the point sources and hot spot bubbles had less enriched 13 = same way for the CO2 reduction and acetate fermentation ? CCH4 values (-79.5 ± 2.3%o, n 34) than bubbles collected from background traps or by stirring surface pathways (equations (2) and (3)); however, ac values have been utilized to differentiate between dominant pathways of sediments (-61.6 ± 5.7%o, n = 60) (t-value = 21.485 P < methanogenesis in natural and artificial systems [Sugimoto 0.0001) (Figure 3), the latter being similar to typical values and Walda, 1995 Waldron et al., 1999b; Chasar et al., reported in the literature for northern lakes and wetlands 2000a; Chanton et al., 2006; Prater et al., 2007]. (-64%o [Quay et al., 1988]; -61%o [Martens et al., 1986]; [16] Second, we also used a simple mixing model to -58%o [Lansdown et al., 1992]), including Siberian alasses estimate the relative proportion of the acetate fermentation (typical round landforms in permafrost terrain, consisting of and CO2 reduction pathways: a shallow lakes surrounded by wetlands; -61.1 ± 4.4%o, [Nakagawa et al., 2002]). Point source CH4 trapped in lake ice as ice koshkas (-69.3 ± 4.3%o, 11 = 4) during the entire 13 winter was more enriched in ? CH4 than fresh point source bubbles (-79.7 ± 3.0%o, n = 13) (t-value = 5.4315, where f is the proportion of CH4 produced by CO2 CO2 P < 0.0001). reduction; face is the proportion of CH4 produced by acetate 13 [19] The ?D of lake water was -154 ± 2.6 at 1-m depth in fermentation;?C CH4 is the isotope ratio of measured CH4, 13 the mixture of both pathways; and b CH4(C02) is the Shuchi Lake, and was more depleted at depth in three lakes isotope ratio of CH4 produced by the CO2 reduction (-158.7±2.1%0 at 10-m Shuchi Lake; -161 ±8.1 at 15-m, Tube Dispenser Lake; and -172 ± 2.9 at 10-m Grass Lake)

6 of 16 G00A08 WALTER ET AL.: ISOTOPES OF ARCTIC LAKE BUBBLING G00A08

sediments (>modern to 3695 years) contained CH4 of younger ages (Figure 4).

3.4. Methane Production Pathways [22] The apparent C fractionation factor (eve) between = CH4 and CO2 was higher in hot spot (ac 1.071 ± 0.006, n = 21) and point source bubbling (ac = 1.073 ± 0.0 11, n = 12) in Siberian lakes and ponds compared to the (aC of background bubbling (ac = 1.048 ± 0.005, n = 20) (Figure 5). Ebullition rate was positively related to the fraction of CH4 produced

via the CO2 reduction pathway as determined through the mixing model (equations (4) and (5) and Table 4) based on 13 , indicating that the CO reduction pathway dom- ? CCH4 2 inated CH4 emitted from high-emission point sources and hot spots, while acetate fermentation appeared to play a more important role in lower-emission background bubbling (Figure 6).

4. Discussion 4.1. Major Gas Constituents in Bubbles [23] A negative linear relationship between the concen-

tration of CH4 and N2 in bubbles (Figure 2a) indicates that CH4 is the gas predominately produced in sediments [Nakagawa et al., 2002]. Bubble N2 content may also be a sensitive indicator of ebullition rates because there is a

strong inverse relationship between the N2 concentrations in bubbles and the rate of ebullition [Chanton et al., 1989) (Figure 2b). Nitrogen is present in pore waters when sediments are deposited and, when depleted, it is resupplied by diffusion from overlying waters. High rates of bubbling

strip N2 from the pore waters, depleting the dissolved N2 pool in pore waters [Kipphut and Martens, 1982; Chanton et al., 1989]. Bubbles collected from hot spots and point 4 sources had the highest CH /N2 ratios, while bubbles released from shallow surface sediments (background, (Table 2). The D of CH which ranged widely in this study ? 4, stirred), where lower ebullition rates were observed, had (- 315%o to -420%o), differed by study region and bubble lower CH /N ratios. Lower CH /N ratio in gas collected type (Figure 3). The of Siberian CH of point sources 4 2 4 2 ?D 4 from ice koshkas compared to gas collected from fresh point and hot spots (-392 ± 8%o, n = 40) was D depleted ? source and hot spot bubbling streams is likely the result of compared to Alaskan hot spots (- 351 ± 5%o, n = 7) (t-value = N2 diffusion from lake water into bubbles that sit under the 12.745, P < 0.000 ). D was more depleted in thermokarst 1 ? CH4 ice at the top of the water column prior to entrapment in ice ponds situated on yedoma (-388% to -402% ) compared o o that grows slowly around the bubbles. to manmade sandy ponds sitting on bedrock (-360%o to [24] Bubbles produced in the anaerobic lake sediments - 381 % ). D of interior laska thermo arst akes o ? CH4 A k l should be free of O ; however, bubbles rise through the (-340% to -355% ) as more depleted than that of the 2 o o w water column absorbing O , and sit in bubble traps at the more northern tundra lakes that lacked intensive thermo- 2 surface for several hours to days prior to collection. Holding karst (-321% to -339% ) (Table 2). Ic koshkas ere o o e w time in the trap likely accounts for the variability observed enriched by 46 ) in Siberia and 24% in Alaska relative o %o o t in O content, particularly between winter and summer the fresh point source counterparts in both regions (Siberia 2 samples (Figure 7). In summer, photosynthesizing periphy- -346 ± 13% , = 4; Alaska -328 ± 5% , n = 22). o n o ton was observed growing in bubble traps, producing O 13 + 2 [20] The ? CC02 of point sources (-12.2 - 7.5%o, n = 12) that could diffuse into trapped CH4-rich bubbles. We and hot spots (- 14.2 ± 4.1 % , = 27) was enriched relative o n suspect that trace amounts of O present in stirred surface to background bubbles (-18.7 ± 4.1 % , n = 27). 2 o sediments are from benthic photosynthesis on the surface of

3.3. Radiocarbon of Bubble CH4 lake sediments. Bubbles from small, stagnant Siberian ponds had the lowest O concentrations, possibly because [21] Lake bubble samples exhibited a wide range of 14C 2 ages, with a substantial number of samples containing 14C_ these ponds lack the wind-driven currents that supply O2 to lake bottoms in larger lakes. Higher O (8.5% and 29%) depleted CH (Table 3). CH from high-emission point 2 4 4 corresponding to very low CH (5.2% and 2.7%) in two sources and hot spots of CH bubbling were older (11,355 4 4 individual outlier bubble samples (individual data points not to 42,900 years), while the low-emission background bub- shown) collected from the nonthermokarst margin of Shu chi bling (1345 to 8845 years) and stirred bubbles from surface

7 of 16 o o Q~ Q ee

~ ~ ;>:l :::j ~ r Vi ~ o-e tTl (/)

o"T'j ~ ;>;1 (J -l n »r ~ ITl 1:0 ~ 0:1 ~ o

oe e ~ Q ee G00A08 WALTER ET AL.: ISOTOPES OFARCTIC LAKE BUBBLING G00A08

freshly from lake sediments (Figure 3 point sources, hot spots and background). Considering a high number of individual samples within a single thermokarst lake, Shuchi Lake, the lack of relationship between O2 concentration and 13 ? CCH4 within the three ebullition types validates the conclusion that CH4 oxidation is not a primary factor influencing the isotope signature in these samples (Figure 13 7), However, when comparing the ?DCH4 and ? CCH4 of fresh Siberian point sources with that of ice koshkas, a slope 2 of 2.5 (R = 0.6) (Figure 3b) suggests that some isotopic enrichment due to CH4 oxidation occurred in CH4, likely

when the point source bubbles sit in the O2-rich lake water under the ice prior to entrapment in the thickening ice. 4.4. Methane Production Pathways

[27] The CO2 reduction pathway has a larger apparent C fractionation factor (equation (3), ac = 1.055-1.090) than acetate fermentation ac = 1.040-1.055) [Whiticar et al., 1986]. However, without further information, the ac has limited diagnostic power given that a host of factors such as environmental variability, temperature, substrate concentrations, and available Gibbs free energies lead to variability in Lake and from Grass Lake are explained by the presence of ac for each pathway [Valentine et al., 2004, Conrad, 2005; photosynthetic benthic algae and moss which produce Penning et al., 2005]. Using the ac as a general guide in Siberian lakes and ponds, the CO2 reduction pathway O2 rich bubblles that mix with tbe CH4-rich bubbles upon their ascent and during entrapment in submerged bubble appeared to be more prevalent in hot spot (ac = 1.071 ± 0,006, n = 21) and point source bubbling ( c = 1.073 ± traps, Like N2, higher O2 concentrations in ice koshkas a (4.4-12.8%,) relative to fresh point source bubbling (3.9± 0.0 11, n = 12), whereas the lower ac of background bubbling 1.048 ± 0.005, n 20) suggests the 1.4%) suggests O2 diffusion into bubbles that sit under ice ac = = exposed to the O2-rich lake water prior to entrapment in influence of acetate fermentation in the sediments where winter lake ice. Given that N2 concentrations increased by these bubbles were produced (Figure 5). This conjecture is 160%, in ice koshkas relative to fresh point sources, while supported by the results of the mixing model (equations (4) O2 concentrations increased by only 13%, suggests that an and (5)), which yielded a range oflikely proportions of CO2

O2- consuming process, such as methane oxidation, also occurs prior to ice entrapment or within the ice. 4.2.Stable Isotopes in Bubbles o ------.--- .....---.--- ..-,...._. ~ __,, "!f...= 1:.':16 , • f [25] The stable isotope signature of CH4 bubbles can be ~'lf- , influenced by multiple factors, including CH4 oxidation, the -10 + o iCc = 1.04 'h isotopic composition of CH precursors, degree of substrate 13 0 4 !ieeo, -20 utilization, temperature, and biochemical pathways of meth- (%~ • anogcncsis [Whiticar et al., 1986; Alperin et al., 1992; -30 Sugimoto and Wada, 1995; Valentine et al., 2004; Templeton et al., 2006; Kinnaman et al., 2007]. -40 '-----~--""'--~---~------' -90 -80 -70 -60 -50 4.3. Methane Oxidation 13!iCe".(%~

rr background [26] Biological CH4 oxidation results in the enrichment of 13 the remaining ?DCH4 and ? CCH4 with no additional + point sOJurce 14 • hotspot fractionation to the reported CCH4 values because they are corrected by any potential fractionation with the 13C values. ~ekoshka

In the literature, a positive correlation between ?DcH4 and 13 13 Figure 5. The (? C and ? CCH4 of different bubble 13 C02 C CCH4 with a slope of 5-13.5 suggests the occurrence of sources collected from Shuchi Lake and Tube Dispenser aerobic oxidation [Coleman et al., 1981; Happell et al., Lake in Siberia. Solid lines are constant carbon isotopic 1994; Powelson and A , 007], while some evidence bichou 2 fractionation (ac) values of 1.04 and 1.06. The ac values of suggests that the slope may be somewhat greater in anaer- bubbles indicate the pathway of CH4 production, in which obic oxidation [Alperin et al., 1988]. While we cannot ac > 1.06 suggests CH4 is produced mainly by CO2 entirely rule out CH oxidation in these study lakes since 4 reduction, and ac < 1,055 suggests CH4 produced our sample sizes were small for some types of bubbling, we increasingly by acetate fermentation, A shift towards lighter concluded that biological oxidation did not cause the 13 ? CC02 values of the ice koshkas (open triangles) relative variation observed in the stable isotope signature of fresh to point sources may represent alteration from the original CH bubbles because no correlation was observed between 4 point source signatures because of CH4 oxidation prior to 13 ?DCH4 and ? CCH4 when looking at all bubbles collected ice enclosure or within the ice.

9 of 16 G00A08 WALTER ET AL.: ISOTOPES OF ARCTIC LAKE BUBBLING G00A08

reduction and acetate fermentation pathways with different different ages, from both modern lake sediments and thawed sediment organic matter reactivity (Table 4). The results of permafrost C which fixed over the span of up to tens of this analysis suggested the dominance of the CO2 reduction thousands of years. Given that CO2 reduction is a key pathway for point source and hot spot bubbling, while pathway for CH4 production in thermokarst lakes, the acetate fermentation contributed to background ebullition 14C-depleted pool of dissolved inorganic carbon (DIC) 14 (Figure 6). contributes directly to C-depleted values of CH4 in 14 [28] A host of factors can influence methanogenic path- bubbles (equation (2)). The C age of CH4 was related ways including substrate quality, pH, temperature, diversity positively to the magnitude of CH4 ebullition according to of archea, H2 partial pressure, and iron (Fe) content in different ebullition categories (Figure 4). High-emission northern aquatic sediments [Nozhevnikova et al., J 994, point sources and hot spots of CH4 bubbling were older Valentine et al., 2004, Conrad, 2005; Penning et al., (11,355 to 42,900 years), while the younger ages of low- 2005; Blodau et al., 2008). High availability of labile emission background bubbling (1345 to 8845 years) and organic substrates in lake and wetland sediments, particu- stirred bubbles from surface sediments (>modern to 3695 larly in sediments containing live plants, can support acetate years) indicated that a larger proportion of more modern production [Duddleston et al., 2002], leading to methano- substrates fueled methanogenesis. Similar ancient radiocar- genesis by acetate fermentation; whereas environments with bon ages of CH4 bubbles (14,760 to 26,020 years) (Table 3) less labile organic substrates, or the absence of particular from thermokarst lakes in interior Alaska suggest that this compounds exuded by living plants, can be dominated by pattern is not unique to Siberia and may occur across the CO2 reduction pathway [Nakagawa et al., 2002]. northern high latitudes. Temperature decreases with depth in the North Siberian 4.6. Organic Substrates for Methanogenesis in thermokarst lakes, and the CO reduction pathway is 2 Thermokarst Lakes favored at low temperatures [Nozhevnlkova et al., 1994). While low pH may lead to the build up of acetate in some [30] Nakagawa et al. [2002] suggested that the oldest 14 CH4 ages that they measured (up to 93.1 pmC, or acidic bogs with a dominance of CO2 reduction pathway, relatively high pH in Siberian lake sediments ranging from 500 years B.P.), which came from deeper lakes, indicated 7.1 to 9.1 (K. Walter, unpublished data, 2002-2004) the contribution of older CH4 that was produced from suggests this is not the case in these lakes. Oligotrophic conditions in wetlands have also been shown to favor the CO2 reduction pathway, but this seems unlikely in the thawed yedoma horizons of Siberian lakes, where soil nitrogen and phosphorus concentrations are high [Dutta et al., 2006).

4.5. Radiocarbon Ages of CH4 Ebullition 14 [29] Despite the wide range in Cage dates of CH4 from Siberia and Alaska (Table 3), the large number of samples depleted in 14C indicate the influence of substrates derived from ancient organic matter in supporting methanogenesis and ebullition. These results differ from other lakes and 14 wetlands with modem CCH4 ages indicating the production of CH4 from recently produced organic matter [Wahlen et al., 1989; Chanton et al., 1995; Chasar et al., 2000b; Nakagawa et al., 2002]. Only Zimov et al. [1997] have 14 reported C ages of CH4 as old as 27,000 years, and these were measured from two of the same lakes used in this study. Rather than reflecting the absolute age of any particular substrate, radiocarbon ages of CH4 in this study may ref1ect a mixture of CH4 produced from substrates of

10 of 16 G00A08 WALTER ET AL.: ISOTOPES OF ARCTTC LAKE BUBBLING G00A08

create anaerobic environments that facilitate productivity of fen vegetation and associated CH4 production via the fermentation pathway [Prater et al., 2007]. Deep, open- water thermokarst lakes represent a different situation because the labile properties of 14C-depleted Pleistocene organic matter can, under the right circumstances, be preserved for centuries to millennia because organic matter is frozen in permafrost. Upon thaw in deep, anaerobic lake bottoms, this Pleistocene-age organic matter is readily converted to 14C-depleted DIC, leading to production of CH4 at greater depths and emitted through hot spots. These hot spots appear to represent conduits that funnel or integrate methane production over large volumes at depth (Figure 8). Using the mean CH4 production potential observed in laboratory incubations of thawed yedoma - (145 g CH4 m 3 soil a-1 we estimate that at least 2.5 m3 to 8.5 m3 of thawed yedoma would be required to sustain observed hot spot ebullition emissions of 2175 ± 1195 mg -1 CH4 d . Relatively younger radiocarbon ages of CH4 emitted through point sources and particularly from background bubbling indicate that Holocene-age organic matter also contributes in part to methanogenesis (Table 3 and Figure 4). [32] The relationships between CH4 emission rate and 14 CCH4 age (Figure 4) and CO2 reduction pathway (Figure 6) demonstrate that CH4 production at depth differs from CH4 production in shallow lake sediments (Figure 8). At depth, despite the lower concentration of organic matter in Pleistocene-aged yedoma as compared to the overlying younger organic-rich lake sediments, the large volume of the thaw bulb beneath lakes contains a large, labile pool of 14C-depleted organic matter deposited in lakes by permafrost thaw. This pool enhances CH4 produced in microsites

primarily through CO2 reduction, resulting in high emission rates as bubbles from microsites are channeled out of sediments through bubble pathways. In shallower surface sediments, Holocene-aged organic matter, which represents terrestrial and aquatic detritus that accumulated on lake bottoms, may produce CH4 under a combination of CH4 production pathways. and may be subject to methane oxi- recalcitrant material. In this study the exceedingly high rates dation in surface sediments when O2 is present. We did not -1 -I of hot spot ebullition (up to >30 L CH4 spot d [Walter et observe evidence for CH4 oxidation in the few background al., 2006]) with exceptionally old radiocarbon ages (14CH4 bubble samples in this study. Similarly to other nonthermo- 0.5 to 1.2 Pille, or 39,000 to 43,000 years B.P.) suggests that a karst lake and wetland environments, fresh organic sub- considerable amount of CH4 is produced at depth in Siberian strates associated with modern aquatic plant and algae thermokarst lakes, and that the organic matter source in production in thermokarst lakes appears to fuel methano- Pleistocene loess is relatively labile. Laboratory incubations genesis at least in part in surface sediments via the acetate of Pleistocene organic matter extracted from undisturbed fermentation pathway. yedoma permafrost confirmed thc high quality of organic substrates contained in the deep lake horizons of North 4.7. Variation of ?D-CH4 in Lake Bubbles [33 Using the mean precipitation 18O inputs of -21%o Siberia [Zimov et al., 1997; Walter et al., 2007a]. ] ? to the Kolyma River Basin [Welp et al., 2005] with the [31] Radiocarbon-depleted peat accumulates over long 18 Local Meteorological Water Line ( D = 7.0 * O - 1.7, time periods in anaerobic lake and wetland environments ? ? 1 R2 = 0.99), we estimated the mean of precipitation in our because of slow decomposition of poor quality organic ?D Siberian study sites to be -158%o. This value is similar to matter, particularly under cold conditions [Smith et al., the weighted average of monthly data of ?D in rainwater 2005]. Because of the recalcitrant nature of peat, CH4 (-156%o) from 1997 to 1999 in Yakutsk [Nakagawa et al., emitted from peatlands is dominated by the decomposition 2002 , to the southeast of our Siberian study region, and to of fresh, labile terrestrial substrates such as root exudates ] the mean annual < D of all precipitation for interior Yukon that were fixed during recent photosynthesis [King et al., ? Territory, Canada (-160%o [Anderson et al., 2005]), which 2002; Chasar et al., 2000b; Chanton et al., 1995]. In is again similar to the region of our boreal study lakes shallow thermokarst features such as collapse scar bogs, (B. Finney, personal communication, 2005). The semiarid the predominant role of thermokarst erosion may be to

II of 16 G00A08 WALTER ET AL.: ITSOTOPES OF ARCTTC LAKE BUBBLING G00A08

climates of the interior boreal regions of Alaska and Siberia [35] Thennokarst lakes expand by thawing permafrost promote lake water evaporation, resulting in a slight deute- along their margins. In the yedoma region of North Siberia, rium enrichment of water in some lakes (-154.0 ± 2.6%oat Pleistocene-age, massive ice wedges are up to 80-m deep 1 m,-158.7 ± 2.1 %o at 10 m, Shuchi Lake) (Table 2). The and occupy 50-90% of the permafrost by volume [Zimov et ?D of lake water in other boreal lakes was -128.8 ± 0.7%o al., 1997, 2006]. Here the isotopic signature of water (Smith Lake, interior Alaska [Chanton et al., 2006]), -159 ± released from thawing ice wedges should contribute to the 2%o (interior Yukon Lake Jellybean [Anderson et al., 2005]), signature of environmental water where CH4 is produced. and -136 to -117%o (East Siberian alasses [Nakagawa et Cross sections of yedoma ice wedges measured near our al.,2002]). boreal lake study sites in Siberia had hydrogen isotopes [34] Isotopic separations between the ?D of environmen- ranging from 50 -260 to -235%o [Vasilchuk et al., 2001]. The highly depleted D reflects precipitation under cold tal water and CH4 in high-latitude wetlands was described ? H2O by Chanton et al. [2006] on the basis of the fractionation of Pleistocene climate conditions.Another possible explana- tion for the variation in the observed ?D H4 alues is deuterium during methanogenesis (?DCH4 = 1.55 ?H2O - C v 145.4, r2 = 0.69 in Alaskan samples). Assuming a similar variation in in situ H2 concentrations [Burke, 1993]. evaporative enrichment between ?D of precipitation and H2O 4.8. Using Ebullition Patchiness to Estimate Whole- ?D of lake water in interior Alaska to that of Siberia H2O Lake and Regional Isofluxes for Methane (~2%o), and using the equation of Chanton et al. [2006], we [36] We determined an isotope signature of annual CH4 would expect ?DCH4 of -397%o in Siberian lakes. This expected value was indeed close to the observed mean emissions (isoflux) from two Siberian lakes by weighting the seasonal isotope signature of each component of the flux ?DCH4 values for background (-380 ± 13%o, n = 3), point source (-384 ± 6%o, n = 10) and hot spot (-394 ± 4%o, by the relative contribution of each component to whole- = lake annual emissions (Table 5). We used 95% of whole- n 32) ebullition. Particularly low?DCH4 values in hot spot bubbles from Tube Dispenser Lake, a deep lake lake emissions in our calculations because the isotope undergoing active thermokarst erosion, were on the order signature of CH4 emitted by molecular diffusion, which accounted for 5 ± % of the annual flux [Walter et al., of -416 ± 4%o, n = 2, suggesting possibly that hot spot CH4 1 emitted from these thermo karst lakes was produced in an 2006], was not determined in this study. This new method environment with a different water source than modem lake of weighting different bubble sources improves emission water. estimates for lakes because it accounts for the patchiness of

12 of 16 G00A08 WALTER ET AL.: ISOTOPES OF ARCTIC LAKE BUBBLING G00A08

ebullition flux, a parameter of natural lake and wetland emissions that is typically not addressed. If we had neglected the diversity in ebullition dynamics, excluding the point source and hot spot emissions, our isotope results for North Siberian lakes would have been biased towards isotope signatures reflecting background bubbling and stirring of surface sediments, which are the only components that most studies consider. [37] Similarly, taking into account the distribution of point source and hot spot bubbling yielded a more accurate estimate of whole lake CH4 isotope fluxes (Table 5). The point source-weighted distribution of CH4 isotopes resulted in average whole-lake emission isotope signatures of ?DCH4 13 14 - 368%o, ? CCH4 -70.3%o, and CCH4 age 16,524 years 13 (Table 5). The ? . CCH4 was lighter in the whole-lake flux- weighted estimate than values derived by stirring surface sediments (-62.0%o) or trapping background bubbling (-63.4%o). The radiocarbon age of CH4 emissions was the parameter influenced most by the different measurement techniques. The more ancient flux-weighted estimate of 16,524 years reflects the importance of Pleistocene-aged organic matter released from permafrost upon thaw of in deeper lake sediments [Zimov et al., 1997], while the much younger age of CH4 in bubbles stirred from surface sediments (175 years for one sample from intensive study lakes, 998 ± 1659 years, n = 6 for all Siberian lakes) and background bubbling (4271 ± 2650 years, n = 7) indicates contributions of younger organic matter sources in methanogenesis closer to the sediment surface. Radiocarbon age dating of lake sediment cores for 17 lakes in North Siberia supports this interpretation with modern ages of organic matter at the surface and Pleistocene-age (up to 48,500 to 55,900 ± 6170 years (14C-dead)) organic matter in deeper sublake strata where yedoma thawed (data not shown). [38] The ability to improve lake CH4 emission estimates by accounting for the patchiness of different bubble sources that have distinct isotopic compositions enables researchers to estimate more accurately whole lake and regional isofluxes. Assigning CH4 isotope values to measured emissions yields isofluxes that can be used by inverse modelers to better constrain sources and sinks of atmospheric CH4. In this study, extrapolating the whole-lake isoflux that includes point source and hot spot emissions from Siberian thermokarst lakes to the areal extent of yedoma territory (106 km2), -1 l3 yielded isofluxes of ?DCH4 - 0.096 Gt %o a , ? CCH4 -1 14 16 -0.0183 Gt %o a , and CCH4 age 4.3 x 10 years (Table 4) for a large region of Siberia that has been underrepresented in global estimates of CH4 emissions from wetlands and from which lake ebullition emissions have been altogether excluded [Matthews and Fung, 1987; Aselmann and Crutzen, 1989; Botch et al., 1995]. [39] Results from two inverse modeling studies using CH4 isotopes suggested that, compared with bottom-up estimates of current atmospheric CH4 sources, the inverse estimates required larger tropical CH4 fluxes from both bacterial and biomass burning sources with a simultaneous reduction of northern sources [Mikaloff Fletcher et al., 2004a, 2004b]. The source-process inversion [Mikaloff Fletcher et al., 2004a] attributed the decrease in northern hemisphere sources to a reduction in fossil fuel and landfill emissions; while the regional inversion approach [Mikaloff Fletcher et al., 2004b] assigned the largest CH4 source

13 of 16 G00A08 WALTER ET AL.: ISOTOPES OF ARCTIC LAKE BUBBLING G00A08

centrations of CH , higher concentrations of N and were decrease to boreal Eurasian wetlands (comparing bottom-up 4 2, formed by nearly equal contributions of CO reduction and estimates of fluxes versus prediction of the inverse model). 2 acetate fermentation. Their relatively young radiocarbon Output from the inversion scenarios predicted emissions of ages suggest that Holocene-age organic matter sources, at 9-24 Tg CH a-1 from boreal Eurasia as a sum of all 4 least in part, fueled methanogenesis. sources, which were grouped into three categories: bacterial [43] 2. We characterized a second bubble source, with CH , biomass burning, and fossil fuels. Our results from 4 14C-depleted CH high CH concentrations, lower concen- Siberia are not consistent with the findings of Mikaloff 4, 4 trations of N , and extremely high CH emission rates. Fletcher et al. [2004b] because instead of a reduction of 2 4 [44] We hypothesize that the extremely high emission northern CH4 sources, which is required by the inversions, we observed increased CH emissions from Siberian ther- rates may be explained by bubble focusing. As CH4 4 production exceeds its solubility limits, CH bubbles come mokarst lakes [Walter et al., 2006] and isofluxes from 4 Siberian lakes that are more l3C-depleted than values out of solution forcing their way through lake sediments to lower pressure states. Small bubble streams merge into assumed by Mikaloff Fletcher et al. [2004b]. Inverse modeling must reconcile this additional source of high-latitude larger byways, like the tributaries of rivers joining into the main flow channel. The deeper the site of CH4 production, atmospheric CH4 (lake bubbles), in particular from northern Eurasian yedoma lakes, which has now been characterized the stronger the stream of bubbles that coalesces from a 13 large volume of sediments into a point source or hot spot of and whose ? CCH4 is depleted (-70.3%o) relative to the emission that exits through a small hole (< cm diameter) at typical value used for northern wetland emissions (-58%o) the sediment water interface. It is possible that point sources and the annual mean value of atmospheric CH4 (-47.3%o). A recent first-order estimate of pan-arctic lake emissions evolve into hot spots as thaw bulbs deepen during thermo- -1 karst lake development; however long-term observation of suggests that arctic lakes contribute 24 ± 10 Tg CH4 a by individual point sources and hot spots would be required to the mode of point source and hot spot bubbling [Walter et 13 al., 2007b]. If significantly? C-depleted CH4 is character- test this hypothesis. Presumably the radiocarbon ages would istic of point source and hot spot bubbling from the wider get older with time. Continuous flux measurements and lake range of arctic and subarctic lakes, which seems to be the bottom benchmarkers showed that hot spot vents in the 13 case on the basis of the ? CCH4 of Alaskan lakes in Table 2, Siberian thermokarst lakes remained in the same location then this ~6% contribution towards the global atmospheric for at least 4 years (K. M. Walter et al., personal observa- annual CH4 budget from lake ebullition, a previously tion, 2006). In contrast, background bubbling represents unaccounted for source, should play a role in inverse nonchanneled or weakly channeled bubbling. Methane modeling. bubbles released as background flux likely form in small 14 [40] Our documentation of a large, C-depleted CH4 microsites closer to the sediment-water interface, and can source from lake ebullition must also be considered in more easily escape the sediments as individual bubbles. models, which until now have attributed high-latitude 14C- [45] The alternative hypothesis to the tributary hypothesis free CH4 and recent changes to high-latitude CH4 concen- is that point sources and hot spots are from the decay of trations to leaky gas pipelines, coal mining and natural particulate organic matter (e.g., tree trunk, dead mammoth), seepage from gas reservoirs in Siberia [Wahlen et al., 1989; which is testable by coring or excavating the hot spot. Dlugokencky et al., 2003], not to aquatic sediments. Esti- Nondestructive geophysical methods that have been used in 1 mates of 4 C-CH4 derived from fossil fuel energy range peatlands [Comas et al., 2005] such as ground penetrating -1 from 95 to 110 Tg CH4 a [IPCC, 2001; Mikaloff Fletcher radar and electrical resistivity could also be used to examine et al., 2004b]. Annual emissions from Siberian lakes, 3.8 Tg the sediment structure and gas contents of lake sediments -1 CH4 a with an average radiocarbon content of ~12 pMC and thaw bulbs. [Walter et al., 2006], are less than 3.5% of fossil fuel CH4 [46] The particular characteristics of hot spot bubbling are sources. However, radiocarbon ages up to 26,000 years not unique to North Siberian yedoma lakes. Given that we 14 (3.9 pMC) from Alaskan thermokarst lakes suggest that found hot spots with CH4 of high concentration and C 14 C-depleted CH4 ebullition is not unique to Siberia, and depletion in Alaskan thermokarst lakes as well, we propose should be more thoroughly quantified for lakes and reser- that these two distinct zones of CH4 bubble production voirs globally. Given the large pool of organic matter locked (deep point sources versus shallow background) occur up in boreal and arctic permafrost (~950 Gt C [Zimov et al., across geographical regions in all lakes in which thermo- 2006]), continued warming of permafrost in the future karst erosion delivers a large, labile source of organic [Sazonova et al., 2004; Lawrence and Slater, 2005] could 14 substrate to deep anaerobic lake sediments. 13 lead to accelerated release of C-depleted CH4 from [47] In this study we characterized the distinct ? CCH4 14 expanding thermokarst lakes. and C-depeted CH4 signatures of arctic lake ebullition, combining them with improved bottom-up flux estimates 5. Conclusions [Walter et al., 2006; K. M. Walter etl., submitted manuscript, 2008], to reveal a large new source of high-latitude [41] On the basis of the concentrations and isotopic atmospheric CH4. Qualitative assessment of this new iso- compositions of gases in bubbles from North Siberian lakes tope CH4 source contradicts patterns presented by recent we have distinguished two major types of bubbles that inverse modeling, which predicted a reduction in boreal represent two zones of CH4 production in lakes (Figure 8): wetland sources relative to other latitudes in contrast to [42] 1. Bubbles stirred from surface sediments in lakes or bottom-up source estimates. Instead of providing a Eurasian captured in randomly placed traps that represent back- source reduction scenario, we suggest an increase in boreal ground bubbling, had young radiocarbon ages, lower con- wetland sources with 14C signatures that overlap with

14 of 16 G00A08 WALTER ET AL.: ISOTOPES OF ARCTIC LAKE BUBBLING G00A08 estimates of fossil fuel emissions. Since thermokarst erosion Chariton. J. P, D. Fields, and M. E. Hines (2006), Controls on the hydrogen isotopic composition of biogenic methane from high latitude terrestrial is a driving factor of CH4 emissions in arctic lakes, and wetlands, J. Geophys. Res .111, G04004, doi: 10.1 029/2005JG000134. thermokarst lake area appears to be increasing in zones of Chasar, L. S., .I. P. Chariton, P. H. Glaser, and D. I. Siegel (2000a), Methane continuous permafrost since 1970 [Smith et al., 2005; concentration and stable isotope distribution as evidence of rhizospheric Walter et al .. 2006]. understanding the isotopic implications processes: Comparison of a fen and bog in the Glacial Lake Agassiz peatland complex, Ann. Bol. (London), 86, 655 ~663, doi: 1 0.1006/ of further thermokarst lake expansion as permafrost in arctic anbo.2000.1172. regions continues to warm and thaw will help atmospheric Chasar. L. S., J. P. Chanton, P. H. Glaser, D. I. Siegel, and .I. S. Rivers (2000b), Radiocarbon and stable carbon isotopic evidence for transport modelers define CH4 sources and predict changes. and transformation of DOC, DIC and CH4 in a northern Minnesota peatland, Globul Biogeochem. Cycles; 14, 1095 ~ 1105, doi: I 0. 1029/ [4N] ACknowledgments. We thank I.R. Welp and S.P. Davidov for 1999GBOOl22 I. active contributions throughout the research; Jim Prater, Dana Fields, and Chen, Y.-H., and R. G. Prinn (2006), Estimation of atmospheric methane Burt Wolf for laboratory assistance; D. Draluk, E. Ricter, and C. Thompson emissions between 1996 and 2001 using a three-dimensional global che- for field assistance; the Northeast Science Station and Toolik Lake Field mical transport model, J. Geophys. Res., III, D 10307, doi: 10.1 029/ Station for logistic support; K. Dutra and the University of Florida for 2005.1 0006058. helping prepare the radiocarbon targets: D. Valentine, R. Ruess, B. Finney, Coleman, D. D., B . .I. Risatti, and M. Schoell (1981), Fraction of carbon and three anonymous reviewers for constructive reviews. Research funding and hydrogen isotopes by methane oxidizing bacteria, Geochim. Cosmo- was provided by the National Science Foundation (NSF) through the chim, Acta, 45, 1033~ 1037, doi:l0.1016/0016-7037(81)90129-0. Russian-American Initiative on Shelf-Land Environments of the Arctic Coleman, M. L., T, 1. Sheperd,.I. J. Durham, J. E. Rouse, and G. R. Moore (RAISE) of the Arctic System Science Program (ARCSS), NSF EAR (1982), Reduction of water with zinc for hydrogen isotopic analysis, (0628349, NSF DEB 0516326, the International Center for Arctic Research Anal. Chem., 54. 993~995, doi:10.l021/ac00243a035. Global Change Fellowship Program, Environmental Protection Agency Comas, X., L. Slater, and A. Reeve (2005), Spatial variability in biogenic STAR Fellowship Program, the NASA Earth System Science Fellowship gas accumulations in peat soils is revealed hy ground penetrating radar Program, and the Bonanza Creek LTER (Long-Term Ecological Research) (GPR), Geophys. Rr!s. Lett., 32, LOX401, doi: 10.1 029/2004GL022297. program (funded jointly by NSF grant DEB-0423442 and USDA Forest Conrad, R, (1989), Control of methane production in terrestrial ecosystems. Service, Pacific Northwest Research Station grant PNW01 -JV 1126 I952-231). in Exchange of Trace Gases Between Terrestrial Ecosystems and the Atmosphere, edited by M. O. Andreae and D. S. Schimel, pp. 39--58, References John Wiley, New York. Conrad, R. (2005), Quantification of methanogenic pathways using stable Alperin. M . .I., W. S. Reeburgh, and M. J. Whiticar (1988), Carbon and carbon isotopic signatures: A review and a proposal, Org. Geochem., 36, hydrogen fractionation resulting from anaerobic methane oxidation, Glo- 739 - 752, doi:l0.1 016/j.orggeochem.2004.09.006. hal Biogeochem. Cycles, 2, 279--288. Dlugokencky, E. J., S. Houweling, L. Bruhwiler, K. A. Masarie, P. M. Alperin, M. J., N. E. Blair, D.B. Albert, T. M. Hoehler, and C. S. Martens Lang, J. B. Miller, and P. P. Tans (2003), Atmospheric methane levels (1992), Factors that control the stable isotope composition of methane off: Temporary pause or a new steady-state", Geophys. Res. Lett., 311(19), produced in an anoxic marine sediment, Global Biogeochem. Cycles, 6, 1992, doi: 1 0.1 029/2003GL018126. 271-291, doi:10.1029/92GB01650. Duddleston, K. N., M. A. Kinney, R. P. Keine, and M. E. Hines (2002), Anderson, L., M. B. Abbott, B. P. Finney, and S. J. Bums (2005), Regional Anaerobic microbial biogeochemistry on a northern bog: Acetate as a atmospheric circulation change in the North Pacific during the Holocene dominant metabolic end product, Global Biogeochem. Cycles, 16(4), inferred from lacustrine carbonate oxygen isotopes, Yukon Territory, 1063, doi:l0.1029/2001GB001402. Canada, Qual. Res .. 64, 2 1-35, doi.: 10.1 016/j.yqres.2005.03.008. Dutta, K., E. A. G. Schuur, S. A. Zirnov, J. T. Randerson, and J. C. Neff Aselmann, I., and P. J. Crutzen (19 9), Global distribution of natural fresh- 8 (2006), Potential carbon release from permafrost soils of northeastern water wetlands, rice paddies, their net primary productivity, seasonality, Siberia, Global Change Biol, 12,2336-2351, doi:101111/j.1365- and possible methane emissions, J. Atmos. Chcm., s. 307~358, 2486.2006.01259.x. doi: 1 0.1 007/BF00052709. Fung, I., J. John. J. Lerner, E. Matthews, M. Prather, L. P. Steele, and P. J. Bustvikcn. D .. J. Cole, M. Pace, and L. Tranvik (2004), Methane emissions Fraser (1991), Three-dimensional model synthesis of the global methane from lakes: Dependence of lake characteristics, two regional assessments, cycle,.J. Geophys. Res., 96, .13,033-· 13,065, doi:l0.1029/91JDOI247. and a global estimate, Global Biogeochem. Cycles, 18, GB4009, Hamilton, T. D. (2003), Glacial geology of the Toolik Lake and upper doi: 10. I 029/2004GB002238. Kuparuk River regions, edited by D. A. Walker, BioI. Pap. Univ. Alaska Blodau, c., R. Rees, H. Flessa, A.Rodionov, G. Guggenberger, K.-H. 26, lnst. of Arctic Biol., Fairbanks, Alaska. Knorr, O. Shibistova, G. Zrazhevskaya, N. Mikheeva, and O. A. Kasansky Happell .I., .I. P. Chanton, and W. Showers (1994), The infiuence of

(200R), A snapshot of CO2 and CH4 evolution in a thermokarst pond near methane oxidation on the stable isotope composition of methane emitted Igarka. northern Siberia,.J. Geophys. Res., doi: 10.1 029/2007JG000652, in from Florida swamp forests, Geochim. Cosmochim. Acta, 58, 4377~ press. 4388, doi: 10.1016/0016-7037(94)90341-7. Botch, M. S., K. I. Kobak, T. S. Vinson, and T. P. Kolchugina (1995), Hein, R., P. J. Crutzen, and M. Heimann (1997), An inverse modeling Carbon pools and accumulation in peatlands of the former Soviet Union, approach to investigate the global atmospheric methane cycle, Global Globa] Biogeachcm. Cvcles, 9, 37 - 46, doi: I O. I 029/94GB03 I 56. Biogeochem. Cycles, 11, 43 ~ 76, doi: 10.1 029/96GB03043. Bousquet. P., et al., (2006), Contribution of anthropogenic and natural Holmes, R. M., and R. Lammers (2006), The arctic system and global sources to atmospheric methane variability, Nature. 443, 439--443, change: Why bother with Russia, paper presented at Workshop on Facil- doi: 1 0.138/nature05132. itating U.S.-Russian Environmental Change Research in thc Russian Burke, R. A. (1993), Possible influence of hydrogen concentration on Arctic, U.S. Natl. Sci. Found" St. Thomas, V.I., 11 ~ 16 June. microbial methane stable hydrogen isotopic composition, Chemosphere. Hornibrook, E. R., F. J. Longstaffe, and W. S. Fyfe (2000), Evolution of 26(,( 1 -4), 55-67. stable carbon isotope compositions from methane and carbon dioxide in Casper, P., S. C. Maberly, G. H. Hall, and B. J. Finlay (2000). Fluxes of freshwater wetlands and other anaerobic environments, Geochim, Cos- methane and carbon dioxide from a small productive lake to the atmo- mochim. Acla, 64, 1013~ 1027, doi:1O.1016/S0016-7037(99)00321-X. sphere. Biogeochemistry 49, 1 ~ 1 9, doi: 00.1 023/A-3A1006269900174. Houweling, S., T. Kaminski, F. Dentener, J. Lelieveld, and M. Heimann Ch'111lon,.I. P., C. S. Martens, and C. A. Kelley (1989), Gas transport from (1999), Inverse modeling of methane sources and sinks using the adjoint methane-saturated tidal freshwater and wetland sediments, Limnol. Ocea- of a global transport model, J. Geophys. Res., lii4, 26,137~26,160, nogr, 34, 807~819. doi: 10.1 029/1999JD900428. Chan ton, .I., J. Bauer, P. Glaser, D. Siegel, E. Ramonowitz, S. Tyler, Intergovernmental Panel on Climate Change (lPCC) (2001), Climate e. Kelley, and A. Lazrus (1995), Radiocarbon evidence fix the substrates Change 2001: The Scientific Basis: Contribution of' Working Group I supporting methane formtion within northern Minnesota peatlands, Geo- to the Third Assessment Report of the Intergovernmental Panel On Cli- chim. Cosmochim. Acta, 59, 3663-3668. doi:10.1016/0016-7037(95) male Change, edited by J. T. Houghton et al., Cambridge Univ. Press, 0024()-7 .. New York. Chan ton . .J.P. I .. C. Chasar, P. Glaser, and D. Siegel (2005), Carbon and Intcrgovernmental Panel on Climate Change (IPC(,) (2007), Climate hydrogen isotopic effects in microbial methane from terrestrial environ- Change.2001: The Physical Scicnceasis: Contribution of' Working ments, in Stable lsotopes and Biosphere-Atmosphere interactions, Phy- Group 1 to the Fourth A..ssessment Report of the Intergovernmental Panel siological Ecology Series, edited by L. B. Flanagan, J. R. Ehleringer, and on Climate Change, edited by S. Solomon et al., Cambridge Univ. Press, D. F. Patuki, chap. 6, PP'. 85- l05, Elsevier, Amsterdam. New York.

15 of 16 G00A08 WALTER ET AL.: ISOTOPES OFARCTIC LAKE BUBBUNG G00A08

Keppler, F., J. T. G. Hamilton, M. Brab, and T. Rockmann (2006), Methane Smith, L. C, Y.Sheng, G. M. MacDonald, and L D. Hinzman (2005), Dis- emissions from terrestrial plants under aerobic conditions, Nature, 439, appearing arctic lakes, Science, 30S, 1429, doi: I0.1 I26/science. 1108142. 187-191, doi:10.1038/nature04420. Stuiver, M., and H. Polach (1977),Reporting of 14C data, Radiocarbon, IV, King, J. Y, W. S. Reeburgh, K. K.Theiler, G. W. Kling, W. M. Loya, L. C. 355-363. Johnson, and K. J. Nadelhoffer (2002), Pulse-labeling studies of carbon Sugimoto, A., and E. Wada (1995), Carbon isotopic composition ofbacter- cycling in the Arctic tundra ecosystems: The contribution of photo- ial methane in a soil incubation experiment: Contributions of acetate and synthates to methane emission, Global Biogeochem. Cycles, 16(4), C02/H2, Geochim. Cosmochim. Acta, 59, 1329·-1337, doi: I 0.1 016/ 1062, doi:10.1029/200IGBOOI456. 0016-7037(95)00047-4. Kinnaman,F. S., D. L. Valentine, and S. C. Tyler (2007),Carbon and Templeton, A. S., K.-I-I. Chu,L. Alvarez-Cohen, and M. E. Conrad (2006), hydrogen isotope fractionation associated with the aerobic microbial oxi- Variable carbon isotope fractionation expressed by aerobic CH.-oxidizing dation of methane, ethane, propane and butane, Geochim. Cosmochim. bacteria, Geochim. Cosmochim. AC/iI, 70, 1739-1752, doi:IO.IOI61 ACta, 7/,271-283, doi:10.1016/j.gca.2006.09.007. j.gca.2005.12.002. Kipphut, G. w., and C. S. Martens (1982), Biogeochemical cycling in an Valentine, D. L., A. Chidthaisong, A. Rice, W. S. Reeburgh, and S. Tyler organic-rich coastal marine basin. 3. Dissolved gas transport in methane (2004), Carbon and hydrogen isotope fractionation by moderately ther- saturated sediments, Geochim. Cosmochim. Acta, 46, 2049-2060, mophylic methanogens, Geochim. Cosmochim. Acta, oli, 1571 ··1590, doi: 10.1 0 16/0016-7037(82)90184-3. doi: I 0.1 016/j.gca.2003.1 0.012. Kling, G., G. W. Kipphut, and M.C. Miller (1992), The flux of CO2 and Vasil'chuk, Y K., A. C. Vasil'chuk, D. Rank, W. Kutschera, and.l. C. Kim (2001), Radiocar on dating of d . plots in late Pleistocene ice- CH from lakes and rivers in arctic Alaska, Hvdrobioiogia; 240, 23-36. b 18 dD 4 wedges of the Duvanny Yar (lower Kolyma River, northern Yakuria), Lansdown, J. M., P. D. Quay, and S. L. King (1992), CH production via CO 4 2 Radiocarbon, 43, 541 -553. reduction in a temperate bog: A source of 13C-depleted CH , Gcochim. 4 Wahlen, M., N. Tanaka, R. Henry, B. Deck,.1. Zeglen,.1. S. Vogel,J. Southon, Cosmochim. Acta, 56, 3493·-3503, doi: 1 0.1 016/00 16-7037(92)90393-W. A. Shernesh, R. Fairbanks, and W. Broecker (1989), Carbon-14 in Lawrence, D. M., and A. G. Slater (2005), A projection of severe near- methane sources and in atmospheric methane: Contribution from fossil surface permafrost degradation during the 21 st century, Geophys. Res. carbon, Science, 245, 286·290, doi: I 0.1 I26/science.245.4915.286. Lett., 32, L24401, doi:l0.102912005GL025080. Waldron, S., J. M. Lansdown, E. M.Scott, A. E. Fallick, and A. .I. Hall Lowe, D. c., C. A.M. Brenninkmeijer, G. W. Brailsford, K. Lassey, A. J. (1999a), The global influence of H isotopic composition of water on that Gomez, and E. G. Nisbet (1994), Concentration and DC records of atmo- of bacteriogenic methane from shallow freshwater environments, Geo- spheric methane in New Zealand and Antarctica: Evidence for changes in chi m. Cosmochim. A cia, 63, 2237 - 2245, doi: 10. 1 0 16/S00 16- methane sources, J. Geophys. Res., 99, 16,913 - 16,925, doi:l 0.1 0291 7037(99)00192-1. 94JD0090R. Waldron, S., I. A. Hall, and A. E. Fallick (1999b), Enigmatic stable isotope Martens, C.S., N. E. Blair, C.D.Green, and D. J. Des Marais (1986), dynamics of deep peat methane, Global Biogeochem. Cycles. 13, 93 Seasonal variations in the stable carbon isotopic signature of biogenic 100, doi: I0.1 029/1 998GB900002. methane in a coastal sediment, Science, 233, 1300- 1303; doi: 10.1126/ Walter, K. M., S. A. Zimov, J.P.Chariton, D. Verbyla, and F. S. Chapin III science. 1 1536566. (2006), Methane bubbling from Siberian thaw lakes as a positive feed- Matthews, E., and I. Fung (1987), Methane emission from natural wetlands: back to climate warming, Nature, 443, 71 - 75, doi: I 0.1 038/nature05040. Global distribution, area, and environmental characteristics of sources, Walter, K. M., M. E. Edwards, G. Grosse, S. A. Zimov, and F. S. Chapin III Global Biogeochem. Cycles, 1,61-86, doi:10.1029/GBOOliOOlp00061. (2007a), Thermokarst lakes as a source of atmospheric C . during the Mikaloff Fletcher, S. E., P. P. Tans, L. M. Bruhwiler, J. B. Miller, and H4 last deglaciation, Science, 3111, 633 -636, doi: I 0.1 I 26/science. 1142924. M. Heimann (2004a), CH. source estimated from atmospheric observa- Walter, K. M., L. C. Smith, and F. S. Chapin III (2007b), Methane bubbling tions ofCH and its 13C/12C isotopic ratios: 1. Inverse modeling of source 4 from northern lakes: Present and future contributions to the global processes, Glob,d Biogeochem. Cycles, 18, GB4004, doi:IO. 1029/ methane budget, Philos. Trans. R. Soc. Ser. A, 365, 1657 -1676. 2004GB002223. Welp, L. R., J. R. Randerson, J.C. Finlay, S. P. Davidov, G. M. Zimova, Mikalotf Fletcher, S. E., P. P. Tans, L. M. Bruhwiler, J. B. Miller, and A. I. Davidova, and S. A. Zimov (2005), A high resolution time series of M. Heimann (2004b), CH source estimated from atmospheric observa- 4 oxygen isotopes from the Kolyma River: Implications lor the seasonal tions of CH4 and its 13C/12C isotopic ratios: 2. Inverse modeling of CH4 dynamics of discharge and basin-scale water use, Geophys. Res. lett/., 32, fluxes from geographic regions, Globed Biogeochem. Cycles, 18, L14401, doi:10.l029/2005GL022857. GB4004, doi: 10.1 029/2004GB002223. Whiticar, M. J., E. Faber, arid M. Schoell (1986), Biogenic methane lor- Nakagawa, F., N.Yoshida, Y Nojiri, and V. N. Makarov (2002), Production marion in marine and freshwater environments: CO2 reduction vs. acetate of methane from alasses in eastern Siberia: Implications from its 14C and fermentation - Isotope evidence, Geochim, Coschim Acta, 50, 693·· stable isotope compositions, Global Biogeochem. Cycles, /6(3), 1041, 709, doi:l 0.1 0 16100 16-7037(86)90346-7. doi: I 0.1 029/2000GBOO 1384. Worthy, D. E., J. I. Levin, F. Hopper, M. K. Ernst, and N. B. A. Trivett Nozhevnikova, A. N., O. R. Kotsyurbenko, and M. V. Simankova (1994), (2000), Evidence for a link between climate and northern wetland Aceteogenesis at low temperature, in Acetogenesis, edited by H. L. methane emissions, J. Geophys. Res., 105, 4031-·4038, doi: 10.1 029l Drake, pp. 416-431, CPC Press, New York. 19991090 1100. Penning, H., C. M. Plugge, P. E. Galand, and R. Conrad (2005), Variation Zhuang, Q., J. M. Melillo, M. C. Sarofim, D. W. Kicklighter,A. D. of carbon isotope fractionation in hydrogenotrophic methanogenic micro- McGuire, B. S. Felzer, A. Sokolov, R. G. Prinn, P.A. Steudler, and bial cultures and environmental samples at different energy status, Global S. Hu (2006), CO and CH. exchanges between land ecosystems and Change Bioi., II, 2103-2113. 2 the atmosphere in northern high latitudes over the 21 st century, Geo- Powelson, D. J. C., and 1'. Abichou (2007), Methane oxidation in biofilters phys. Res. Lett., 33, L17403, doi:10.1029/2006GL026972. measured by mass-balance and stable isotope methods, Environ. Sci. Zimov, S. A., Y. V. Voropaev, I. P.Semiletov, S.P. Davidov, S. F. Prosiannikov, Technol., 41, 620--625, doi: I 0.1 02 I/es061 656g. F. S. Chapin III, M. C. Chapin, S. Trumbore, and S. Tyler (1997), North Prater, .I. L., J. P. Chanton, and G. J. Whiting (2007), Variation in methane Siberian lakes: A methane source fueled by Pleistocene carbon, Science. 271, production pathways associated with permafrost decomposition in col- ROO-802, doi:l 0.1 I 26/science.277.5327.800. lapse scar bogs of Alberta, Canada, Global Biogeochem. Cvcles, 21, Zimov, S. A., E. A. G. Schuur, and F. S. Chapin III (2006), Permafrost and GB4004, doi: I0.1 029/2006GB002866. the global carbon budget, Science, 312, 1612- 1613, doi: 1 0.11261 Quay,P. D., S. L. King, J. M.Lansdown, and D. O. Wilbur (1988), Isotopic science. I 128908. composition of methane released from wetlands: Implications lor the increase in atmospheric methane, Global Biogeochem. Cycles, 2, 385-· 397, doi: I 0.1 029/GB002i004p00385. J. P. Chanton, Department of Oceanography, Florida State University, Reeburgh, W. S., J. Y King, S. K. Regli, G. W. Kling, N. A. Auerbach, and Tallahassee, FL 32306-4320, USA. ([email protected]) D. A. Walker (1998), ACH emission estimate for the Kuparuk River basin, 4 F. S. Chapin Ill, Institute of Arctic Biology, University of Alaska Alaska,./. Geophys.Res., 103,29,005-29,013, doi:IO.1029/98JD00993. Fairbanks, Fairbanks, AK 99775,USA. (tenychapin@uafedu) Roulet, N. T., A. Jano, C. A.Kelly, L. F. Klinger, T.R. Moore, R. Protz, E. A. G. Schuur, Department of Botany, University of Florida, J. A. Ritter, and W. R. Rouse (1994), Role of Hudson Bay lowland as a Gainesville, FL 32611, USA.(tschuurr utl.edu) source of atmospheric methane, .I. Geophys.Res., 99, 1439-1454, @ K. M. Walter, Institute of Northern Engineering and International Arctic doi: I 0.1 029/93JD00261. Research Center, University of Alaska Fairbanks, Fairbanks,AK 99775, Sazonova, 1'. S., V. E. Romanovsky, J. E. Walsh, and D. O. Sergueev USA. ([email protected]) (2004), Permafrost dynamics in the 20th and 21 st centuries along the S. A. Zirnov, Northeast Science Station, Cherskii, Republic of Sakha, East Siberian transect, J Geophys. Res., 109, DO II 08, doi: I 0.1 0291 Russia. ([email protected]) 2003J D003680.

16 of 16