Arctic regions and their water bodies are affected by a rapidly warming climate. Arctic lakes and small ponds are known to act as an important source of atmospheric methane.
However, not much is known about other types of water bodies in permafrost
regions, which include major rivers and coastal bays as a transition type
between freshwater and marine environments. We monitored dissolved methane
concentrations in three different water bodies (Lena River, Tiksi Bay, and
Lake Golzovoye, Siberia, Russia) over a period of 2 years. Sampling was
carried out under ice cover (April) and in open water (July–August). The
methane oxidation (MOX) rate and the fractional turnover rate (
In the Lena River winter methane concentrations were a quarter of the summer concentrations (8 nmol L
The winter situation seemed to favor a methane accumulation under ice, especially in the lake with a stagnant water body. While on the other hand, in the Lena River with its flowing water, no methane accumulation under ice was observed. In a changing, warming Arctic, a shorter ice cover period is predicted. With respect to our study this would imply a shortened time for methane to accumulate below the ice and a shorter time for the less efficient winter MOX. Especially for lakes, an extended time of ice-free conditions could reduce the methane flux from the Arctic water bodies.
Worldwide, the mixing ratio of methane has been increasing rapidly since 2000, from 2.1 ppb yr
Lakes are important sources of atmospheric methane on a regional to global scale (Bastviken et al., 2004; Cole et al., 2007), and their contribution is predicted to increase in response to climate change and rapidly warming waters (O'Reilly et al., 2015; Tan and Zhuang, 2015; Wik et al., 2018). Most of the methane produced in lake sediments enters the atmosphere via ebullition (Bastviken et al., 2004; Walter et al., 2007), a temperature-sensitive transport mode with high spatial and temporal heterogeneity (DelSontro et al., 2015). The role of Arctic rivers as a methane source to the shelf seas is poorly described. Some studies present rivers as strong methane sources (Morozumi et al., 2019), while other studies revealed a complex pattern of riverine methane input (Bussmann et al., 2017).
One major drawback from most of these studies is that sampling was conducted
in the ice-free season, although most of the year Arctic water bodies are
ice covered. Thus, the seasonal variation could not be captured within those
studies. The ice cover on lakes decouples the water body from the atmosphere
and the circulation changes from wind-driven to thermohaline. After ice
formation a stable winter stratification is set up. As there is no more external oxygen supply, enhanced anaerobic degradation leads to accumulation
of methane,
Rivers of permafrost regions are characterized by an ice season of
An important filter, counteracting the methane flux into the atmosphere, is microbial methane oxidation. Methane can be oxidized under anoxic conditions close to sediment horizons where it is produced (Martinez-Cruz et al., 2017; Winkel et al., 2018) or during migration through the oxic water column to the atmosphere (Mau et al., 2017a; Bussmann et al., 2017). Under ice cover, it is important to consider methane oxidation below ice as it may reduce the total amount of methane emitted to the atmosphere during ice-off. Active methane oxidation and a methanotrophic community have been shown for permafrost thaw ponds and lakes (Kallistova et al., 2019). Yet, the methane oxidation capacity in such lakes during ice cover with low temperatures and low oxygen concentrations is unknown. In a study covering several boreal lakes, methane oxidation was restricted to three lakes, where the phosphate concentrations were highest (Denfeld et al., 2016). Rates of methane oxidation during the winter have been found to be much lower than summer rates, yet there is no clear consensus on the factors limiting methane oxidation in winter (Ricão Canelhas et al., 2016). In addition to oxygen concentration, the geological background (i.e., yedoma-type permafrost lakes versus non-yedoma-type lakes) also had a significant impact on the methane oxidation rate (Martinez-Cruz et al., 2015).
Our study tests the hypothesis that winter ice blocks methane emissions, leading to the accumulation of methane in the underlying water bodies. By studying hydrographically different water bodies (lake, river, and sea), we expect insights into the influence of water column dynamics on methane accumulation to result. In addition, we measure methane oxidation rates in the water column and in melted ice to assess oxidation as a potential sink.
Map of the study area in the Lena River and Buor-Khaya Bay (Siberia, Russia). The inset shows details of the sampling at Lake Golzovoye. Sampling locations in winter are shown in red and summer sampling locations in green. Created by Bennet Juhls.
This study was conducted on the southern coast of Bykovsky Peninsula in northeast Siberia, Russia (Fig. 1). Thermokarst lakes in that area commonly originated in the early Holocene when surficial permafrost started to thaw, leading to accumulation of lake sediments with organic contents of about 5 %–30 % (Biskaborn et al., 2016; Schleusner et al., 2015). Thermokarst lakes in the Lena River delta seem to be ice free a little later after the coastal ice breakup, depending strongly on the air temperature in the individual year (Bennet Juhls, unpublished data).
Offshore of the Bykovsky Peninsula, part of the Yedoma Ice Complex is submerged, and subsea permafrost is currently degrading. The coastline erodes
at mean rates of between 0.5 and 2 m yr
The Lena River has a mean annual discharge of 581 km
In the course of several expeditions to the Lena Delta (Siberia, Russia), we were able to repeatedly sample the same locations in winter and summer over the years (Table 1).
Locations and sampling dates of water samples and ice cores for dissolved methane (M-conc) and methane oxidation rates (MOX).
In September 2016, water samples were taken in the Bykovskaya Channel and mouth of the Lena River (Overduin et al., 2017). In April 2017 with ice cover on the water bodies, ice cores were taken at Lake Golzovoye, the Lena River, and Tiksi Bay, and the water below the ice was also sampled. Lake Golzovoye is an oval-shaped thermokarst lake about 0.5 km in diameter with a maximal depth of 10 m, surrounded by yedoma uplands at various stages of degradation and with no ice grounding in its center (Spangenberg, 2018; Strauss et al., 2018). Tiksi Bay is a shallow brackish bay at the southern end of Buor-Khaya Bay but still strongly influenced by the Lena River outflow. The water column is usually stratified, with a colder, more saline water underlying the brackish surface layer (Overduin et al., 2016). The water of the Lena River was sampled near Samoylov island (main channel). In July and August 2017, we sampled the same locations (Lena River near Samoylov, Tiksi Bay, and Lake Golzovoye) with open water (Strauss et al., 2018). The transect to the “outer” Tiksi Bay has been investigated repeatedly over the previous years (Bussmann, 2013; Bussmann et al., 2017). In April 2018, again under-ice samples were taken from the Lena River (Kruse et al., 2019).
In winter, water samples at the ice–water interface were taken with a 1 L
water sampler (Uwitec Austria) and transferred to 0.5 L Nalgene bottles. In the
field camp, the water was transferred with a 60 mL syringe into glass bottles, closed with butyl stoppers and crimps, poisoned with 0.2 mL 25 %
In winter 2017, due to problems of freezing, 40 mL of sample water was shaken for 2 min with 20 mL nitrogen in a 60 mL syringe. This headspace was then transferred into glass bottles filled with a saturated NaCl solution. Comparative measurements showed no significant difference between these two sampling strategies (Triputra, 2018). This data set has been published already:
In winter 2017, in addition to water sampling, we also investigated ice cores
for their methane content and methane oxidation rates. For each station three ice cores were drilled with a Kovacs Mark II ice coring system (9 cm diameter). One core was used to measure the in situ temperature and back-up,
one core was used for methane analysis, and the third core was drilled for later
molecular analyses. For determining the methane oxidation rates and later
methane concentrations, the ice cores were processed at the Research Station
Samoylov Island. The top 10 cm, a 10 cm mid-section, and three 10 cm sections at the bottom of the core were cut off and transferred to special PVDF gas sampling bags (Keika Ventures). The remaining parts of the cores were kept frozen. The bags were evacuated and the cores melted within approx. 5 h in a water bath at 8
Methane concentrations were determined via the headspace method by adding 20 mL
of
The MOX rate was determined by adding radioactive tritiated methane to
triplicate samples (Bussmann et al., 2015). The principle of the MOX rate determination is based on the ratio of produced tritiated hydrogen from the added tritiated methane. This ratio corrected for the incubation time gives the fractional turnover rate (
In a set of experiments, we also assessed the influence of temperature on the MOX rate. Water samples (main channel, April 2017) that were incubated at temperatures from 1, 4, 7, and 10
Profiles of water temperature and conductivity were measured with a CastAway CTD (SonTek) in summer 2016 and in winter and summer 2017. Water depth measurements were made with an echo-sounding device (Garmin), every 10 m along the profile. Water velocity was measured in three horizons at each vertical profile: 0.2, 0.6, and 0.8
In the Lena River in summer 2016, median methane concentrations were 37 nM
(
Median summer and winter methane concentrations at the Lena River, Lake Golzovoye, and Tiksi Bay in the years 2016–2018. Bright columns indicate summer values, and dark columns indicate winter values. The asterisks indicate significant differences between summer and winter data.
In winter 2017, the water column under the ice of the Lena River was about
1.3
In summer 2017, the water discharge in Bykovskaya Channel was 5313.4 m
In Lake Golzovoye, in summer 2017, the median methane concentration was 49 nM (
In Tiksi Bay and in summer 2017, the median methane concentration was 14 nM
(
Ice cores were taken at Lake Golzovoye and in Tiksi Bay, whereas no ice core data are available for the Lena River itself (Strauss et al., 2018). Methane concentrations in the ice cores of Lake Golzovoye and Tiksi Bay were rather low (both with a median of 9 nM). No depth gradients from the ice surface, middle section, and the three lowermost sections were evident. In a closeup for the bottom layers, there was a slight increase in methane towards the ice–water interface for the ice cores from Lake Golzovoye, but not from Tiksi Bay.
Figure 3 shows the median methane concentrations in the ice cores and in the water from the ice–water interface. Water column concentrations were 11 times and 109 times higher than in the ice cores, for Tiksi Bay and Lake Golzovoye, respectively, with a median of 102 and 985 nM (Bussmann and Fedorova, 2019). However, in one core of Lake Golzovoye (core no. 24), concentrations were orders of magnitude higher throughout the core (854–11091 nM) and 6954 nM in the water below Fig. 2 (Fig. 3).
Median methane concentrations in the ice cores and in the water below the ice. Data from Tiksi Bay are shown in light grey and data for Lake Golzovoye in dark grey, with core no. 24 shown separately in white. Note the logarithmic scale.
Methane oxidation rates were determined in the melted water from the ice
cores from the different locations and in water from the Lena River. Due to
logistic restraints at the field sites, no direct measurements of MOX in the
waters of Lake Golzovoye and Tiksi Bay were possible. In the first step we
determined the fractional turnover rate
The highest MOX rates were found in the water below station 24 in Lake Golzovoye (20.36 nmol L
Box plot of the calculated methane oxidation rates (MOX) in water under ice cover at Lake Golzovoye, at the location of ice core no. 24, Tiksi Bay, and the Lena River. Note the logarithmic scale.
To assess the influence of temperature on the MOX, we incubated water samples at different temperatures and determined their MOX rate. As expected, with increasing temperature the MOX rate also increased (Fig. 5). The
Influence of incubation temperature on methane oxidation rate for Lena River water, winter 2017.
In this study we compared the methane concentration under ice cover (winter) with open-water situations (summer) in three different water bodies.
In winter the methane concentrations in the Lena River were 4 times lower
than in summer (Table 2). The Lena River displays a reduced but still
substantial water flow/discharge under ice cover. In 2017, the discharge in winter (March and April with 2830 and 2185 m
Comparison of methane concentration in water and ice as well as methane oxidation rates (MOX) at different sites and in different seasons.
In winter there are only a few possible sources of methane left. The surrounding soils of the drainage basins are all frozen. The ground below the main channels of the Lena is still unfrozen (Fedorova et al., 2019); however the sediment consists of coarse grain sizes and is poor in organic material (Rivera et al., 2006), and we do not expect any in situ methane production. Especially in the Lena River, a substantial amount of particulate organic carbon (POC) originates from thermokarst-induced, abrupt collapse of Pleistocene Ice Complex deposits. These events mainly occur in late summer. The signal however is still visible in winter (Wild et al., 2019). With these collapses methane could also be imported to the river. So, we could only detect low methane concentrations in winter. In contrast, in summer, the active-layer soils from the drainage basin allow for several sources of methane and thus increased methane concentrations in summer. Also, methane could be transported from the southern Lena catchment towards our study area, as is suggested for particulate organic matter (Winterfeld et al., 2015). At least during the warm season, methane production from (temperate) river sediments is possible (Bednařík et al., 2019).
In Tiksi Bay, we observed an increase of a factor of 7 in dissolved methane under ice cover, compared to open-water conditions (Table 2). Tiksi Bay is part of Buor-Khaya Bay and via the central Laptev Sea perennially connected to the Arctic Ocean. Not much is known about tidal surge or water movement in Tiksi Bay under ice cover. It is anticipated that the ice cover on Tiksi Bay will lead to a decrease in tidal amplitudes and velocities (Fofonova et al., 2014). The structure of ice formation in Tiksi Bay also suggests that even in winter it is still an open system connected to the outer bay (Spangenberg et al., 2020). Sources of methane could be through diffusion of methane from the underlying sediment (Bussmann et al., 2017), where methane is produced by the degradation of organic material. However, as aerobic methane oxidation in the water column is impaired by low temperatures, methane concentrations in water increase.
In Lake Golzovoye, dissolved methane concentrations increased by a factor of 40 from summer to winter (Table 2). Lake Golzovoye is an isolated freshwater lake with presumably only a weak thermohaline circulation (Leppäranta, 2015; Spangenberg et al., 2020). A similar seasonal pattern of methane among lake waters of the Mackenzie Delta has been observed, ranging from very high concentrations at the end of winter beneath lake ice (
The role of water velocity and water column mixing is not clear, but our data suggest more methane accumulates under ice in a stagnant water body such as a lake than in a water body with running water such as a river. Water column turbulent diffusivity has a major influence on the methane cycle, where higher turbulence potentially leads to a greater proportion of methane being oxidized, and lower turbulence leads to a greater proportion being stored (Vachon et al., 2019).
The median methane concentration of all ice cores for Lake Golzovoye and Tiksi Bay was 9 nM, which was supersaturated compared to atmospheric concentrations, for which the equilibrium concentration would be 5 nM. More details on the ice formation in the different water bodies are given in Spangenberg et al. (2020). Compared to the methane concentrations in the water, the concentrations in the ice were 1–2 orders of magnitude lower (Table 2). This means that, in terms of methane, a complete separation of the water body from the atmosphere can be assumed. As mentioned earlier in this study and in Spangenberg et al. (2020), core no. 24 (LK-3) in Lake Golzovoye had much higher methane concentrations throughout the core and visible inclusions of (methane) bubbles. We assume that core no. 24 was located above an active ebullition site, which might have slowed ice formation and prolonged direct methane release to the atmosphere.
In the ice itself, 28 % of the samples showed methane oxidation capability. During ice formation most free-living bacteria are lost from the liquid phase through incorporation into the ice, while bacterial aggregates remain in the water (Santibáñez et al., 2019). In an experimental setup, Wilson et al. (2012) show that multiple freeze–thaw cycles in water from freshwater lakes reduce the total bacterial cell number at least 100 000-fold. In addition, methanotrophic bacteria are particular sensitive to freezing and thawing (Green and Woodford, 1992; Hoefman et al., 2012). These findings could explain the reduced activity of methanotrophic bacteria within the ice cores.
Also, we did not detect any discoloration or other indications of photosynthesis or other biological processes in the bottom layer of the ice cores. Thus, we conclude that the ecosystem of freshwater ice and its lower margin does not reach the richness observed in polar sea ice (Leppäranta, 2015).
In this study we determined the methane oxidation rate with tritiated methane as a tracer. The advantage of the tracer injection method is that natural low concentrations are hardly altered, and thus we assume that our values are close to the actual rates. The fractional turnover rate
Our data span 3 orders of magnitude, ranging from 0.02 nmol L
In previous years we determined MOX in the study area during summer, applying the same method as in this study. Therefore, we can approach a seasonal comparison (winter vs. summer), assuming interannual variability is negligible and neglecting spring and autumn mixing. To estimate the importance of ice cover on the overall MOX, we assume an ice coverage of 270 d for Lake Golzovoye and Tiksi Bay (Cortés and MacIntyre, 2020) and 160 d for the Lena River (Shiklomanov and Lammers, 2014). By multiplying the respective winter and summer MOX with the days of ice cover and days of open water, we can calculate the amount of methane oxidized during ice cover versus ice-off time.
For the Lena River and permafrost lakes, we compare our winter data with summer data obtained in July 2012 (Osudar et al., 2016). For the Lena River, with a median MOX of 22.8 nmol L
For MOX in lakes, summer rates from small lakes near Research Station Samoylov Island were 36 times higher (median 107 nmol L
For Tiksi Bay there are also summer values of MOX available (Bussmann et al., 2017). However, with a median summer rate of 0.419 nmol L
There still seems to be no clear consensus on the factors limiting MOX in winter. In several boreal lakes MOX was restricted to lakes where the phosphate concentrations were highest (Denfeld et al., 2016). Another study reports that in winter MOX is mainly controlled by the dissolved oxygen concentration, while in the summer it was controlled primarily by the methane concentration (Martinez-Cruz et al., 2015). The stratification of lakes determines the availability of methane and oxygen for the methanotrophic bacteria and thus strongly influences MOX (Kankaala et al., 2006, 2007).
Temperature is also an important factor affecting winter MOX. MOX is observed at temperatures of 2
Temperature dependence (
Environmental conditions between winter and summer conditions certainly differ and may also affect the population structure of methanotrophs. Some
psychrophilic strains adapt to colder temperatures (20
In this study we compared the methane inventory (concentrations) and the biological sink (methane oxidation) of three polar aquatic environments under summer and winter conditions. For a complete budget, the methane sources should be known, as there is methane input from the sediment, by either diffusion or ebullition and lateral input by groundwater, river flow, or water circulation in the bay. Additional sinks for the systems are methane flux from the water into the atmosphere and lateral output by water circulation. In the following we apply our results on the methane cycle of the three different environments.
In the river we find higher methane concentrations and higher MOX in summer. The low concentrations in winter are probably due to low methane input from the frozen borders and a reduced but still effective dilution of methane by the water flow (Fedorova et al., 2019). MOX is low and thus will not contribute to the removal of methane from the river. The ice-off on the river will probably not increase methane emissions, as only minor amounts are accumulated under the ice.
In the lake, we observed a strong accumulation of methane in winter under ice cover. Thus, either the methane sources are strengthened and/or the sinks have weakened. In winter there is an active cycle of methanogenesis and (anaerobic) methane oxidation in the sediment (Liebner et al., 2021). However, we assume that this activity is the same or less than in summer. Ebullition does occur in winter (as shown for ice core no. 24) and thus will lead to locally increased methane concentrations. The methane sink and flux from the water into the atmosphere is cut off by the ice cover; thus the only remaining sink is MOX, which is reduced by low temperature and other environmental factors as discussed above. During and after ice-off, altered or weakened water column stratification will allow a mixing of the water column. This results in increased methane emission but also enhanced MOX as more oxygen and nutrients will become available (Utsumi et al., 1998). In summer increased MOX and methane flux from the water lead to reduced methane concentrations in the water.
In the bay, we observed an accumulation of methane under ice and higher concentrations in winter. Thus, we assume that the sinks have weakened, with a stable or reduced methane input. Our comparison shows that MOX does not change significantly between the seasons; thus the other main sink, transport via water exchange of the bay with the shelf water, is reduced during winter because of the ice cover (Fofonova et al., 2014), and direct flux from open water is reduced by the ice cover. There is probably still an input of methane from the sediments, which results in a slight accumulation of methane. The ice-off in the bay will result in increased methane emissions and also reduced methane concentrations when water circulation in the bay restarts.
In a changing, warming Arctic, a shortened time of ice coverage on lakes and
rivers is predicted (Prowse et al., 2011; Newton and Mullan, 2020; Benson et al., 2012). This could be
Thus, an extended time of ice-free conditions could reduce the methane emissions from Arctic water bodies. However, it has to be kept in mind that not much is known about the MOX during water column mixing in spring or autumn.
Our work on an eastern Siberian lake, river, and marine bay showed that methane accumulates under ice cover during the winter and is consumed differently in the three water bodies. Our study was restricted to late winter and midsummer, which represent two extremes of the annual cycle. Other processes during autumn mixing, ice-on, and ice-off are not considered.
Two main physical factors affecting the methane cycle in the water bodies under ice cover are the water velocity and the ice cover itself. In most of our ice cores no concentration gradient between the bottom of the ice cores and the top was obvious. As we could hardly detect any MOX within the ice cores, we assume that methane is not integrated into the ice during freeze-up. Therefore, the ice cover seems to effectively prevent any methane flux from the highly accumulated methane concentrations in the water towards the atmosphere. In the river with running water under the ice cover, only a minor accumulation of methane was observed. In the bay with a restricted but still present water movement, dilution or mixing with other water bodies, allowed for a moderate accumulation of methane. In the small lake, we assume a stagnant water body with a subsequent accumulation of high amounts of methane.
The biotic counterpart of the observed methane accumulation is microbial
methane oxidation (MOX). In most cases, MOX in summer was much higher than
in winter. We observed a strong dependence of MOX on the temperature, and
with in situ temperatures of only 1
A shortened time of ice coverage on the water bodies is predicted with increasing temperatures in the Arctic. With respect to our study this would imply a shortened time for methane to accumulate below the ice and a shorter time for the less efficient winter MOX. Especially for lakes, an extended time of ice-free conditions could reduce the methane flux from the Arctic water bodies.
Data on methane concentration and MOX are available at the PANGAEA database (
All authors carried out fieldwork and measurements and collected samples. IB performed the methane and MOX analyses. IB, BJ, PPO, and MW contributed to the initial and final versions of the paper.
The authors declare that they have no conflict of interest.
This study was part of the Helmholtz program PACES, Topic 1.3. We are thankful to the logistics department of the Alfred Wegener Institute, particularly Waldemar Schneider. Logistical support for the fieldwork was provided by the Russian Hydrographic Service (Hydrobase Tiksi).
Matthias Winkel was supported by the Helmholtz Young Investigators Group of Susanne Liebner (VH-NG-919) and further supported by the German Ministry of Education and Research by a grant to Dirk Wagner (03G0836D). We acknowledge support by the Open Access Publication Funds of Alfred-Wegener-Institut Helmholtz-Zentrum für Polar- und Meeresforschung. The article processing charges for this open-access publication were covered by a Research Centre of the Helmholtz Association.
This paper was edited by Zhongjun Jia and reviewed by two anonymous referees.