PUBLICATIONS
Journal of Geophysical Research: Biogeosciences
RESEARCH ARTICLE
10.1002/2014JG002872
Key Points:
• Subarctic tundra was experimentally
warmed, thawed, and dried
• More old carbon was respired when
soils were thawed and dried
• Warming and thaw increased
methane emission
Supporting Information:
• Figures S1–S3 and Tables S1 and S2
Correspondence to:
S. M. Natali,
[email protected]
Citation:
Natali, S. M., et al. (2015), Permafrost
thaw and soil moisture driving CO2 and
CH4 release from upland tundra,
J. Geophys. Res. Biogeosci., 120, 525–537,
doi:10.1002/2014JG002872.
Received 25 NOV 2014
Accepted 18 FEB 2015
Accepted article online 22 FEB 2015
Published online 25 MAR 2015
Permafrost thaw and soil moisture driving CO2
and CH4 release from upland tundra
Susan M. Natali1, Edward A. G. Schuur2,3, Marguerite Mauritz2,3, John D. Schade1,4, Gerardo Celis2,3,
Kathryn G. Crummer2,5, Catherine Johnston6, John Krapek7, Elaine Pegoraro2,3, Verity G. Salmon2,
and Elizabeth E. Webb2
1
Woods Hole Research Center, Falmouth, Massachusetts, USA, 2Biology Department, University of Florida, Gainesville,
Florida, USA, 3Center for Ecosystem Science and Society, Northern Arizona University, Flagstaff, Arizona, USA, 4Biology
Department, St. Olaf College, Northfield, Minnesota, USA, 5School of Forest Resources and Conservation, University of
Florida, Gainesville, Florida, USA, 6School of Marine Sciences, University of Maine, Orono, Maine, USA, 7School of Natural
Resources and Extension, University of Alaska Fairbanks, Fairbanks, Alaska, USA
Abstract
As permafrost degrades, the amount of organic soil carbon (C) that thaws during the growing
season will increase, but decomposition may be limited by saturated soil conditions common in high-latitude
ecosystems. However, in some areas, soil drying is expected to accompany permafrost thaw as a result of
increased water drainage, which may enhance C release to the atmosphere. We examined the effects of
ecosystem warming, permafrost thaw, and soil moisture changes on C balance in an upland tundra ecosystem.
This study was conducted at a water table drawdown experiment, established in 2011 and located within the
Carbon in Permafrost Experimental Heating Research project, an ecosystem warming and permafrost thawing
experiment in Alaska. Warming and drying increased cumulative growing season ecosystem respiration by ~20%
over 3 years of this experiment. Warming caused an almost twofold increase in decomposition of a common
substrate in surface soil (0–10 cm) across all years, and drying caused a twofold increase in decomposition
(0–20 cm) relative to control after 3 years of drying. Decomposition of older C increased in the dried and in the
combined warmed + dried plots based on soil pore space 14CO2. Although upland tundra systems have been
considered CH4 sinks, warming and ground thaw significantly increased CH4 emission rates. Water table depth
was positively correlated with monthly respiration and negatively correlated with CH4 emission rates. These
results demonstrate that warming and drying may increase loss of old permafrost C from tundra ecosystems,
but the form and magnitude of C released to the atmosphere will be driven by changes in soil moisture.
1. Introduction
Increasing air temperatures across the Arctic (Intergovernmental Panel on Climate Change 2013) have
been associated with permafrost warming and thaw [Brown and Romanovsky, 2008; Jorgenson et al., 2006;
Romanovsky et al., 2010]. Permafrost extent is expected to continue to decline with future warming [Koven
et al., 2013; Lawrence et al., 2012; Schuur et al., 2013; Slater and Lawrence, 2013], which will move a significant
amount of carbon (C) from thermally protected to biologically available pools [Grosse et al., 2011; Harden
et al., 2012; Schuur et al., 2008, 2013]. As a result, C losses to the atmosphere are expected to shift the Arctic
from a C sink [McGuire et al., 2009] to a source by the end of the 21st century [Hollesen et al., 2011; Koven
et al., 2011; Schaefer et al., 2011], further amplifying climate change [MacDougall et al., 2012]. These
changes have already been detected experimentally [Natali et al., 2014, 2011; Welker et al., 2000] and
observed across Arctic tundra, where growing season C uptake has been increasing, but where, on an
annual basis, there is a net loss of C to the atmosphere [Belshe et al., 2013; Oechel et al., 1993; Trucco
et al., 2012].
The potential loss of permafrost C to the atmosphere may be driven not only by changes in temperature but
also by associated changes in soil hydrology. By restricting vertical water flow, permafrost maintains a perched
water table and saturated soils across the Arctic. As the permafrost surface deepens, surface water may drain
to deeper soil layers, reducing the extent of wetland areas in high latitudes [Avis et al., 2011]. Evidence from
lake drying studies suggests that water drainage will be most pronounced in the discontinuous permafrost
zone [Smith et al., 2005; Yoshikawa and Hinzman, 2003], where permafrost temperatures are close to thawing
[Osterkamp and Romanovsky, 1999]. Yet at the same time, permafrost thaw can increase soil moisture in lowland
NATALI ET AL.
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525
Journal of Geophysical Research: Biogeosciences
10.1002/2014JG002872
regions or as a result of localized ground slumping that results from melting ground ice. Even in upland
areas that may experience large-scale soil drying, localized ground subsidence can result in collapsed areas that
are saturated, interspersed with adjacent unsubsided and dryer areas [Jorgenson et al., 2001; O’Donnell et al.,
2012; Vogel et al., 2009]. These changes in soil moisture can further increase permafrost degradation as the
accumulation of surface water affects heat flux into soils and promotes increased thaw [Jorgenson et al., 2010;
Subin et al., 2013].
Changes in soil moisture are particularly important because soil moisture and temperature are the main
environmental drivers of tundra C exchange [Oberbauer et al., 2007; Oechel et al., 1998; Shaver et al., 2006]. In a
multiple-site comparison of International Tundra Experiment sites, Oberbauer et al. [2007] found that the
effect of warming on ecosystem respiration was dependent upon soil moisture. Sites that had the greatest
increase in ecosystem respiration with warming were the dryer sites, suggesting that well-drained areas
will be most responsive, in terms of C loss, to warming and ground thaw. However, in addition to the total
amount of permafrost C that may be released to the atmosphere as the climate warms, the form of C released
—CO2 or methane (CH4)—will be driven, in large part, by soil moisture changes [Christensen et al., 1997;
Kane et al., 2013; Olefeldt et al., 2013; Schuur et al., 2008[van Huissteden et al., 2011]]. As CH4 has 28–34-fold
larger global warming potential than CO2 on a 100 year time interval [Myhre et al., 2013], the effect of changes
in temperature and moisture on climate will be driven by the combined effect of CO2 and CH4 emissions
to the atmosphere.
Despite the recognized importance of temperature and moisture on C dynamics in northern ecosystems,
in situ moisture and temperature manipulation experiments are limited [Chivers et al., 2009; Oechel et al.,
1998; Olivas et al., 2010; Turetsky et al., 2008]. Previous research in lowland systems demonstrated that
water table drainage decreased gross primary productivity [Chivers et al., 2009] and increased ecosystem
respiration [Oechel et al., 1998; Olivas et al., 2010]. However, no studies have examined the combined effects
of permafrost thaw and soil moisture changes on ecosystem C dynamics in upland tundra, where permafrost
thaw will likely result in increased drainage [Smith et al., 2005], or in discontinuous regions, where complete
loss of permafrost is expected by the end of the 21st century [Slater and Lawrence, 2013]. In this study we
examined how these two key variables—temperature and moisture—affect ecosystem C balance in an
upland tundra ecosystem located in the discontinuous permafrost zone in Alaska. This work was conducted
within the Carbon in Permafrost Experimental Heating Research (CiPEHR) project, an ecosystem warming and
thawing experiment initiated in 2008, which was expanded in 2011 to include a water table manipulation
treatment. Previous work from CiPEHR demonstrated that, although warming increased the thawed C pool,
decomposition was restricted by anoxic soil conditions in the warmed plots, where ground subsidence
increased saturation [Natali et al., 2011]. We hypothesized that combined warming and drying will enhance
decomposition of soil C and decrease plant C uptake, leading to significant CO2 losses from the ecosystem.
However, we expected highest rates of CH4 emissions from the warmed plots, which have both deeper thaw
and increased soil saturation. Here we present growing season CO2 exchange from 3 years of experimental
warming and drying. We also measured soil and ecosystem 14CO2 to determine if potential C losses were driven
by recently fixed or older C sources. We implemented a common substrate decomposition experiment to
determine warming and drying effects on soil decomposition on an annual basis. Additionally, we measured
CH4 fluxes from the experimental plots after 1 and 3 years of combined warming and drying.
2. Methods
2.1. Site Description
The warming and drying (i.e., water table drawdown) experiment is located in the northern foothills of the
Alaska Range (~670 m elevation) in the region of Eight Mile Lake, Alaska (63°52′59″N, 149°13′32″W). The
experiment is situated on moist acidic tundra on a relatively well-drained gentle northeast facing slope.
Soils comprise an organic horizon, 0.35–0.45 m thick, above a cryoturbated mineral soil that is a mixture of
glacial till and loess. The active layer, which thaws annually during the growing season, reaches a maximum
depth of ~65 cm, below which is the perennially frozen permafrost layer. Air temperature (2004–2013)
ranges from a monthly average of 18.0 ± 1.8°C in January to 13.4 ± 0.5°C in July, with a mean annual temperature
of 2.7 ± 0.4°C. Average growing season precipitation (2004–2013) is 216 ± 24 mm. Vegetation at the site is
dominated by the tussock-forming sedge, Eriophorum vaginatum, and deciduous shrub, Vaccinium uliginosum.
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Journal of Geophysical Research: Biogeosciences
10.1002/2014JG002872
a
Table 1. Experimental Treatment Effects on Environmental Conditions (Average ± Se)
Ambient
Dry
Warm
Warm + Dry
103 ± 3
113 ± 2
102 ± 3
-
b
W
2011¯
W
2012¯
W
2013¯
2011
2012
2013
W
2011¯
W
2012¯
W
2013¯
W
2011¯
W
2012¯
W
2013¯
Snow Depth (cm)
22 ± 1
59 ± 3
76 ± 2
-
3.2 ± 0.3
4.0 ± 0.3
3.9 ± 0.3
Growing Season (May–September) Soil Temperature (°C)
3.5 ± 0.2
3.4 ± 0.4
4.2 ± 0.2
4.1 ± 0.4
4.2 ± 0.2
4.3 ± 0.3
3.8 ± 0.2
2.9 ± 0.4
1.4 ± 0.2
Winter (October–April) Soil Temperature (°C)
4.2 ± 0.1
2.3 ± 0.3
2.9 ± 0.3
1.2 ± 0.1
1.4 ± 0.2
1.0 ± 0.1
38.0 ± 1.0
44.3 ± 1.1
44.2 ± 0.9
Average Thaw Depth, June–Sept. (cm)
40.0 ± 1.1
43.8 ± 3.7
47.1 ± 2.0
53.2 ± 5.6
43.5 ± 1.9
49.8 ± 3.5
58.8 ± 1.4
60.3 ± 1.3
62.4 ± 1.8
Maximum Thaw Depth (cm)
55.9 ± 0.8
62.3 ± 5.3
62.0 ± 1.9
68.8 ± 6.1
63.6 ± 2.9
68.4 ± 4.3
23.3 ± 1.6
22.3 ± 1.7
23.5 ± 1.2
Water Table Depth (cm)
23.1 ± 1.6
19.9 ± 1.9
21.5 ± 1.7
16.5 ± 1.9
26.0 ± 1.6
21.0 ± 1.7
56.8 ± 3.2
46.3 ± 3.0
40.3 ± 1.8
Volumetric Soil Moisture, 0–20 cm (%)
48.5 ± 1.9
64.3 ± 3.9
43.9 ± 3.0
57.3 ± 5.7
37.4 ± 2.7
47.1 ± 3.4
c
3.5 ± 0.2
4.2 ± 0.2
4.3 ± 0.2
c
3.1 ± 0.4
1.5 ± 0.2
1.1 ± 0.2
42.6 ± 0.7
52.6 ± 2.0
50.4 ± 2.8
d
W
2011¯
W
2012¯
W
2013¯
57.8 ± 1.5
65.2 ± 2.9
71.5 ± 3.2
e
2011
W
2012
2013
22.8 ± 1.8
21.1 ± 1.2
23.2 ± 2.7
f
D
2011¯
D
2012
2013
47.3 ± 1.1
48.0 ± 2.3
42.4 ± 2.7
a
Superscript letters denote treatment differences as a result of warming and drying based on seasonal averages.
Underlined letters are alpha = 0.05, otherwise alpha = 0.1.
b
Recorded 18–21 April 2011, 14–17 April 2012, and 5 April 2013.
c
Averaged across 5, 10, 20, 40 cm depths.
d
Measured from 16 to 19 September in all years.
e
Distance from ground to water table surface; June to September.
f
Volumetric water content from 0 to 20 cm depth; June to September.
Other common vascular plants include Carex bigelowii, Betula nana, Rubus chamaemorus, Empetrum nigrum,
Rhododendron subarcticum, V. vitis-idaea, Andromeda polifolia, and Oxycoccus microcarpus. Nonvascular
plant cover is dominated by Dicranum sp., feather moss (primarily Pleurozium schreberi), and Sphagnum sp.,
as well as several lichen species (primarily Cladonia spp.) [Natali et al., 2012].
2.2. Experimental Design
The CiPEHR project, which was initiated in 2008, warms air and soil and thaws permafrost. Soil warming was
achieved using 1.5 m tall snow fences (8 m long; Figure S1a in the supporting information) that trap an
insulating layer of snow, resulting in 2–3°C warmer soil during the snow-covered months [Natali et al., 2011].
The six replicate fences were arranged in three experimental blocks. Just prior to melt out in spring, the
additional accumulated snow on the experimental plots was removed down to ambient levels to ensure
similar melt-out dates between warmed plots and control plots and to prevent excess moisture inputs to
the experiment. By ensuring similar melt-out dates between treatments, this experiment is not examining
the effects of changes in snow-free period on ecosystem C balance. The mean depth of the snowpack at the
time of snow removal was 52 cm in the control plots and 106 cm in the warmed plots (2011–2013; Table 1).
Plots were snow free by 1 May in 2011 and 2012 and by 1 June in 2013. Air warming was achieved using
0.36 m2 × 0.5 m tall open-top chambers (Figure S1b in the supporting information) that were placed on the
plots during the growing season (May to September in 2011–2012 and June to September in 2013). While
NATALI ET AL.
©2015. American Geophysical Union. All Rights Reserved.
527
Journal of Geophysical Research: Biogeosciences
a
10.1002/2014JG002872
b
Figure 1. (a) Diagram of experimental design showing one of six replicate snow fences containing combined warming and
drying plots (i.e., DryPEHR, black and white-filled rectangles). The dashed line marks the areal extent of the snowpack,
X denotes open-top warming chambers, and circles represent water wells. The grey squares represent experimental
plots from the CiPEHR project (not included in this study). The diagram is not drawn to scale. (b) Each drying plot contained
2–3 subplots; one was used exclusively for measuring (left ) CO2 fluxes and the other was used for other sampling including
14
(right) C and CH4 fluxes. The drying plot shown in this photo is a combined warming and drying treatment.
previous work at this site examined winter soil warming and growing season air warming both independently
and combined (CiPEHR), here we examine combined air and soil warming treatments only and their interaction
with drying (24 total plots, 6 per treatment). When we refer to warming in this study, we refer to combined
air and soil warming. Further description of the field site and warming experiment can be found in Natali et al.
[2011, 2012, 2014].
The water table drawdown experiment (“DryPEHR”) was established within the footprint of the CiPEHR
project (Figure S1c in the supporting information) in June 2011. At each of the six snow fences, we installed
two water table drawdown plots (+drying), so that each fence contained one of each treatment type:
ambient (no drying/no warming), dry (+drying/no warming), warm (no drying/+warming), and warm + dry
(+drying/+warming). Soil warming began in 2008 as part of the CiPEHR experiment, while air warming
and drying began in 2011. Each drying plot consisted of a 2.5 m × 1.5 m area, bordered by a metal sheet
inserted ~60 cm into the ground to the permafrost surface in order to reduce lateral water flow (Figure 1).
Each drying and control plot contained two or three subplots: one subplot contained soil temperature
and moisture sensors and was used for measuring CO2 fluxes, while the others were used for destructive
and other nondestructive samplings.
Water table drawdown was achieved using an automated pumping system, which was controlled by a
Campbell Scientific CR1000 data logger. The data logger actuated the pumping system by turning pumps
on/off based on water table depth, which was measured continuously by pressure transducers (Campbell
Scientific CS450) located in water wells inside and outside of the drying plots. Water table pumping began
in June once groundwater was thawed and ended when the water began to freeze in mid-September. In
early September, when nighttime temperatures were below 0°C, pumping only occurred during the day to
maintain functioning pumps and transducers. As a result, water table and soil moisture were variable in the
drying plots during periods in early and late growing seasons when freezing limited pumping.
2.3. Environmental Monitoring
An Onset HOBO (Bourne, MA) weather station, which was centrally located between the experimental plots
(~100 m distance), measured and recorded air temperature, rainfall, photosynthetically active radiation
(PAR), wind speed and direction, air pressure, and relative humidity. Growing season air temperatures
(2011: 9.4°C, 2012: 9.1°C and 2013: 9.3°C) were slightly lower than the 2004–2013 average (9.8°C ± 0.3°C).
Growing season precipitation in 2011 (164 mm) and 2013 (138 mm) were lower than the 10 year average
(216 mm), while 2012 precipitation (228 mm) was slightly higher. Plot-level air temperature was measured
at 15 cm from the ground surface in every flux chamber using negative temperature coefficient thermistors
and recorded to a Campbell Scientific CR1000 (Logan, UT) data logger.
NATALI ET AL.
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Journal of Geophysical Research: Biogeosciences
10.1002/2014JG002872
Soil temperature and moisture were recorded in half-hour intervals using Campbell Scientific CR1000
data loggers. Soil profile temperatures (5, 10, 20, 40 cm) were measured in each of the 24 flux plots using
constantan-copper thermocouples. Volumetric water content (VWC) was measured in all 24 flux locations
from the soil surface to 20 cm depth using site-calibrated Campbell CS615 and CS616 water content
reflectometer probes. Soil moisture is reported from June to September, which is the period when soils
were thawed down to 20 cm. Water table depth was measured from 1 to 3 times per week throughout
the snow-free period. Thaw depth (the thickness of unfrozen ground during the growing season) was
measured weekly in three locations just outside each flux plot using a metal depth probe.
2.4. Common Substrate Decomposition
We examined warming and drying effects on soil organic matter decomposition using a common
substrate, cellulose filter paper, which allowed us to determine how changes in the soil environment
affected decomposition, while holding substrate composition constant. The use of cellulose as a common
substrate also allowed us to compare our results to other studies [e.g., Pries et al., 2013]. The cellulose
decomposition bags measured decomposition at two depths—from 0 to 10 cm and from 10 to 20 cm.
Each bag was composed of four 7.5 × 5.0 cm pieces of Whatman P8 cellulose filter paper (Whatman,
Piscataway, NJ). The cellulose papers were weighed (0.3 g ± 0.01 g), arranged two by two so that there
were two subreplicates per bag at each depth and sealed in 2 mm fiberglass mesh cut to 21.0 × 13.5 cm.
Filters were corrected for initial water content using a subsample of five filters each day that decomposition
bags were prepared; these filters were weighed, then dried for 24 h at 60°C, and reweighed to obtain
moisture content, which was less than 3% of the filter weight. Bags were deployed in mid-September of
2011 and 2012 and left in the field for 1 year. After removal, the bags were rinsed to remove soil and frozen
for transport back to the laboratory, where bags were dried at 60°C for 24 h. We used paintbrushes and
fine-pointed tweezers to carefully remove soil and roots from the filter papers before measuring their final
weight to determine percent mass loss. Further description of the decomposition bag method can be found
in Pries et al. [2013].
2.5. CO2 Flux Measurements
Net ecosystem exchange (NEE) is a measure of the net flux of CO2 from an ecosystem and is the balance of
uptake of CO2 by primary producers (gross primary productivity, GPP) and loss via respiration (Reco). We
measured NEE and Reco, (NEE when PAR < 5 μmol m2 s1) and estimated GPP as the difference between
the two measured fluxes. While using nighttime or dark Reco measurements may impact Reco and GPP
estimates, these widely used methods are not expected to alter relative treatment responses nor have any
consequences for NEE. We use positive values of NEE to indicate net CO2 uptake by the ecosystem. We
measured NEE using three automated CO2 flux systems, each of which measured CO2 exchange from eight
flux chambers, that is, each of the three systems measured fluxes from all of the experimental plots at
two snow fences each. Automated measurements were collected every 1.5 h beginning the first week of
May (June in 2013) through the last week of September. Chambers measured CO2 fluxes continuously but
were rotated weekly off of this experiment because the automated system was used to monitor CO2
exchange at both CiPEHR (data not presented here) and DryPEHR. During periods when fluxes were not
measured, data were gap filled as described below. For flux measurements, air was circulated between
the CO2 chamber and an infrared gas analyzer (LI-820, LICOR Corp., Lincoln, Nebraska) at 1 L min1 for
1.5 min, and CO2 concentrations were measured at 1 s intervals. Flux data were recorded to a Campbell
Scientific CR1000 data logger. Further details about the automated flux system can be found in Vogel et al.,
2009 and Natali et al., 2011, 2014.
An empirical correction factor based on weather station PAR measurements was applied to account for
the effect of reduced light transmission through the flux chamber walls and light interception by the
chamber support structures. Automated flux measurements were filtered to remove estimates that
may have been biased by environmental conditions; measurements that occurred when wind speeds
exceeded >7 m s1 were removed because the fluxes were generally erratic (~5% of measurements).
Irregular fluxes due to known measurement error or equipment failure were also removed. A total of
~50,000 growing season CO2 flux measurements were used to parameterize CO2 flux models for the
C balance estimates.
NATALI ET AL.
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Journal of Geophysical Research: Biogeosciences
10.1002/2014JG002872
2.6. Growing Season CO2 Balance Calculations
Carbon balance during the growing season was estimated by gap-filling flux measurements using response
functions to environmental factors. Net ecosystem exchange was modeled using a hyperbolic equation
describing the relationship between NEE and PAR:
NEE ¼
ða PAR Gpmax Þ
Rd
½ða PARÞ þ Gpmax (1)
where α is the initial linear slope of the light response curve (quantum yield, μmol CO2 m2 s1), Gpmax is
the maximum photosynthesis (μmol CO2 m2 s1) at light saturation, and Rd is the dark ecosystem respiration
(i.e., NEE at PAR = 0). Parameters for equation (1) (α, Gpmax, Rd), which were obtained monthly (May through
September) for each of the 24 flux plots, were determined using univariate nonlinear regression using the least
squares method (SAS NLIN, SAS 9.0).
For growing season Reco, we used NEE measurements when PAR < 5 μmol m2 s1 to develop exponential
relationships between Reco and soil temperature (Ts, 10 cm depth):
Reco ¼ R expβ Ts
(2)
where R is the basal respiration and β is the rate of respiration change. Parameters for equation (2) (R, β)
were estimated for the growing season for each of the 24 flux plots using nonlinear regression with least
squares estimation (SAS NLIN).
2.7. Soil and Ecosystem Respiration Δ14CO2
The effects of warming and drying on the age of respired CO2 were determined by radiocarbon (Δ14C)
analysis of soil profile and ecosystem respiration. Respiration Δ14CO2 values reflect contributions from
decomposition of old C (i.e., before the 1950s bomb testing), which has negative Δ14C values, decomposition
of decadal-aged C with Δ14C values higher than atmospheric (i.e., postbomb C), and autotrophic respiration
with Δ14C values at, or slightly higher than, atmospheric (26‰ in 2013) due to respiration of recently fixed C.
Soil pore space Δ14CO2 was measured from gas samples collected during the first two weeks of August in
2011–2013 from permanently installed soil gas wells located in each plot at 10 and 20 cm depths. The gas
wells were made of stainless steel tubing (0.3175 cm ID), which was perforated and covered with mesh at
the bottom and extended aboveground 10 cm to fittings with gas-tight stopcocks. Air was pumped from
each gas well at 1.0 L min1 for 1 min through a 13X molecular sieve to quantitatively trap CO2. Ecosystem
respiration Δ14CO2 was measured at permanently installed 25 cm diameter PVC collars, which extended 8 cm
into the moss/soil layer. To collect gas samples, we sealed a 10 L chamber over each collar, and atmospheric
CO2 was scrubbed from the chamber by pumping chamber air through soda lime for 45 min while
maintaining CO2 concentrations at ~380 ppm to maintain ambient concentrations. Chamber air was
then pumped through a molecular sieve trap for 15 min. In the laboratory (University of Florida, UF), the
molecular sieve traps were heated to 625°C to desorb CO2. Carbon dioxide was then purified and analyzed
for δ13C and Δ14C. Graphitized samples were sent to UC Irvine W.M. Keck Carbon Cycle Accelerator Mass
Spectrometry Laboratory for Δ14C analysis, and δ13C was analyzed on a ThermoFinnigan continuous flow
isotope ratio mass spectrometer at UF. The 13C/12C isotopic ratios measured on the traps were used to correct
for atmospheric air in the gas wells and respiration chambers.
2.8. CH4 Flux Measurements
We measured CH4 fluxes from ambient, warm, and warm + dry plots in mid-August 2011 and early June and
early September 2013 using the PVC chambers used to sample Reco Δ14CO2, as described above. We did
not measure CH4 from dry plots that were not warmed because drying effect on water table in these plots
was minimal compared to ambient, where the water table was already below the ground surface. Four 20 mL
gas samples were collected with 30 mL syringes from each sealed chamber over a 30 min interval, and
each sample was transferred to a 20 mL overpressurized vial. Samples were analyzed for CH4 on an HP 5890
gas chromatograph equipped with a flame ionization detector and a molecular sieve 13X packed column.
Data were analyzed and quality controlled, using standard field and laboratory blanks, at Colorado State
University and University of Alaska Fairbanks. CH4 flux was estimated as the rate of change in concentration
over time, calculated from linear regression analysis.
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Journal of Geophysical Research: Biogeosciences
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2.9. Statistical Design and Analyses
Data were analyzed with a mixed linear model analysis of variance (ANOVA; PROC MIXED, SAS 9.0) using a
blocked split-plot design with warming and drying as main fixed factors and fence (unit of replication) as a
random factor, nested in block, which was also a random factor. Because the main factors (warming and
drying) were crossed, a significant warming effect refers to an effect of warming across drying plots, and
similarly, a significant drying effect refers to drying effects across warming plots. A warming/drying effect
that occurred specifically in one of the four treatments (e.g., warming + drying) would be detected by a
warm × dry interaction. We used repeated measure ANOVA to examine changes over the growing season and
between years with the additional variable month/yr and fence as the unit of replication for time effects. For
soil temperature, measurement depth was included as an additional fixed factor, nested within treatment
and fence. Growing season thaw depth values exclude May because plots were being installed in May 2011,
and in 2013, plots were not snow free until June. The following variables were log transformed for statistical
tests to meet the assumptions of normality: thaw depth, VWC, and winter soil temperature (translated
then logged). We performed ANOVAs on ranked data for 14C and CH4, because data were not normally
distributed after standard transformations. The sample size for main effects was six (i.e., number of replicates),
and we used Satterthwaite’s approximation to determine denominator degrees of freedom [Satterthwaite,
1946]. We used linear regression analysis to examine the relationship between water table depth and CH4
and CO2 emissions. Family-wise error rates (alpha = 0.05 significant; alpha < 0.10 marginally significant) were
controlled using Hochberg’s method for planned contrasts or Tukey’s method for all pair-wise comparisons.
All errors presented are 1 standard error of the mean.
3. Results
3.1. Environmental Variables
Winter soil temperatures were significantly higher in the warmed plots compared to control plots across
the 3 years of the experiment (F = 47.18, P < 0.001) and in each individual year (P < 0.05). However, the
magnitude of the treatment effects varied across years (warm x year, F = 13.08, P < 0.001) and corresponded
with interannual variation in snow depth and air temperature (Table 1). Winter soil temperatures
were higher in all depths in the warmed plots compared to control plots, but the warming effect was
greatest in deeper soils; soils were 45% warmer at 40 cm, 36% at 20 cm, 31% at 10 cm, and 30% at 5 cm
(warm × depth F = 4.23, P = 0.007). There was no detected effect of the drying treatment on winter
soil temperature and no significant warming or drying effects on growing season soil temperature. As
expected, there were significant main effects of depth and year on both growing season and winter soil
temperatures (P < 0.001).
While soil temperatures did not differ significantly during the growing season, experimental warming did
increase the depth of ground thaw. The average growing season thaw depth (2011–2013) was 14% deeper
in the warm plots compared to control plots (F = 15.06, P = 0.001), but there was no detected effect of
drying treatment on average ground thaw (P = 0.16; Table 1). As with average growing season thaw depth,
warming increased maximum thaw depth (i.e., active layer depth), and there was no detected effect of
drying on active layer depth (Table 1). Average growing season thaw depth varied significantly among
years (P < 0.001); 2011 was shallowest across treatments (41 ± 1 cm), followed by 2013 (47 ± 1 cm), with
deepest thaw in 2012 (49 ± 2 cm).
Water table depth tended to be shallower (closer to the ground surface) in the warm plots and deeper in
the dry plots (Table 1). Treatment effects on water table depth varied across months and years for both
warming (month interaction, 2012; F = 8.46, P < 0.001) and drying (month interaction, 2011: F = 4.39,
P = 0.007; 2013: F = 3.67, P = 0.02; Figure S2 in the supporting information). The effectiveness of the water
table manipulation was greater in the warmed plots, where the water table was lowered by 17% in warm
+ dry plots compared to those warmed without drying (2011–2013 growing season averages; Table 1).
As with water table depth, both drying and warming treatments significantly altered soil moisture. Across the
3 years of the experiment, soils were 13% wetter in the warm plots (F = 5.09, P = 0.03) and 14% dryer in the dry
plots (F = 7.19, P = 0.01) than their respective control plot treatments. The drying treatment significantly
decreased the average growing season soil moisture in 2011 (P = 0.005) and marginally decreased the soil
NATALI ET AL.
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Journal of Geophysical Research: Biogeosciences
10.1002/2014JG002872
moisture in 2012 (P = 0.07), but the
differences were not significant in
2013, when all soils were at their
driest (Table 1). Both warming and
drying effects varied across months
(warm × month, dry × month, and
warm × dry × month; P < 0.05), with
the greatest changes in soil moisture
in July and August (Figure S3 in the
supporting information).
3.2. Decomposition
Figure 2. Warming and drying effects on annual rates of decomposition
of a common substrate (cellulose) placed in soil at (a) 0–10 cm and
(b) 10–20 cm depths.
Cellulose decomposition was
significantly higher at 0–10 cm depth
(29 ± 3% annual mass loss) compared
to decomposition in 10–20 cm depth (21 ± 3% mass loss) (F = 11.14, P = 0.001). Warming increased
decomposition in 0–10 cm soil (0–10 cm; warm × depth, F = 3.88, P = 0.05), where mass loss was almost
twofold higher in warmed plots compared to ambient, and the drying treatment doubled cellulose
decomposition in 2013 across depths (dry × year; F = 3.66; P = 0.06) (Figure 2).
3.3. CO2 Flux
There was a significant drying and warming interaction effect on cumulative growing season Reco (warm × dry;
F = 6.98, P = 0.01; Figure 3). There were no detected differences in cumulative GPP or NEE (P > 0.10); however,
treatment effects on these fluxes varied across months and years (Table S1 in the supporting information).
In most months, Reco was higher in the dry plots, with significantly higher Reco in June and July of 2012
(P < 0.05) and 2013 (marginally significant, P < 0.10). There were no significant drying effects on CO2 fluxes
in 2011, which was the first year that the experiment was initiated. Across all years of the experiment,
monthly Reco and water table depth were positively correlated (R2 = 0.19, P < 0.001; Figure 4a); Reco was
higher when water table surface was deeper (i.e., dryer soils). Warming increased GPP and NEE in June
2012 (P < 0.05), and drying decreased NEE in July 2012 (F = 3.05, P = 0.09).
There was significantly older soil CO2 respired at 20 cm depth from experimentally dried soils compared
to ambient, particularly from soils that were both warmed and dried (Figure 5; F = 5.52, P = 0.03) (control:
2 ± 9‰; dry: 8 ± 14‰; warm: 1 ± 10‰; warm + dry: 23 ± 9‰). There were also significant interannual
differences in Δ14CO2 from 20 cm depth; in the driest year, 2013, Δ14CO2 was the most negative (28 ± 3‰),
followed by 2011 (2 ± 7‰), and 2012 (12 ± 5‰). There were no detected treatment or year effects on
Δ14CO2 from 10 cm wells or from ecosystem respiration, where Δ14CO2 was dominated by recently fixed
carbon (Reco: 27 ± 3‰; 10 cm wells: 9 ± 3‰; 20 cm wells: 8 ± 5‰; Table S2 in the supporting information).
3.4. CH4 Flux
Warming caused a significant increase in the rate of CH4 emissions to the atmosphere, but the warming
effect was offset when combined with drying. There was a significant warming effect in September 2013
Figure 3. Warming and drying effects on 3 year (2011–2013) average cumulative growing season (a) ecosystem respiration,
(b) gross primary productivity, and (c) net CO2 exchange (NEE). Monthly and annual fluxes can be found in Table S1 in
the supporting information.
NATALI ET AL.
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532
Journal of Geophysical Research: Biogeosciences
10.1002/2014JG002872
(F = 2.28, P = 0.05) and nonsignificant but similar
trends in August of 2011. There were no detected
treatment effects in June of 2013 when CH4 flux
across treatments was negligible (Figure 6). There
was a negative correlation between CH4 emissions
and monthly mean water table depth (R2 = 0.16,
P < 0.001; Figure 4b).
4. Discussion
4.1. Environmental Effects of the
Experimental Treatments
The experimental treatments significantly deepened
ground thaw and dried soils, resulting in an
increase in the amount of biologically available
organic C. The ~15% increase in ground thaw
caused by the warming treatment is in line with
changes expected across the Arctic in the coming
century. These changes are already underway in
this region [Osterkamp and Romanovsky, 1999;
Trucco et al., 2012] and across the Arctic, where
permafrost extent has been declining and active
layer depths have been increasing over the past
several decades [Jorgenson et al., 2006; Jorgenson
Figure 4. Relationship between water table depth (WTD;
et al., 2001; Quinton et al., 2011]. In upland areas,
distance below ground surface) and (a) monthly ecosystem
similar
to our study site, soil drying is expected to
respiration (Reco) for all growing season months from
2
accompany
permafrost degradation as a result of
2011 to 2013 (Reco = 1.2 × WTD + 41.2; P < 0.001, R = 0.19)
increased drainage in response to deepening of
and (b) CH4 emission rates measured in 2011 and 2013
2
(CH4 = 16.7 × WTD + 393.4; P = 0.003, R = 0.16). Note that
the water table [Hinzman et al., 2005; Yi et al., 2009].
higher water table values represent dryer soil conditions.
Widespread soil drying in the discontinuous zone
may already be occurring, but as soil drying is
less obvious than well-documented occurrences of lake drainage [Smith et al., 2005; Yoshikawa and
Hinzman, 2003], changes in soil moisture may be overlooked. While landscape-scale drying is one possible
outcome of permafrost thaw, localized ground subsidence that results from thawing of ice-rich permafrost
can also result in saturated soils in subsided zones [O’Donnell et al., 2012; Trucco et al., 2012; Vogel et al., 2009],
as occurred in the experimentally warmed plots in this study, which were ~15% wetter than control plots.
Increased soil moisture can also accelerate ground thaw because of soil moisture effects on thermal conductivity
[O’Donnell et al., 2009; Zona et al., 2012]. While we did not detect experimental drying effects on active
layer depth in this study, this may have been, in part,
a result of the size of the experimental plots or of the
limited and variable drying in the early and late parts of
the growing season.
Figure 5. Warming and drying effects on
collected from 20 cm soil pore space.
NATALI ET AL.
14
CO2
These experimental and observed changes in soil moisture
and ground thaw can have significant implications for
ecosystem C cycling. Previous research at this experiment
suggested that ground subsidence in the warmed plots
resulted in saturated, anoxic soils that may have limited
aerobic decomposition [Natali et al., 2011]. Therefore, we
hypothesized that combined warming and drying would
enhance decomposition of soil C more than warming
alone. Results from our common substrate decomposition
experiment show that while both warming and drying
increased decomposition, the combined treatments did not
enhance decomposition more than warming alone. There
©2015. American Geophysical Union. All Rights Reserved.
533
Journal of Geophysical Research: Biogeosciences
10.1002/2014JG002872
was a twofold increase in cellulose mass loss in surface
soils (0–10 cm) as a result of warming but no detected
warming effect in deeper soils (10–20 cm), which were
wetter and more often within the saturated zone below
the water table. Cellulose decomposition in 2013 was
twofold higher in the dry plots; however, unlike the
warming treatment, there was a significant treatment
effect across depths. These results differ from the
conclusions of Pries et al. [2013], a study conducted at
CiPEHR and at a nearby permafrost thaw gradient and
which suggested that decomposition will increase in
wetter soils. However, in that study, wetter soils were
associated with ground thaw so that wetter areas were
Figure 6. Warming and drying effects on rates of CH4
also warmer and more deeply thawed. As a result,
emissions. The positive flux represents flux to the
moisture effects in that study may have been confounded
atmosphere, and the negative flux is the uptake by
by increased temperature as well as by thaw effects on
the ecosystem.
nutrient availability [Natali et al., 2011] and microbial
biomass and community composition [Sistla et al., 2013], whereas in this study, moisture and temperature
were manipulated independently and in combination.
We expected that Reco would be highest in the warm + dry plots as a result of increased decomposition of
thawed C in oxic soil above the water table. Across all treatments, deeper water table depth (i.e., dryer soils)
was positively correlated with higher monthly Reco, and combined warming and drying did increase Reco
by 20%. However, both warming and drying treatments individually caused a similar increase in Reco, which
suggests that there may have been a trade-off between increased autotrophic respiration in the warm
plots versus an increase in heterotrophic respiration in the dry plots. An increase in heterotrophic respiration
was supported by soil pore space 14CO2, which was older in the dry plots, suggesting an additional input
of older microbial-respired CO2 when soils are dried; however, further dual-isotope analysis is needed to
partition Reco losses into multiple contributing sources [Pries et al., 2013].
The magnitude of the observed warming effect on Reco was similar to that observed at adjacent plots
within this experimental network (i.e., CiPEHR), where combined air and soil warming increased Reco by
25% after 3 years of warming [Natali et al., 2014]. However, in that previous study, air and soil warming also
increased GPP by 40%, whereas in this study the warming impact on GPP was less than 10%. As a result of
the limited GPP response, we saw no net change in CO2 uptake by the ecosystem during the growing season,
as has been observed in other tundra warming experiments [Lupascu et al., 2014; Natali et al., 2014]. The
lack of detected GPP response to warming in this study may have been driven, in part, by high variation
in plant composition among plots; GPP and NEE were significantly correlated with E. vaginatum biomass,
which was highly variable across the warming and drying plots, but not significantly affected by the experimental
treatments (data not shown). We also expected that drying would decrease plant C uptake as a result of water
stress, but vascular plants in the dried plots did not appear to be water stressed based on CO2 uptake, soil
moisture, and foliar δ13C (data not shown) results.
Upland tundra have been shown to be CH4 sinks with occasional pulse releases of CH4 during wet periods
[Jørgensen et al., 2015; Whalen and Reeburgh, 1990]; however, ground subsidence associated with permafrost
thaw may shift some upland areas to CH4 sources [Nauta et al., 2015], as was found in our warmed and thawed
plots. This observed increase in CH4 emission rates was likely a result of changes in both methanogenesis
(CH4 production) and methanotrophy (CH4 consumption). In this upland ecosystem, methanogenesis, which is
an anaerobic process, occurs in subsided areas and in the saturated zone at the base of the active layer. Our
experimental warming treatment increased the volume of thawed and saturated soils by 33%, likely supporting
the increased CH4 production. At the same time, since the water table in the warmed plots was closer to the
ground surface, the amount of CH4 consumed by methanotrophic bacteria/archaea was likely reduced alongside
the reduction in the volume of oxic soils. The increase in CH4 emissions was driven, in part, by shallower water
table but may also have been driven by increased inputs of labile C [Olefeldt et al., 2013; Strom et al., 2005, 2003]
and changes in methanogen communities that accompany thaw [Mondav et al., 2014].
NATALI ET AL.
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534
Journal of Geophysical Research: Biogeosciences
10.1002/2014JG002872
In contrast, in the warmed plots that were also dried, a larger proportion of CH4 produced in the saturated zone
was likely oxidized in surface soil before reaching the atmosphere [Chowdhury and Dick, 2013; Sturtevant et al.,
2012]. A warmer climate with dryer soils would therefore decrease CH4 flux to the atmosphere or increase
CH4 uptake; however, saturated pockets of subsided ground may serve as CH4 sources. Substantial increases in
CH4 emissions have been observed as a result of ground subsidence and ground thaw in lowland ecosystems
[Christensen et al., 2004; Johnston et al., 2014; Klapstein et al., 2014; Turetsky et al., 2002; Wickland et al., 2006].
As shown here, these subsided zones are also important sources of CH4 in upland ecosystems. While our
experimental treatment has not yet altered plant community composition, plant composition is an important
driver of ecosystem carbon emissions, and particularly so for CH4 fluxes, because vascular transport of CH4
by sedges allows for CH4 to bypass the oxic soil zone [King et al., 1998; Schimel, 1995; Verville et al., 1998].
Ongoing monitoring of the plant community is needed to determine interactions between plant community
shifts and changes in soil moisture and ground thaw. Finally, while this experiment uses snow addition as a
tool for insulating soils in the winter, we did not examine how changes in snow duration will impact
ecosystem CO2 exchange. Snowmelt has occurred earlier across the Arctic [Euskirchen et al., 2007], and
snow duration is expected to continue to decline as the climate warms [Christensen et al., 2013], which may
result in a marginal increase in net CO2 uptake during the early snow-free season. Despite these additional
expected ecosystem responses that were not measured in this study, our results highlight the importance of
understanding thaw-induced landscape changes on the balance between pooling and drained areas and
implications for net CH4 and CO2 exchange.
5. Summary and Conclusions
Experimental warming resulted in significantly deeper thaw depths and water table drawdown-caused dryer
soils during the growing season, and these environmental changes significantly impacted C cycling. As
expected, warming and drying increased ecosystem respiration and common substrate decomposition
and resulted in older CO2 respired from soils. We also expected that drying would decrease plant C uptake,
leading to significant CO2 losses from the ecosystem. We did not see the expected decline in plant C
uptake in the dry plots, suggesting that the drying treatment did not induce water stress or impact leaf
gas exchange. While this upland ecosystem has been considered a CH4 sink, we detected CH4 emissions
from all plots, and the warmed plots, which were also wetter, had significantly higher rates of CH4 release.
Future efforts should focus on obtaining higher-resolution CH4 data and determining if these results
are applicable to tundra ecosystems arctic-wide. These results highlight the importance of changes in
ground thaw and soil moisture on both the magnitude of C losses as well as the form of C released as
permafrost thaws.
Acknowledgments
This work was supported by NSF OPP
grants 1312402 and 1019324 to Natali,
DOE award SC0006982 to Schuur,
Denali National Park fellowship to
Schade, and NSF LTER grant 1026415.
We thank two anonymous reviewers for
their input on the manuscript; S. Dunn,
T. Harms, J. Jones, and J. von Fischer for
CH4 laboratory analysis; and C. Pries,
A. Baron Lopez, C. Trucco, J. Hollingsworth,
and BNZ LTER for research assistance
and logistics support. Data for this
paper are freely available at Bonanza
Creek LTER Web page: http://www.lter.
uaf.edu/data.cfm.
NATALI ET AL.
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