Global Change Biology (2012), doi: 10.1111/j.1365-2486.2012.02770.x
High arctic heath soil respiration and biogeochemical
dynamics during summer and autumn freeze-in – effects
of long-term enhanced water and nutrient supply
C A S P E R T . C H R I S T I A N S E N * , S A R A H H . S V E N D S E N * , N I E L S M . S C H M I D T † and
ANDERS MICHELSEN*‡
*Physiological Ecology Group, Terrestrial Ecology Section, Department of Biology, University of Copenhagen, Universitetsparken
15, DK-2100, Copenhagen Ø, Denmark, †Department of Bioscience, Aarhus University, Frederiksborgvej 399, 4000, Roskilde,
Denmark, ‡Center for Permafrost, University of Copenhagen, Øster Voldgade 10, DK-1350, Copenhagen K, Denmark
Abstract
In High Arctic NE Greenland, temperature and precipitation are predicted to increase during this century, however,
relatively little information is available on the role of increased water supply on soil CO2 efflux in dry, high arctic ecosystems. We measured soil respiration (Rsoil) in summer and autumn of 2009 in combination with microbial biomass
and nutrient availability during autumn freeze-in at a dry, open heath in Zackenberg, NE Greenland. This tundra site
has been subject to fully factorial manipulation consisting of increased soil water supply for 14 years, and occasional
nitrogen (N) addition in pulses. Summer watering enhanced Rsoil during summer, but decreased Rsoil in the following
autumn. We speculate that this is due to intensified depletion of recently fixed plant carbon by soil organisms. Hence,
autumn soil microbial activity seems tightly linked to growing season plant production through plant-associated
carbon pools. Nitrogen addition alone consistently increased Rsoil, but when water and nitrogen were added in
combination, autumn Rsoil declined similarly to when water was added alone. Despite several freeze-thaw events, the
microbial biomass carbon (C) remained constant until finally being reduced by ~60% in late September. In spite of significantly reduced microbial biomass C and phosphorus (P), microbial N did not change. This suggests N released
from dead microbes was quickly assimilated by surviving microbes. We observed no change in soil organic matter
content after 14 years of environmental manipulations, suggesting high ecosystem resistance to environmental
changes.
Keywords: carbon pools, CO2 emission, freeze-thaw, gas flux, global change, Greenland, microbial activity, nutrient availability,
soil respiration, tundra
Received 19 October 2011 and accepted 26 April 2012
Introduction
Global circulation models (GCMs) predict warming
and increased precipitation in arctic and boreal regions
(ACIA, 2005; IPCC, 2007; Stendel et al., 2008)
throughout the 21st century. In tundra and boreal forests, large amounts of organic matter have accumulated in soils, with between a third to half of global
soil carbon (C) stock stored here (Post et al., 1982; Tarnocai et al., 2009). Soil temperature and moisture are
principal factors determining heterotrophic soil activity
(Nadelhoffer et al., 1991) and there is considerable concern that climatic changes may enhance soil organic
matter decomposition, increasing release of CO2 to the
atmosphere. Despite long and cold winters in arctic
Correspondence: Casper T. Christiansen, Department of Biology,
Queen’s University, Biosciences Complex, 116 Barrie Street,
Kingston ON K7L 3N6, Canada, e-mail: [email protected]
© 2012 Blackwell Publishing Ltd
and boreal ecosystems, substantial microbial activity
continues beyond the warm growing season and
throughout the entire cold season (e.g. Clein & Schimel, 1995; Oechel et al., 1997; Fahnestock et al., 1998;
Grogan & Chapin, 1999; Jones et al., 1999; Welker et al.,
2000; Schimel et al., 2004; Elberling, 2007). With an arctic non-growing season lasting 9–10 months, ecosystem
carbon sequestration in summer may be offset by
cumulative soil CO2 efflux during autumn and winter
(Zimov et al., 1996; Oechel et al., 1997; Fahnestock
et al., 1998, 1999; Grogan & Chapin, 1999; Jones et al.,
1999; Welker et al., 2000; Schimel et al., 2004). As a
result, tundra ecosystems may indeed perform as net
carbon sinks during summer whereas they are infact
net carbon sources when viewed over the course of a
full year (Oechel et al., 2000). Summer soil CO2 efflux
comes primarily from root respiration and soil microbial decomposition of recently fixed plant C (i.e. plant
litter and root exudates) (Hobbie et al., 2000) whereas
1
2 C . T . C H R I S T I A N S E N et al.
soil respiration (Rsoil) in frozen soils is more complex
and poorly understood; microbes appear to rely less
on detritus decomposition and more on soluble substrate (Clein & Schimel, 1995; Michaelson & Ping, 2003;
Schimel et al., 2004) remaining in unfrozen water films
surrounding soil particles (Oquist et al., 2009; Tilston
et al., 2010). Due to relatively high soil temperatures
and an active layer near its maximum extent (Olsson
et al., 2003), autumn Rsoil has the highest flux rates of
the cold season (e.g. Zimov et al., 1996; Oechel et al.,
1997), yet this period of year has been largely
overlooked regarding investigations into arctic biogeochemistry.
Predictions indicate that temperature and precipitation changes will be most pronounced during autumn
and winter in the Arctic (ACIA, 2005; IPCC, 2007;
Stendel et al., 2008). This emphasizes the need to fully
understand the processes controlling soil C dynamics
both during the growing season and beyond if we want
to develop adequate models of annual net ecosystem C
balance. For instance, enhanced decomposition and soil
respiration following increased soil water availability
have been reported for dry high arctic ecosystems during summer (Robinson et al., 1995; Illeris et al., 2003),
but we currently do not know if these responses in the
microbial community continue during the autumn
freeze-in period. It appears, though, that a marked shift
from summer microbial nitrogen (N) immobilization
(Jonasson et al., 1999) to winter net N mineralization in
alpine (Brooks et al., 1996), subarctic (Grogan &
Jonasson, 2003) and arctic (Schimel et al., 2004) soils
takes place. This may be of great importance for plant
productivity in the following growing season due to N
limitations of arctic ecosystems (e.g. Shaver & Chapin,
1980; Chapin & Shaver, 1985).
During the autumn freeze-in period, as air temperatures fluctuate around zero, soils are exposed to several
freeze-thaw cycles (FTCs), which may result in pulses
of increased soil respiration (Skogland et al., 1988;
Schimel & Clein, 1996) and changes in soil nutrient
levels and microbial biomass (Skogland et al., 1988;
Schimel & Clein, 1996; Brooks et al., 1998; Lipson et al.,
1999; Larsen et al., 2002, 2007; Grogan et al., 2004). This
happens as a fraction of the microbial community is
killed and surviving cells assimilate the released compounds as labile nutrients. However, other studies have
reported subtle or no effects of FTCs on soil microbial
communities (Lipson et al., 2000; Grogan et al., 2004;
Sjursen et al., 2005; Mannisto et al., 2009), although, the
apparent inconsistencies in FTC results may be, to some
extent, attributed to differences in experimental
methodology (see review by Henry, 2007).
In this study, we investigate soil biogeochemical
dynamics in a high arctic dry heath during summer
and autumn freeze-in. Soil respiration was measured
from July to October 2009 to compare growing season
and autumn effluxes, and we further examined fluctuations in soil nutrient availability and microbial biomass in autumn. To simulate effects of increased
summer precipitation, which is expected in climate
models for NE Greenland for this century (Stendel
et al., 2008), and enhanced soil nutrient availability
due to warming (Hobbie & Chapin, 1998), the study
site has been subject to long-term (14 years) manipulation consisting of increased water supply and
occasional nitrogen (N) addition in pulses. We
hypothesized that increased water addition would
enhance microbial biomass and activity (Illeris et al.,
2003). Fertilization was hypothesized to stimulate
plant production and enhance root exudation, increasing microbial activity indirectly, and to lead to a subsequent slow release of N from dying microbes
(Sorensen et al., 2008).
Materials and methods
During 2009, soil respiration was measured from 6 July to 6
October combined with soil biogeochemical measurements
from 1 September to 7 October in the Zackenberg Valley, NE
Greenland (74°30′ N, 21°00′ W). Annual mean temperature is
7.8 °C and annual mean precipitation is approximately
261 mm, mainly ( 84%) falling as snow (1996–2005 averages,
Hansen et al., 2008). The study site is an arid lowland dry
open heath/semi desert situated approximately 300 m south
of the Zackenberg Research Station on gravel mineral soil.
Due to wind exposure and dry soil conditions, plant cover is
less than 50%, dominated by the dwarf shrub Dryas octopetala 9 integrifolia and with graminoids such as Kobresia myosuroides, Carex rupestris, and Poa glauca (Illeris et al., 2003).
Experimental setup
The experimental setup was comprised of six blocks each
containing four plots of 0.5 9 0.5 m with four randomized
treatments; control, water addition, N amendment, and combinations hereof. The original setup also included factorial
phosphorus (P) addition (Illeris et al., 2003), but plots with P
amendment were excluded from measurements and sampling in the present study. The plots have been watered
weekly during the growing season since 1997, combined with
nitrogen amendment in 1996, 1997 and 2007. The rate of fertilizer added was 3.75 g N m 2 (added as NH4NO3) in each of
the three amendment years. Water addition consisted of 2 L
of water added weekly during July and August, corresponding to an additional supply of 8 mm of precipitation weekly
per plot, which is roughly equivalent of twice the natural
occurring precipitation during the growing season (Hansen
et al., 2008). In 2009 summer watering was extended until
September 11th due to a prolonged period with daytime
temperatures above 0 °C.
© 2012 Blackwell Publishing Ltd, Global Change Biology, doi: 10.1111/j.1365-2486.2012.02770.x
HIGH ARCTIC BIOGEOCHEMICAL DYNAMICS 3
Soil respiration measurements
In 1996, 23 cm long cylindrical PVC chambers (diameter = 10.2 cm; area = 0.008 m2) were inserted 10 cm into the
ground in each plot (Illeris et al., 2003). Headspace volumes
were measured prior to the study and were approximately 1 L.
To secure that only soil respiration (Rsoil) was measured, the
chambers were placed in areas without aboveground vegetation, allowing for measurements of respiration stemming solely
from soil microbial and faunal heterotrophic respiration and
roots. An EGM-4 Environmental Gas Monitor (PP Systems, Hitchin, United Kingdom) was used to measure weekly soil CO2
efflux (6 July–6 October) when connected to chambers via plastic tubes through an airtight PVC lid. The EGM-4 was kept at
operational temperature by using a thermal insulating, heated
polystyrene box. From 6 July to 16 September CO2 concentration was logged every 20 s for a duration of 2 min, while later
measurements (21 September–6 October) were performed with
intervals of 60 s for a duration of 5–10 min due to reduced soil
CO2 emission. Soil CO2 efflux was calculated based on linear
increases in chamber headspace CO2 concentrations using SAS
9.1 (SAS Institute 2003). The EGM-4 was fitted with an internal
humidity sensor and automatically corrected CO2 concentrations for increases in water vapour (Hooper et al., 2002). When
small patches of snow were present inside chambers, volume
and density of snow were measured to correct for loss of air volume inside the chambers. Snow inside chambers was only
apparent in October and constituted on average less than 4% of
total chamber volume. Snow removal may initiate CO2 flux
from the soil that is non-representative of actual CO2 production, i.e. a chimney effect (Grogan et al., 2001; Grogan & Jonasson, 2006; Björkman et al., 2010), and therefore snow was not
removed from plots during this study. Snow cover was always
blown away by wind from the treatment plots within a couple
of days, except for block one which consequently was omitted
from the study after 26 September.
Microclimate
When measuring soil respiration, soil temperatures were
measured using a handheld digital thermometer. Furthermore,
a Tinytag Plus 2 model TGP-4020 (Gemini Data Loggers,
Chichester, United Kingdom) fitted with an external temperature probe was inserted 5 cm into the ground adjacent to the
experimental setup, allowing for hourly soil temperature
recordings from 6 September and onwards. Photosynthetically
active radiation (PAR) and air temperature data were obtained
from the nearby meteorological weather station (Jensen &
Rasch, 2010). Soil moisture, integrated over 0–6 cm depth, was
determined using a Theta probe (6 July–7 September) until soil
freezing inhibited using the probe.
wanted to limit destructive soil sampling. Roots were
removed by hand sorting and soil samples were subsequently
sifted through a 2 mm sieve to remove stones. Gravimetric
soil moisture content was determined by drying subsamples
(10 g) at 80 °C for 48 h. Fine roots (diameter <1 mm) were
washed and dried as above to determine dry weight. Soil
organic matter (SOM) content was estimated by loss on ignition when burned at 550 °C for 6 h. All fresh soil samples
were homogenized and stored at 5 °C for no more than 2 days
before subsamples were exposed to the fumigation-extraction
method (Brookes et al., 1985); fresh soil (10 g) was vacuum
incubated with ethanol-free chloroform (CHCl3) for 24 h, after
which the soil was extracted for 6 h with 50 mL of deionized
water, to release soil microbial content of C (MBC), N (MBN)
and P (MBP). Another 10 g of fresh soil was extracted as
above, but without fumigation, to recover soil inorganic N
and P and dissolved organic C (DOC) and N (DON). Blanks
without sample were included to detect contamination during
extraction and filtration. All extracts were filtered through
Whatman GF-D (pore size 2.7 lm) glass microfiber filters
(Whatman Ltd.; Maidstone, UK) and immediately frozen at
18 °C until further analyses.
All extracts were analyzed for DOC using a TOC-5000A
total organic analyzer (Shimadzu, Kyoto, Japan). To determine inorganic NH4+-N and NO3 -N concentrations, nonfumigated extracts were analyzed colometrically with a FIA
STAR 5000 flow injection analyzer (FOSS Tecator, Höganäs,
Sweden). Total dissolved N (TDN) was determined for all
extracts with the FIA STAR 5000. Total dissolved P (TDP)
was measured in both fumigated and non-fumigated
extracts with FIA STAR 5000. DON was calculated as TDN
in digested, non-fumigated samples minus inorganic N in
undigested, non-fumigated samples. MBC, MBN, and MBP
were estimated as the difference between C, N, and P contents of fumigated vs. non-fumigated samples (Brookes
et al., 1985). To correct for incomplete extractability, a conversion factor (KEC) of 0.45 was used for MBC (Joergensen,
1996), and a factor of 0.4 for MBN (KEN) and MBP (KEP)
(Jonasson et al., 1996). Total soil (all plots) and root (control
plots) content of N and P were measured spectrophotometrically after acid digestion.
Soil depth profile
To investigate deep soil biogeochemistry a depth profile
(D 9 W 9 L = 70 9 35 9 35cm) was dug adjacent to the
experimental setup on 10 September. The soil was divided
into 5 cm horizons and six replicate samples were obtained
from each horizon to a depth of 60 cm. No roots were encountered below 60 cm. Soil samples were obtained, treated and
analyzed as above, but without fumigation-extraction.
Nutrient availability and microbial biomass
Data treatment
Soil samples were only collected from 1 September to 7
October using a soil corer (length = 5 cm; diameter = 4 cm).
No soil samples were taken during summer as our focus was
on autumn soil biogeochemical dynamics and because we
All statistical analyses were conducted using SAS v.9.1 (SAS
Institute, 2003). Prior to analysis, data were tested by visual
inspection of distributions. Where necessary, data were transformed (log or square root transformation) to achieve variance
© 2012 Blackwell Publishing Ltd, Global Change Biology, doi: 10.1111/j.1365-2486.2012.02770.x
4 C . T . C H R I S T I A N S E N et al.
homogeneity. After analysis, model validity was tested by
visual inspection of the distribution of residuals and residuals
plotted against predicted values. None of these indicated
faulty outliers or deviations from the assumptions of
normality.
Pearson product moment correlation analyses were performed between Rsoil and air and soil temperatures and
selected soil nutrient and microbial variables (using only
control plots). To test for treatment effects repeated measures linear mixed model analyses (RM LMM) were performed using PROC MIXED with nitrogen addition (N),
water addition (W), and interaction (WN) hereof included as
fixed main effects. Day of year was set as repeated factor
with subject set to Plot. Day of year was also used as linear
covariate with fixed effects interactions in the soil respiration
analysis. Covariance structure was determined by the twomodel fit criteria AIC-output from PROC MIXED (Littell
et al., 1996). Tukey’s test was used to test for significant differences (P < 0.05) between measurement dates (control plots
only) regarding soil nutrient availability and microbial biomass.
Soil respiration rates (control plots only) were related to
air temperature throughout the study period using the classic van’t Hoff first-order exponential relationship to quantify summer and autumn soil CO2 efflux (Grogan &
Jonasson, 2005). The model corresponds to the following
equation: Soil respiration = a expbT, where soil respiration is
the measured daytime rate, a and b are fitted constants,
and T is air temperature (°C). To estimate the magnitude of
circumpolar high arctic dry heath soil CO2 efflux, we
obtained areal extent data from Bliss & Matveyeva (1992)
and from the Arctic Circumpolar Vegetation Map (Walker
et al., 2005). From Bliss & Matveyeva (1992) we used their
definition of high arctic semi deserts (estimated cover:
1005 9 106 km2, which is the equivalent of 18% of the total
ice-free landmasses in the Arctic). Walker et al. (2005) provided us with areal data on prostrate dwarf shrub vegetation (map unit P1) in the high arctic vegetation subzones A,
B, and C (estimated cover: 269 9 106 km2, corresponding to
5.3% of the total non-glacier Arctic).
The soil depth profile data were analyzed using one-way
ANOVA’s with depth as factor. P-values less than 0.05 are
considered significant, and only significant differences and
tendencies (0.05 < P 0.1) are reported.
Results
Environmental conditions
Mean air temperatures for July, August and September
were 8.6 °C, 4.6 °C, and 2.3 °C, respectively (Fig. 1),
slightly warmer than the 1996–2005 averages reported
for the Zackenberg area (Hansen et al., 2008). From 1
July to 10 October a total of 109 mm precipitation was
recorded. July and August each received twice the
average precipitation while September received three
times the average (Hansen et al., 2008). All precipitation
from September and onward fell as snow. Incoming
photosynthetically active radiation (PAR) peaked in
July and generally continued to decline throughout late
summer and autumn (Fig. 1).
Local soil conditions
Soil temperatures at 2 and 5 cm depth ranged from
23.1 °C to 9.8 °C and 20 °C to 6.5 °C, respectively
(Fig. 1), with no significant differences between treatments. TDR soil moisture (6 July–7 September,
Fig. 2a) and gravimetric soil moisture (2 September–
30 September, Fig. 2b) was significantly higher in
watered treatments (RM LMM; F1,14 = 50.87, P <
0.001 and F1,38.9 = 9.02, P < 0.01, respectively). Soil
pH was 7.25 ± 0.04 (control plots, n = 6 ± SE) and
was slightly but significantly lower in nitrogen-added
plots
(pH = 6.99 ± 0.06
SE)
(two-way
ANOVA;
F8,15 = 9.18; P < 0.01). During autumn, fine root biomass decreased to approximately ¼ of the initial biomass (Fig. 3a) with no overall treatment effects. Root
N and P concentrations increased from 2 to 20
September and declined thereafter (Fig. 3b and c,
respectively).
Soil respiration
Soil respiration rates (control plots only) were generally around 0.13 g CO2 m 2 h 1 throughout July and
August before declining to 50% on 1 September. During the freeze-in period in September and October,
Rsoil was reduced by more than 95% compared to
summer rates (Fig. 4). We found strong positive relationships between Rsoil and air temperature (control
plots; rp = 0.91; n = 72; P < 0.0001), soil temperature
at 2 cm depth (rp = 0.92; n = 72; P < 0.0001) and at
5 cm depth (rp = 0.93; n = 72; P = 0.0001). Autumn
soil respiration correlated with MBC (rp = 0.39;
n = 24; P = 0.05) and marginally correlated with DON
(rp = 0.31; n = 34; P = 0.08), but did not correlate with
MBN, DOC or soil moisture. During summer and
autumn, an RM LMM revealed significant effects of
water addition (F1,93.1 = 6.64; P = 0.01), day of year
(F1,93.2 = 612.90; P < 0.0001), and the interaction
between day of year and water addition (F1,93.2 = 6.49;
P = 0.01) as well as a tendency for an interaction
between water addition and nitrogen amendment
(F1,60 = 3.30; P = 0.07). Respiration rates (control plots)
were related to air temperature, using a first-order
exponential relationship: Rsoil = 0.0444 9 e0.0824 9 T,
where T is air temperature (F1,70=141.0; r = 0.82;
P < 0.0001). Modelled CO2 lost during summer (1 July
–14 August) amounted to 96 g CO2 m 2 whereas
autumn losses (15 August–1 October) amounted to
© 2012 Blackwell Publishing Ltd, Global Change Biology, doi: 10.1111/j.1365-2486.2012.02770.x
HIGH ARCTIC BIOGEOCHEMICAL DYNAMICS 5
Fig. 1 Hourly mean of air temperature (gray line), daytime mean soil temperature at 2 cm depth (open circles, n = 24 ± SE), hourly
mean of soil temperature at 5 cm depth (black line), mean daytime (09:00–17:00) photosynthetically active radiation (PAR) (dotted line)
and precipitation (open bars) from 1 July–10 October at Zackenberg, NE Greenland. Dashed line indicates 0 °C. The soil temperature
probe at 5 cm depth was covered in 30 cm of snow from 26 September and onward.
(a)
(b)
Fig. 2 Mean soil moisture a) measured by TDR-probe and b) measured gravimetrically in summer and autumn 2009 at Zackenberg,
NE Greenland. Treatments are C-control, N-nitrogen amendment, W-water addition and combination thereof (n = 6 ± SE). Results of
repeated measures linear mixed model analyses of watering on soil moisture are shown above bars as: **P 0.01.
52 g CO2 m 2. Using data from Bliss & Matveyeva
(1992) and Walker et al. (2005), we calculated circumpolar High Arctic open dry heath tundra summer soil
CO2 efflux amounting to 96 and 26 gigatonnes (1 9
1012 kg), whereas autumn soil CO2 efflux was 52 and
14 gigatonnes, respectively.
© 2012 Blackwell Publishing Ltd, Global Change Biology, doi: 10.1111/j.1365-2486.2012.02770.x
6 C . T . C H R I S T I A N S E N et al.
(a)
(b)
(c)
(d)
(e)
(f)
(g)
(h)
(j)
(k)
(i)
(l)
Fig. 3 Root biomass (a); root N (b) and P (c) content; soil NO3 (d) and NH4+ and (e); dissolved organic N (DON) (f), dissolved P
(TDP) (g) and dissolved organic C (DOC) (h); soil microbial C (MBC) (i), microbial N (MBN) (j), microbial P (MBP) (k) and microbial
C : N ratio (l) during the 2009 autumn freeze-in period at Zackenberg, NE Greenland (control plots, n = 6 ± SE). Soil microbial biomass
was not measured after September 22nd due to a chloroform deficit. Different letters indicate significant differences between weekly
measurements (P 0.05).
Nutrient availability
Soil NO3 concentration in 0–5 cm depth peaked on 20
September followed by a decline, although not significant (Fig. 3d). A significant increase in soil NH4+ was
recorded on September 15 and 22 (Fig. 3e), coinciding
with air temperature venturing above 0 °C after periods of freezing (Fig. 1). After peaking on 22 September,
soil NH4+ levels decreased drastically (~50%) during
the following week. DON and total dissolved P (TDP)
followed a similar pattern as soil inorganic N, increasing until 22 September and decreasing to one third
(DON, Fig. 3f) or one fourth (TDP, Fig. 3g) on 30
September. Total soil P was 0.24 ± 0.01 SE mg P g 1
soil (control plots) and was significantly reduced by
water addition (two-way ANOVA; F3,20 = 4.16; P = 0.05).
SOM content ranged from 3.99 ± 0.35 SE% to 4.8 ± 0.39
SE% during the study period (control plots), with no
effect of treatments during autumn (RM LMM). There
were no effects of treatments on NH4+, DON, DOC,
TDP or SOM (RM LMM), but a significant decrease in
soil NO3 in watered treatments was observed (RM
LMM; F1,17.3 = 4.29; P = 0.05). Total soil N was
1.06 ± 0.1 SE mg N g 1 soil (control plots) and was
© 2012 Blackwell Publishing Ltd, Global Change Biology, doi: 10.1111/j.1365-2486.2012.02770.x
HIGH ARCTIC BIOGEOCHEMICAL DYNAMICS 7
Fig. 4 Mean daytime soil respiration (n = 6 ± SE) during summer and autumn at Zackenberg, NE Greenland. Treatments are C-control, N-nitrogen amendment, W-water addition and WN-combination thereof. Result of repeated measures linear mixed model analysis
with significant main factor effects of treatments and interactions shown as: †P 0.1; **P 0.01.
reduced by water addition but not when water and
nitrogen was combined, leading to a significant W 9 N
interaction (two-way ANOVA; F3,20 = 7.01; P < 0.05).
Microbial biomass
Microbial content of C (control plots) was 10–
12 mg C g 1 SOM until 22 September when a
sudden drop of approximately 60% was recorded
(Fig. 3i), corresponding to 16.8 ± 4.1 SE g C m 2.
Watering increased MBC during the study (RM LMM;
F1,101 = 3.84; P = 0.05). MBN was significantly lower on
10, 15, and 22 September than on 2 September (Fig. 3j).
After an initial increase during mid-September the soil
microbial C : N ratio declined drastically on 22 September (Fig. 3l) due to the sudden decline in MBC with less
change in MBN. There were no effects of treatments on
soil microbial N and the microbial C : N ratio.
Microbial content of P declined throughout September (Fig. 3k), and was significantly decreased by nitrogen addition (F1,7.88 = 12.16; P = 0.01) across the study
period (RM LMM).
Soil depth profile
The soil profile revealed maximum concentrations of N
near the surface and decreasing concentrations with
depth (Fig. 5a). The peaks in total N were similar to
peaks in SOM concentrations occurring at 15 cm and
35 cm depth (Fig. 5c), revealing a buried organic rich
A-horizon. Total P also showed similar peaks as SOM,
although less apparent (Fig. 5b). Soil bulk density was
highest at 40–50 cm (Fig. 5d). Belowground plant biomass peaked in the upper 10 cm of the soil profile and
decreased with depth (Fig. 5e). Soil moisture followed
the same trend and peaks as SOM, increasing with
depth until 40 cm depth where after a sharp decline in
moisture was recorded (Fig. 5f) due to increasing sand
content. The permafrost layer was encountered at
93 cm depth on 10 September. One-way ANOVA’s
revealed significant relationships between soil depth
and total N (F11,60 = 18.82; P < 0.0001), SOM (F11,60 =
10.38; P < 0.0001), total P (F11,60 = 4.28; P = 0.0001),
bulk density (F11,57 = 2.86; P < 0.01), root biomass
(F11,60 = 23.51; P < 0.0001), and moisture (F11,57 = 5.97;
P < 0.0001). Total C, N and P to 60 cm depth was
15.5 ± 1.1 SE kg C m 2, 623 ± 45.7 SE g N m 2 and
146 ± 3.4 SE g P m 2, respectively.
Discussion
Soil respiration
Our study revealed strong seasonal differences in soil
CO2 efflux and responses to soil water and nutrient
manipulations. Summer Rsoil rates (control plots) were
comparable to other high arctic studies (e.g. Christensen et al., 1998; Mertens et al., 2001; Elberling, 2003;
Elberling & Brandt, 2003; Illeris et al., 2003). During
autumn, Rsoil decreased to 5% of summer Rsoil as
declining air and soil temperatures correlated strongly
(rp > 0.9) with the observed temporal decline of Rsoil.
Previous studies have documented substantial cold season CO2 losses in the Low Arctic (e.g. Oechel et al.,
1997; Fahnestock et al., 1998; Grogan & Chapin, 1999;
Jones et al., 1999; Welker et al., 2000), but studies
addressing high arctic Rsoil are few, in particular during
autumn. Our observed autumn rates were comparable
to Rsoil reported from Dryas sp./Cassiope tetragona heaths
and meadow communities in Svalbard (Elberling, 2007;
Morgner et al., 2010; Strebel et al., 2010), although late
autumn measurements were considerably lower in our
study, probably as a result of a colder climate and significantly lower plant biomass at our site.
The chambers used for respiration measurements
were inserted in 1996. At present, this excludes live root
biomass from the upper 10 cm of the soil and this may
potentially lead to altered microenvironment, soil CO2
© 2012 Blackwell Publishing Ltd, Global Change Biology, doi: 10.1111/j.1365-2486.2012.02770.x
8 C . T . C H R I S T I A N S E N et al.
(a)
(b)
(c)
(d)
(e)
(f)
Fig. 5 Soil biogeochemical depth characteristics at the heath study site at Zackenberg, NE Greenland. Characteristics include total soil
N (a) and P (b); soil organic matter content (SOM) (c); bulk density (d), root biomass (e) and soil moisture (f). n = 6 for all characteristics, data shown with ±SE.
efflux and reduced input of plant associated carbon.
However, our summer respiration rates equalled fluxes
measured by Illeris et al. (2003) in 1997, using the same
study site, suggesting that our experimental design did
not change soil properties significantly. Due to no
aboveground plant biomass in the measurement chambers and absence of root biomass from the upper
10 cm, soil respiration is most likely derived primarily
from bulk soil carbon pools and less from plant-associated pools (i.e. root respiration, root exudation, and
detritus), which, however, are more labile and fluctuate
strongly between seasons. Bulk soil and plant-associated carbon pools have been shown to be equally
important regarding ecosystem respiration on an
annual basis in subarctic heath (Grogan & Jonasson,
2005).
Long-term effects of increased summer precipitation and
enhanced N supply
Warming and increased precipitation are predicted for
the Arctic region in the near future (ACIA 2005; IPCC,
2007). Because differentiation of arctic vegetation types
is ultimately determined by topography and soil water
regime, effects of climate warming will also depend
strongly on soil moisture (Illeris et al., 2004a). In contrast to our hypothesis, we found that simulated
enhanced summer precipitation had distinct effects on
© 2012 Blackwell Publishing Ltd, Global Change Biology, doi: 10.1111/j.1365-2486.2012.02770.x
HIGH ARCTIC BIOGEOCHEMICAL DYNAMICS 9
summer and autumn soil respiration. Our measurements revealed a significant effect of water addition
during the full study period with the significant interaction between water addition and measurement dates
indicating that the effect changed over time: In summer, watering increased Rsoil, lasting at least until 14
August, similar to the findings of Illeris et al. (2003). In
contrast, watering decreased Rsoil during autumn,
apparent from 9 September onward (Fig. 4). Water and
nutrient addition in combination tended to increase soil
efflux during summer whereas in autumn the combined treatment reduced respiration, similar to water
addition alone. N amendment alone slightly increased
Rsoil consistently throughout summer and autumn,
indicating that increased soil moisture was the primary
driver for the observed effect of the combined treatment. Arctic tundra vegetation is strongly nutrient limited (e.g. Shaver & Chapin, 1980; Chapin & Shaver,
1985; Chapin et al., 1995; Illeris et al., 2004b) and N
amendment enhanced primary production at our site
(photosynthesis measured on vegetation adjacent to soil
respiration chambers; Christiansen et al., in press). We
speculate that this, in turn, provided N-treated soils
with increased and/or better quality carbon substrate
via root exudation, enhancing soil CO2 efflux. We
stress, however, that we possibly underestimate this
indirect N-amendment effect because we measured respiration from chamber bases without roots in the upper
10 cm soil. On average, soil respiration rates in this
study accounted for ~40-60% of total ecosystem respiration (unpublished data).
The soil depth profile revealed a buried organic
A-horizon evident from both SOM and total N content.
This is not a unique characteristic of this particular dry
heath ecosystem; rather it may be a feature of the greater
study area as similar relict horizons have been reported
from a number of different sites within the Zackenberg
valley (Elberling & Brandt, 2003; Elberling et al., 2008).
The buried A-horizon coincided with increased moisture content in the soil profile. Substantial CO2 production has been shown in deep soil organic horizons
(Elberling & Brandt, 2003) and N fertilization has been
shown elsewhere to enhance deep soil carbon mineralization (Fierer et al., 2003; Mack et al., 2004) if the active
layer exceeds the buried SOM layers (Nowinski et al.,
2010). Thus, it is possible that the observed increase in
soil respiration in N treated plots came from deeper soil
carbon mineralization, primed by nutrient addition.
Likewise, if water addition increased deep soil moisture,
the observed increase in soil respiration could stem from
enhanced decomposition of buried SOM, i.e. older bulk
soil carbon. Although this may potentially help explain
the increase in summer Rsoil in watered treatments, it
does not explain the decrease during autumn, however.
Due to the unusually high amounts of summer precipitation in 2009 one could have expected a reduced
effect of experimental watering on Rsoil. This was not
the case, suggesting strong water limitation on microbial activity. During the growing season, root carbon
inputs to the soil are one of the primary sources of
labile substrate for the soil microbial community in dry
alpine (Lipson et al., 2002) and high arctic tundra (Illeris et al., 2003). The decline in autumn soil CO2 efflux in
watered treatments hints at a limited winter labile substrate pool (Hobbie et al., 2000; Schimel et al., 2006)
being depleted. During winter, microbes metabolize
soluble substrates (Clein & Schimel, 1995; Michaelson
& Ping, 2003; Schimel et al., 2004) retained in unfrozen
waterfilms (Oquist et al., 2009; Tilston et al., 2010) and
depletion of this substrate pool would have strong
implications for total wintertime respiration, potentially
limiting soil microbial activity during the cold season.
The effect of watering on autumn Rsoil may seem small,
compared to summer rates, but due to the long cold
season the cumulative effect may constitute a significant reduction of annual carbon losses.
Ice formation in soils may reduce the release of CO2
due to ice effectively acting as a barrier between soil
pore spaces and the atmosphere (Elberling & Brandt,
2003; Morgner et al., 2010) which potentially could be a
concern regarding our findings of reduced CO2 release
during autumn freeze-in. However, Clein & Schimel
(1995) manipulated soil moisture and found that, even
when soils were frozen, drought reduced respiration.
Together with the clear transitional period of reduced
effect of watering in early September prior to freezing,
we are confident our results are not subject to significant ice formation in soils.
Soil biogeochemical dynamics
We observed substantial fluctuations in soil nutrient
availability and microbial biomass during autumn. The
decline in MBC of ~60% in late September took place
after a prolonged period of freezing and subsequent
thawing. Similarly, Skogland et al. (1988) and Larsen
et al. (2007) reported decreases of ~40–50% in MBC following a single freeze-thaw event. The decline in MBC
coincided with soil inorganic N, P and DON levels
reaching season maxima. Soil DON, inorganic N and P
levels all declined following 22 September, suggesting
either microbial and/or root uptake. In spring, freezethaw events are critical concerning plant uptake of
available soil N and subsequent growing season productivity (Lipson et al., 1999; Grogan & Jonasson, 2003;
Schimel et al., 2004), and subarctic plant N uptake has
been reported to occur at the onset of winter (Grogan &
Jonasson, 2003). In our study, root content of N and P
© 2012 Blackwell Publishing Ltd, Global Change Biology, doi: 10.1111/j.1365-2486.2012.02770.x
10 C . T . C H R I S T I A N S E N et al.
peaked on 20 September, followed by possible freezinginduced root damage and N plus P decline on 22 and
30 September whereas soil N and P peaked on 22
September, before declining. Microorganisms are more
efficient than plants in acquiring pulses of nutrients
(Andresen et al., 2008) and MBN did not show the same
drop as MBC, suggesting microbial N uptake.
Microbial C : N ratio increased from early to
mid-September, which suggests a shift from bacteria
toward fungi-dominated soil microbial community
(Jensen et al., 2003). The microbial composition was significantly altered on 22 September with the sudden
decline of MBC and no change in MBN, causing the
C : N ratio to drop to a season low. Distinct soil microbial communities between summer and winter have
been reported for arctic (Mcmahon et al., 2011), subarctic (Monson et al., 2006), and alpine ecosystems (Schadt
et al., 2003; Lipson & Schmidt, 2004) and we speculate
that the gradual change in microbial C : N ratio reflects
a shift toward a cold season microbial community dominated by mainly ectomycorrhizal fungi associated with
the roots of the three dominant plant species; Dryas,
Salix and Kobresia (Michelsen et al., 1998). Thus, the offset in microbial C : N ratio on 22 September might be
linked to the drop in root biomass and N and P concentrations after freezing, and a freezing-induced crash of
the root-associated autumn microbial community. In an
alpine, subarctic heath, ectomycorrhizal colonization of
Salix roots in spring was only 50% of that in autumn,
suggesting winter loss of mycelium (Clemmensen &
Michelsen, 2006).
Despite several freeze-thaw incidents, we did not
record changes in MBC until the drop on 22 September,
corresponding to 16.8 ± 4.1 SE g MBC m 2. The question remains; where did all the carbon go? Similar to
our study, Larsen et al. (2007) reported a steep drop in
MBC following spring FTC in subarctic heath, and with
no apparent changes in Rsoil and DOC. It seems
unlikely that a decline of ~40% (Larsen et al., 2007) to
~60% (this study) would not impact Rsoil or DOC levels
when considering the short time span in which the carbon was lost in both studies. Large methane bursts may
occur during autumn freeze-in (Mastepanov et al.,
2008), but methanogenesis requires anaerobic conditions, as in e.g. waterlogged soils in wet sedge or fen
ecosystems, which was not the case in this dry heath. In
dry arctic tundra, methane consumption is more likely
to occur than actual methane production (Christensen
et al., 2000). Therefore, we cannot attribute the lost
carbon to significant methane production. Extreme
environmental conditions may facilitate alteration of
the microbial composition between summer and winter
(Schadt et al., 2003) and the fumigation–extraction
process has varying impact on different microbial
communities (Anderson & Domsch, 1978; Tate et al.,
1988), resulting in changed extraction efficiency of
MBC. During autumn freeze-in, we suspect that using a
fixed KEC to account for non-extracted microbial biomass may not yield appropriate estimates of MBC.
Thus, future investigations into changes in microbial
diversity and extractability from summer to winter are
needed for verification. KEC has previously been
reported in the range of 0.23–0.84 in arable, grassland
and forest soils (Joergensen, 1996) and 0.22–0.6 in arctic
soils (Cheng & Virginia, 1993) and even small changes
in extractability may have great impact on MBC.
Response in soil organic matter turnover to enhanced
water and nutrient supply
This particular high arctic heath has been subject to
14 years of enhanced nutrient and summer water addition. During this the annual mean air temperature in
the Zackenberg valley has risen 2.3 °C (Hansen et al.,
2008). Despite our long-term experimental manipulations we found no changes in SOM content across treatments and organic matter content was similar to SOM
measured in 1997 (Illeris et al., 2003); average SOM content in 2009 (control plots only, across study period)
was 4.4 ± 0.12 SE%, whereas SOM content in 1997 was
4.4 ± 0.38 SE% (control plots only, data from Illeris
et al., 2003) with no effect of treatments. Resistance to
climate warming in other High Arctic ecosystems has
recently been reported for soil microbial communities
(Walker et al., 2008; Lamb et al., 2011) and vegetation
composition and cover (Hudson & Henry, 2010; Elmendorf et al., 2012). Note, however, that our SOM measurements are from the upper 5 cm of soil. Currently,
we do not know if changes in belowground SOM took
place (see Mack et al., 2004). Short- (Wookey et al., 1994,
1995; Press et al., 1998; Robinson et al., 1998) and longterm (Christiansen et al., in press) studies have previously reported little or no effects of water addition on
dry high arctic tundra vegetation. However, as shown
by Illeris et al. (2003) and Lamb et al. (2011), dry tundra
respiration rates may increase significantly, following
soil watering. Here we show that although increased
soil moisture enhances summer soil CO2 efflux, this
may lead to decreased rates in cold season soil CO2
efflux. We speculate that increased summer soil respiration, together with low plant production and low
input of root exudates in the colder period, may lead to
intensified depletion of recently fixed plant carbon substrate, ultimately decreasing respiration rates as
observed. The lack of response in SOM content across
treatments and time suggests high ecosystem resilience
to changes in soil moisture and nutrient availability,
which are soil biogeochemical properties that are
© 2012 Blackwell Publishing Ltd, Global Change Biology, doi: 10.1111/j.1365-2486.2012.02770.x
H I G H A R C T I C B I O G E O C H E M I C A L D Y N A M I C S 11
expected to change during climate change. Field studies
have reported enhanced soil respiration in response to
warming, although the initial rise in efflux tends to
decline to control levels within a few years (Oechel
et al., 2000; Melillo et al., 2002). This is most likely due
to changes in SOM composition and availability (Hartley et al., 2008) and soil microbial efficiency in using
carbon (Allison et al., 2010). At our study site, more
investigations are needed to investigate how the buried
SOM has responded to water and nutrient additions.
Our modelling of summer and autumn soil efflux
showed that autumn carbon loss by Rsoil constituted
50% of summer losses, representing 52 and 96 g CO2 m 2
lost, respectively. We used data from Bliss & Matveyeva (1992) and Walker et al. (2005) to calculate a rough
estimate of high arctic circumpolar dry heath tundra
soil CO2 efflux during summer and autumn. This
amounted to between 26 and 96 gigatonnes of CO2 lost
during summer and 14 to 52 gigatonnes of CO2 lost
during autumn. Our calculations of circumpolar soil
respiration are crude, but nevertheless represent a very
clear indication of the significance of including autumn
gas exchange in annual carbon budgets.
Future climate warming during autumn has the
potential to increase ecosystem carbon loss, making
autumn carbon balance an even greater factor concerning annual carbon budgets. This study suggests that
cold season soil activity is linked to growing season
plant production. The decline in autumn Rsoil in
watered treatments is possibly due to intensified depletion of a limited winter labile carbon pool. Changes in
precipitation patterns may significantly affect summer
and autumn soil activity, potentially altering cold
season soil CO2 efflux. SOM stocks, at least in the
uppermost soil layer, seem resistant to nutrient and
water addition and climate warming (background temperature increase), indicating that a large part of annual
carbon loss comes from plant-associated carbon pools,
rather than decomposition of older pools of SOM, i.e.
bulk soil carbon stock.
Acknowledgements
This work was supported by the Danish Council for Independent Research | Natural Sciences, and the Danish National
Research Foundation. Aarhus University is thanked for access
to and logistics at Zackenberg. We would like to thank the
reviewers of an earlier version of the manuscript for their
constructive comments.
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