Soil Biology & Biochemistry 43 (2011) 942e953
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Soil Biology & Biochemistry
journal homepage: www.elsevier.com/locate/soilbio
Plant production, and carbon and nitrogen source pools, are strongly intensified
by experimental warming in alpine ecosystems in the Qinghai-Tibet Plateau
Li Na a, b, c, Wang Genxu a, *, Yang Yan a, Gao Yongheng a, Liu Guangsheng a, b
a
Key Laboratory of Mountain Environment Evolvement and Regulation, Institute of Mountain Hazards and Environment, Chinese Academy of Sciences, 610041 Chengdu, China
Graduate School of Chinese Academy of Sciences, 10039 Beijing, China
c
Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, 130012 Changchun, China
b
a b s t r a c t
Article history:
Received 10 February 2010
Received in revised form
29 December 2010
Accepted 7 January 2011
Available online 31 January 2011
The aim of this study was to assess initial effects of warming on the nutrient pools of carbon and nitrogen
of two most widespread ecosystem types, swamp meadow and alpine meadow, in the Qinghai-Tibet
Plateau, China. The temperature of the air and upper-soil layer was passively increased using open-top
chambers (OTCs) with two different temperature elevations. We analyzed air and soil temperature, soil
moisture, biomass, microbial biomass, and nutrient dynamics after 2 years of warming. The use of OTCs
clearly raised temperature and decreased soil moisture. The aboveground plant and root biomass
increased in all OTCs in two meadows. A small temperature increase in OTCs resulted in swamp meadow
acting as a net carbon sink and alpine meadow as a net source, and further warming intensified this
processes, at least in a short term. On balance, the alpine ecosystems in the Fenghuoshan region acted as
a carbon source.
Ó 2011 Elsevier Ltd. All rights reserved.
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Keywords:
Alpine ecosystem
Experimental warming
Short term
Plant growth
Carbon pool
Qinghai-Tibet Plateau
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a r t i c l e i n f o
1. Introduction
Global warming has been causing worldwide ecosystem
changes. Within the last century, the mean global surface temperature has increased by 0.67 0.2 C. For the 21st century, an
increase in mean global temperature between 1.8 and 4.0 C over
the next 100 years is predicted (IPCC, 2007). Arctic and alpine
regions are likely to be particularly affected by the climate warming
because observed temperature increases in these areas are higher
than anywhere else (IPCC, 2007). Moreover, high latitude/altitude
ecosystems might be more sensitive because plant growth is often
accustomed to low temperature environment (Körner, 1998), and
soil respiration is more sensitive to warming at lower temperature
(Kirschbaum, 1995). The Qinghai-Tibet Plateau located in the
central part of the troposphere in the mid-latitude westerlies, is
regarded as the Earth’s third pole and the highest unique territorial
unit in the world. Thus, its ecosystems and natural environment are
inherently fragile and instable, making them especially vulnerable
to global warming. In fact, the air temperature in the Source Region
of the Yangtze River has increased 0.06 C every 10 years for the
* Corresponding author.
E-mail address: [email protected] (W. Genxu).
0038-0717/$ e see front matter Ó 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.soilbio.2011.01.009
past 40 years (Ecology and Environment of Three Rivers’ Source
Region Compilation Committee, 2002).
Moreover, the high latitude/altitude ecosystems store the
greatest fraction of carbon stocks in soils (IPCC, 2007). Compared to
soils from temperate ecosystems, cold soils are found to comprise
more labile soil organic matter (SOM) because cold soil contains
slower decomposition and humification processes (Jenny, 1926;
Sjögersten et al., 2003). The carbon content in Qinghai-Tibet
Plateau soil was significantly higher than that in soils in other areas
(Fan et al., 2003). Changes in climate are predicted to stimulate the
release of a substantial portion of this reservoir by increasing soil
respiration, thereby turning alpine ecosystems from a net sink to
a net source of atmospheric CO2 (Biasi et al., 2008; Knorr et al.,
2005; Oechel et al., 1993; Tarnocai, 1999). The stimulation of soil
respiration by increased temperatures, however, could be counterbalanced by declining soil moisture (Saleska et al., 1999),
changing carbon inputs from plants (Oberbauer et al., 2007),
declining resource availability, or an ‘acclimatization’ through
physiologically adapting microbial communities (Luo et al., 2001;
Melillo et al., 2002). Moreover, the response of soil CO2 effluxes
to rising temperature also depends on how plants and their C
allocation to belowground sinks respond to warming
(Schindlbacher et al., 2009). Winter biological processes are
contributing to return the arctic ecosystems to a carbon sink
L. Na et al. / Soil Biology & Biochemistry 43 (2011) 942e953
during the growing season (from May to September). The study site
is underlain by permafrost. Alpine meadow and swamp meadow
are the two most typical vegetations. Alpine meadow ecosystem
consists mainly of cold meso-perennial herbs grow in conditions
where a moderate amount of water is available. This ecosystem’s
primary vegetation is consisted of Kobresia pygmaea (C. B. Clarke),
K. humilis (C. A. Meyer ex Trautvetter) Sergievskaja, Kobresia capillifolia (Decaisne) (C. B. Clarke), Kobresia myosuroides (Villars) Foiri,
Kobresia graminifolia (C. B. Clarke), Carex atrofusca Schkuhr subsp.
(minor (Boott) T. Koyama), and Carex scabriostris (Kukenthal).
Swamp meadow populated by hardy perennial hygrophilous or
hygro-mesophilic herbs under waterlogged or moist soil conditions, mainly occurs in patches or strips in the mountains, widevalley terraces and rounded hills, which represent a small portion
of the study region. These areas are dominated by Kobresia tibetica
Maximowicz, Stipa aliena Keng and Festuca spp. (Zhou, 2001).
2.2. Experimental design
In our experiment, we followed the methods of the International Tundra Experiment and used open-top chambers (OTC) as
a passive warming device to generate an artificially warmed environment (Marion et al., 1997). The experiment was conducted with
a comparative trial design in two meadows, both with vegetation
coverage of above 70%. In July 2008, we installed 12 OTCs in total:
three pairs of two heights in each of alpine meadow and swamp
meadow. The OTCs, which were hexagonal in shape with 60
inwardly inclined sides, are made of 6 mm-thick, translucent
synthetic glass, this material has high solar transmittance in visible
wavelengths (about 90%) and low transmittance in the infrared
(heat) range (<5%) (Marion et al., 1997) (Fig. 1). All the top opening
of OTCs was 60 cm, OTCs of 40 cm in height covers an area of
0.98 m2, and OTCs of 80 cm height covers an area of 2.01 m2. These
OTCs were in use throughout the entire length of the experiment.
For comparisons of the warming effect of OTCs, the air temperature
20 cm above the soil surface was measured in OTCs and in the
control plots in each meadow. Measurements were taken at 30-min
intervals during the growing seasons of the experimental period
(2008e2009) by automatic recording thermometers and thermistor sensors (FDR) (CS616, USA). The results were auto-transmitted
to recorders (Campbell AR5, Avalon, USA). A control plots
(50 50 cm, 0.25 m2) were also established in the vicinity of each
height of OTC, and four control plots were set up in total. With the
exception of light exposure, the selected plots in the same meadow
were seemed to have similar microhabitat characteristics. The
distance between OTCs and adjacent control plots was between 3
and 4 m, and the distance between the replicate blocks ranged from
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(Turunen et al., 2004; Welker et al., 2004). For example, due to the
snow-holding capacity of shrubs, the insulating properties of snow,
a soil layer that has a high water content because it overlies nearly
impermeable permafrost, and hardy microbes that can maintain
metabolic activity at temperatures of 6 C or even lower, deciduous shrubs have been shown to profit from warmer conditions, as
demonstrated in several studies from moist tussock tundra (Sturm
et al., 2005; Weintraub and Schimel, 2005).
Low temperature and short growing seasons are considered to
be among the most important limiting factors for the performance
of alpine plants (Gugerli and Bauert, 2001; Wang et al., 2001).
Longer growing season and temperature enhancement may reinforce photosynthetic capacity and growth rates of the alpine plants
(direct temperature effect). Although the effects of rising temperature on single process have been studied extensively, a comprehensive understanding of the response of entire ecosystem to
climate warming still remains unexplored (Rustad et al., 2001).
Many studies on the effect of experimental warming on C dynamics
between ecosystems and the atmosphere were carried out in boreal
forests (Niinistö et al., 2004; Bronson et al., 2008), at high latitudes
(Oechel et al., 1993; Oberbauer et al., 2007), and in lichen-rich
dwarf shrub tundra (Biasi et al., 2008). The results of these studies
were ecosystem-dependent responses in C fluxes with initial C
losses in dry tundra and boreal forests, but dampened effects under
anoxic conditions. The only study conducted at high altitude was in
a dry alpine meadow in Colorado, with results showing that soil
heating had stronger indirect (rather than direct) effects on soil
C cycling by changing plant species composition and inducing
moisture limitations for soil respiration (Saleska et al., 1999). To our
knowledge, there is a lack of studies on experimental warming at
high altitude, including in alpine meadow and swamp meadow,
commonly found on the Kobresia humilis meadow of the QinghaiTibet Plateau (Zhou et al., 2000; Zhao et al., 2006). There are even
less accessible studies on the warming effects on plantesoil
nutrient dynamics.
In order to understand the effects of global warming on
biogeochemical circles of the alpine ecosystem on the QinghaiTibet Plateau, our study seeks to examine the effects of warming on
carbon and nitrogen contents in two alpine ecosystems with
undisturbed soils and thick organic layers using open-top chambers (OTCs). The swamp meadow is typical of more favorable
locations with abundant soil nutrients and water regimes; whereas
the alpine meadow has poor soil nutrients and low soil water
content. Since the two meadows are characterized by different
thermal conditions, it is expected that they will have different
responses to warming. This experiment tests the following
hypotheses: (1) the plant growth in high altitude and cold-climate
ecosystems is mainly limited by low temperature, vegetative
production of two alpine meadows will increase under a warmer
condition; (2) since the two meadows are characterized by
different thermal and soil conditions, nutrient dynamics in swamp
meadow ecosystem is expected to contrast with alpine meadow
under warming conditions.
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2. Materials and methods
2.1. Study site
The experiment was undertaken in alpine meadow and swamp
meadow, which represent the most common (70% in area) vegetation types in the Fenghuoshan region (34 430 4300 N, 92 530 3400 E)
in the hinterland of Qinghai-Tibet Plateau, China. It represents an
area of 112.5 km2; with an altitude of around 4600e4800 m. The
climate is cold and dry. The mean annual temperature is 5.3 C,
and the mean annual precipitation is 269.7 mm, 80% of which falls
Fig. 1. Open-top chamber (OTC1) and associated control plot (right) in an alpine site.
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L. Na et al. / Soil Biology & Biochemistry 43 (2011) 942e953
about 6 to 8 m. The experiment was carried out in 2008 and 2009,
and the second growing season lasted from 6 July to 30 September.
The experiment consisted of three different treatments with two
different levels of elevated temperatures in the two meadows. They
were (1) swamp meadow (Site S) (34 430 43.900 N, 92 530 34.100 E,
altitude 4763 m) control plot (control), (2) swamp meadow 40 cm
high OTC with temperature increased by 2.98 C (OTC1), (3) swamp
meadow 80 cm high OTC with temperature increased by 5.52 C
(OTC2), (4) alpine meadow (Site A) (34 430 35.700 N, 92 530 45.300 E,
altitude 4754 m) control plot (control), (5) alpine meadow 40 cm
high OTC with temperature increased by 2.59 C (OTC1), (6) alpine
meadow 80 cm high OTC with temperature increased by 5.16 C
(OTC2).
2.3. Soil and plant sampling and analysis
2.4. Data analysis
Net plant C uptake: the warming effect on net C uptake by plants
was roughly estimated by multiplying measured growth effect by
the estimate of plant biomass production.
Percentage of coarse fraction (relative gravel mass) was calculated as: (dry mass > 0.25 mm)/(total dry mass) 100.
Plant tissue C (or N) content (g m2) was calculated on an area
and depth basis from biomass samples and plant C (or N) concentration analyses.
Soil organic C (or N) content (g m2) ¼ D B C ((100 S)/
100) 1000, where D is the soil depth (cm), B is the soil bulk
density (g m3), C is the soil organic carbon (or total nitrogen)
concentration in the sieved (<0.25 mm) soil fraction (g kg1), and S
is the percentage of the coarse fraction (>0.25 mm) in the sample
(%), i.e., the gravel was excluded from the analysis.
All data were tested for homogeneity of variances before further
testing. No data transformation was done since data met the
assumption of homogeneity of variances. The data were analyzed
with a three-way ANOVA using the sampling date, soil depth and
site as factors. Furthermore one-way ANOVA followed by a t-test
was used to determine the differences in parameters examined
separately for each vegetation type and harvest time. Values in the
text and figures are means standard error (SE). For each of the
statistical analyses, the levels of significance were P < 0.05*, and
0.01**, and 0.001***, n.s. means no statistical significance. The
statistical evaluation was done using SPSS 12.0 for Windows.
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2.3.1. Field sampling and estimation of aboveground
and root biomass
Soil and plant samples were taken three times during the
growing season (15e18 June, 2e4 August, and 20e22 September),
representing the beginning, vigorous, and ending of the growing
season. Each of OTC and control plot was further split into four
subplots (each subplot had an area of 625 cm2) for plant biomass
harvest and soil analysis. All the plants were clipped from four
randomly sampled subplots in each randomly sampled plot, and
were placed in paper bags. The soil and root samples were taken at
a depth of 20 cm, with constituted the mor layer (0e5 cm) and
mineral layer (5e20 cm) of the soil using a corer with a diameter of
5 cm. Three soil cores were made in each OTC in one date (beginning of season for example). And each sample core was vertically
cut in two pieces: One was stored at 4 C until the analyses could be
performed on the water content and microbial C and N. The other
one was used for organic carbon (OC) and total nitrogen (TN). The
air-dried soil samples were crumbled by hand to pass through a 2mm diameter sieve to remove large particles from the finer soil.
Large root fragments and associated soil were then washed with
a 0.25 mm sieve to retrieve fine roots. No attempt was made to
distinguish between live and dead roots. The soil bulk density was
also measured at the depths of 0e5 cm and 5e20 cm using cutting
rings with a 5.3 cm diameter. The air-dried soil samples were
passed through a 2 mm sieve to remove the coarse fraction (gravel
and roots), and then weighed. All vegetation materials were oven
dried (48 h, 80 C) and then weighed for further chemical analysis.
Standing dead plant and litters were collected at the end of the
growing season (late September) in the experiment. They were
collected randomly in each 20 cm 20 cm plot. All litter samples
were oven dried to constant weights at 80 C for 48 h, and the
weights were recorded.
Vegetation and soil samples were grounded in agate mortar,
passed through a 60-mesh sieve, and analyzed for organic carbon
(OC) and total nitrogen (TN) concentrations in a VarioEL elemental
analyzer.
2.3.2. Determination of C and N in soil and plant
Microbial biomass was analyzed using the fumigatione
extraction technique (Jenkinson and Powlson, 1976; Vance et al.,
1987). 5 g soil samples were extracted in 0.5 M K2SO4 for 1 h.
Meanwhile, another set of 5 g sub-samples was fumigated with
ethanol-free chloroform for 24 h, and then extracted in a similar
manner. Part of the dried soil was used for analysis of OC and TN.
Both the unfumigated and fumigated soil extracts were filtered
through Whatman GF/D filters. The difference between the
concentrations in the fumigated and unfumigated extracts was
used to estimate the amount of C or N in the microbial biomass. To
account for incomplete extractability, a correction factor of 0.45
was used for microbial C (Joergensen, 1996) and a factor of 0.40 for
microbial N (Jonasson et al., 1996). For the soil profile data, soil and
microbial C and N pools were calculated per square meter of the
entire soil layer.
3. Results
3.1. Warming effects of OTCs
The height of OTCs 40 cm (OTC1) and 80 cm (OTC2) above the
soil surface made the air flow rather slow, most of the heat could
not be emitted to the environment. In this study, the temperature
inside the OTCs was higher than the other similar studies
(Erschbamer, 2001; Marion et al., 1997; Kudernatsch et al., 2008).
During the growing season (from May to September), the air
temperature (based on mean daily temperature) increased 2.98 C
(OTC1) and 5.52 C (OTC2) at Site S (Fig. 2). At Site A, the air
temperature inside the OTCs raised 2.59 C for OTC1 and 5.16 C for
OTC2. A measurement of the soil moisture at 20 cm depth showed
decrement with temperature enhancement, but there was no
statistical difference between the two treatments and the control.
The mean soil water content at Site S was 51.58% in the control plot,
49.13% in the OTC1 plots and 48.04% in the OTC2 plots. At Site A, the
soil water content decreased by 1.83% in the OTC1 plots and
significantly decreased by 7.71% in the OTC2 plots.
A typical daily series of air and soil temperature (3 August 2009)
is shown in Fig. 3. For most of the period, the temperature curve of
the OTC2 was above the OTC1 and above the control plots; this was
true for the air temperature as well as for the soil temperature.
Although warming effect of the OTCs occurred during both day and
night, but it occurred primarily during the day possibly because of
the high sun radiation.
3.2. Differences in plant and soil properties under two meadows
The contents of OC and TN in plant and soil, water content, and
root biomass at the two soil layers were significantly higher at Site S
L. Na et al. / Soil Biology & Biochemistry 43 (2011) 942e953
945
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Fig. 2. Air temperature and soil water content in control, OTC1 and OTC2 plots during the growing season (2009) at Site A (a, c) and Site S (b, d) with warming treatment.
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than Site A, while the contents of C/N ratio in root were greater at
Site A than Site S (Table 1). However, the contents of microbial C,
aboveground biomass, C/N ratio in aboveground, C/N ratio in soil
and microbes were higher at Site S than Site A (Table 1). The bulk
density, the content of microbial N in 0e5 cm soil layer and C/N
ratio in root showed no difference.
3.3. Standing dead plant matter and litter
In our experimental sites, the accumulation of standing dead
plant matter and litter decreased in response to warming (Table 2).
At Site S, the biomass of standing dead matter and litter respectively dropped by 15.49% and 31.57% in OTC1 (P < 0.05), and 25.47%
and 43.94% in OTC2 plots (P < 0.01). The biomass of standing dead
matter and litter at Site A generally mirrored that at Site S. The
decreases in percentages were 18.72% and 25.00% in OTC1
(P < 0.05), and 29.36% and 40.34% in OTC2 (P < 0.01).
Table 1
Plant and soil properties at Site S and Site A.
Variable
Depth
(cm)
Site S
Water content (%)
0e5
5e20
0e5
5e20
0e5
5e20
0e5
5e20
0e5
5e20
0e5
5e20
0e5
5e20
0e5
5e20
0e5
5e20
0e5
5e20
0e5
5e20
0e5
5e20
40.6
38.9
0.83
0.94
2.6
4.1
160.9
285.8
16.3
14.5
268.4
356.4
17.9
6.2
15.0
57.3
6.7
4.4
3.5
2.3
67.9
39.7
51.6
58.6
0.5
Bulk density
(g cm3)
Soil organic C
(kg m2)
Soil total N
(g m2)
Soil C/N ratio
Microbial C
(mg g1 SOM)
Microbial N
(mg g1 SOM)
Microbial C/N ratio
Root biomass
(kg m2)
Root organic C
(kg m2)
Root total N
(g m2)
Root C/N ratio
Aboveground
biomass
(kg m2)
Plant organic C
(kg m2)
Plant total N
(g m2)
Plant C/N ratio
Fig. 3. Diel temperature variations in OTC1, OTC2 and control plots (3 August 2009),
measured 20 cm above (air) and 5 cm below (soil) the soil surface at Site S.
Site A
4.5
3.8
0.1
0.1
0.2
0.4
25.4
41.6
4.2
2.0
16.5
21.6
3.4
1.1
2.9
7.9
0.1
0.6
0.3
0.3
8.2
5.1
10.3
12.7
0.1
23.5
20.1
0.86
0.92
0.5
1.1
40.1
111.0
11.4
10.3
148.8
206.1
15.1
4.2
9.8
49.1
1.4
0.78
0.4
0.2
7.5
3.6
54.5
60.2
0.3
Significance
2.6
2.7
0.2
0.1
0.08
0.2
6.5
13.3
3.5
1.4
14.3
19.1
3.1
0.8
2.2
6.5
0.06
0.1
0.03
0.02
1.1
0.7
11.2
14.3
0.07
***
***
n.s.
n.s.
***
***
***
***
*
*
**
**
n.s.
*
*
*
***
***
***
***
***
***
n.s.
n.s.
**
363.1 17.9
125.3 12.7
**
11.8 1.4
4.9 1.4
**
30.7 8.4
25.4 5.8
**
The levels of significance were P < 0.05*, and 0.01**, and 0.001***, n.s. means no
statistical significance.
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L. Na et al. / Soil Biology & Biochemistry 43 (2011) 942e953
Table 2
The biomass of standing dead and litter in the control, OTC1 and OTC2 plots after 2
years of warming treatments (g m2).
Type of sampling
Standing dead
Litter
Site S
Control
OTC1
OTC2
85.2 12.8**
72.0 13.8*
63.5 14.7a
39.6 11.2**
27.1 9.6*
22.2 7.5a
Site A
Control
OTC1
OTC2
23.5 3.6*
19.1 3.3
16.6 3.1
17.6 2.1*
13.2 2.4
10.5 2.8
The levels of significance were P < 0.05*, and 0.01**, and 0.001***, n.s. means no
statistical significance.
3.4. Plant growth and production
The trend of the OC and TN contents in plants in OTCs at the two
sites was similar to the trend of growth responses (Fig. 7). Both
warming in OTC1 and OTC2 plots increased the contents of OC and
TN at Site S, and the increase was especially significant in the
vigorous growth periods (P < 0.01). The OC and TN contents at Site
A also increased in OTC1 plots, but decreased in OTC2 plots.
Differences in OC and TN contents of all the plant tissue type
were significant with the exception of aboveground plant and in
the beginning of the growing season (Fig. 7). At the beginning of the
growing season, the contents of OC and TN varied similarly at the
two sites. The warming effects improved the accumulation of OC
and TN in OTC1 plots, but reduced these contents in OTC2 plots.
During the vigorous growth period, OC and TN contents in plant
increased significantly in OTC1 at Site S, especially the roots in the
depths of 0e5 cm and 5e20 cm (P < 0.05). Compared to OTC1,
higher warming effects in OTC2 plots made a less increments in OC
and TN contents, and the OC and TN contents seemed to allocate
more in root tissue in 5e20 cm depth layer. At Site A, the warming
effects caused noticeable change in the OC and TN accumulation.
For OTC2, however, the OC and TN contents in both aboveground
plant and root decreased significantly (P < 0.01). The OC and TN
contents at two sites showed opposite trends at the end of growing
season. The OC and TN contents at Site S displayed an increasing
trend like that in the beginning of the growing season, At Site A, the
OC and TN contents decreased significantly in the OTC1 and OTC2
plots, and diminished in OTC1 plots (P < 0.05). The higher warming
effect in OTC2 aggravated this trend (P < 0.01).
In the control and OTC1 plots, there were few seasonal changes in
the soil OC and TN contents at the two sites, but the seasonal
changes were pronounced in the OTC2 plots (Fig. 8). At Site S, the OC
and TN in OTC1 experienced few changes compared to that in the
control plots throughout the growing season, but the allocation
proportion seemed to allocate more in 5e20 cm depth soil layer. In
OTC2 plots, the OC and TN contents were the lowest in the beginning
of the growing season (0.30 kg m2 and 4.01 kg m2, respectively),
and increased until its peak during the vigorous growing season
(0.62 kg m2 and 10.22 kg m2, respectively), and then decreased
until the end of growing season. The variation of OC and TN contents
was different at Site A (Fig. 8). It is obvious that the soil OC and TN
contents peaked in OTC1 plots in the beginning of growing season,
and shrunk in the vigorous growing season. At the end of growing
season, the OC and TN contents had no significant changes due to
warming, except for slight increases at the depth of 0e5 cm.
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There were pronounced seasonal variations in above and
belowground biomass at the two sites (Fig. 4). In each control plot
of the two sites, the total biomass reached the highest value in
August (2.59 kg m2 at Site A, and 24.32 kg m2 at Site S). The total
plant biomass at the two sites significantly increased after 2 years
of warming (P < 0.05), mainly due to the strong response in sedges,
which were responsible for 90% of the total biomass gain (Fig. 5),
with the ecological dominance of sedges didn’t change significantly
at two meadows (Fig. 6).
Significant growth increments were observed in OTCs at Site S
(Fig. 4(a)). In the beginning of the growth (June), the total biomass
increased, but not significantly. The total biomass was greatly
enhanced during the vigorous growth period in August. The
increase was especially significant in the root biomass of both the
OTC1 and OTC2 plots (P < 0.05). Interestingly, the total biomass of
OTC2 was a little smaller than that of OTC1. It appeared that the
biomass allocation patterns changed significantly from the upper
soil to the deeper soil layers in OTC2 plots. At the end of the
growing season (September), the biomass decreased in both the
control and the warmed plots as compared to the statuses recorded
in August. Because of the lower soil moisture (Table 1), the biomass
of Site A was approximately 1/10e1/8 of that at Site S (Fig. 4(b)). In
general, the responses of plant growth to warming at Site A in three
growing stages were similar to that at Site S. The differences were
only evident in the beginning of the growing season in OTC2 plots.
The biomass production inside the OTC2 increased at a greater rate
than that in OTC1, with the most significant increment occurring at
the soil depth of 5e20 cm (P < 0.05). Total biomass increased
significantly at the end of the growing season in OTC1, with the
largest increment occurring at the 0e5 cm soil depth (P < 0.01).
3.5. Pools of OC and TN in plant and soil
Fig. 4. The aboveground and root biomass in the control, OTC1 and OTC2 plots at Site S (a) and Site A (b) with warming treatments. The values are means (þS.E.) of three
replicate plots.
L. Na et al. / Soil Biology & Biochemistry 43 (2011) 942e953
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Fig. 5. The aboveground biomass of sedges, forbs and total in the control, OTC1 and OTC2 plots at Site S (a) and Site A (b) in the vigorous growing season. The values are means
(þS.E.) of three replicate plots.
3.6. Ecosystem pools of OC and TN
4. Discussion
There were pronounced seasonal variations in the pools of OC
and TN in the control plots at the two sites during the growing
season. In the control plots, the OC and TN contents reached the
lowest value in the beginning of the growing season, then increased
to hit a peak, and decreased until the end of growing season (Fig. 9).
Different responses were found in the pools of OC and TN at two
sites due to temperature enhancement. At Site S, the warming in
OTC1 plots caused increase in the pools of OC and TN throughout
the growing season. The warming in OTC2 plots significantly
decreased the OC pool by 3.45 kg m2 and the TN pool by
0.23 kg m2 in the beginning of he growing season (P < 0.001)
(Fig. 9(a, b)), with the main decreases occurring in the soil. In the
following growing season, the pools of OC and TN significantly
increased, and the elevations were greater than those in OTC1 plots.
At Site A, the pools of OC and TN increased by 25.8% and 23.8% due
to the warming effects in the OTC1 plots in the beginning of
growing season. The main increases were contributed to the soil
and root tissue (Fig. 9(c, d)). During the vigorous and the end of the
growing season, the pools of OC and TN decreased. The warming
effect in OTC2 plots caused reduction of the pools of OC and TN for
the entire growing season, except for the OC pool at the beginning
of the growing period.
4.1. Differences in soil and plant properties under
Site S versus Site A
im
de
Along with the favorable water condition and nutrients availability at Site S, all of which attributed to the higher plant biomass,
contents of plant and soil OC and TN, microbial biomass C and N
(Table 1) at Site S than those at Site A. If C/N ratio, is used as proxy
determining the chemical recalcitrance to microbial decay (Swift
et al., 1979; Melillo et al., 1982), then the higher contents of OC
and TN in the roots and aboveground plant at Site S and the lower
root C/N ratio at the depth of 0e5 cm at Site S indicated that the
roots might be more degradable at Site S, at least for microbes
(Table 1).
Fig. 6. The ecological dominance of sedges in the control, OTC1 and OTC2 plots at Site
S and Site A with warming treatments in the vigorous growing season. The values are
means (þS.E.) of three replicate plots.
4.2. Warming effects on plant growth and production
Higher mean temperature likely results in longer growing
seasons and concomitant changes in plant phenology (Rustad et al.,
2001). The warming effect of the presence of chambers was
believed to be a major contributing factor to standing dead plant
matter and litter decomposition as the increased temperature
facilitated microbial activities (Hollister, 2003). Furthermore, there
was a decrease of standing dead plant matter and litter in the
warmed plots at both sites compared to the control plots. Although
the decrease in standing dead plant matter might have been
exaggerated in warmed plots, the trend of decreasing litter accumulation in response to warming suggests that the patterns of
nutrient cycling and carbon balance in the alpine ecosystems
studied here were changing (Hollister, 2003). In this study, the
accumulation of standing dead plant matter in response to warming might be primarily related to two factors. First, there was an
obvious increase in plant growth due to temperature enhancement
(Fig. 4). Because dead plant leaves may take several years to fall and
decompose (Flanagan and Bunnell, 1980; Heal and French, 1974), if
the rate of decomposition lags behind the rate of plant growth,
there will be an annual accumulation of dead biomass. Second, in
the warmed plots, there was a shift in abundance toward large
sedges, which generally maintained standing dead matter longer
than most other growth forms such as forbs.
After 2 years of artificial temperature enhancement, marked
changes in plant biomass was found at two sites. The impacts of
temperature enhancement on plant production and biomass reallocation of alpine and tundra ecosystems have been studied in
several warming experiments. Many of them found significant
L. Na et al. / Soil Biology & Biochemistry 43 (2011) 942e953
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948
im
Fig. 7. Seasonal change of plant TN and OC in aboveground, and roots in the control, OTC1, and OTC2 plots at Site S (a, b) and Site A (c, d) after 2 years of warming treatments.
Fig. 8. Seasonal change of soil TN and OC contents in the control, OTC1, and OTC2 plots at Site S (a, b) and Site A (c, d) after 2 years of warming treatments.
949
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L. Na et al. / Soil Biology & Biochemistry 43 (2011) 942e953
Fig. 9. Seasonal pools of TN and OC in soil and plants in the control, OTC1, and OTC2 plots at Site S (a, b) and Site A (c, d) after 2 years of warming treatments.
positive effects on growth and reproduction of vegetations (Biasi
et al., 2008; Erschbamer, 2001; Gugerli and Bauert, 2001;
Klanderud, 2005; Kudo and Suzuki, 2003; Sandvik et al., 2004;
Totland, 1997, 1999; Totland and Nylehn, 1998; Wada et al., 2002;
Welker et al., 1997), reports of no apparent effects (Kudo and
Suzuki, 2003; Sandvik et al., 2004) or even negative responses
(Saavedra et al., 2003; Wada et al., 2002) were in the minority. Arft
et al. (1999) conducted a meta-analysis, and found significant
effects of temperature enhancement on vegetative growth and
reproductive success of alpine plants. In our study, aboveground
plant and root biomass were significantly increased by warming
throughout the growing season, at least in the short term. However,
greater temperature elevation in OTC2 plots led to smaller increments of biomass than that in OTC1 plots at both sites due to the
water limitation, and the biomass allocation became more likely to
be evenly distributed in the deeper soil layer (5e20 cm) (Fig. 7(a,
b)). It has been suggested that the plant growth in high altitude and
cold-climate ecosystems is mainly limited by low temperature
(Rehder, 1970) and nutrients (Bliss et al., 1981; Chapin and Shaver,
1985). Although warming could lead to greater plant production,
negative effects are also possible. For example, leaf mass of Pseudotsuga menzeisei saplings grown for 4 years in outdoor failed to
adequately respond to a 3.5 C increase of air temperature using
sunlit chambers (Olszyk et al., 1998). In our experiments, the mean
air temperature in OTC2 increased by more than 5.0 C during the
growing season, which presumably might exert a greater stress on
the ecosystems than that experienced on the OTC1 plots or during
Olszyk’s experiments. The proposed explanation for this decline
was that the buds were released from winter dormancy earlier in
the OTCs, which caused the needles to expand abnormally such
that the leaf area index, and hence plant growth was shrunk relative to those in control plots (Apple et al., 1998). A meta-analysis of
the experimental warming on plant growth found that the
magnitude of the effect size for the responses of plant productivity
was not significantly related to the magnitude of the warming
treatment (delta temperature) (Rustad et al., 2001). This contrasts
markedly with the results from individual studies, which have
demonstrated strong correlations between temperature and plant
growth, at least in the short term (Jonasson et al., 1999). Multiple
responses to warming can occur simultaneously, and the net
response may be difficult to predict (Rustad et al., 2001).
The vegetative growth of alpine plants across the two sites
increased after 2 years of experimental manipulation, substantiating our hypothesis that there would be a significant increase in
vegetative growth early in the experiment (Fig. 7). The initial
response of alpine plants to the warmer conditions was relatively
consistent across the circum arctic and in the alpine of the northern
hemisphere, supported by other site-specific findings, including
those by Chapin and Shaver (1985) and others. Our data are novel in
that we conducted a temperature enhancement experiment at two
warming gradients at two different alpine meadows, where sedges
represented the dominant component of the vegetation (Wang
et al., 2001). It is possible that temperature enhancement should
result in a direct effect of either increasing the plant growth or
prolonging the growing season, or an indirect effect of increased
nutrient availability. The increased rate of litter decomposition and
N mineralization may also indirectly contribute to the growth of
plants. Both direct and indirect effects of warming may be particularly important for ecosystems in high latitude and/or high altitude, in which temperature and soil nutrients level are likely to be
950
L. Na et al. / Soil Biology & Biochemistry 43 (2011) 942e953
the limiting factors (Rustad et al., 2001; Nadelhoffer et al., 1991), or
in some cases, the meristem network of tundra or alpine plants, i.e.,
source-sink carbon relations (Tissue and Oechel, 1987).
Finally, it is often possible to consider an extrapolation and
generalization using super ordinate functional levels (e.g. growth
forms, plant functional types) (Bernhardt, 2005). On the level of
growth forms, the results of our study are in line with other
warming experiments carried out in cold-climate ecosystems;
sedges are particularly stimulated by temperature enhancement
(Harte and Shaw, 1995; Sullivan and Welker, 2005; Zhang and
Welker, 1996). In these studies, there were different responses to
warming in these different community types. Differences in the
response among different growth forms could also be due to their
different morphology. A large leaf area, such as that on K. tibetica at
Site S and K. pygmaea at Site A and the physiological capacity to
alter patterns of resource allocation are two of the reasons given for
the opportunistic behavior of the sedges (Zhang and Welker, 1996).
The first should also be true for most sedge species. Another reason
for the strong response of sedges is the ability to utilize favorable
conditions at the end of the growing season (Welker et al., 1997;
Zhang and Welker, 1996).
4.3. Warming effects on the nutrient pools
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Vegetation and soil responses to warming can be caused by
direct (e.g. higher photosynthetic capacity, higher growth rates, or
longer growing season) or indirect temperature effects (e.g. higher
release of nutrients from soil organic matter) (Jonasson et al., 1999;
Rustad et al., 2001). In the control plots, OC and TN contents in soil
at Site S were relatively high, compared to the contents at Site
A (Table 1; Figs. 7 and 8). The markedly higher water content and
favorable soil condition found at Site S, as compared to Site A,
facilitated the accumulation of the biomass of plants both above
and belowground at Site S, resulting in increases of accumulation of
organic matter in soil, and thereby possibly increasing soil water
holding capacity (Brady and Weil, 1999). On the other hand, the
increases in plant productivity would result in a greater storage of C
and N in plant and an increased flux of C to soils in the forms of leaf
and root litter. This could at least partially offset the warminginduced increase of C flux from soils to the atmosphere via soil
respiration (Rustad et al., 2001).
Litter quality can be of decisive importance for microorganisms
engaged in the decay of organic matter, and for the subsequent
release of nutrients available for plants (Emmett et al., 2004). The
root C/N ratio at Site S was lower than that at Site A (Table 1). The
low degradation at Site S may have caused an accumulation of
organic matter in soil (Wedin and Tilman, 1990; Kristensen and
Henriksen, 1998), and thus increase soil water holding capacity
(Brady and Weil, 1999). In addition, a markedly thicker turf
(5e20 cm) and litter layer existed in the upper layer of soil at Site
S than at Site A (Wang et al., 2007). On one hand, the litter might
prevent the cold temperature from directly affecting the soil, acting
as a thermal insulation and water conservation tool. On the other
hand, the thick turf layers implied the presence of more labile
compounds (Gimingham, 1972). Since the microbial activity in
cold-climate ecosystems is limited by low temperature conditions
(Rehder, 1970), temperature can be of decisive importance for
microorganisms engaged in the decay of organic matter, and for the
subsequent release of nutrients available for plants (Emmett et al.,
2004). When the temperature increased, microorganisms engage in
the decay of organic matter in litter and soil, it means the amount of
both litter and soil organic matter decrease. As shown in Fig. 8b, we
can see that the extend litter decomposed to the soil was much
higher than that the soil organic matter decomposed to the air in
OTC2 plots at Site S. In our study, the alpine ecosystems are in
permafrost habitats, soil and vegetation in this region are greatly
influenced by the permafrost (Wang et al., 2001). With the growing
season, the permafrost melts, the active soil layer becomes thicker,
and thus the soil OC and other nutrients may infiltrate into the
deeper soil with the soil water, the allocation proportion of soil OC
appeared to transfer from the upper-soil layer to the deeper soil
layer.
In our study, both temperature enhancements in OTC1 and
OTC2 plots had significant impact on microbial biomass C and N
contents (Table 3). The temperature was of great importance for
microbes in both sites affecting both microbial biomass and soil
nutrients dynamics. A temperature enhancement should result in
an increase of organic matter decomposition, and thereby promote
nitrogen mineralization (Nadelhoffer et al., 1991). The slow
decomposition of soil organic matter during winter likely increases
the availability of oxidizable substrates and microbial populations
in the spring. As temperatures rise, there would be a flush of
microbial activity associated with the oxidation of these materials
(Ivarson and Sowden, 1970; Ross, 1972). At both sites, there was
evidence of this flush at the depths of 0e20 cm in the beginning of
the growing season, with increased contents of OC and TN in soil
and plant in OTC1 plots. Interestingly, the contents of OC and TN
decreased (instead of increased) in the OTC2 plots, particularly in
the soil layer (P < 0.05) (Figs. 7 and 8). While increasing temperature may have stimulated the growth of plants and accumulated
nutrients in plant tissue and soil in OTC1 plots at the two sites, the
warming effect caused soil moisture to decrease, but within a small
range (Fig. 2; Table 3), which should not be a threatening factor for
the microbes. The higher temperatures in OTC2 plots at Site S may
have intensely activated the microbes. The nutrients and moisture
in soil may have been favorable and sufficient for the microbes to
Table 3
Three-factor variance analysis with water content as covariate, soil at Site S and Site
A after 2 years of warming treatments.
Variable
Site S
Soil OC
Soil TN
Microbial C
Microbial N
Root OC
Root TN
Plant OC
Plant TN
Site A
Soil OC
Soil TN
Microbial C
Microbial N
Root OC
Root TN
Plant OC
Plant TN
Soil depth (cm)
Date
Water content
OTC1
OTC2
0e5
5e20
0e5
5e20
0e5
5e20
0e5
5e20
0e5
5e20
0e5
5e20
n.s.
*
***
**
*
*
***
**
*
n.s.
**
*
n.s.
n.s.
**
n.s.
n.s.
**
**
n.s.
*
***
**
***
**
***
n.s.
n.s.
***
**
**
*
*
**
***
**
**
*
**
**
**
**
***
*
***
***
**
**
***
**
**
**
**
**
n.s.
**
0e5
5e20
0e5
5e20
0e5
5e20
0e5
5e20
0e5
5e20
0e5
5e20
*
**
***
**
***
**
n.s.
***
**
***
***
***
***
***
n.s.
n.s.
*
***
**
**
**
**
***
**
n.s.
***
***
n.s.
**
*
**
***
**
***
*
*
*
**
*
**
n.s.
*
n.s.
n.s.
**
**
**
***
**
**
**
*
n.s.
**
n.s.
**
The levels of significance were P < 0.05*, and 0.01**, and 0.001***, n.s. means no
statistical significance.
L. Na et al. / Soil Biology & Biochemistry 43 (2011) 942e953
period. The soil in OTC2 sequestrated more OC (P < 0.05) than the
soil in OTC1 plots. These results were in accordance with the recent
reports carried in arctic tundra (Turunen et al., 2004; Welker et al.,
2004), where the deciduous shrubs was shown to profit from
warmer temperatures, as demonstrated in several studies from
moist tussock tundra (Sturm et al., 2005; Weintraub and Schimel,
2005). At Site A, as compared to Site S, soil moisture changed
significantly with warming. Compared to the control plots, warming effects caused more OC in soil to be released to the atmosphere
in OTC1 plots. The larger increasing temperature in OTC2 plots
accelerated this process, implying that Site A could be the net OC
source as a result of warming in a short term. Since low soil
moisture most likely reduces soil decomposition in these dry
ecosystems, soil OC loss may further decline with long-term
warming (Biasi et al., 2008).
5. Conclusions
Our study shows that swamp meadow and alpine meadow
ecosystems responded differently to warming than most other
arctic and high altitude ecosystems. Like most other studies, the
growth and productivity at the two sites were strongly accelerated
with warming, whereas pools of organic carbon and total nitrogen
reacted differently to artificial warming at two sites. The temperature enhancement overall resulted in swamp meadow acting as
net carbon sink and alpine meadow as net carbon source. Further
warming will strengthen this trend. In the Source Region of the
Yangtze River, the area covered by alpine meadow is about 9.2
times larger than the area covered by swamp meadow (Wang et al.,
2001). The trends of carbon source effects, therefore, may be
intensified by global warming on the Source Region of the Yangtze
River in the short term. This information partly supports the
hypothesis that climate warming may transform high altitude
ecosystems from net carbon sinks into net carbon sources. It can be
concluded that the responses of individual ecosystem processes to
warming strongly depends upon the ecosystem type itself. In order
to understand and predict the effects of warming on alpine
ecosystems accurately, more artificial temperature experiments on
more variable ecosystem types are necessary.
im
de
survive, resulting in more decomposed organic matters released to
the soil. This may have caused the OC and TN contents to decrease
in plant and soil, especially at the depth of 5e20 cm. At Site A, the
limitation of moisture tended to more severe with increasing
temperature (Table 3), resulting in lower apparent temperature
sensitivity in the field (Kirschbaum, 2000). Goncalves and Carlyle
(1994) reported that microbial biomass did not respond to
warmer soil temperatures because microbial activity was restricted
by soil moisture content. Results reported here in OTC2 at Site
A agreed with the results of Goncalves and Carlyle (1994); the
lowest level of microbial biomass occurred at Site A with OTC2,
which might be attributed to an cumulative effect of warming, the
decline of soil moisture, the limitation in soil nutrients supply for
plants, and the decline in the availability of labile C sources for soil
microbes (Peterjohn et al., 1994; Arft et al., 1999). Moisture limitation may sometimes mask the responses to temperature, particularly at relatively high temperatures (Davidson et al., 1998).
OC and TN contents in plant and soil both peaked during the
vigorous growing period in the control plots. Warming effects in
OTC1 plots had significant direct effect on plant growth and tissue
OC and TN contents at the two sites (Fig. 7; Table 3). At Site S,
temperature and water condition become more suitable for plants
and microbes in OTCs. The higher gross photosynthesis most likely
resulted from the significantly increased plant biomass and nutrients in the warmed plots (Figs. 4, 7 and 8). The escalated plant
nutrients most likely improved plant associated respiration
(Kirschbaum, 2000). Warming effects in OTC2 plots, however,
activated microbes significantly, and enhanced organic matter
decomposition, resulting in a noticeable increase in soil nutrients
and translocation of nutrients in both root and soil from upper-soil
layer to deeper layer. The trends persisted until the end of the
growing season (Fig. 9). At Site A, warming caused higher net
ecosystem carbon loss in the warmed soils compared to soils at
ambient temperatures and lower warming temperature (Fig. 9).
This contrasts with the most often cited explanation for the lack of
response or negative response to increasing temperature, which is
that the concomitant decline in soil moisture is often associated
with warming. At individual sites, reduced or lower soil moisture
had been cited for the decline in soil respiration response to
warming (McHale et al., 1998; Peterjohn et al., 1994; Rustad and
Fernandez, 1998). In our study, despite the decrease in soil moisture, high net ecosystem OC and N loss were detected at Site
A (Fig. 9). This might be attributed to the high altitude and
permafrost region of the ecosystem, where the temperature was an
extreme limiting factor for the plant and microbes. When the
environment was exposed to warming, the higher temperature and
soil moisture may have intensely activated the microbes, resulting
in more decomposed organic carbon released to the air, caused the
pools of OC and TN to decrease. The fluctuation of the pools of plant
and soil nutrients in the end of the growing season was consistent
with the variations of temperature in the vigorous growing season.
These results supports our hypothesis that alpine meadow
ecosystem may at least temporarily act differently compared to the
swamp meadow ecosystem as a result of climate warming.
Although plant biomass increased with warming temperature
and higher soil nutrient availability, the contents of OC and TN in
plant tissues and soil responded differently to the warming at both
sites (Figs. 7 and 8). Climate warming is expected to alter the
nutrients composition of the vegetation and the soil of many
ecosystems in the long-term (Walker et al., 2006). In our study, the
warming effects in OTC1 plots at Site S sequestrated more OC
throughout the growing season, and it acted as net OC sinks.
However, the Site S ecosystem in the OTC2 plots, at least in the
short term, turned to net OC source in the beginning of growing
season. It then returns to net OC sink during the following growth
951
Acknowledgments
We would like to thank the National Basic Research Program
(973) (2007CB41150) and National Science Fund for Distinguished
Young Scholars (40925002) of China for funding this project. Our
gratitude extends to the Fenghuoshan Field Station of the Northwest Research Institute Co., Ltd. of China Railway Engineering
Corporation for their assistance in the field and the Southwest
University for their assistance in chemical analysis. The authors
wish to thank Wang Junfeng, Bai Wei, Sun Xiangmin, and Li Chunjie
for field sampling and an anonymous reviewer for providing
valuable comments and guidance.
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