ORIGINAL PAPER

Temporal patterns of soil CO2 efflux in a temperate Korean Larch(Larix olgensis Herry.) plantation, Northeast China

Wenzhong You • Wenjun Wei • Huidong Zhang •

Tingwu Yan • Zhaokai Xing

Received: 19 August 2012 / Revised: 20 March 2013 / Accepted: 24 May 2013

� Springer-Verlag Berlin Heidelberg 2013

Abstract There is little information available regarding

seasonal and annual variations in soil CO2 efflux from Korean

Larch plantations, which are an important component of for-

ests’ carbon balance in temperate China. In this study, the soil

respiration rate (Rs), soil temperature (T10) and soil moisture

(SM10) at 10 cm depth were observed in a Korean Larch

(Larix olgensis Herry.) plantation in Northeast China from

2008 to 2012. Mean Rs in growing season (GS) varied greatly,

ranged from 2.32 ± 0.08 to 3.88 ± 0.09 lmol CO2 m-2 s-1

(mean ± SE) over the period of 2008–2012. In comparison

with T-model, the increase of explained variability by

applying both T10 and SM10 to the T-M model is very small. It

is indicated that Rs was controlled largely by T10 in the present

study. By accounting for 22.2 and 17.7 % of the total soil CO2

emissions in 2010/2011 and 2011/2012, respectively, the soil

CO2 efflux in dormant season (DS) was an essential compo-

nent of the total soil CO2 efflux. The Q10 value in the study

period was always smaller for GS than DS, suggesting that soil

carbon cycling may be more sensitive to the temperature

changes at low than at high temperature range. These results

indicated that climate changes may have great potential

impacts on temperate Larch plantations in Northeast China,

owing to soil carbon emissions of Larch plantation during the

long period of DS being more sensitive to T10 than in GS, and

played a significant role in the annual forest ecosystems car-

bon budget.

Keywords Korean Larch plantation � Soil respiration

rate � Soil CO2 efflux � Growing season � Dormant season

Abbreviations

Rs Soil respiration rate

T10 Soil temperature at 10 cm depth

SM10 Soil moisture at 10 cm depth

TA Air temperature

PPT Precipitation

GS Growing season

DS Dormant season

Fg Soil carbon efflux in growing season

Fd Soil carbon efflux in dormant season

Ft Annual total soil carbon efflux

Introduction

Soil CO2 efflux in forests is the second largest carbon flux

in terrestrial ecosystems (Fahey et al. 2005; Janssens et al.

2001), and plays a significant role in global carbon cycling

(Luan et al. 2011; Maier and Kress 2000; Zhu et al. 2009).

To estimate forest ecosystem carbon cycling, reliable field

data pertaining to the carbon budget from a variety of forest

types are required. The soil carbon efflux has been shown

to account for 70 % of ecosystem carbon flux in temperate

forests (Law et al. 1999); accordingly, it is crucial to study

the soil carbon efflux in temperate forests to best under-

stand global carbon cycling (Davidson et al. 1998; Kang

et al. 2003; Pang et al. 2012; Wang et al. 2006, 2011,

2012).

Larch-dominated forests are a major portion of the forest

ecosystem in temperate China, which account for 9.4 % of

the total forest biomass carbon sink in these areas (Zhou

Communicated by U. Luettge.

W. You � W. Wei (&) � H. Zhang � T. Yan � Z. Xing

Liaoning Academy of Forestry, Shenyang 110032, China

e-mail: wwj0318@126.com

123

Trees

DOI 10.1007/s00468-013-0889-6

et al. 2000). There are 6.4 million hectares of Larch

plantations in China, of which 73 % are planted in

Northeast China (including Liaoning, Jilin and Heilongji-

ang provinces). Since the twentieth century, large areas of

Larch-dominated plantations were established after the

primary forests were harvested for industrial logging (Chen

et al. 1994), and they have now become the major com-

ponents of forests in these areas (accounting for 17.01 and

15.69 % of the total forest area in 1994–1998 and

1999–2003, respectively) in recent decades (Chinese

Administration of Forestry (CFA) 1999, 2004). Conse-

quently, the dynamics of soil carbon efflux in temperate

larch plantations would have a great effect on carbon

cycling in Northeast China.

Recent studies have reported that total soil respiration

during the dormant season (DS) (Fd, g C m-2 season-1) in

northern ecosystems is important in calculations of global

carbon cycling (Alm et al. 1999; Fahnestock et al. 1999;

Grogan and Jonasson 2006). Northeast China is located in

the mid-latitude of the northern hemisphere, and the dor-

mant season in this region usually lasts for more than

200 days each year. Appreciable ecosystem respiration

occurs during winter (January–March), which strongly

suggests that biological activity and biogeochemical car-

bon cycling are active and important throughout winter

(Grogan and Jonasson 2005). The Fd is an essential com-

ponent of total annual soil respiration (Oechel et al. 1997;

Vourlitis and Oechel 1999; Zimov et al. 1996) because the

majority of leaf litter is supplied to the forest floor in

deciduous forests during autumn, and these materials likely

contribute to Fd due to their decomposition (Uchida et al.

2005). Most studies of carbon dynamics in forests in

Northeast China have been conducted during the growing

season (GS), and the mean soil respiration rate (Rs, lmol

CO2 m-2 s-1) during GS was applied to estimate the CO2

efflux in GS (Fg, g C m-2 season-1) from soil in these

areas (Wang and Yang 2007; Zhang et al. 2008; Zhu et al.

2009). However, Brooks et al. (2004) found that Ft has

been shown to be overestimated by 71 and 111 % in

deciduous and coniferous forests, respectively, when Fd

was not included. The Fd values in Larch plantations in

Northeast China have not been fully determined, and the

factors controlling seasonal variability of the Rs are not

completely understood. Moreover, elevated CO2 concen-

trations in the atmosphere accelerate the rising winter

temperatures in mid-latitudes in the Northern Hemisphere,

and may result in greater emissions of CO2 to the atmo-

sphere from soil during DS (Li et al. 2010). Consequently,

it is necessary to estimate Fd more accurately to fully

understand the seasonal and annual variations of soil car-

bon efflux and its abiotic impact factors.

In this study, the seasonal and interannual variations of

Rs and its major driving abiotic factors [air temperature

(TA, �C), precipitation (PPT, mm), soil temperature

(T10, �C) and soil moisture (SM10, %) at 10 cm] were

studied during the period of May 2008 to April 2012 in a

temperate Korean Larch (Larix olgensis Herry.) plantation

in Northeast China. The major objectives of the present

study were to determine: (1) how Rs varied during seasons

and years; (2) how much the Fd contributed to total soil

efflux annually (Ft, g C m-2 year-1); (3) estimated Fg, Fd

and Q10 values among seasons and years; and (4) how

seasonal Rs, Fg, Fd and Q10 were affected by abiotic factors

(TA, PPT, T10 and SM10).

Materials and methods

Site description

In this study, experiments were carried out in the Bingla

Mountain Forest Ecological Station in Liaoning Province,

northeast China (124�450–125�150E, 42�200–42�400N). The

study area is located in the warm-mid temperate transition

region. The area is subject to a continental monsoon cli-

mate (with a strong monsoon windy spring, a warm and

humid summer, and a dry and cold winter), with the lowest

temperature of -31.6 �C occurring in January, and the

highest temperature of 34.7 �C occurring in July. The

annual mean temperature was 6.2 �C and the annual

average effective cumulative temperature (C10 �C) was

1,374.3 �C. The annual average precipitation was

669.6 mm, of which rains almost falls in June, July and

August, and snows almost fall in December, and January,

February next year. The snow began to accumulate in late

November and the maximum depth was 35 cm in the late

January. A continuous snowpack lasted from the late

November to the end of March in next year.

The selected Korean Larch plantation was established

after clear cutting of the primary vegetation, which con-

sisted of broadleaved Korean pine (Pinus koraiensis Sieb.

et Zucc.), in the 1960s. The Larch plantation grew on the

northwest slope of the mountain at altitude between 320

and 450 m. The stand was 46-year old in 2008, and the

stand density was 930 trees ha-1. The mean diameter at

breast height (DBH) was 17.3 cm, the mean height was

15.0 m and the canopy density was 80 %.

Measurement of soil respiration rate

An open-flow chamber method was used to measure the

Rs in the present study. Three 30 m 9 20 m permanent

plots at altitude of 320, 380, and 450 m were set up in

the Korean Larch plantation. Four polyvinyl chloride

(PVC) collars (21.34 cm inside diameter, 11.43 cm

height) were located diagonally at equidistant points in

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123

each plot for Rs measurement, and the litter was allowed

to remain on the surface during the experiment. The

PVC collars were inserted into the soil to a depth of

10 cm, and remained there from July 2007 so that the

sampling points remained under natural conditions. These

PVC collars supported the chamber and sealed it against

the surface. The air within the chamber was continuously

circulated through a portable CO2 infrared gas analyzer

(Li-8100) (Li-cor Inc, Lincoln, NE, USA). Measurement

of Rs in GS was started from May 2008, and the Rs in

DS from October 2010. The Rs was measured on rainless

days 1–3 times a month in GS, and 1–2 times in DS

because of the meteorological limitations (especially for

the cold weather). The above-ground portion of the live

plant in the collars was clipped to avoid the effects of

photosynthesis in GS. The snowpack was kept undis-

turbed to prevent the effects of snow depth changes on

soil temperature in DS. The DS was defined as being the

duration when the leaves falling began for most local

deciduous species to sprout began the next year. GS was

roughly from Julian day 119 in April to 270 in Sep-

tember, and DS was approximately from Julian day 271

in September to 118 in April the next year in present

study. The Rs was measured at 9:00–11:00 a.m., because

studies conducted in northeast China have revealed that

the Rs is closer to its diurnal mean value at this time

(Wang and Yang 2007; Zhang et al. 2008; Zhu et al.

2009). The mean Rs for each collar was determined

based on the average of three values calculated from

three repeated measurements at each collar.

Measurement of abiotic factors

The T10 and SM10 were measured at the same time as the

Rs using a thermometer attached to the Li-8100. The values

were corrected by the T10 and SM10 values obtained using a

109-L temperature probe and CS616-L water content

reflectometer (Campbell Inc., North Logan, UT, USA)

present in the forest microclimate gradient observation

system in Bingla Mountain Forest Ecological Station. The

forest microclimate gradient observation system was set up

near the Rs measurement plots in 2008 and the T10 and

SM10 values were monitored every 10 min. In a frozen soil,

oven drying method under a constant temperature of

105 �C was applied to the soil samples got by aluminum

specimen box for obtaining the SM10 in DS instead. The TA

was observed through HMP45D relative humidity and

temperature probe (Transcat Inc, Rochester, NY, USA),

and PPT was measured through 52202 tipping bucket rain

gauge (R. M. Young Inc, Traverse City, MI, USA) every

10 min, which were installed on the automatic meteoro-

logical station in Bingla Mountain Forest Ecological

Station.

Data analysis

T10 and SM10 both have great impacts on Rs. In the present

study, exponential curve fitting was conducted to analyze

the relationships between Rs and T10 in GS and DS (T

model; Eq. 1), and exponential-power curve fitting was

applied to describe the relationship between Rs and the

T10–SM10 interaction (T-M model; Eq. 2). Curve fitting

was accomplished using SigmaPlot 10.0.

Rs ¼ b0eb1T10 ð1Þ

Rs ¼ b0eb1T10 SMb2

10 ð2Þ

where b0, b1 and b2 are regression coefficients.

The Q10 value was calculated by Eq. 3.

Q10¼ e10b1 ð3Þ

The best fitting models obtained and the continuous

monitoring of T10 and SM10 data were used to assess the Fg

during 2008 and 2011, and Fd in 2010/2011 and 2011/

2012. The T10 and SM10 in 2008–2012 observed through

the forest microclimate gradient observation system near

the Rs measurement plots were applied to the best fitting

models to evaluate the Rs, then the Rs values acquired with

day as the step were summed for the Fg and Fd. Finally, the

Fg in 2010 and the following Fd in 2010/2011 were added

together to obtain the Ft for 2010/2011, so did Ft in 2011/

2012 (Eq. 4). In view of that the Rs data were only

available for these successive GS and DS in the present

study.

Ft ¼ Fg þ Fd ð4Þ

Linear curve fitting was used to analyze the interannual

relationship between seasonal mean Rs, Fg, Fd, Q10 value

and abiotic factors (TA, PPT, T10, and SM10). Curve fitting

was performed through applying SigmaPlot 10.0 as well.

Results

Seasonal and interannual variations in soil respiration

rate and abiotic factors

Mean Rs in GS varied greatly, ranged from 2.32 ± 0.08 to

3.88 ± 0.09 lmol CO2 m-2 s-1 (mean ± SE) over the

period of 2008–2012 (Table 1). However, there was little

variation in mean Rs in DS, with 0.6 ± 0.06 lmol CO2

m-2 s-1 in 2010/2011 and 0.42 ± 0.02 lmol CO2

m-2 s-1 in 2011/2012 (Table 1).

Seasonal variations in Rs followed a bell-shaped curve in

the Korean Larch plantation (Fig. 1a). In comparison with

SM10, seasonal variations of Rs exhibited more similar

variation patterns with TA and T10 during the periods of

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123

2008–2012 (Fig. 1). During GS, the maximum Rs occurred

in the end of July in 2008 (5.95 lmol CO2 m-2 s-1) and

2009 (3.61 lmol CO2 m-2 s-1), mid of August in 2010

(5.91 lmol CO2 m-2 s-1), and early July in 2011

(5.55 lmol CO2 m-2 s-1) (Table 1; Fig. 1a). During DS,

the minimum Rs appeared in mid of January in 2011

(0.08 lmol CO2 m-2 s-1) and early February in 2012

(0.01 lmol CO2 m-2 s-1) (Table 1; Fig. 1a).

Effects of abiotic factors on soil respiration rate

during the growing season and dormant season

Soil temperature and moisture are two of the most important

abiotic factors controlling Rs (Lloyd and Taylor 1994;

Buchmann 2000; Schlesinger and Andrews 2000). The

variations in Rs in Korean Larch plantations could be

described by T10 using an exponential equation (T model).

Table 1 Soil respiration rate (Rs, lmol CO2 m-2 s-1) of Korean Larch plantation during growing season (GS) and dormant season (DS) from

2008 to 2012

Soil respiration rate Growing season Dormant season

2008 2009 2010 2011 2010/2011 2011/2012

Mean ± SE 3.88 ± 0.09 2.32 ± 0.08 3.21 ± 0.13 2.9 ± 0.17 0.6 ± 0.06 0.42 ± 0.02

Range 1.17–5.95 0.89–3.61 0.93–5.91 0.66–5.55 0.08–1.83 0.01–1.91

SE standard error

Fig. 1 Variations of soil respiration rate (Mean ± SE, a), soil

temperature at a depth of 10 cm (Mean ± SE, b), soil moisture at a

depth of 10 cm (Mean ± SE, c), air temperature (Mean, d) and

precipitation (Mean, e) in Larch plantation in growing seasons (open

circle) and dormant seasons (closed circle) during 2008 and 2012.

The dotted lines within the dormant seasons indicated the periods

with snow cover. The horizontal axis of a, b, c and d were Julian day,

and the horizontal axis of e was month. SE standard error

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123

This model explained 56, 36, 62 and 48 % of Rs variability

during GS in 2008, 2009, 2010 and 2011 (p \ 0.0001),

respectively, and 71 and 56 % during DS in 2010/2011 and

2011/2012 (p \ 0.0001), respectively (Figs. 2, 3). In the

present study, T10 and SM10 were both applied to describe

variation in Rs (T-M model) as well, and they were found to

explain 58, 37, 68 and 55 % during GS in 2008, 2009, 2010

and 2011, respectively, and 78 and 67 % during DS in

2010/2011 and 2011/2012 (p \ 0.0001), respectively

(Table 2). Although the T-M models explain more of the Rs

variability than T model, the increase of explained variability

by adding SM10 to the model is very small. The Rs in the

Korean Larch plantations from 2008 to 2012 is mainly

controlled by soil temperature. Therefore, the T models were

applied to estimate Fg and Fd during 2008 and 2012.

Comparisons of soil CO2 efflux and Q10 value

between the growing season and dormant season

The Fg from 2008 to 2011 were 549, 306, 480 and

429 g C m-2 season-1, respectively (Table 3). The Fd was

137 g C m-2 season-1 in 2010/2011, and 92 g C m-2

season-1 in 2010/2011 (Table 3). The Ft was 618 g C

m-2 year-1 in 2010/2011, and 521 g C m-2 year-1 in

2011/2012, in which Fd accounted for 22.2 and 17.7 %,

respectively.

The Q10 values calculated through the T-M model were

2.2, 1.62, 3.29, and 2.18 in GS in 2008, 2009, 2010 and

2011, respectively. The Q10 values in DS were larger than

in the corresponding GS, which were 3.67 and 3 during DS

in 2010/2011 and 2011/2012, respectively (Table 3).

10 12 14 16 18 20 22 24Soi

l res

pira

tion

rate

(R

s)/µ

mol

CO

2 m

-2 s

-1

0

1

2

3

4

5

6

7Rs=0.927exp(0.079T10) R

2=0.56 p<0.0001 n=189

(a)

12 14 16 18 20 22 24 26 28.5

1.0

1.5

2.0

2.5

3.0

3.5

4.0Rs=0.94exp(0.048T10) R

2=0.36 p<0.0001 n=79

(b)

0

1

2

3

4

5

6

7Rs=0.39exp(0.119T10) R

2=0.62 p<0.0001 n=65

Soi

l res

pira

tion

rate

(R

s)/µ

mol

CO

2 m

-2 s

-1

Soil temperature at 10 cm depth (T10)/°C Soil temperature at 10 cm depth (T10)/°C

(c)

12 14 16 18 20 22 24 6 8 10 12 14 16 18 20 22 240

1

2

3

4

5

6Rs=0.743exp(0.078T10) R

2=0.48 p<0.0001 n=71

(d)

Fig. 2 The relationship between the soil respiration rate (Rs) and soil temperature at a depth of 10 cm (T10) (T model) in Larch plantation during

growing seasons (GS) in 2008 (a), 2009 (b), 2010 (c) and 2011 (d)

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123

Interannual impacts of abiotic factors on mean soil

respiration rate, soil carbon efflux and Q10 values

Rs, Fg and Fd had significant positive relationship with TA,

T10 and PPT (Figs. 4a, b, d, 5a, b, d), but had no significant

relationship with SM10 (Fig. 4c, 5c). However, the Q10

values were not significantly correlated with TA, T10, SM10

and PPT (Figs. 6a–d).

Discussion

Effects of soil temperature and soil moisture on soil

respiration rate

Rs was considered to be controlled largely by soil tem-

perature, which was supported by the findings that the T

model was insignificantly improved by introducing SM10

Soil temperature at 10 cm depth (T10)/°C Soil temperature at 10 cm depth (T10)/°C

-10 -5 0 5 10 15Soi

l res

pira

tion

rate

(R

s)/µ

mol

CO

2 m

-2 s

-1

Soi

l res

pira

tion

rate

(R

s)/µ

mol

CO

2 m

-2 s

-1

0.0

.5

1.0

1.5

2.0

2.5

Rs=0.45exp (0.13T10) R2=0.71 p<0.0001 n=103

(a)

-10 -5 0 5 10 15

0.0

.5

1.0

1.5

2.0

2.5(b)

Rs=0.36exp (0.11T10) R2=0.56 p<0.0001 n=209

Fig. 3 The relationship between the soil respiration rate (Rs) and soil temperature at a depth of 10 cm (T10) (T model) in Larch plantation during

dormant seasons (DS) in 2010/2011 (a) and 2011/2012 (b)

Table 2 The relationship between soil respiration rate (Rs) and soil temperature at a depth of 10 cm (T10), soil moisture at a depth of 10 cm

(SM10) (T-M model) in Larch plantation during the period of 2008–2012

Season Years T-M model R2 p n T10 range (�C) SM10 range (%)

Growing season 2008 Rs ¼ 0:424e0:089T10 SM0:93910

0.58 \0.0001 189 11.3–23 21.7–39.4

2009 Rs ¼ 0:303e0:063T10 SM0:7210

0.37 \0.0001 79 13.2–25.9 29.5–67.5

2010 Rs ¼ 0:052e0:121T10 SM1:60710

0.68 \0.0001 65 12.7–21.9 33.5–82.9

2011 Rs ¼ 0:1e0:1T10 SM0:58310

0.55 \0.0001 71 7.75–24.3 24.8–50.9

Dormant season 2010/2011 Rs ¼ 0:82e0:14T10 SMð�0:19Þ10

0.78 \0.0001 103 -8.24 to 11.73 32.3–53.3

2011/2012 Rs ¼ 5:1e0:16T10 SMð�0:9Þ10

0.67 \0.0001 209 -6.4 to 12.8 14.4–42.9

Table 3 Seasonal Q10 values and soil carbon efflux during the period of 2008–2012

Growing season Dormant season

2008 2009 2010 2011 2010/2011 2011/2012

T10 (Mean ± SE, �C) 17.81 ± 0.23 18.84 ± 0.41 17.43 ± 0.31 16.74 ± 0.53 1.71 ± 0.62 0.6 ± 0.3

Q10/T model 2.20 1.62 3.29 2.18 3.67 3.00

Q10/T-M model 2.44 1.88 3.35 2.72 4.06 4.95

Soil carbon efflux (g C m-2 season-1) 549 306 480 429 137 92

SE standard error

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123

as a variable (T-M model) (Table 2; Figs. 2, 3). This result

was consistent with other studies (Wang and Yang 2007;

Wang et al. 2011). The T model fits better in DS than

during GS, which indicated that Rs can be better explained

through T10 in DS than in GS. Similar trends were observed

in that soil temperature was the best explanatory variable to

characterize the variation of Rs in DS (Grogan and Jonas-

son 2005; Schlentner and Van Cleve 1985), and the Rs in

DS was more sensitive to T10 than during GS. This dis-

tinction may be important because respiration from bulk

soil and plant-associated carbon pools can differ

significantly in their apparent sensitivity to temperature

variations occurring through winter and summer (Grogan

and Jonasson 2005). Moreover, the relationship between air

and soil temperature is likely to be far more complicated in

winter than in summer because of the potential influence of

snow cover as a thermal insulator (Taras et al. 2002). The

differences in snow accumulation resulted in corresponding

differences in soil temperature, and the ecosystem respi-

ration was found to be sensitive to increases in snow

accumulation up to 1 m (Grogan and Jonasson 2005). The

snowpack was present in the forest for a long period of

Seasonal mean air

Sea

sona

l mea

n so

il

(µm

olC

O2

m-2

s-1)

0

1

2

3

4

5

Seasonal mean soil

at 10 cm depth (T10)/°C

Rs=0.11TA+1.11

R2=0.86 p<0.01

Rs=0.15T10+ 0.36

R2=0.85 p<0.01

Seasonal mean soil

at 10 cm depth (SM10)/%

Rs=0.02SM10+1.4

R2=0.01 p>0.1

Seasonal mean precipitation (PPT)/mm

-5 0 5 10 15 0 5 10 15 25 30 35 40 45 50 55 200 300 400 500 600 700

Rs=0.06PPT-0.27 R2=0.67 p<0.05

resp

iratio

n ra

te

temperature (TA)/°C temperature moisture

Fig. 4 The interannual relationship between the seasonal mean soil respiration (Rs) and air temperature (TA, a), soil temperature at a depth of

10 cm (T10, b), soil moisture at a depth of 10 cm (SM10, c), precipitation (PPT, d) in Larch plantation during 2008 and 2012

0

100

200

300

400

500

600

Sea

sona

l soi

l CO

2

efflu

x/(g

m-2

a-1

) Fg/d=13.9TA+191

R2=0.80 p<0.05

Fg/d=19.3T10+ 97

R2=0.78 p<0.05

Fg/d=3.6SM10+199

R2=0.02 p>0.1

Fg/d=0.81PPT-7.7 R2=0.71 p<0.05

-5 0 5 10 15 0 5 10 15 25 30 35 40 45 50 55 200 300 400 500 600 700

Seasonal mean airtemperature (TA)/°C

Seasonal mean soil

at 10 cm depth (T10)/°C

Seasonal mean soil

at 10 cm depth (SM10)/%

Seasonal mean precipitation/mmtemperature moisture

Fig. 5 The interannual relationship between the total soil CO2 efflux

in growing season (Fg) and dormant season (Fd) and air temperature

(TA, a), soil temperature at a depth of 10 cm (T10, b), soil moisture at

a depth of 10 cm (SM10, c), precipitation (PPT, d) in Larch plantation

during 2008 and 2012

Q10

val

ue

1.5

2.0

2.5

3.0

3.5

4.0Q10=3-0.04TAR2=0.44 p>0.1

Q10=3.4-0.06T10R2=0.47 p>0.1

Q10=0.03M10+1.17

R2=0.14 p>0.1Q10=2.7-1.4*105PPT R2=1.14*10-5 p>0.1

Seasonal mean air Seasonal mean soil

at 10 cm depth (T10)/°C

Seasonal mean soil

at 10 cm depth (SM10)/%

Seasonal mean precipitation/mm

-5 0 5 10 15 0 5 10 15 25 30 35 40 45 50 55 200 300 400 500 600 700

temperature (TA)/°C temperature moisture

Fig. 6 The interannual relationship between the Q10 values and air temperature (TA, a), soil temperature at a depth of 10 cm (T10, b), soil

moisture at a depth of 10 cm (SM10, c), precipitation (PPT, d) in Larch plantation during 2008 and 2012

Trees

123

time, but may be very light during winter in Northeast

China. The limited snowpack could lead to relatively

ineffective thermal insulation against low air temperatures,

and a low Fd due to more severe soil temperatures that limit

decomposers (Schlesinger and Andrews 2000). Further-

more, when snowfall is relatively low, trees can influence

the spatial pattern of deposition and/or subsequent redis-

tribution by wind, resulting in preferential accumulation,

and the potential for snow trapping by local topography

within forest land. At the end of DS, we also found that Rs

fluctuated as in other studies (Grogan and Jonasson 2005),

which may have been caused by the alternate freezing and

thawing. Pinck et al. (1961) reported that a single freeze–

thaw cycle could kill up to 50 % of the microbial biomass,

and may induce variations of Rs (Uchida et al. 2005). Such

frequent occurring of alternate freezing and thawing caused

by the severe temperate variation, interannual uneven

snowpack depth and duration in our study site may affect

the Rs indirectly in DS. These uncertain factors perhaps

caused that soil CO2 emissions in our study site would be

more sensitive to the climate change in DS than in GS.

Seasonal and interannual variation of Q10 value

Q10 is considered to be an index of the sensitivity of Rs to

temperature (Lloyd and Taylor 1994; Janssens and Pileg-

aard 2003; Pang et al. 2012; Wang et al. 2010). In this

study, the Q10 value calculated using the T model varied

from 1.62 to 3.29 in GS during 2008–2011, and from 3.67

to 3 during DS in 2010–2012 (Table 3). However, these

variations were not significantly related with annual or

seasonal variations of TA and T10 in the present study

(Fig. 6a, b). In addition, the Q10 values could also be

influenced by root biomass, litter input, microbial popula-

tion and activity, and other processes, such as plant phe-

nological patterns (Curiel Yuste et al. 2004). During the

period of 2008–2012, the Q10 value calculated by T models

was always smaller for GS than DS (Table 3). It was

consistent with the conclusion that Q10 was lower in areas

with higher temperatures than in those with lower tem-

peratures (Raich and Schlesinger 1992), suggesting that the

temperature changes may have stronger implications on Rs

at low- than at high temperature range (Chen et al. 2010).

The short-term laboratory incubation of Arctic tundra soil

showed that the range of the mean Q10 was even greater,

ranging from 7.8 to -134 (Mikan et al. 2002). There is also

evidence that the temperature sensitivity of Rs is not con-

stant (Table 3) (Luo et al. 2001; Xu and Qi 2001; Drewitt

et al. 2002; Janssens and Pilegaard 2003). Moreover, Q10

changes seasonally in response to root biomass and litter

input, which depend on vegetation types and phenology, as

well as the composition of the microbial community and

other physiological and ecological acclimatization in

response to substrate supply, which affects Q10 through its

respiratory capacity in soil (Atkin et al. 2000; Bowden

et al. 1993; Boone et al. 1998; Cornwell et al. 2008; Curiel

Yuste et al. 2004; Valverde-Barrantes 2007; Widen and

Majdi 2001). Furthermore, Boone et al. (1998) found that

the different seasonal Q10 values of Rs observed through

GS in a temperate forest were primarily determined by

variations of root respiration in response to seasonal tem-

perature changes.

Soil CO2 efflux of Larch forests in Northeast China

Temperate Larch forests cover a large area in Northeast

China. The Ft of Dahurian Larch (Larix gmelinii Rupr.)

natural forest and plantation in cool-temperate China are

706.33 g C m-2 year-1 (Great Khingan Mountain, Inner

Mongolia Autonomous Region) and 405 g C m-2 year-1

(Maoer Mountain, Heilongjiang province) (Table 4)

(Zhang et al. 2008; Wang and Yang 2007). In this study,

the Ft ranged from 521 to 618 g C m-2 year-1, which was

obtained in the mid- and warm-temperate transition zones

(Table 3). Total Ft at our site was higher than that of a

similar Larch plantation at a cool-temperate site, but much

lower than that of a natural Larch forest in a cool-temperate

area. The results for the Larch plantations were similar to

those of many other studies that suggested CO2 released

from soil in most forests decreased from warm to cold

regions (Grogan and Jonasson 2006; Janssens and Pileg-

aard 2003). However, the opposite was found for natural

Larch forest in cold areas, for which the amount of CO2

released was larger than that of plantations in both warm

and cold regions, which was primarily caused by the higher

amount of organic carbon accumulated in litter and soil in

old natural forest (Raich and Tufekcioglu 2000; Singh et al.

2008; Valverde-Barrantes 2007) (Table 4). These findings

implied that the abiotic factors (temperature and water) and

biotic factors (soil organic carbon content, litter storage)

have complex interaction effects on Ft, but are mostly

dependant on biotic factors.

Importance of soil CO2 efflux during the dormant

season in total soil CO2 efflux in mid-latitude

ecosystems

The Fg ranged from 306 to 549 g C m-2 season-1 during

2008 and 2011, which varied greatly with coefficient of

variance (CV) 23 % in these 4 years. This distinction would

be caused by the large interannual variation of TA, T10 and

PPT, as Fg was significantly correlated with these three fac-

tors (Fig. 5a, b, d). A large number of Ft estimates from mid-

latitude ecosystems were based on observations taken in GS

because of meteorological limitations for DS measurements.

Measurements of Fd in the present study showed amounts of

Trees

123

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Trees

123

carbon loss from the Korean Larch forest floor throughout the

215-day DS. In this study, the Fd of the Larch plantation were

from 137 to 92 g C m-2 season-1 in DS in 2010/2011 and

2011/2012(Table 3). In comparison with other estimates of

Fd in mid-latitude regions, our results were larger than the Fd

of peatlands in eastern Finland, low arctic tundra communi-

ties in Toolik Lake in Alaska, mountain forests in Austria,

and alpine and sub-alpine forests in the Western Chugach

Mountains in Alaska (Alm et al. 1999; Fahnestock et al. 1999;

Schindlbacher et al. 2007; Sullivan et al. 2010) (Table 5),

while it was similar to the estimates of Fd of natural snowdrift

communities in Toolik Lake in Alaska and cool-temperate

forests in Japan (Fahnestock et al. 1999; Mariko et al. 2000)

(Table 5). The contribution rate of Fd to Ft ranged from 17.7

to 22.2 % in this study (Tables 3, 5), which was within the

range of 6–23 % of the Ft throughout the dormant season

obtained in many studies conducted in mid-latitude ecosys-

tems (Alm et al. 1999; Fahnestock et al. 1999; Mariko et al.

2000; Mast et al. 1998; McDowell et al. 2000; Mo et al. 2005;

Schindlbacher et al. 2007; Sullivan et al. 2010; Zimov et al.

1996) (Table 5). Special emphasis was placed on the

importance of the Fd as a component of the annual soil carbon

budget (Aurela et al. 2002). Some microbial decomposition

may occur at temperatures as low as -10 to -17 �C (Panikov

and Dedysh 2000). Conditions are suitable for microbial

activity in boreal and subarctic organic soils throughout the

winter, caused by the soil surface temperature fell below the

limit but the temperatures in deeper layers are usually more

favorable (Aurela et al. 2002). Fd over the long DS constitute

a considerable carbon loss that should be taken into account

to best understand the ecosystem carbon budget in mid-lati-

tude ecosystems.

Acknowledgments This study was financially supported by the

National key basic research and development program (No

2011CB403201), the Special Fund for Forestry Scientific Research in

the Public Interest (No 201204101), the National Key Technologies

R&D Program of China (No 2012BAD22B04), the Doctoral Initial

Fund Project of Liaoning Province (No 20111144) and the CFERN &

GENE Award Funds on Ecological paper. We are grateful to Dr.

Fusheng Chen and Prof. Chunjiang Liu for their valuable comments

and suggestions on the manuscript.

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