Ecological Indicators 32 (2013) 245252

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Ecological Indicators
journal homepage: www.elsevier.com/locate/ecolind

Environmental indicators for estimating the potential soil respiration rate in alpine zone
Akihiro Moriyama a , Seiichiro Yonemura b , Shigeto Kawashima a, , Mingyuan Du b , Yanhong Tang c
a b c

Division of Environmental Science and Technology, Kyoto University, Oiwakecho, Kyoto, Japan Agro-Meteorology Division, National Institute for Agro-Environmental Sciences, 3-1-3 Kannondai, Tsukuba, Ibaraki 305-8604, Japan Environmental Biology Division, National Institute for Environmental Studies, 16-2 Onogawa, Tsukuba, Japan

a r t i c l e

i n f o

a b s t r a c t
Soil respiration is the main form of carbon ux from soil to atmosphere in the global carbon cycle. The effect of temperature on soil respiration rate is important in evaluating the potential feedback of soil organic carbon to global warming. We incubated soils from the alpine meadow zone and upper rocky zone along an altitudinal gradient (44005500 m a.s.l.) on the Tibetan Plateau under various temperature and soil moisture conditions. We evaluated the potential effects of temperature and soil moisture on soil respiration and its variation across altitudes. Soil respiration rates increased as the temperature increased. At 60% of soil water content, they averaged 0.215.33 mol g soil1 day1 in the alpine meadow zone and 0.110.50 mol g soil1 day1 in the rocky zone over the experimental temperature range. Soil respiration rates in the rocky zone did not increase between 25 and 35 C, probably because of heat stress. Rates of decomposition of organic matter were high in the rocky zone, where the CN ratio was smaller than in the middle altitudes. Soil respiration rates also increased with increasing soil water content from 10% to 80% at 15 C, averaging 0.042.00 mol g soil1 day1 in the alpine meadow zone and 0.030.35 mol g soil1 day1 in the rocky zone. Maximum respiration rates were obtained in the middle part of the alpine slope in any case of experimental temperature and soil moisture. The change patterns in soil respiration rate along altitude showed similar change pattern in soil carbon content. Although the altitude is a variable including various environmental factors, it might be used as a surrogate parameter of soil carbon content in alpine zone. Results suggest that temperature, soil moisture and altitude are used as appropriate environmental indicators for estimating the spatial distribution of potential soil respiration in alpine zone. 2013 Elsevier Ltd. All rights reserved.

Article history: Received 27 October 2012 Received in revised form 10 March 2013 Accepted 30 March 2013 Keywords: Soil respiration rate Alpine region Altitude Temperature Soil moisture Mountain slope Soil carbon content

1. Introduction Global carbon cycle has long-term impacts on climate systems by changing the concentrations of atmospheric greenhouse gases (IPCC, 2007). Understanding of carbon cycles is therefore essential for our understanding of global warming. Carbon dioxide release from soils (soil respiration) is regarded as a main carbon ux in the global carbon cycle. Generally, the total soil respiration rate in the global carbon cycle is about 7755 1015 g C year1 (Raich and Potter, 1995; IPCC, 2004). And, being roughly estimated, soil organic carbon stocks is 1500 1015 g C (Schlesinger and Andrews, 2000; Jansson et al., 2010), carbon stocks in vegetation is 500 1015 g C and carbon stocks in the atmosphere is 750 1015 g C (IPCC, 2004). Moreover, soil respiration rate is balanced against net primary

Corresponding author. Tel.: +81 075 753 6154; fax: +81 075 753 6476. E-mail address: sig@kais.kyoto-u.ac.jp (S. Kawashima). 1470-160X/$ see front matter 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ecolind.2013.03.032

production and litter inputs. For this reason, investigation on the environmental controls on soil respiration is very important for predicting future climate change. Alpine ecosystems, generally, have high soil organic carbon stocks because of their association with cold, humid climates (Post et al., 1982). In soil organic carbon decomposition, the Q10 value which is a measure of the rate of change of the respiration rate when the temperature is increased by 10 C is about 2 at soil temperatures over 20 C, whereas Q10 values increase with decreasing temperature (Kirschbaum, 1995). Very high Q10 values (as high as 200) have been reported at soil temperatures below 0 C (Mikan et al., 2002; Kato et al., 2005). Alpine ecosystems are therefore sensitive to climate change, and it has been predicted that future global warming will lead to even more rapid soil organic carbon decomposition in alpine areas than in the lowlands, increasing CO2 concentrations in the atmosphere and accelerating global warming (Schlesinger and Andrews, 2000). Moreover, this trend is also clear in cold regions (Kirschbaum, 2000; Coteaux et al., 2001). Currently, eld

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measurements show that both soil organic carbon decomposition rates and soil respiration rates decrease with altitude (Coteaux et al., 2002; Chang et al., 2009), showing that temperature is a main factor controlling soil organic carbon decomposition rates and soil respiration rates in alpine ecosystems. Q10 of forest soils in Austria and Spain over 250 C incubation temperature range did now show any altitudinal trends (Schindlbacher et al., 2010). In contrast, in a similar series of measurements along a latitudinal transect, the temperature-related soil organic carbon decomposition decrease with decreasing latitude was counteracted by a soil water content decit induced by higher temperature (Bottner et al., 2000), thus indicating that soil water content affects the response of soil organic carbon decomposition to temperature. However, the abovementioned reports covered forest ecosystems, and there have been few studies of grassland ecosystems, especially in East Asia (for examples of such reports see Cao et al., 2004; Suh et al., 2009). The Tibetan Plateau is a mainly alpine grassland ecosystem (steppe or meadow) and occupies a vast area of Eastern Asia, so it contains large stocks of soil organic carbon. For example, Wang et al. (2002) reported soil organic carbon stocks of 33.52 1015 g C and annual soil respiration of 1.17 1015 g C in various grassland soils (00.75 m sampling depth) on the Tibetan Plateau. An area of 162,700 km2 was investigated. These results, and the vast area of East Asia occupied by the plateau, imply that the area is a major contributor to global carbon cycles. Ohtsuka et al. (2008) investigated soil organic carbon stocks in the alpine meadow zone (44005100 m a.s.l) and upper rocky zone (52005300 m a.s.l) of the Tibetan Plateau, at altitudes from 4400 to 5300 m. They found a specic altitudinal distribution of soil organic carbon stocks, with a clear peak at 4950 m, implying that grazing would affect the carbon cycle in the lower-altitude parts of alpine meadow zones. Moreover, they investigated the decomposition of cellulose in cotton strips (by calculating loss of mass of the strips) as a proxy for the relative rate of decomposition of soil organic carbon. Mass loss, and therefore decomposition potential, was markedly higher in the alpine meadow zone than in the rocky zone. However, temperature, soil water content and other factors have complex inuences on each other in eld measurements, and for this reason it is difcult to clarify the mechanism of decomposition of soil organic carbon from such measurements. Moreover, eld data from very high altitudes, such as those on the Tibetan Plateau, are not readily available from other previous studies. We therefore performed soil incubation experiments to measure the potential rates of respiration of soil from a large altitudinal transect under various temperature and soil water content conditions. In this paper, we aimed to clarify the effects of environmental indicators such as temperature and soil moisture on soil respiration rate along altitude in alpine meadow area. We also discuss the importance of the altitude as an environmental indicator for estimating soil respiration in alpine region.

altitude of 44005100 m a.s.l) to the rocky zone (at the altitude of 52005500 m a.s.l). Along the gradient, vegetation cover increased with increasing altitude from 4400 to 4950 m a.s.l and decreased with increasing altitude from 4950 m a.s.l to 5500 m a.s.l. Patches of plants (e.g., Arenaria kansuensis and Poa calliopsis) were found at 5300 m a.s.l. in the rocky zone, but the vegetation cover there was almost 0% (Ohtsuka et al., 2008). Meteorological measurements have been made at all soil sampling sites along the slope every 30 min since August 2005 by using the meteorological station equipped with sensors and a data logger (HOBO weather station, Onset Computer, Bourne, MA, USA). The tower is used to monitor temporal changes in air temperature at 1.5 m height, soil temperature and soil moisture at 5, 20 and 50 cm depth with permanently installed instruments (air temperature, S-THA-M006; soil temperature, S-TMB-M006; soil moisture, S-SMA-M006). Air and soil temperature in mid-August decreased gradually with increasing altitude on the study slope (44005300 m a.s.l). 2.2. Soil sampling Five duplicates of soil samples were taken at a depth of 05 cm. The amount of soil organic carbon at 05 cm depth amounts about half of soil organic carbon (Ohtsuka et al., 2008). So, we consider that we can use 05 cm of soil in order to compare altitude differences in soil carbon dynamics. The soil samples were well mixed and then sieved through a 2 mm mesh to remove the majority of the plant roots and stones. The samples were then stored in the refrigerator at 2 C for 2 months. Before the incubation experiments (see below), the total soil carbon content and soil total nitrogen content were measured by a CN-analyzer ((NC-900, Sumika Chemical Analysis Service, Japan)); water-holding capacity (WHC) were measured by sand column method. The original soil moisture content was about 3040% of WHC. 2.3. Measurement of potential soil respiration rate To investigate the effects of temperature and soil water content on soil respiration, we performed two kinds of incubation experiments in laboratory. The rst was incubation under constant soil water content and varying temperatures; the second was incubation under constant temperature and varying soil water contents. Three soil samples from each altitude were used for each incubation experiment. In the rst experiment, the three soil samples were incubated for 40 days at 5, 15, 25 or 35 C under 60% WHC. This water content is generally considered to be the optimum for soil respiration (Howard and Howard, 1993). In the second experiment, the three soil samples were incubated for 40 days at 15 C under 10%, 20%, 40%, 60% or 80% WHC, considering that ranges of soil temperature of places is low although 25 C is used for most incubation studies. All samples were placed in 63.5 mL (average value) inner volume of vials. Amount of soil placed in vials were 1 or 2 g by dry weight. In the rst experiment water was added to adjust soil moisture content to be 60% WHC. In the second experiment, all the samples were dried until 20% level of WHC. Then, the water was added to reach planned soil moisture. The sampled soil always experiences drying and wetting in elds. So, the moisture adjustment seems not to cause artifacts. After one week of pre-incubation, the CO2 concentration in each vial was measured at 35 day intervals by introducing small volume (0.25 mL, taken volume was 0.4 mL) of vial air to CO2 -free N2 carrier gas with a ow rate of 500 ml min1 , which was then introduced to a CO2 infrared analyzer (LI7000, LI-COR INC, USA). Actually area (V s) of peaks of CO2 on the response of the CO2 analyzer was calculated by an integrator (CR6A, Shimadzu, Kyoto, Japan) and was

2. Materials and methods 2.1. Study site and sampling sites The study was performed in alpine grassland on the Tibetan Plateau, close to Damxung (91.08 E, 30.29 N). The study area lay within the Kobresia meadow zone (ca. 32005300 m a.s.l), which is dominated by Kobresia pygmaea and Kobresia humilis (Ohtsuka et al., 2008). A south-east-facing slope in the Nyainqentanglha Mountains, near Damxung, was selected as the sampling area. Nine soil-sampling sites were selected on the slope along an altitudinal gradient (i.e., at 4400, 4500, 4650, 4800, 4950, 5100, 5200, 5300 and 5500 m a.s.l.) from the alpine meadow zone (at the

A. Moriyama et al. / Ecological Indicators 32 (2013) 245252 Table 1 Temperature characteristics at the observation sites. Altitude (m a.s.l) Annual mean air temperature ( C) Annual mean soil temperature ( C) Monthly mean soil temperature at 5 cm depth ( C) Maximum 8.4 (July) 8.6 (July) 9.5 (July) 9.7 (July) 9.5 (July) 12.6 (June) 15.2 (June) 15.9 (July) 17.6 (June) Minimum

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5 cm 5500 m 5300 m 5200 m 5100 m 4950 m 4800 m 4650 m 4500 m 4400 m 4.4 2.8 2.2 1.5 0.0 1.1 1.6 2.6 3.2 1.1 2.5 3.4 3.2 4.0 5.6 5.5 6.5 8.1

20 cm 1.4 2.4 3.0 3.2 3.9 5.4 5.5 7.5 7.3

50 cm 1.6 2.2 3.3 3.4 4.2 6.1 5.4 6.6 7.7

11.0 (February) 2.6 (March) 1.8 (March) 1.4 (March) 0.1 (March) 1.1 (January) 2.1 (January) 0.6 (January) 0.6(January)

referred to reference gas containing 0.995% of CO2 with N2 base (Takachiho Kagaku Kogyo, Tokyo, Japan). We put the same volume of air (0.4 mL) at the atmospheric-level CO2 concentration into vials after the sampling to compensate inner pressure of vials. High CO2 concentrations suppress soil respiration and prevent accurate measurement of innate respiration rates. Therefore, during the incubation period, when the CO2 concentration inside the vials exceeded 20,000 ppm the air inside the vials was exchanged with air from outside to decrease the CO2 concentration. To minimize the suppression effect and eliminate the initial instable data, after repeating the try and error, the respiration rate were calculated by averaging the change in CO2 concentration within each vial over the rst 9 days. The soil respiration rate Rs (mol g soil1 day1 ) was calculated as follows: Rs = CPV RT (1)

where ELT is the activation energy by temperature dimension, RsLT,0 and bLT are regression parameters. The fourth is the Gaussian model (OConnel, 1990): Rs = RsG,0 exp(aG T + bG T 2 ) (5)

where RsG,0 , aG , and bG are regression parameters. Furthremore, the carbon decomposition rate per unit of carbon can be a useful indicator for modeling soil carbon dynamics. We obtained the carbon decomposition rate (% day1 ) by integrating soil respiration rate over the petiod and by dividing soil carbon and integrated period. 3. Results 3.1. Meteorological data and soil properties Temperature characteristics at the observation sites are shown in Table 1. Annual mean air temperature and annual mean soil temperature decreased with increasing altitude. The lapse rate of air and soil temperatures was about 0.6 C/100 m. Table 2 shows the carbon and nitrogen properties of the soils at the observation sites. Soil carbon content increased with increasing altitude from 4400 to 4950 m and then decreased with increasing altitude from 4950 to 5500 m. Soil nitrogen content increased with increasing altitude from 4400 to 5100 m and then decreased with increasing altitude from 5100 m to 5500 m. The CN ratio increased with increasing altitude from 4400 to 4950 m and then decreased with increasing altitude from 4950 to 5500 m. In summary, soil carbon content, soil nitrogen content and CN ratio all showed clear peaks at an altitude of 49505100 m. Soil carbon content averaging in the alpine meadow zone at 44005100 m were 3.86 times those in the rocky zone at 52005500 m, and soil nitrogen content averaging in the alpine meadow zone at 44005100 m were 3.71 times those in the rocky zone at 52005500 m. In the alpine meadow, maximum soil carbon content value at 4950 m were 4.83 times minimum value at 4400 m and maximum soil nitrogen content value at 5100 m were

where C is the CO2 concentration change in each vial, P is the air pressure in the vials (ppm), V is the air volume (=vial volume solid soil volume water volume) of the vial (mL), R is the gas constant (m2 kg s2 K1 mol1 ) and T is the temperature (K) of the air in the vial. Contribution of CO2 solved in water is also a problem. It is very difcult to know the amount of CO2 in water. We assumed 1 as a general solubility of CO2 in water. The error resulting from this problem is within 2%, considering the waterair ratio in vials. Error can be considered within several % resulting from procedures in the experiment and we consider that the level of error is satisfactory in our study. Soil respiration rates depend highly on temperature. There are several formulations to estimate temperature sensitivity at each altitude (Tuomi et al., 2008). The rst formulation: Q10 = RsT +10 RsT (2)

where RsT is the respiration rate at temperature T (mol g soil1 day1 ) and RsT+10 is the respiration rate at temperature T + 10 (mol g soil1 day1 ), gives a parameter, the temperature coefcient or Q10, which is a measure of the rate of change of the respiration rate when the temperature is increased by 10 C. The second formulation is the Arrhenius equation that gives a parameter, activation energy EA : Rs = A exp EA RT (3)

Table 2 Carbon and nitrogen properties of the soils at the observation sites. Altitude (m a.s.l) 5500 m 5300 m 5200 m 5100 m 4950 m 4800 m 4650 m 4500 m 4400 m C content (%) 0.40 0.67 2.83 8.28 8.66 6.00 3.19 2.75 1.68 0.011 0.008 0.053 0.278 0.259 0.051 0.028 0.041 0.004 N content (%) 0.04 0.05 0.21 0.58 0.56 0.46 0.26 0.23 0.16 0.001 0.002 0.006 0.015 0.011 0.003 0.004 0.004 0.001 C/N ratio 10.6 12.3 13.7 14.3 15.6 13.0 12.1 11.9 10.9

where A is a regression parameter, EA is the activation energy (KJ mol1 ), R is the gas constant (m2 kg s2 K1 mol1 ) and T is temperature (K). The third formulation is those by Lloyd and Taylor (Lloyd and Taylor, 1994): Rs = RsLT,0 exp ELT T + bLT (4)

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6.0
4400 m

3.67 times minimum value at 4400 m. Thus, soil carbon content and nitrogen content varied widely in the alpine meadow.
Soil respiration rates (mol g soil-1day-1)

4500 m

5.0

4650 m 4800 m 4950 m 5100 m 5200 m

3.2. Changes in potential soil respiration rate with altitude and temperature We examined the changes in potential soil respiration rate with sampling altitude at various incubation temperatures (Fig. 1). With incubation at 5 C, soil respiration rates increased with sampling altitude from 4400 to 4950 m and decreased from 4950 to 5300 m, peaking at 0.89 mol g soil1 d1 at an altitude of 4950 m. With incubation at 15, 25 and 35 C, soil respiration rates showed patterns similar to that at 5 C, with peaks at an altitude of 4950 m (Fig. 1). The peak respiration rate at 35 C was 5.99 times that at 5 C, and the peak respiration site was consistent with the site with the peak soil carbon content (Fig. 1, Table 2). The rate of increase of soil respiration rate with altitude was not constant: the rate of increase at 46504950 m was higher than that at 44004650 m. Similarly, the rate of decrease was not constant but was highest at 51005200 m. We also examined the changes in soil respiration rates with temperature at various altitudes (Fig. 2). Soil respiration rate increased consistently with increasing temperature, except at altitudes of 5300 and 5500 m. At 5300 m the respiration rate still increased with temperature, but the rate of increase from 25 to 35 C was lower than that from 5 to 25 C, unlike at lower sites. At 5500 m the soil respiration rate increased from 5 to 25 C but decreased from 25 to 35 C. The Q10 and activation energy were calculated to assess the temperature sensitivity of soil respiration (Table 3). Q10 values were calculated on the basis of the respiration rates at 515 C (low), 1525 C (middle) and 2535 C (high) temperatures. Several formulations that represent temperature dependence were used for data tting. Q10 decreased with increasing temperature at all altitudes. The Q10 values at 48005100 m were generally higher than those at the upper and lower sites for middle and high temperature. The activation energy values at 48005100 m were higher than those at the upper and lower sites. At the averaging value, the activation energy in the alpine meadow zone

4.0

3.0

5300 m 5500 m

2.0

1.0

0.0 0 5 10 15 20 25 30 35 40

Temperature (C)
Fig. 2. Relationships between respiration rate and incubation temperature in soils sampled at various altitudes under 60% water holding capacity (WHC). Error bars are standard deviation values for triplet soil samples.

(average value 40.8 kJ mol1 ) was higher than that in the rocky zone (35.2 kJ mol1 ). 3.3. Changes in potential soil respiration rate with altitude and soil water content We examined the changes in soil respiration rate with sampling altitude at various soil water contents (as a ratio of WHC) during incubation (Fig. 3). At any water content except 10%, soil respiration rate increased consistently with increasing altitude from 4400 to 4950 m, and then decreased from 4950 to 5300 m, showing a clear peak at an altitude of 4950 m. Soil respiration rate showed similar patterns at all water contents, but the peak respiration rate at 80% water content was 9.52 times that at 10%. The rates of increase in respiration rate at 46504950 m were higher than those at 44004650 m, and rates of decrease at 51005300 m were higher than that at 49505100 m. On the other hand, at 10% of WHC there were inconsistent patterns, in that soil respiration rate decreased from 4400 m to 4650 m.

5400
5400

5200
5200

Altitude (m a.s.l)

5000

Altitude (m a.s.l)

5000

4800
5 C

4800 10 20 4600 40 60 80 4400 0.0 0.5 1.0 1.5 2.0 2.5 3.0

4600

15 C 25 C 35 C

4400 0.0 1.0 2.0 3.0 4.0 5.0 6.0

Soil respiration rates ( mol g soil-1 day-1)

Fig. 1. Altitudinal comparisons of soil respiration rates at various incubation temperatures under 60% of WHC. Error bars are standard deviation values for triplet soil samples.

Soil respiration rates (mol gsoil-1 day-1)

Fig. 3. Altitudinal comparisons of soil respiration rates at various soil water contents (as a percentage of WHC) under 15 C of soil temperature. Error bars are standard deviation values for triplet soil samples.

A. Moriyama et al. / Ecological Indicators 32 (2013) 245252 Table 3 Q10 values and activation energy for the soil respiration rates. Eq. (2) (Exponential) Altitude (m a.s.l) 5500 m 5300 m 5200 m 5100 m 4950 m 4800 m 4650 m 4500 m 4400 m Q10 values 515 2.58 2.56 2.34 2.31 2.45 2.52 2.57 2.55 2.48 1525 1.66 1.51 1.61 1.7 1.62 1.55 1.57 1.48 1.58 2535 0.96 1.04 1.34 1.52 1.52 1.62 1.41 1.3 1.44 Eq. (3) (Arrhenius) EA (kJ mol1 ) 34.3 33.2 38.2 42.1 42 42.7 40.6 37.1 40.5 Eq. (4) (Lloyd and Taylor) ELT ( C1 ) 101.8 44.2 81.4 331.7 173.1 115.5 70.0 14.9 14.1 bLT ( C) 25.0 12.7 20.7 57.2 36.6 25.9 19.0 3.1 2.4 Q10 values 515 2.33 2.47 2.42 2.09 2.24 2.50 2.36 2.77 2.97 1525 1.66 1.53 1.65 1.75 1.72 1.74 1.60 1.34 1.34 2535 1.40 1.28 1.38 1.55 1.48 1.45 1.34 1.15 1.15 Eq. (5) (Gaussian) aG ( C1 ) 0.096 0.101 0.099 0.081 0.091 0.092 0.101 0.129 0.152 bG ( C2 ) 0.00103 0.00129 0.00113 0.00060 0.00085 0.00085 0.00122 0.00210 0.00259 Q10 values 515 2.12 2.12 2.15 1.98 2.08 2.11 2.15 2.38 2.73 1525 1.72 1.63 1.72 1.76 1.76 1.78 1.68 1.56 1.62

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2535 1.40 1.26 1.37 1.56 1.48 1.50 1.32 1.03 0.97

Soil respiration rates (mol g soil-1day-1)

We also examined the changes in soil respiration rate with soil water content at various altitudes (Fig. 4). Except at 4400 m, soil respiration rates increased with increasing soil water content, but the rate of increase decreased with increasing soil water content. At 4400 m, the soil respiration rate decreased with increasing soil water content from 40% to 60%. 3.4. Relationship between potential soil respiration rate and carbon content Soil respiration rates varied widely, and under the temperatures and soil water contents used they peaked at 4950 m (Figs. 1 and 3). Soil respiration rate was positively correlated with soil carbon content (R2 > 0.98) (Figs. 5 and 6). The slope of the regression line increased with temperature, and the value of the slope at 35 C was 6.38 times that at 5 C (Fig. 5). The slope of the regression line increased with soil water content, and the value of the slope at 80% was 12.4 times that at 10% (Fig. 6). We calculated the carbon decomposition rates at 60% of WHC, as indicated by the mass of carbon emitted from the soil during the incubation period (Fig. 7). At 5 C incubation (nearest to eld temperature), decomposition rates in the alpine meadow zone (45005100 m), excluding those at 4400 m, were almost at. They increased with increasing altitude in the rocky zone (52005500 m). At the bottom of the alpine meadow zone (4400 m) the decomposition rates were a little larger than at the middle altitudes. Similar trends were observed at higher temperatures. Moreover, the total amount of decomposed organic carbon (about
2.5 4400 m

6.0
5 C y = 0.58x + 0.06 R = 0.99

5.0

15 C
25 C

4.0

35 C

y = 0.36x + 0.20 R = 0.99

3.0
y = 0.22x + 0.15 R = 0.99

2.0
y = 0.09x + 0.05 R = 0.99

1.0

0.0 0.0 2.0 4.0 6.0 8.0 10.0

Soil carbon content (%)

Fig. 5. Relationships between respiration rate and soil carbon content at various incubation temperatures under 60% of WHC. Error bars are standard deviation values for triplet soil samples.

2.5
10 y = 0.20x + 0.16 R = 0.98 y = 0.18x + 0.14 R = 0.98 y = 0.15x + 0.13 R = 0.98

Soil rrespiration rate (mol gsoil-1 day-1)

20 2.0 40 60 80 1.5

Soil respiration rates (mol gsoil -1 day-1)

4650 m 2.0 4950 m 5100 m 5300 m 1.5 5500 m

1.0 y = 0.09x + 0.05 R = 0.96 0.5 y = 0.02x + 0.03 R = 0.77 0.0

1.0

0.5

0.0 0.0 10.0 20.0 30.0 40.0 50.0 60.0 70.0 80.0 90.0

0.0

2.0

4.0

6.0

8.0

10.0

Soil water content (%)

Fig. 4. Relationships between respiration rate and water content (as a ratio of water-holding capacity) in soils sampled at various altitudes under 15 C of soil temperature. Error bars are standard deviation values for triplet soil samples.

Soil carbon content (%)

Fig. 6. Relationships between respiration rate and soil carbon content at various soil water contents (as a ratio of water-holding capacity) under 15 C of soil temperature. Error bars are standard deviation values for triplet soil samples.

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10, 25, 40, and 60 mol g soil C1 day1 ), as estimated from the total CO2 emitted at 5, 15, 25, and 35 C during the incubation period, was about 0.1%, 0.25%, 0.4%, and 0.6%, respectively, of the total soil organic carbon. 4. Discussion We discuss the temperature effect, soil moisture effect, and altitudinal effect on potential soil respiration rate. 4.1. Temperature effect on potential soil respiration rate The decreases in soil respiration rate in the high temperature range in the rocky zone can be explained by two factors. First, the microbes in the eld soil at higher altitudes (especially at 5300 and 5500 m) had been under colder soil temperatures (Table 1) and might have adjusted to the colder conditions. In other words, high temperature stress on the soil microbes could have depressed soil respiration rates, especially at 5300 and 5500 m. Second, a lack of substrate for the microbes depressed soil respiration rates, especially at 5300 and 5500 m, possibly because of the low soil carbon content (Table 2). However, low carbon content was not necessarily the reason for the lack of substrate, because the decomposition rate was larger in the rocky zone than in the alpine meadow zone (Fig. 7). Therefore, the rst hypothesis is the most likely explanation for the depressed soil respiration at 35 C at higher altitudes. In other words, high temperature stress might depressed soil respiration rates and decreased the temperature effect on soil respiration rates at 5300 and 5500 m. Even excluding the limitations on the increase in soil respiration rate from 25 to 35 C at 5300 and 5500 m because of high temperature stress, soil respiration rates did not increase exponentially but linearly at 44005200 m (Fig. 2). This differs from the exponential increase expected if soil water content or other factors are not limiting (Raich and Schlesinger, 1992; Lloyd and Taylor, 1994; Rey et al., 2005; Rodeghiero and Cescatti, 2005). Suh et al. (2009) reported that soil respiration rates increased exponentially with temperature in an alpine meadow soil on the Tibetan Plateau. The linear increase in respiration rates in our experiment suggests that rates were limited by other controlling factors. In general, the factors limiting respiration are soil water content (Howard and Howard, 1993; Zimmermann et al., 2009), size of the substrate pool

(Wang et al., 2002; Kirschbaum, 2006; Song et al., 2010), physical and chemical protection of the substrate (Davidson and Janssens, 2006), and freezing (Mikan et al., 2002; Kato et al., 2005). However, we suspect that high temperatures are also stressful for soils in alpine meadows, because soil respiration rates at 35 C might show depressed increase compared with exponential change. 4.2. Soil moisture effect and its implications In general, low respiration rates result from depression of microbial activity if the soil water content is extremely low or high; maximum soil respiration rates are therefore observed at approximately 60% of WHC (Howard and Howard, 1993; Rey et al., 2005; Suh et al., 2009). Lack of available water inhibits microbial activity (Davidson and Janssens, 2006), and extremely high water content slows oxygen diffusion and thus slows microbial activity (Davidson et al., 2006). Plateaus in respiration rates are therefore often observed under conditions without such inhibitions, and maximum respiration rates are often observed at approximately 60% of WHC, when soil water conditions are neither too low nor too high for soil microbes. However, the response of soil respiration rate to soil water content is inuenced by the soil type or the nature of the soil organic carbon, and it soil respiration rates often increase with increasing soil water content more than about 80% of WHC (Howard and Howard, 1993). Suh et al. (2009) reported that soil respiration peaked at 60% of WHC in an alpine meadow on the Tibetan Plateau. However, we found that the respiration rate at our study site increased with increasing soil water content (from 10% to 80% of WHC) in soil carrying vegetation similar to that used in the study by Suh et al. (2009), even though with similar vegetation and climate one would expect the soil organic carbon qualities to be similar. This discrepancy is one of the remaining problems. 4.3. Altitudinal changes in potential soil respiration rate Soil respiration rates changed along an altitudinal gradient and peaked at 4950 m (Fig. 1). They increased with increasing temperature under the study conditions (535 C). Respiration rates also increased with increasing soil water content. From our results, we were able to categorize the temperature responses of soil respiration rates into three patterns (Table 3, Figs. 1 and 2). In the rst pattern, the respiration rate varied slightly at low altitudes (44004650 m). In the second pattern, the respiration rate varied widely in the middle altitudes (48005200 m). In the third pattern, the respiration rate varied slightly (especially at high temperatures) at high altitudes (53005500 m). At 5 C incubation, the maximum soil respiration rate (at 4950 m) was 8.1 times the minimum value (at 5300 m). The similar response patterns of soil respiration rates at low and high altitudes were consistent with a lack of substrate, because the soil carbon contents at these altitudes were lower than at the middle altitudes. The site (at 5500 m) with the lowest soil carbon content, as well as a low CN ratio, had the strongest limitation of soil respiration rate (Fig. 2, Table 2). Thus, soil carbon content affected soil respiration rates across altitudes. These results are consistent with those of Rodeghiero and Cescatti (2005), who reported increasing soil respiration rates with increasing soil organic carbon stocks in the Italian Alps, and of Wang et al. (2002), who reported a positive correlation between soil organic carbon content and soil respiration rates in Australian soils. Overall, our results, as well as those of these previous studies, indicate the importance of soil carbon content to the control of soil respiration rates, even in vertically different soils. Furthermore, the CN ratio is generally larger if the organic matter is fresh. Our data (Table 2, Figs. 1 and 3) showed that an abundance of relatively fresh organic matter contributed to the vertical peak in soil respiration

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Decomposition rates (% per 9 days)

Fig. 7. Altitudinal comparison of decomposition rates at various soil temperature under 60% of WHC. Error bars are standard deviation values for triplet soil samples.

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variable including various environmental factors, it might be used as a surrogate parameter of soil carbon content in alpine zone. To estimate the spatial distribution of soil respiration in alpine zone, temperature, soil moisture and altitude are used as appropriate environmental indicators. Acknowledgements

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The work was funded principally by the Global Environment Research Coordination System, Ministry of the Environment, Japan to the project Early detection and prediction of climate warming based on long-term monitoring on the Tibetan Plateau and partly by KAKENHI (23310017). References

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Bottner, P., Coteaux, M.M., Anderson, J.M., Berg, B., Bills, G., Bolger, T., Casabianca, H., Romany, J., Rovira, Pere., 2000. Decomposition of 13 C-labelled plant material in a European 6540 latitudinal transect of coniferous forest soil: simulation of climate change by translocation of soils. Soil Biol. Biochem. 32, 527543. Cao, G., Tang, Y., Mo, W., Wang, Y., Li, Y., Zhao, X., 2004. Grazing intensity alters soil respiration in an alpine meadow on the Tibetan plateau. Soil Biol. Biochem. 36, 237243. Chang, Z., Feng, Q., Si, J., Su, Y., Xi, H., Li, J., 2009. Analysis of the spatial and temporal changes in soil CO2 ux in alpine meadow of Qilian Mountain. Environ. Geol. 58, 483490. Coteaux, M.M., Bottner, P., Anderson, J.M., Berg, B., Bolger, T., Casals, P., Romany, J., Thiry, J.M., Vallejo, V.R., 2001. Decomposition of 13 C-labelled standard plant material in a latitudinal transect of European coniferous forests: differential impact of climate on the decomposition of soil organic matter compartments. Biogeochemistry 54, 147170. Coteaux, M.M., Sarmiento, L., Bottner, P., Acevedo, D., Tiery, J.M., 2002. Decomposition of standard plant material along an altitudinal transect (653968 m) in the tropical Andes. Soil Biol. Biochem. 34, 6978. Davidson, E.A., Janssens, I.A., 2006. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440, 165173. Davidson, E.A., Janssens, I.A., Luo, Y., 2006. On the variability of respiration in terrestrial ecosystems: moving beyond Q10. Glob. Change Biol. 12, 154164. Du, M., Kawashima, S., Yonemura, S., Zhang, X., Chen, S., 2004. Mutual inuence between the human activities and the climatic change in Tibetan Plateau during recent years. Glob. Planet. Change 41, 241249. Howard, D.M., Howard, P.J.A., 1993. Relationships between CO2 evolution, moisture content and temperature for a range of soil types. Soil Biol. Biochem. 25, 15371546. IPCC, 2004. Chapter 3: the carbon cycle and atmospheric carbon dioxide. In Climate Change 2004, pp. 183-237. IPCC, 2007. Chapter 7: couplings between changes in the climate system and biogeochemistry. In Climate Change 2007: Working Group I Report The Physical Science Basis, pp. 499587. Jansson, C., Wullschleger, S.D., Kalluri, U.C., Tuskan, G.A., 2010. Phytosequestration: carbon biosequestration by plants and the prospects of genetic engineering. Bioscience 60, 685696. Kato, T., Hirota, M., Tang, Y., Cui, X., Li, Y., Zhao, X., Oikawa, T., 2005. Strong temperature dependence and no moss photosynthesis in winter CO2 ux for a Kobresia meadow on the Qinghai-Tibetan plateau. Soil Biol. Biochem. 37, 19661969. Kirschbaum, M.U.F., 1995. The temperature dependence of soil organic matter decomposition, and the effect of global warming on soil organic C storage. Soil Biol. Biochem. 27, 753760. Kirschbaum, M.U.F., 2000. Will changes in soil organic carbon act as a positive or negative feedback on global warming? Biogeochemistry 48, 2151. Kirschbaum, M.U.F., 2006. The temperature dependence of organic-matter decomposition still a topic of debate. Soil Biol. Biochem. 38, 25102518. Lloyd, J., Taylor, J.A., 1994. On the temperature dependence of soil respiration. Funct. Ecol. 8, 315323. Mikan, C.J., Schimel, J.P., Doyle, A.P., 2002. Temperature controls of microbial respiration in arctic tundra soils above and below freezing. Soil Biol. Biochem. 34, 17851795. OConnel, A.M., 1990. Microbial decomposition (respiration) of litter in eucalypt forests of southwestern Austtalia: an empirical model based on laboratory incubations. Soil Biol. Biochem. 22, 153160. Ohtsuka, T., Hirota, M., Zhang, X., Shimono, A., Senga, Y., Du, M., Yonemura, S., Kawashima, S., Tang, Y., 2008. Soil organic carbon pools in alpine to nival zones along an altitudinal gradient (44005300 m) on the Tibetan Plateau. Polar Sci. 2, 277285. Post, W.M., Emanuel, W.R., Zinke, P.J., Stangenberger, A.G., 1982. Soil carbon pools and world life zones. Nature 298, 156159. Raich, J.W., Schlesinger, W.H., 1992. The global carbon dioxide ux in soil respiration and its relationship to vegetation and climate. Tellus 44B, 8199.

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Annual total soil respiration (mol g

soil-1

year-1)

Fig. 8. Estimated annual total soil respiration along the altitude.

at the middle altitudes (48005200 m), because vegetation is quite limited at high altitudes in the rocky zone (53005500 m) and that the biomass produced by grasses at low altitudes is soon consumed by cattle. The conditions at our study sites, especially at the lower altitudes, can be considered indicative of overgrazing (Du et al., 2004). We made preliminary calculation to estimate the prole pattern of soil respiration rate in natural condition on the alpine slope. The calculation was performed by combining the experimental results with the actual environmental conditions. The actual conditions are the observed soil temperature and moisture in situ in 2009, when the data were taken with a less trouble through one year. As this is a preliminary estimation, the temperature and moisture data were applied to the experimental relations using a simple linear interpolation. The estimated annual total soil respirations along the altitude are shown in Fig. 8. At this study site, Ohtsuka et al. (2008) reported that the decomposition potential (as indicated by the loss of mass over 1 year of cotton strips inserted into the soil) in the alpine meadow zone (44005100 m) was signicantly higher than that in the rocky zone (52005300 m). The prole of soil respiration along the altitude that we calculated (Fig. 8) is consistent with the prole of decomposition potential reported by Ohtsuka et al. (2008). Soil temperature decreased with increasing altitude (Table 1) and decomposition rates at higher altitudes were depressed by low temperatures. Because our experiments were performed under controlled conditions, we consider that we obtained more general information about the factors controlling soil respiration. Moreover, at higher altitudes the soil freezing period is longer; this freezing prevents diffusion of substrate (Mikan et al., 2002; Kato et al., 2005) and depresses microbial activity (Kato et al., 2005). This could explain very lower rates in the rocky zone in the eld experiments. We evaluated the effects of temperature and soil moisture on soil respiration and its variation across altitudes. Maximum respiration rates were obtained in the middle part of the alpine slope in any case of experimental temperature and soil moisture. The change pattern in soil respiration rate along altitude shows similar change pattern in soil carbon content along altitude. Altitude dependence of soil respiration rate is thought to originate from the soil carbon content on the alpine slope. Although the altitude is a

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A. Moriyama et al. / Ecological Indicators 32 (2013) 245252 Song, M., Jiang, J., Cao, G., Xu, X., 2010. Effects of temperature, glucose and inorganic nitrogen inputs on carbon mineralization in a Tibetan alpine meadow soil. Eur. J. Soil Biol. 46, 375380. Suh, S., Lee, E., Lee, J., 2009. Temperature and moisture sensitivities of CO2 efux from lowland and alpine meadow soils. J. Plant Ecol. 2, 225231. Tuomi, M., Vanhala, P., Karhu, K., Fritze, H., Liski, J., 2008. Heterotrophic soil respiration comparison of different models describing its temperature dependence. Ecol. Model. 211, 182190. Wang, G., Qian, J., Cheng, G., Lai, Y., 2002. Soil organic carbon pool of grassland soils on the Qinghai-Tibetan Plateau and its global implication. Sci. Total Environ. 291, 207217. Zimmermann, M., Meir, P., Bird, M.I., Malhi, Y., Cchauana, A.J.Q., 2009. Climatic dependence of heterotrophic soil respiration from a soil-translocation experiment along a 3000 m tropical forest altitudinal gradient. Eur. J. Soil Sci. 60, 895906.

Raich, J.W., Potter, C.S., 1995. Global patterns of carbon dioxide emissions from soils. Glob. Biogeochem. Cycles 9, 2336. Rey, A., Petsikos, C., Jarvis, P.G., Grace, J., 2005. Effect of temperature and moisture on rates of carbon mineralization in a Mediterranean oak forest soil under controlled and eld conditions. Eur. J. Soil Sci. 56, 589599. Rodeghiero, M., Cescatti, A., 2005. Main determinants of forest soil respiration along an elevation/temperature gradient in the Italian Alps. Glob. Change Biol. 11, 10241041. Schindlbacher, A., de Gonzalo, C., Daz-Pins, E., Gorra, P., Matthews, B., Incln, R., Zechmeister-Boltenstern, S., Rubio, A., Jandl, R., 2010. Temperature sensitivity of forest soil organic mater decomposition along two evevation gradients. J. Geophys. Res. 115, G03018, doi: 10.129/2009JG001191. Schlesinger, W.H., Andrews, J.A., 2000. Soil respiration and global carbon cycle. Biogeochemistry 48, 720.