SSRN Id4554607

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1 Title
2 Temperature sensitivity of organic carbon decomposition increases with increasing
3 mean residence time in Japanese forest surface soil
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5 Author names and affiliations
6 Jun Koarashia,*, Koichi Moriyaa,b, Hirohiko Naganoc, Mariko Atarashi-Andoha,
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7 Shigehiro Ishizukad
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9 aNuclear Science and Engineering Center, Japan Atomic Energy Agency, Ibaraki
10 319-1195, Japan
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11 bGraduate School of Engineering, Nagoya University, Nagoya 464-8603, Japan
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12 cInstitute of Science and Technology, Niigata University, Niigata 950-2181, Japan
13 dDepartment of Forest Soils, Forestry and Forest Products Research Institute, Ibaraki
14 305-8687, Japan
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16 Corresponding author
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17 E-mail address: koarashi.jun@jaea.go.jp (J. Koarashi)
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This preprint research paper has not been peer reviewed. Electronic copy available at: https://ssrn.com/abstract=4554607
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19 Abstract
20 Understanding the sensitivity of soil organic carbon (SOC) decomposition to
21 temperature is vital to accurately predict the soil C response to global warming.
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22 However, the temperature sensitivity of the decomposition of SOC that is stored in the
23 mineral soil remains unclear. Thus, this study aimed to quantify the temperature
24 sensitivity of SOC pools with different mean residence times (MRTs) ranging from
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25 days to approximately a century in the upper 20 cm of the mineral soil. Based on the
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26 finding that the MRT of SOC varied according to the soil type and depth, soil samples
27 were collected from three Japanese forests using thin-layer sampling. These samples
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were incubated at two laboratory temperatures (20°C and 30°C) for >100 days. Using a
29 three-pool first-order decomposition model and radiocarbon (14C) measurements of the

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30 acid-insoluble fractions of the samples, the soil C was separated into three (active, slow,
31 and resistant) SOC pools with varying MRTs. The relationship between the MRT and
32 temperature sensitivity (Q10 value) of the pools was then determined. The active SOC
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33 pool was identified as a small (<0.7% of the total SOC) rapidly cycling (generally <2
34 weeks) C pool at all depths. The slow pool was a much larger (23%–52%) C pool that
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35 cycled on a timescale of decades to more than a century. Across all sites and depths, the
36 Q10 values increased from 1.1 to 4.0 with increasing MRTs and were greater than 2.0
37 for all SOC pools with an MRT >40 years. Although the mechanisms controlling the
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38 overall degradability and temperature sensitivity of SOC are not yet fully understood,
39 our results demonstrate that a large amount of C (1.4–3.2 kg C m−2 in the top 15 cm)
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40 that has been stabilized over decades in the surface mineral soil is highly vulnerable to
41 warming.
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43 Keywords
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44 Soil organic carbon (SOC); Mean residence time (MRT); Temperature sensitivity (Q10);
45 Decomposition; Radiocarbon (14C); Three-pool model
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47 Funding
48 This work was supported by the Japan Society for the Promotion of Science (JSPS)
49 KAKENHI (grant numbers 23380096, 15H04523).
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51 CRediT authorship contribution statement
52 Jun Koarashi: Conceptualization, Methodology, Investigation, Visualization, Writing –
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original draft, Funding acquisition. Koichi Moriya: Methodology, Investigation.
54 Hirohiko Nagano: Formal analysis, Visualization. Mariko Atarashi-Andoh:

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55 Investigation. Shigehiro Ishizuka: Investigation.
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58 1. Introduction
59 The microbial decomposition of soil organic carbon (SOC) is an essential
60 component of the global carbon (C) cycle (IPCC, 2021) because it produces a carbon
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61 dioxide (CO2) emission flux from the soil to the atmosphere (also known as soil
62 heterotrophic respiration). Globally, this soil heterotrophic respiration is estimated to be
63 approximately 6–8 times greater than that of the anthropogenic CO2 emission flux
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64 (Bond-Lamberty and Thomson, 2010; Bond-Lamberty et al., 2018; IPCC, 2021).
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65 Therefore, changes in the SOC decomposition rate could have a considerable impact on
66 the global C cycle. The microbial decomposition of SOC is a temperature-sensitive
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process (Davidson and Janssens, 2006). Therefore, global warming is expected to
68 enhance the soil heterotrophic respiration (Bond-Lamberty et al., 2018; Nissan et al.,
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69 2023) and consequently the CO2 concentration in the atmosphere, which can then
70 potentially accelerate global warming due to the positive feedback loop (Jenkinson et al.,
71 1991; Crowther et al., 2016). However, there is no consensus regarding the magnitude
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72 and timescale of this warming-induced effect on soil heterotrophic respiration, largely
73 due to a lack of quantitative insight into the temperature sensitivity of SOC

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74 decomposition (Zhou et al., 2009; Bradford et al., 2016).
75 The temperature sensitivity of SOC decomposition has previously been
76 characterized by the Q10 value, a factor by which the SOC decomposition rate increases
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77 when the temperature increases by 10°C (Davidson and Janssens, 2006). In Earth
78 System Models (ESMs, i.e., coupled climate–carbon cycle models), a function using
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79 this parameter value is widely utilized to evaluate the warming-induced effect on soil C
80 emission (Potter et al., 1993; Friedlingstein et al., 2006; Todd-Brown et al., 2013;
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81 Foereid et al., 2014). Although the Q10 value for SOC decomposition can vary
82 depending on environmental and biological factors such as the temperature and SOC
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83 properties (Davidson and Janssens, 2006; Hamdi et al., 2013; Meyer et al., 2018), most
84 ESMs employ a fixed Q10 value (1.5 or 2.0) for all soil types and SOC properties (Cox
85 et al., 2000; Jones et al., 2005; Friedlingstein et al., 2006; Foereid et al., 2014). It has
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86 recently been suggested that the feedback magnitude of soil heterotrophic respiration on
87 warming may be underestimated by 25% if an assumed invariant Q10 value is used for
88 ESMs (Zhou et al., 2009). Therefore, quantifying the actual temperature sensitivity of
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89 SOC decomposition is pivotal to accurately predict the future of the global C cycle and
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90 Earth’s climate (Conant et al., 2011; Todd-Brown et al., 2013; Foereid et al., 2014).
91 SOC is a complex mixture of plant-derived and microbially-transformed organic
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materials with varying degrees of biochemical recalcitrance. The fundamental principles
93 of enzyme kinetics (also known as the “carbon quality-temperature hypothesis”) suggest

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94 that the temperature sensitivity of the microbial SOC decomposition ought to increase
95 with increasing biochemical recalcitrance of organic compounds (Bosatta and Ågren,
96 1999; Davidson and Janssens, 2006). This behavior has been observed in the
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97 decomposition of organic materials in organic (O) horizons (Wetterstedt et al., 2010).
98 However, in mineral soil (below the O horizon), the temperature sensitivity of organic
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99 material decomposition may be obscured by a range of physical, chemical, and
100 biological mechanisms (Davidson and Janssens, 2006). Although Fang et al. (2005) and
101 Vaughn and Torn (2019) showed that labile and stable SOC pools responded similarly
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102 to increases in temperature, a review by Conant et al. (2011) considered a number of
103 studies (Knorr et al., 2005; Conant et al., 2008) which indicated that a resistant SOC
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104 pool was more sensitive to temperature than that of a labile SOC pool (thus supporting
105 the carbon quality-temperature hypothesis). There are also studies that show opposite
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106 results (Giardina and Ryan, 2000; Fissore et al., 2009). These contradictory results may
107 be due to the SOC pools utilized in these studies that differ in their overall SOC stability
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108 (degradability). This may be governed by not only the SOC biochemical recalcitrance
109 but also some other mechanisms operating in the mineral soils, such as the physiology
110 of soil microorganisms and physicochemical destabilization and stabilization processes
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111 (Davidson and Janssens, 2006; von Lützow and Kögel-Knabner, 2009; Qin et al., 2019).
112 The mean residence time (MRT, a reciprocal of turnover time) of SOC in the
113 mineral soil is not a direct indicator of its biochemical recalcitrance; instead, it is
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114 indicative of the overall degradability of the SOC that interacts with the soil constituents
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115 under actual environmental conditions. Generally, the current ESMs separate the soil C
116 into several conceptually defined SOC pools with different MRTs (Friedlingstein et al.,
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2006; Todd-Brown et al., 2013; Foereid et al., 2014): for example, active (with MRTs
118 of years or shorter), slow (MRTs of decades to a century), and resistant (MRTs of
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119 centuries or longer) SOC pools. Because the surface soil (upper 20–30 cm of mineral
120 soil) stores a large amount of SOC with MRTs of decades to centuries (Schimel et al.,
121 1994; Trumbore et al., 1996; Falloon et al., 1998; Gaudinski et al., 2000; Koarashi et al,
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122 2009; Ota et al., 2013), it is likely that the long-term (over the next century) response of
123 soil C to climate change will be largely determined according to the response of the
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124 slow SOC pool to increasing temperatures. Therefore, quantifying the relationship
125 between the MRT (particularly <100 years) and temperature sensitivity of SOC could
126 improve our ability to predict the magnitude and persistence of the carbon cycle–climate
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127 feedback effects through the use of these ESMs.
128 In the present study, we aimed to explore the relationship between the MRT and
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129 temperature sensitivity of SOC in the surface mineral soil. For this purpose, the soil
130 type and depth were used as surrogates for the SOC degradability under actual
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131 environmental conditions. This is because even within the upper 20–30 cm of mineral
132 soil, the MRT of SOC differs depending on the soil type and depth (Scharpenseel et al.,
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133 1989; Trumbore, 2000; Koarashi et al., 2009), possibly because of the simultaneous
134 operation of several SOC stabilization mechanisms at varying degrees. Soil samples
135 were collected using thin-layer sampling from the surface layers of three Japanese forest
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136 sites, and the samples were incubated at two laboratory temperatures for >100 days. A
137 three-pool first-order decomposition model (Paul et al., 2001; 2006; Grandy and
138 Robertson, 2007; Fissore et al., 2009) was fitted to the incubation results to separate the
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139 soil C into three (active, slow, and resistant) SOC pools with different MRT ranges.
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140 During the three-pool separation, the size and MRT of the resistant SOC pools were
141 estimated based on the C and radiocarbon (14C) analyses of the soil samples after acid
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hydrolysis treatment (Leavitt et al., 1996; Paul et al., 2006; Fissore et al., 2009). This
143 approach allowed us to obtain SOC pools with a variety of MRTs (days to centuries),
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144 and thus to determine the SOC decomposition temperature sensitivity of the pools (as
145 Q10 values), and consequently, the relationship between the MRT and Q10 value.
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147 2. Materials and methods
148 2.1. Study sites

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149 The study was performed at three forest sites (AP, OG, and IB) in Japan (Table 1).
150 The AP site is a cool–temperate, deciduous, broadleaved forest dominated by
151 70–80-year-old Japanese beech (Fagus crenata) with virtually no understory. The OG
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152 site is a temperate, deciduous, broadleaved forest dominated by Japanese beech (Fagus
153 crenata) and Japanese oak (Quercus crispula) with no understory. The IB site is a
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154 temperate, coniferous forest dominated by approximately 50-year-old Japanese larch
155 (Larix leptolepis) with low bamboo bushes (Sasamorpha borealis). The mean annual
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156 temperature (MAT) and mean annual precipitation (MAP) ranged from 6.1°C–10.7°C
157 and 1207–1990 mm, respectively, across the three sites.
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158 The soil types have been classified as Andosol for the AP and OG sites (Ishizuka et
159 al., 2006; Yoshinaga et al., 2002) and Cambisol for the IB site, using the classification
160 of the Food and Agricultural Organization (IUSS working Group WRB, 2015). The soil
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161 pH was all acidic (4.5–4.7) and the soil at the AP and OG sites had a strong influence of
162 volcanic ash deposition. The pyrophosphate extractable aluminum (Alp) and iron (Fep)
163 contents were higher in the AP and OG soils than in the IB soil (Table 2). The contents
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164 of the acid oxalate extractable and dithionite-citrate extractable Al and Fe (Alo, Feo, Ald,
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165 and Fed, respectively) were also higher in the AP and OG soils than in the IB soil. In the
166 AP and OG soils, the Alo + 1/2Feo value was greater than 20 g kg−1, which is the value
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that is used as the diagnostic criterion for andic soil properties to distinguish between
168 volcanic ash and non-volcanic ash soils (Imaya et al., 2007).
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170 2.2. Collection and treatment of soil samples
171 Soil samples were collected from the AP site in September 2008, OG site in
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172 January 2007, and IB site in March 2009. At all of the sites, three cores of mineral soil
173 (9.5 cm in diameter and >20 cm long) were taken after removing the O horizons. The
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174 soil cores were divided into seven layers (0–2, 2–4, 4–6, 6–8, 8–10, 10–15, and >15 cm
175 depth intervals) in the laboratory, and composited according to the layers. Parts of the
176 thin-layered soil samples were sieved using a mesh with 4-mm openings, and the visible
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177 plant roots in the sieved samples were removed with tweezers. The soil samples from
178 the AP and IB sites were immediately incubated and those from the OG site were stored
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179 at 6°C in sealed plastic bags for a few days before incubation.
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181 2.3. Incubation procedure
182 The soil samples (9–229 g dry weight equivalent depending on the soil depth) were
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183 placed in open-top jars (jar volumes of 100, 300, or 500 mL) and incubated for >100
184 days in the dark under two laboratory incubation temperature (LIT) conditions of 20°C
185 (LIT20) and 30°C (LIT30). The soil moisture content was not adjusted before
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186 incubation and the moisture content remained the same as the field moisture conditions
187 at the time of sampling (0.72–1.52, 1.04–1.39, and 0.62–0.80 g-water g−1-dry soil for
188 the AP, OG, and IB soil samples, respectively). The moisture content was maintained
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189 during incubation by adding deionized water to the soil. Throughout the incubation
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190 period, the jars were periodically placed into a larger, open-topped container that was
191 then enclosed with a soil CO2 flux system setup (LI-6400 with a soil flux chamber
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6400-09, LI-COR, USA) to measure the CO2 emission rates of the soil samples. The
193 total effective volume enclosed was 2.1 L.

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195 2.4. Soil fractionation and C isotope analysis
196 Portions of the thin-layered soil samples were dried at 50°C in an oven and then
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197 sieved using a mesh with 2-mm openings, and the visible plant roots were removed with
198 tweezers. Approximately 2–10 g of the <2-mm soil samples (bulk soil samples) were
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199 subject to acid hydrolysis treatment (1.2 M HCl at 80°C for 2 h, three times, Koarashi et
200 al., 2009). After treatment, the samples were neutralized by washing with deionized
201 water and dried to obtain the acid-insoluble SOC fractions (AISF).
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202 The bulk soil and AISF samples were homogenized by grinding and the C content
203 of the samples were measured using a total organic C analyzer (TOC-5000 with a solid
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204 sample module: SSM-5000A, Shimadzu, Japan). Preparation of samples for 14C analysis
205 was performed according to the procedure detailed by Koarashi et al. (2009). Briefly,
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206 the samples were combusted in quartz tubes sealed with a clean CuO wire and Ag foil
207 under vacuum conditions. The CO2 generated in the tubes was cryogenically purified
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208 and recovered, which was then used to prepare the graphite targets for 14C
209 measurements with an accelerator mass spectrometer (AMS) at the Aomori Research
210 and Development Center, Japan Atomic Energy Agency (JAEA-AMS-MUTSU). The
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211 subsamples of the purified CO2 were also used to measure the 13C isotopic signature
212 (13C) with an isotopic ratio mass spectrometer (MAT-252, Finnigan MAT, Bremen,
213 Germany). All radiocarbon data were reported using 14C notation, which is the per mil
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214 (‰) deviation of the 14C/12C ratio of the sample from that of the absolute 14C standard
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215 in 1950, with correction for the mass-dependent isotope fractionation in the
216 environment to a constant 13C value of −25‰ (Stuiver and Polach, 1977). The
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analytical uncertainty of the 14C values was ~5‰ (1 standard deviation (SD)).
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219 2.5. Quantifying sizes and MRTs of the three SOC pools
220 The size and MRT of the three SOC pools (active, slow, and resistant) were
221 quantified according to the well-established three-pool first-order decomposition model

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222 (Paul et al., 2001; 2006; Grandy and Robertson, 2007; Fissore et al., 2009):
223 CT(t) = Ca exp(−ka t) + Cs exp(−ks t) + Cr exp(−kr t), (1)

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224 where CT(t) represents the total SOC at time t; Ca, Cs, and Cr represent the initial sizes
225 of the active, slow, and resistant SOC pools, respectively (i.e., CT(0) = Ca + Cs + Cr);
226 and ka, ks, and kr represent the decomposition rate constants for the three SOC pools,
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227 respectively.
228 In this study, it was assumed that the resistant SOC pool in the model was
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229 represented by the AISF fraction obtained after the acid hydrolysis (Leavitt et al., 1996;
230 Paul et al., 2006; Fissore et al., 2009), considering the relatively long MRT of the
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231 AISF-C (see section 3.3). Hence, the resistant pool size (Cr) was determined to be the
232 same as the AISF-C size. To determine the MRT for the resistant SOC pool, the MRT
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233 of the AISF fraction was estimated based on the 14C result, using a time-dependent,
234 steady-state model (Trumbore et al., 1996; Gaudinski et al., 2000; Koarashi et al.,
235 2012):
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236 F(t) = k ‧ Fatm(t−1) + F(t−1) ‧ (1−k−), (2)
237 where F(t) is the fraction of the modern C (F14C), which is equivalent to Δ14C/1000 + 1,
238 in the SOC pool at year t; k is the decomposition rate constant for the SOC pool (y−1);
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239 Fatm(t−1) is the F14C of CO2 in the atmosphere at year t−1; F(t−1) is the F14C in the
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240 SOC pool at year t−1; and  is the radioactive decay constant for 14C (y−1). Fatm(t−1)
241 was derived from the atmospheric 14C-CO record (Koarashi et al., 2009). Using this
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model, the Δ14C value of the SOC can be predicted to identify a value of k that best
243 explains the measured Δ14C value, following this the MRT can be estimated as k−1 (in
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244 years).
245 The CO2 emission rate during the incubation at a constant temperature can be
246 represented by the differentiated form of Eq. (1):

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247 E(t) = −dCT(t)/dt = ka Ca exp(−ka t) + ks Cs exp(−ks t) + kr Cr exp(−kr t) (3)
248 Given the long 14C-derived MRTs (in excess of 100 years, see section 3.3) for the
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249 resistant SOC pools and thus the small values for kr in the Eq. (3), it is clear that the
250 resistant SOC pool contributes almost nothing to the measured CO2 emission rates over
251 the 100 days of the incubation. Therefore, the CO2 emission during the incubation can
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252 be considered as a two-pool phenomenon:
253 E(t) = ka Ca exp(−ka t) + ks Cs exp(−ks t) (4)

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254 Using Eq. (4), the parameter values for Ca and Cs (= CT(0) − Ca − Cr), and ka and ks
255 at LIT20 and LIT30 (i.e., ka20, ka30, ks20, and ks30) that best explain the observed
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256 changes in the CO2 emission rates during incubation at LIT20 and LIT30, were
257 determined by minimizing the residual sum of squares in the fitting results. The MRTs
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258 for the active and slow SOC pools at LIT20 and LIT30 (i.e., MRTa20, MRTa30,
259 MRTs20, and MRTs30) were calculated as the reciprocals of ka20, ka30, ks20, and ks30,
260 respectively. Finally, the MRT at the field MAT (MRTMAT) for the active and slow SOC
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261 pools were estimated using the obtained MRT values at LIT20 and the conversion factor,
262 Q10(20−MAT)/10, with the value of Q10 evaluated in the manner described in section 2.6.
263 The model fitting to the observations was performed using R software 4.1.1 (R core
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264 team, 2021) with the minpack.lm package (Elzhov et al., 2023). The R package solved
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265 the nonlinear least-squares equations through a modification of the
266 Levenberg-Marquardt algorithm and provided the statistical significance (p < 0.05) of
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the estimated parameters (Elzhov et al., 2023).
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269 2.6. Quantifying temperature sensitivity of the active and slow SOC pools
270 For all soil layers, the Q10 values for the active and slow SOC pools were
271 calculated as:

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272 Q10 = k30 / k20, (5)
273 where k20 and k30 are the decomposition rates for the SOC pool at 20°C and 30°C,
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274 respectively (Conant et al., 2008).
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276 2.7. Statistical analysis

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277 Statistical differences between the means of two groups were examined using a
278 t-test at the 5% (p = 0.05) significance level. Statistical relationships between two
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279 variables were examined by the significance of the Pearson correlation coefficient at the
280 5% (p = 0.05) significance level.

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281
282 3. Results
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283 3.1. SOC stock in the forest surface soils
284 The three forest sites investigated in this study differed in the amount and depth
285 profile of the SOC in their surface soil (Table 3). The SOC stocks in the upper 15 cm of
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286 the mineral soil were 5.8, 9.1, and 3.4 kg C m−2 at the AP, OG, and IB sites,
287 respectively. The SOC density (kg C m−2 cm−1-depth) decreased with depth at the AP
288 and IB sites, but was nearly constant and remained high down to ~20 cm at the OG site.
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290 3.2. CO2 emission rates
291 In the incubation study, temporal changes in the CO2 emission rate (normalized to
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the soil C content, in mg C g−1-soil C day−1) for all the soil layers showed a similar
293 two-phase pattern with relatively fast rates during the early incubation period followed
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294 by slower rates thereafter (Fig. 1). The CO2 emission rate was highest at the beginning
295 of the incubation, dropped rapidly at around day 40, and then remained low and
296 relatively constant through day 120. Regarding the depth trend in the soil profiles, the
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297 CO2 emission rate was generally higher in shallower soil layers than in the deeper soil
298 layers. At nearly all depths and sites, the CO2 emission rate at LIT30 was higher than
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299 that at LIT20. Throughout the incubation period, the CO2 emission rate was highest in
300 the IB soil where the SOC stock was the lowest and the amount of organically
301 complexed Al (Alp) and short-range-order minerals (Alo and Feo) were the lowest
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302 among the three sites (Table 2).
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304 3.3. AISF fraction
305 Although the AISF-SOC density (in kg C m−2 cm−1-depth) differed among the
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306 three forest surface soils (Table 3), it was positively correlated (r2 = 0.95, p < 0.0001, n
307 = 21) with the total SOC density across the sites and at all depths, indicating that the
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308 AISF-SOC represents a similar proportion of the total SOC in the different soils.
309 The 14C values for the bulk SOC steeply decreased with depth at all sites (Table
310 3) with positive values at the shallower depths and negative values at the deeper depths,
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311 indicating that overall the older and thus slower-cycling SOC was present in the deeper
312 depths. The positive 14C values observed in the upper soil layers indicated that the
313 SOC in these layers has a significant component of organic C labeled with “bomb” 14C
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314 that was deposited from the atmospheric nuclear weapon testing conducted in the late
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315 1950s and early 1960s. The AISF fraction was similar in the depth profile of 14C as the
316 bulk soil, but was generally lower in the 14C value than the bulk soil. The AISF-C was
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enriched in 14C compared with the bulk soil C that was observed in the top two layers at
318 the AP site, which probably reflects a higher relative contribution of “bomb” 14C (i.e.,
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319 decades-old C) to the AISF fraction than to the bulk soil C. The MRTMAT for the
320 AISF-C was estimated based on the 14C value, which increased with depth and ranged
321 from 85–1070 years (Table 4).

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323 3.4. Partitioning of the SOC pools and their contribution to the total CO2 emission
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324 The size and MRT of the active and slow SOC pools were determined through
325 fitting the decomposition model (Eq. (4)) to the observed CO2 emission rate over time.
326 For all sites, depths, and times, the modeled CO2 emission rates reproduced the
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327 observed rates well. Fig. 2 shows examples of the fitting results for the top 0–2 cm and
328 bottom 15–21 cm soil layers of the OG site at LIT20 and LIT30. All fitting results are
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329 provided in Fig. A1 of the Appendix.
330 With the obtained parameters, the active SOC pool was identified at all depths as a
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331 small sized pool (0.1–3.4 g C m−2 cm−1-depth), which accounted for only 0.1%–0.7% of
332 the total SOC (Table 4). The MRTMAT of the active SOC pool ranged from 3 days to 12
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333 weeks. There were no apparent depth trends in either of the proportional size or
334 MRTMAT of the pool. Because of the short MRT, the active pool contributed the most
335 (63%–96%, average: 85%, estimated by dividing the SOC content by MRTMAT) to the
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336 CO2 emission rate at the time when incubation started (Table 4). However, the
337 contribution of this pool to the total CO2 emission decreased to <10% within 30–50
338 days (Figs. 2 and A1). Some exceptions showed a longer MRTMAT (74–85 days) for the
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339 active pools in the upper 0–6 cm of the soil layers at the AP site. These deviations may
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340 be partly due to a lack of CO2 emission rate measurements for these layers during the
341 first few days of incubation (Figs. 1 and A1), which resulted in an underestimation of
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the initial rate of CO2 emission by the model fitting and thus an overestimation of the
343 MRTMAT.
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344 In contrast to the active SOC pool, the slow SOC pool represented a significant
345 proportion of the total SOC (23%–52%, 30%–38%, and 31%–47% for the AP, OG, and
346 IB soils, respectively) at all sites and depths (Table 4). The MRTMAT estimated for the
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347 slow SOC pool ranged from 12–231 years. Note that the MRTMAT values for the two
348 soil layers (6–8 and 8–10 cm) of the OG site are not included in the following
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349 discussion because the fitting model analysis indicated that the decomposition of the
350 slow SOC, which is characterized by ks (the reciprocal of MRT), for these layers was
351 not statistically significant (p > 0.05) to explain the observed change in the CO2
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352 emission rate. Because of the size and MRT, the slow SOC pool constantly contributed
353 to the CO2 emission rate throughout the incubation period (Figs. 2 and A1). The slow
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354 pool was estimated to be responsible for 3%–31% (average: 12%) of the CO2 emission
355 rate at the time that incubation started (Table 4). The contribution of the slow SOC pool
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356 became the most significant after the active SOC pool was exhausted (several tens of
357 days after initiation of incubation) (Figs. 2 and A1). There were also no clear depth
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358 trends in either of the proportional size or MRTMAT of the slow SOC pool. Regarding
359 the site-to-site variability, the MRTMAT for the slow SOC pool was generally short
360 (14–44 years) at the IB site which had the lowest SOC stock and reactive metal content
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361 but had the highest CO2 emission rate among the three sites.
362
363 3.5. Q10 values for the active and slow SOC pools
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364 The results from the model fitting to the CO2 emission rates at LIT20 and LIT30
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365 were used to calculate the Q10 values for the active and slow SOC pools. The Q10 values
366 for the active SOC pools ranged from 1.2–1.7 with an average of 1.4 ± 0.1 (1 SD) (Fig.
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3). The Q10 values for the slow SOC pools ranged from 1.1–4.0 with an average of 2.2 ±
368 0.6 (1 SD). The Q10 value for the slow SOC pool was significantly (p < 0.0001) higher
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369 than that for the active SOC pool. Across all sites and depths, the Q10 values were
370 positively correlated with the MRTMAT for the active (r2 = 0.51, p < 0.001, n = 21) and
371 slow (r2 = 0.74, p < 0.0001, n = 19) SOC pools.

ot
372
373 4. Discussion
tn
374 4.1. SOC dynamics revealed by three-pool partitioning
375 For most of the sites and depths, the three-pool first-order decomposition model
376 with determined parameters explained the observed change in CO2 emission rates with
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377 time well, thereby enabling the separation of the total soil C into three (active, slow, and
378 resistant) SOC pools with different MRT ranges. The active SOC pool was small in size
ep
379 (0.1%–0.7% of the total SOC) and consisted of rapidly cycling (generally <2 weeks) C
380 under the MAT conditions. The slow SOC pool was identified as a much larger C pool
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381 (at least 23%–52%) that cycled on a timescale of decades to more than a century. As
382 evidenced, a rapid decline in the CO2 emission rate during the early incubation stage
16
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383 was observed for a range of soils (Townsend et al., 1997; Hartley and Ineson, 2008;
384 Fissore et al., 2009; Wetterstedt et al., 2010). This decline has previously been
385 interpreted as an indication of the existence of a small, labile SOC pool and a much
iew
386 larger, more recalcitrant SOC pool (Townsend et al., 1997). The quantified sizes and
387 MRTMAT values of the active and slow SOC pools in this study are consistent with this
388 previous interpretation.
v
389 The CO2 emission rate expressed on a per gram soil C (in mg C g−1-soil C d−1)
re
390 basis can be considered an indicator of the SOC degradability. The active SOC pool was
391 found at all depths and showed no clear depth trends in either of the proportional size or
392
er
MRTMAT (Table 4), indicating that the active pool represents a highly degradable part
393 of the SOC that produces the CO2 efflux at a significant rate throughout the soil profile.
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394 Similar sizes and turnover properties have been reported for the soil microbial biomass
395 C (Saggar et al., 1999; Blagodatskaya et al., 2011) and dissolved organic C (Qualls and
396 Bridgham, 2005).

ot
397 Despite the significantly longer MRTMAT for the slow SOC pool than the active
398 SOC pool (Table 4), the slow SOC pool contributed approximately 12% of the CO2
tn
399 emission from the soil even at the beginning of incubation. This was evidently because
400 of the large SOC stock in the slow pool. The possible mechanisms for SOC storage over
401 the timescale of decades to a century in this pool include the following: selective
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402 preservation of inherently recalcitrant organic compounds in plant litter and
403 rhizodeposits (Baldock et al., 1997; Nierop, 1998), production of microbially derived
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404 organic compounds (Kiem and Kögel-Knabner et al., 2003), physical protection of SOC
405 through aggregate formation (von Lützow et al., 2006), and sorption of SOC in the outer
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406 regions of the organo-mineral complexes (Kleber et al., 2007). At the IB site, where a
407 higher CO2 emission rate (and thus higher SOC degradability) was observed, the
17
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408 slow-pool MRTMAT was shorter (generally less than 25 years) than those at the other
409 two sites. This suggests that the regulatory mechanisms controlling the dynamics of the
410 slowly cycling SOC may differ among the sites. For example, there may be a weaker
iew
411 interaction of SOC with the soil minerals at the IB site, as suggested by the
412 mineralogical properties shown in Table 2.
413 The resistant (or AISF) SOC pool contained approximately half to three-quarters of
v
414 the soil C at all depths. Despite the large stock of C in the pool, its contribution to the
re
415 CO2 emission rate was almost negligible because of its long MRTMAT of 85–1070 years.
416 The AISF-SOC pool is assumed to consist of not only highly condensed, biochemically
417
er
resistant humic substances but also the less-resistant organic substances that are strongly
418 associated with the mineral phase and are physically protected in microaggregates
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419 (Leifeld and Fuhrer, 2005; Paul et al., 2008). Although it is likely that the AISF-SOC
420 pool is heterogeneous and contains both faster and slower-cycling C (Trumbore and
421 Zheng, 1996; Koarashi et al., 2009), the overall long MRTMAT of this pool and positive
ot
422 correlation between the amount of total SOC and AISF-SOC suggest the importance of
423 this pool in C accumulation in the forest surface (0–20 cm) soil. This result also implies
tn
424 that the AISF-SOC pool can be increased or decreased due to natural and artificial
425 changes in the environmental conditions, such as climate and land-use changes (Paul et
426 al., 2006).

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427
428 4.2. Temperature sensitivity of SOC with different MRTs

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429 Our approach using laboratory incubation and AISF-14C measurements of the
430 thin-layered soil samples revealed the depth distributions of the size and MRTMAT for
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431 the active and slow SOC pools from the surface soil of three Japanese forests (Table 4).
432 As expected, different MRTMAT values were obtained, particularly for the slow SOC
18
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433 pools, and as a result, SOC pools with an MRTMAT variety (from days to more than a
434 century) were identified across the sites and depths. Using two temperatures (LIT20 and
435 LIT30) for the laboratory incubation conditions, the temperature sensitivity (Q10) of the
iew
436 SOC decomposition rate for the pools was determined, and thus, the relationship
437 between the MRTMAT and Q10 was elucidated.
438 It was found that the Q10 values ranged from 1.1–4.0 and increased with increasing
v
439 MRTMAT (Fig. 3). These results are in agreement with the majority of other published
re
440 incubation studies (Conant et al., 2011), which indicates that the decomposition rate of
441 slowly cycling SOC is more sensitive to increases in temperature than that of the rapid
442
er
cycling SOC. In the field observations at the AP site, Atarashi-Andoh et al. (2012)
443 estimated a higher temperature sensitivity for the SOC decomposition than for the more
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444 rapidly cycling litter decomposition by separating the soil respiration sources using a
445 “bomb” 14C tracer.
446 Based on the kinetic theory (carbon quality-temperature hypothesis), the substrate
ot
447 decomposition response to changes in temperature should show increased sensitivity
448 with greater activation energy or greater intrinsic biochemical recalcitrance (Davidson
tn
449 and Janssens, 2006). However, in soil, the intrinsic temperature sensitivity may be
450 obscured in cases where the environmental constraints (including physical, chemical,
451 and biological mechanisms) impose more stringent limitations on the SOC
rin
452 decomposition rate. Therefore, the determined Q10 values, particularly for the slowly
453 cycling SOC pool, may rather represent the “apparent temperature sensitivity”, which
ep
454 may be lower or higher than the intrinsic temperature sensitivity of the organic materials
455 (Davidson and Janssens, 2006). Although the MRTMAT of the SOC pool is not
Pr
456 necessarily indicative of the biochemical recalcitrance, the apparent Q10 values
457 increased with the MRTMAT. Thus, these results suggest that the attenuation of the SOC
19
ed
458 decomposition temperature sensitivity (MRTMAT < 100 years) caused by environmental
459 constraints in the soils may be slight when compared with the intrinsic temperature
460 sensitivity explained by the carbon quality-temperature hypothesis. This conclusion is
iew
461 consistent with the results of Plante et al. (2009), where no significant differences in the
462 Q10 values were observed for soil (silt loam) samples with different degrees of physical
463 disruption. Alternatively, the present results may suggest that the multiple mechanisms
v
464 operating in the soils themselves are temperature sensitive (Davidson and Jenssens,
re
465 2006; Craine et al., 2010; Conant et al., 2011). For example, Kaiser et al. (2001)
466 reported that the sorption and desorption reactions of SOC with mineral surfaces are
467 temperature dependent.

er
468
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469 4.3. CO2 emission potential of the three SOC pools under global warming
470 Although the mechanisms controlling the degradability and temperature sensitivity
471 of SOC in soils are not yet fully understood, the results of the present study demonstrate
ot
472 that a large quantity of C (1.4–3.2 kg C m−2 in the top 15 cm of mineral soil) that has
473 been stabilized for over decades to roughly a century is highly vulnerable to warming.
tn
474 For all the SOC pools with MRTs of >40 years, the Q10 value was greater than 2.0 (Fig.
475 3), a value that is used equally for different types of SOC pools in most ESMs (Cox et
476 al., 2000; Jones et al., 2005; Friedlingstein et al., 2006; Foereid et al., 2014). Given this,
rin
477 the CO2 emissions from slow SOC pools can remain elevated over the next century,
478 because the pools are large and not depleted even though warming continues to
ep
479 accelerate the rate of SOC decomposition in these pools (Koarashi et al., 2009;
480 Teramoto et al., 2016). The rapidly cycling (active) SOC pools contribute to the current
Pr
481 rate of CO2 emission more than the slowly cycling SOC pools. However, the rapidly
482 cycling pools are not only less temperature sensitive but also small in size, and therefore,
20
ed
483 the elevated CO2 emission from the rapidly cycling SOC pools may not be maintained
484 for decades under the upcoming warmed environments.
485 For the resistant SOC pool, no information was obtained regarding its temperature
iew
486 sensitivity in the present study. Karhu et al. (2010) showed that the temperature
487 sensitivity of SOC decomposition is higher for decadally cycling fractions (Q10 =
488 4.2–6.9) compared with annually (Q10 < 2) and centennially cycling fractions (Q10 =
v
489 2.4–2.8) in typical podzol-type soils of boreal forests. This suggests that some
re
490 mechanisms inhibit the temperature response of SOC that cycles on timescales of a
491 century or longer. The resistant SOC pool that is characterized by a long MRTMAT is
492
er
unlikely to be responsible for the annual CO2 emissions. However, given that the
493 Japanese forest surface soils store a large amount (2.0–5.9 kg C m−2) of C as resistant
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494 SOC, it is possible that even small changes in the SOC decomposition rates in this pool
495 could have a significant impact on the C stock in soil over the next century (Koarashi et
496 al., 2009). Further studies are required to determine whether a shift in the climate
ot
497 conditions can alter the decomposition rate of SOC that has been stabilized for over
498 decades to a century or longer in the surface mineral soil, which could be essential to
tn
499 accurately predict the magnitude and timing of the response of Japanese forest soil to
500 global warming.
501
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502 Acknowledgments
503 The authors thank Sinobu Makimoto of the Japan Atomic Energy Agency (JAEA)
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504 for the support with the laboratory work, Takayuki Tanaka and the rest of the staff at the
505 Aomori Research and Development Center of the JAEA for the AMS-14C
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506 measurements, and Keizo Hirai of the Forestry and Forest Products Research Institute,
507 Masakazu Ota, and Takahiro Nakanishi of the JAEA for discussions. The authors also
21
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508 thank the Iwatehokubu District Forest Office, the Forestry Agency’s Tohoku Regional
509 Forest Office, and the Nagoya University Forest for permission to use the research sites
510 for this study. This work was performed within the framework of the JAEA-FFPRI
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511 Cooperation Research Scheme.
512
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710 Ogawa Forest Reserve. In: Nakashizuka, T., Matsumoto, Y. (Eds.) Ecological
iew
711 Studies Vol. 158, Diversity and Interaction in a Temperate Forest Community:
712 Ogawa Forest Reserve of Japan. Springer-Verlag, Tokyo, pp. 19–26.
713 Zhou, T., Shi, P., Hui, D., Luo, Y., 2009. Global pattern of temperature sensitivity of
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714 soil heterotrophic respiration (Q10) and its implications for carbon-climate feedback.
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715 J. Geophys. Res. 114, G02016.
716
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717 Figure captions
718
719 Fig. 1. Temporal changes in the CO2 emission rates of the surface soil from three forests
iew
720 (AP, OG, and IB) during incubation. The left and right panels show the results
721 at the laboratory incubation temperature (LIT) conditions of 20°C (LIT20) and
722 30°C (LIT30), respectively.
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723
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724 Fig. 2. Examples of the model fitting results for the CO2 emission rates observed in the
725 top 0–2 cm and bottom 15–21 cm layers of the OG soil at the laboratory
726
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incubation temperature (LIT) conditions of 20°C (LIT20) and 30°C (LIT30).
727
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728 Fig. 3. Q10 values versus the mean residence time with the mean annual temperature
729 (MRTMAT) for the active and slow soil organic carbon (SOC) pools of Japanese
730 forest soil.

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2 Temperature sensitivity of organic carbon decomposition increases with increasing

3 mean residence time in Japanese forest surface soil

5 Author names and affiliations

6 Jun Koarashia,*, Koichi Moriyaa,b, Hirohiko Naganoc, Mariko Atarashi-Andoha,

17 E-mail address: koarashi.jun@jaea.go.jp (J. Koarashi)

20 Understanding the sensitivity of soil organic carbon (SOC) decomposition to

21 temperature is vital to accurately predict the soil C response to global warming.

29 three-pool first-order decomposition model and radiocarbon (14C) measurements of the

45 Decomposition; Radiocarbon (14C); Three-pool model

49 KAKENHI (grant numbers 23380096, 15H04523).

52 Jun Koarashi: Conceptualization, Methodology, Investigation, Visualization, Writing –

54 Hirohiko Nagano: Formal analysis, Visualization. Mariko Atarashi-Andoh:

59 The microbial decomposition of soil organic carbon (SOC) is an essential

62 heterotrophic respiration). Globally, this soil heterotrophic respiration is estimated to be

66 the global C cycle. The microbial decomposition of SOC is a temperature-sensitive

72 and timescale of this warming-induced effect on soil heterotrophic respiration, largely

73 due to a lack of quantitative insight into the temperature sensitivity of SOC

74 decomposition (Zhou et al., 2009; Bradford et al., 2016).

75 The temperature sensitivity of SOC decomposition has previously been

91 SOC is a complex mixture of plant-derived and microbially-transformed organic

93 of enzyme kinetics (also known as the “carbon quality-temperature hypothesis”) suggest

95 with increasing biochemical recalcitrance of organic compounds (Bosatta and Ågren,

97 decomposition of organic materials in organic (O) horizons (Wetterstedt et al., 2010).

99 material decomposition may be obscured by a range of physical, chemical, and

102 to increases in temperature, a review by Conant et al. (2011) considered a number of

110 of soil microorganisms and physicochemical destabilization and stabilization processes

127 feedback effects through the use of these ESMs.

147 2. Materials and methods

148 2.1. Study sites

150 The AP site is a cool–temperate, deciduous, broadleaved forest dominated by

154 temperate, coniferous forest dominated by approximately 50-year-old Japanese larch

157 and 1207–1990 mm, respectively, across the three sites.

170 2.2. Collection and treatment of soil samples

181 2.3. Incubation procedure

193 total effective volume enclosed was 2.1 L.

195 2.4. Soil fractionation and C isotope analysis

221 quantified according to the well-established three-pool first-order decomposition model

223 CT(t) = Ca exp(−ka t) + Cs exp(−ks t) + Cr exp(−kr t), (1)

246 represented by the differentiated form of Eq. (1):

247 E(t) = −dCT(t)/dt = ka Ca exp(−ka t) + ks Cs exp(−ks t) + kr Cr exp(−kr t) (3)

252 be considered as a two-pool phenomenon:

253 E(t) = ka Ca exp(−ka t) + ks Cs exp(−ks t) (4)

271 calculated as:

272 Q10 = k30 / k20, (5)

274 respectively (Conant et al., 2008).

276 2.7. Statistical analysis

280 5% (p = 0.05) significance level.

302 among the three sites (Table 2).

304 3.3. AISF fraction

321 from 85–1070 years (Table 4).

329 provided in Fig. A1 of the Appendix.

371 slow (r2 = 0.74, p < 0.0001, n = 19) SOC pools.

374 4.1. SOC dynamics revealed by three-pool partitioning

388 previous interpretation.

396 Bridgham, 2005).

402 preservation of inherently recalcitrant organic compounds in plant litter and

412 mineralogical properties shown in Table 2.

426 al., 2006).

428 4.2. Temperature sensitivity of SOC with different MRTs

437 between the MRTMAT and Q10 was elucidated.

445 “bomb” 14C tracer.