Geoderma 129 (2005) 139 146 www.elsevier.

com/locate/geoderma

Incorporating microorganisms as decomposers into models to simulate soil organic matter decomposition
C. Fanga,*, P. Smitha, J.U. Smitha, J.B. Moncrieff b
a

Department of Plant and Soil Science, School of Biological Sciences, University of Aberdeen, Cruickshank Building, St Machar Drive, Aberdeen AB24 3UU, UK b Ecology and Resource Management, School of GeoSciences, University of Edinburgh, Edinburgh EH9 3JU, UK Received 29 August 2003; received in revised form 6 December 2004; accepted 17 December 2004 Available online 22 January 2005

Abstract Current models simulating soil organic matter (SOM) are based on the assumption of first order decomposition. The microbial component of soil organic C (SOC) is mainly simulated as a substrate. The contribution of soil microbe to decomposition as a decomposing agent is implicitly included in the rate constant k and does not change throughout the simulation. The temporal and spatial variation in SOM decomposition/dynamics may have been biased by models, and our prediction of SOM response to global change may have been overestimated, due to missing the feedback effect of microbes on SOM decomposition. We suggest a general model, which explicitly incorporates soil microbe as decomposers of SOM. Future studies in both experiment and modelling are necessary for us to understand interactions between soil microbial abundance and activity, the quality and quantity of SOM pool, and the effects of environmental conditions. D 2005 Elsevier B.V. All rights reserved.
Keywords: Organic matter decomposition; Soil C modelling; Microbial C; Decomposer

1. Introduction Many models have been developed to simulate SOM dynamics and to predict the possible response of SOM under different climate change scenarios or land-use management (such as the CENTURY, DAISY, DNDC, Roth-C, CANDY and other models, see web site of Global Change and Terrestrial
* Corresponding author. Tel.: +44 1224 272789; fax: +44 1224 272703. E-mail address: c.fang@abdn.ac.uk (C. Fang). 0016-7061/$ - see front matter D 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.geoderma.2004.12.038

Ecosystems Soil Organic Matter Network (GCTE SOMNET) at URL: http://yacorba.res.bbsrc.ac.uk/ cgi-bin/somnet). Most of the present models are regarded as process-oriented models, which focus on the processes involving the movement and transformations of matter or energy. Another type of model is referred to as the organism-oriented model, which simulates the flows of matter or energy through different groups of soil organisms (Paustian, 1994). Organism-oriented models are more diverse than are process-oriented models but fewer have been developed (Smith et al., 1998).

140

C. Fang et al. / Geoderma 129 (2005) 139146

SOM decomposition is mainly a process of SOM breakdown and transformation under the action of soil microbes. The function of soil microbes is important and should be properly treated in a SOM model (McGill, 1996; Smith et al., 1998). In most current models, microbial C is taken as one (Parton et al., 1987; Coleman and Jenkinson, 1996) or more components (e.g., labile and resistant microbial C in the DNDC model, Li et al., 1993) of SOM pool. However, the microbial component was only taken as a substrate of decomposition rather than as a decomposer in these models. The contribution of soil microbe to SOM decomposition is implicitly included in the apparent decomposition rate constants of different C pools (Paustian, 1994; McGill, 1996) when a model is parameterized. Due to this treatment of soil microbes, models are independent of temporal and spatial variations in the soil microbial community, and may lack the flexibility to simulate effects of landuse change and agricultural management that have direct impacts on soil microbial biomass and activities. We suggest here a new general model in which the soil microbial community is considered as a decomposer (as well as the dead microbial pool as a substrate), independent of the quantity and quality of SOM pools as substrates. We believe that this approach does have advantages over current SOM models.

2. Current models for SOM decomposition At present, the simulation of SOM decomposition in various models can be generalized as follows: BC KC d f1 T f2 W f3 clayf4 O2 . . . Bt
n X BC Ki Ci d f1 T f2 W f3 clayf4 O2 . . . Bt i1

constant for total organic carbon, C ; K i and K j are rate constants for the i th and j th component of SOC, C i and C j . n is the pool number. f 1(T ), f 2(W ), etc. denote influences of temperature, soil moisture content and other environmental factors on SOM decomposition, or are referred to as reduction factors. Definition of these influences may vary from model to model. a ji is a transfer coefficient of decomposed carbon from the j th to the i th component, presumed equal to zero when j =i (Li et al., 1993; Coleman and Jenkinson, 1996). For a single pool model, total SOM available for microbial decomposition is considered as a homogeneous pool regarding the decomposability (Jenny, 1941), or as a conceptual pool equivalent to a homogeneous substrate (Alvarez et al., 1998; Fang and Moncrieff, 1999). In a multiple pool model, SOM is conceptually divided into labile (including dissolved organic C (DOC), microbial C, etc.) and resistant (passive, resistant or inert C) pools (Parton et al., 1987; Mueller et al., 1996; Coleman and Jenkinson, 1996; Thornley and Cannel, 1997). During a unit time, a fixed percentage of decomposed organic matter is assimilated into microbial biomass and a fixed portion of microbial C will be finally oxidized into CO2 where O2 is not limited (Coleman and Jenkinson, 1996). Although the maintenance respiration of soil microbes has been considered in some models (such as in the DAISY model, Mueller et al., 1996; the C-TOOL model, Petersen et al., 2002), the SOM decomposition or rate constants K s are not linked to microbial biomass and its activity.

3. Model uncertainties without considering soil microorganisms as decomposers 3.1. Overestimating SOM response to global change For a compartment model simulating the decomposition of SOM pools, it is reasonable and convenient to assume that a fixed percentage of decomposed organic C is assimilated by microbes and a fixed portion of microbes will die and thereafter be decomposed. When environmental conditions change, these changes will alter the decomposition rate through reduction factors f 1(T ), f 2(W ) and etc. The microbial pool is consequently changed, and the changed microbial community should lead to a further

BC Bt

n X i1

Ki Ci

n X j1

! aji Kj Cj

d f1 T f2 W f3 clayf4 O2

Eq. (1) is a single pool model and Eqs. (2) and (3) are for multiple pools. K is the decomposition rate

C. Fang et al. / Geoderma 129 (2005) 139146

141

alteration in the rate of SOM decomposition. A model should have a mechanism allowing decomposition rate to be adjusted according to the density and the activity of microbes as the decomposing agent. This mechanism has not been included in current models. We use a newly released dataset for UK climate change (UKCIP02 metadata, available at http:// www.ukcip.org.uk/scenoarios/metadata) and the RothC model to predict SOM dynamics in UK soils from year 1990 to 2080. In most soils in the North and West of the UK, both SOM and microbial C will significantly decline due to global change over that period. The reduction in microbial pool size can exceed 30%. On the other hand, SOM and microbial C may both increase in some UK soils due to global change. The relationship between SOM decomposition and soil microbial biomass is complicated. SOM decomposition rate was reported both affected (Alvarez et al., 1998; Lovell and Jarvis, 1998; Lundquist et al., 1999; Grayston et al., 2001) and unaffected by microbial biomass (Raubuch and Joergensen, 2002; Wang et al., 2003). We observed that soil basal respiration rate is closely related to changes in microbial biomass associated with soil depth, soil sampling method and incubation time (Fang et al., 2005; Fang and Moncrieff, in press). There is no reason to assume that decomposition rate constants of SOM remain unchanged when soil microbial pool size varies significantly, especially for a long term change. The reduction in microbial biomass could slow down SOM decomposition and lead to an accelerated accumulation of SOM in soils. On the other hand, increased microbial biomass could speed up the decomposition and slow down the accumulation of SOM. With a linear assumption between SOM decomposition rate and microbial pool size, model predictions of the soil as a net sink/source to atmospheric C are significantly different from that without the feedback effect of microbial community (Fig. 1). It is interesting that the influence of this feedback on predicted SOM stock is dependent on whether the soil will release or sequester C with respect to global change. The sink strength of the soil with the feedback (b) is always smaller than that without the feedback effect of microbial C (a). For most of the period, b is about half the value in a. However, when a soil is a net C source, the feedback will increase the speed of C release at the early stage

Simulated net change in TOC (ton C ha-1)

4 2 0 -2 -4 -6 2000

(a) (b)

(c) (d)

2020

2040

2060

2080

Year
Fig. 1. Predicted net change in TOC as a sink/source to atmospheric C, using the RothC model (Coleman and Jenkinson, 1996) and predicted climate change data in UK over next century (UKCIP02 climate change scenarios, low emissions). Strengths of sink/source without considering the feedback effect of microbial component on OM decomposition (a for grid 394, d for grid 161) are larger than that OM decomposition is linearly related to microbial C pool in the soil (b for grid 394, c for grid 161).

but slow down later. The source strength with the feedback (c) is only about 21% weaker than that without the feedback (d) at year 2080. A linear relationship may not best define the effects of microbial biomass on SOM decomposition. However, the change in SOM, either as a net C source or as a net sink to atmospheric C, has probably been overpredicted by current models because of missing the feedback of soil microbe on SOM decomposition. 3.2. Biased SOM decomposition along with soil depth The turnover of SOM generally decreases with soil depth (Trumbore, 2000). The ratio of basal respiration to SOM decreases with soil depth, as observed in many soil incubations in the laboratory where ambient conditions were kept the same for samples from different depths (Boyer and Groffman, 1996; Alvarez et al., 1998; Ross et al., 1999; Agnelli et al., 2001). Fig. 2 shows a significant decline in the ratio of microbial respiration rate to total organic C (TOC) with the depth in different Scottish soils. The decrease in the ratio may be partly explained as the increase of the resistant component of SOM (Alvarez et al., 1998) or the decrease of SOM quality along with soil depth gren, 1996). However, in many soils, (Bosatta and A such as in temperate soils or soils developed under

142
0.10

C. Fang et al. / Geoderma 129 (2005) 139146

Birch woodland 0.08

Sitka spruce

Specfic respiration rate over TOC, Cmic and DOC

0.06 0.04 0.02 0.00 Pasture 0.08 0.06 0.04 0.02 0.00 0 10 20 0 10 20 Micro. resp. rate: TOC Micro. resp. rate: Cmic Micro. resp. rate: DOC Scots pine

Soil Depth (cm)

Fig. 2. The variation in ratios of soil microbial respiration rate to TOC, Cmic and DOC with soil depth. Samples were taken from four different soils in Scotland at different depths, and incubated in the laboratory under constant temperature (20 8C) and moisture, with the fresh air being continuously passed through soil chamber. Microbial respiration rate was measured with an infrared gas analyser (LiCor 6252) in differential mode. See Fang and Moncrieff (in press) for details of experiment. Units are mg CO2 g C1 h1, g CO2 g DOC-C1 h1 and g CO2 g Cmic-C1 h1 for the ratio of microbial respiration rate to TOC, DOC and Cmic, respectively.

cold or wet climate, the decrease of SOM turnover rate may not be explained by the variation in SOM quality with depth in all soils. DOC has been proposed as an indicator of the C available to soil microorganisms or the labile component of SOM (Smolander and Kitunen, 2002). The ratio of microbial respiration rate to DOC in Fig. 2 does not show a consistency, declining with the depth in some soils but varying in others. Despite microbial biomass significantly decreased with soil depth, the specific activity of soil microbe (basal respiration rate: Cmic) was consistent in these soils (Fig. 2). For simulating SOM decomposition along with soil depth, decomposition rate constants in Eqs. (1)(3) have to decrease with depth (Boyer and Groffman, 1996; Lomander et al., 1998). This proves to be a difficulty for models, which estimate K i based on fitted quality and composition of SOM pools. Most models used the same K i and partitioning coefficients for SOM pools at all depths. As a result of the assumption of constant K i within soil profile, the

relationship between organic matter (OM) dynamics and environmental conditions may have been biased, because the decomposition of OM in deep soil has been systematically overestimated (or underestimated in surface soil) and temporal variations in microbial community (e.g., microbial biomass, Luizao et al., 1992), OM input and environmental factors (temperature, moisture content, etc.) change with soil depth. Incorporating microbial biomass/activity may help to simulate the decline of C turnover rate with soil depth (Fang and Moncrieff, in press). 3.3. Effects of N/nutrients concentration and other factors on soil microbial community Changes in soil nitrogen (N) or other nutrient concentration will alter SOM decomposition (Amador and Jones, 1993; Henriksen and Breland, 1999; SaiyaCorka et al., 2002). The N input to arable soils is affected or managed by agricultural practice. In natural soils, N concentration or the N:C ratio of

C. Fang et al. / Geoderma 129 (2005) 139146

143

SOM could be affected by global change through increasing mean annual temperature (Post et al., 1985) and global N deposition (Nadelhoffer et al., 1999). Possible explanations of the effects of changing N/ nutrient conditions in the soil on SOM decomposition are through changing microbial biomass (Lovell and Jarvis, 1998; Kouno et al., 1999), microbial activity (Lovell et al., 1995), the fraction of binactiveQ biomass (Lovell and Jarvis, 1998) or the shifting between dormant and active states (Blagodatsky and Richter, 1998; Stenstro m et al., 2001), rather than firstly changing the quantity or quality of SOM. Many other causes, such as pollution or application of biocides and climate conditions, could have immediate effects on microbial community and then SOM decomposition/sequestration. In arable soils, the ratio of Cmic/Corg was reported to be closely related to integrative climatic variables reflecting both temperature and moisture conditions, such as the precipitation evaporation quotient (Insam et al., 1989). Lack of a mechanism of simulating the influence of changing microbial biomass and its activity in current models will restrict models ability to predict soil C sequestration affected by changes in N/nutrient input, pollution management and soil remediation, land-use change and global change. 3.4. Temporal variation in SOM decomposition During the year, soil microbial biomass may have the maxima during summer and the minima in winter (Bardgett et al., 1999). Under field conditions, the seasonal variation in microbial biomass could be up to 90% among different ecosystems or soils, with a global average of about 27% for soils in forest ecosystems and 25.5% for arable soils. However, the seasonal trend in microbial biomass is not clear for some soils (compiled data by Wardle, 1998). If the specific microbial activity is assumed to be relatively consistent through the year (impacts of seasonal variation in temperature and other factors on microbial activity have been accounted for separately in f 1(T ), f 2(W ), etc.), the temporal variation in SOM decomposition should be linearly related to microbial biomass. Basal respiration rate corresponds with the temporal variation in microbial biomass (Lundquist et al., 1999). In current models, the seasonal variation in the rate of SOM decomposition is commonly attrib-

uted to variations in soil temperature, moisture content and the input of plant residue through the time. The influence of temporal variation in microbial biomass/ activity on soil respiration/SOM decomposition is not considered. If rate constants K or K i are initially estimated by fitting a model to short-term data from laboratory incubation, the model will probably underestimate SOM decomposition rate in summer time but overpredict it in winter. If a model is fitted to longterm field data, estimated f 1(T ) includes a part of the effect of seasonal variation in microbial biomass/ activity. The model may overestimate the temperature response of SOM decomposition, or underestimate it if the maximal biomass/activity coincides with lowest temperature. As a result, our prediction of soil-stored carbon to future climate change may be biased.

4. General model for SOM decomposition By the principle, microbial respiration in the soil or the decomposition of soil organic carbon can be defined by a general model as below: X BC KB; Di Bd fi Ci ; Di d f2 T ; W ; clay; O2 ; . . . Bt i 4 where C is the total organic carbon pool as a substrate for decomposition and t is the time; B is the live or active microbial biomass with a specific activity of K B ,D i . Subscripts B and D i denote that microbial activity may be related to the density/diversity of microbes and the quality of carbon component; f 1(C i , D i ) is the dependence of microbial respiration on the quantity, C i , of the i th component and its decomposability/quality/availability, D i ; f 2(T, W, clay, O2, . . .) describes influences of soil temperature, moisture, clay content, oxygen concentration and other environmental conditions on K B ,D i or D i . f 1(D i ,C i ) and f 2(T, W, clay, O 2, . . .) may have different relationships or equations in different models or in different soils. When the transfer of decomposed OM between components is taken into account, Eq. (4) can be re-written accordingly. Eq. (4) only includes direct influences of soil conditions on OM decomposition. Dead microorganisms as a substrate for respiration can be one (or more)

144

C. Fang et al. / Geoderma 129 (2005) 139146

of the simulated SOM pools, if there is such a pool in a model. Dead microorganisms can also be implicitly gren included in a conceptually single pool model (A and Bosatta, 1996; Yang and Janssen, 2000; Fang et al., in press). We believe that the governing Eq. (4) properly generalizes relationships between SOM quantity and quality, microbial biomass and activity, and soil environmental conditions in SOM decomposition, and that above uncertainties in current models could be avoided or improved. In a real soil, it is not easy to estimate K B ,D i independently from D i . Although activities of enzymes have been used as indicators of microbial activity (Henriksen and Breland, 1999; Pascual et al., 2000), it is of little use for modelling purpose. Considering that microbial C only accounts for a small part of SOM under field conditions and that little is known about the temporal variation in microbial diversity and its function, Eq. (4) may be simplified as: X BC B KiV f1 Ci d f2 T ; W ; clay; O2 ; . . . Bt 5

where KV i is the apparent decomposability of the i th component of SOM, including influences of K B ,D i and D i . KV i can be estimated by fitting Eq. (5) to measured data. B is the active microbial biomass, which can be estimated by a ratio of basal respiration rate to glucose-induced respiration rate and the total microbial biomass (Khomutova et al., 2004). If the ratio of active to dormant microbial biomass does not change significantly, B and KV i may be replaced by the total microbial biomass and the average activity (over the total microbial biomass), respectively. The formula of f (C i ) is to be defined. The linear relationship between decomposition rate and SOM concentration in current models (Eqs. (1)(3)) may follow the early work of Jenny (1941). The process of SOM decomposition is an analogue of a chemical reaction of a single substrate. Although such a model has been successfully used and fitted well with observed data, the microbial model (Eqs. (4) and (5)) is theoretically more attractive. In Eq. (4), SOM decomposition is analogous to an enzyme catalyzing reaction. This assumption is in agreement with a variety of contemporary theories and techniques in soil science, such as measuring microbial biomass with substrate-induced respiration, clay protection of

SOM to decomposition, physical partitioning of SOM on particle size. We hypothesize that the first order relationship between microbial respiration rate and the concentration of C pools as substrate exists in soils where organic matter content is low to moderate (such as in some tropical soils, arable soils). A zero order relationship may exist in soils rich in organic matter (for example, in forest floor, some temperate forest soils, boreal and tundra soils) or in deep soil where SOM is relatively high because of the low abundance of microbial biomass. The zero order relationship may be also appropriate for simulating resistant C pools. f 1(C i ) may have a general formula similar to the MichaelisMenten equation, which has been used to simulate microbial growth in the soil (Blagodatsky and Richter, 1998; Blagodatsky et al., 1998). Little information is available in published literature to verify this hypothesis. If it is true that microbial decomposition is not generally related to SOM concentration in soils developed under cold or wet conditions where a large amount of SOM is currently stored, current models may have biased our predication. Further studies, both in theory and experiment, are warranted.

Acknowledgement We thank Dr. Chengyi Zhang for assistance in modelling.

References
Agnelli, A., Ugolini, F.C., Corti, G., Pietramellara, G., 2001. Microbial biomass-C and basal respiration of fine earth and highly altered rock fragments of two forest soils. Soil Biol. Biochem. 33, 613 620. 2gren, G.I., Bosatta, E., 1996. Theoretical Ecosystem Ecology. Understanding Element Cycles. Cambridge University Press, Cambridge, p. 234. Alvarez, C.R., Alvarez, R., Grigera, M.S., Lavado, R.S., 1998. Associations between organic matter fractions and the active soil microbial biomass. Soil Biol. Biochem. 30, 767 773. Amador, J.A., Jones, R.D., 1993. Nutrient limitations on microbial respiration in peat soils with different total phosphorus content. Soil Biol. Biochem. 25, 793 801. Bardgett, R.D., Lovell, R.D., Hobbs, P.J., Jarvis, S.C., 1999. Seasonal changes in soil microbial communities along a fertility gradient of temperate grasslands. Soil Biol. Biochem. 31, 1021 1030.

C. Fang et al. / Geoderma 129 (2005) 139146 Blagodatsky, S.A., Richter, O., 1998. Microbial growth in soil and nitrogen turnover: a theoretical model considering the activity state of microorganisms. Soil Biol. Biochem. 30, 1743 1755. Blagodatsky, S.A., Yevdokimov, I.V., Larionova, A.A., Richter, J., 1998. Microbial growth in soil and nitrogen turnover: model calibration with laboratory data. Soil Biol. Biochem. 30, 1757 1764. Bosatta, E., 2gren, G.I., 1996. Theoretical analysis of carbon and nutrient dynamics in soil profile. Soil Biol. Biochem. 28, 1523 1531. Boyer, J.N., Groffman, P.M., 1996. Bioavailability of water extractable organic carbon fractions in forest and agricultural soil profiles. Soil Biol. Biochem. 28, 783 790. Coleman, K., Jenkinson, D.S., 1996. RothC-26.3Ua model for the turnover of carbon in soil. In: Powlson, D.S., Smith, P., Smith, J.U. (Eds.), Evaluation of Soil Organic Matter Models Using Existing Long-term Datasets, NATO ASI Series I, vol. 38. Springer-Verlag, Heidelberg, pp. 237 246. Fang, C., Moncrieff, J.B., 1999. A model for soil CO2 production and transport: 1. Model development. Agri. For. Met. 95, 225 236. Fang, C., Moncrieff, J.B., in press. The variation of soil microbial respiration with depth in relation to soil carbon composition. Plant Soil. Fang, C., Smith, P., Moncrieff, J.B., Smith, J.U., 2005. Similar response of labile and resistant soil organic matter pools to changes in temperature. Nature 433, 57 59. Fang, C., Smith, P., Smith, J.U., Moncrieff, J.B., in press. A simple strategy for simulating C decomposition in a multi-component pool of soil organic matter. Eur. J. Soil Sci. Grayston, S.J., Griffith, G.S., Mawdsley, J.L., Campbell, C.D., Bardgett, R.D., 2001. Accounting for variability in soil microbial communities of temperate upland grassland ecosystems. Soil Biol. Biochem. 33, 533 551. Henriksen, T.M., Breland, T.A., 1999. Nitrogen availability effects on carbon mineralization, fungal and bacterial growth, and enzyme activities during decomposition of wheat straw in soil. Soil Biol. Biochem. 31, 1121 1134. Insam, H., Parkinson, D., Domsch, K.H., 1989. Influence of microclimate on soil microbial biomass. Soil Biol. Biochem. 21, 211 221. Jenny, H., 1941. Factors of Soil Formation. McGraw-Hill, New York. Khomutova, T.E., Demkina, T.S., Demkin, V.A., 2004. Estimation of the total and active microbial biomasses in buried subkurgan paleosoils of different age. Microbiology 73, 196 201. Kouno, K., Lukito, H.P., Ando, T., 1999. Minimum available N requirement for microbial biomass P formation in a regosol. Soil Biol. Biochem. 31, 797 802. Li, C., Frolking, S., Frolking, T.A., 1993. A model of nitrous evolution from soil driven by rainfall events: 1. Model structure and sensitivity. J. Geophys. Res. 97, 9759 9776. Lomander, A., K7tterer, T., Andre n, O., 1998. Modelling the effects of temperature and moisture on CO2 evolution from top- and subsoil using a multi-compartment approach. Soil Biol. Biochem. 30, 2023 2030. Lovell, R.D., Jarvis, S.C., 1998. Soil microbial biomass and activity in soil from different grassland management treatments

145

stored under controlled conditions. Soil Biol. Biochem. 30, 2077 2085. Lovell, R.D., Jarvis, S.C., Bardgett, R.D., 1995. Soil microbial biomass and activity in long-term grassland: effects of management changes. Soil Biol. Biochem. 27, 969 975. Luizao, R.C.C., Bonde, T.A., Rosswall, T., 1992. Seasonal variation of soil microbial biomassthe effects of clearfelling a tropical rainforest and establishment of pasture in the central Amazon. Soil Biol. Biochem. 24, 805 813. Lundquist, E.J., Jackson, L.E., Scow, K.M., 1999. Wetdry cycles affect dissolved organic carbon in two California agricultural soils. Soil Biol. Biochem. 31, 1031 1038. McGill, W.B., 1996. Review and classification of ten soil organic matter (SOM) models. In: Powlson, D.S., Smith, P., Smith, J.U. (Eds.), Evaluation of Soil Organic Matter Models Using Existing Long-term Datasets, NATO ASI Series I, vol. 38. Springer-Verlag, Heidelberg, pp. 111 133. Mueller, T., Jensen, L.S., Hansen, S., Nielsen, N.E., 1996. Simulating soil carbon and nitrogen dynamics with the soil plantatmosphere system model Daisy. In: Powlson, D.S., Smith, P., Smith, J.U. (Eds.), Evaluation of Soil Organic Matter Models Using Existing Long-term Datasets, NATO ASI Series I, vol. 38. Springer-Verlag, Heidelberg, pp. 275 281. Nadelhoffer, K.J., Emmett, B.A., Gundersen, P., Kjbnaas, O.J., Koopmans, C.J., Schleppi, P., Tietema, A., Wright, R.F., 1999. Nitrogen deposition makes a minor contribution to carbon sequestration in temperate forests. Nature 398, 145 147. Parton, W.J., Schimel, D.S., Cole, C.V., Ojima, D.S., 1987. Analysis of factors controlling soil organic matter levels in Great Plains grasslands. Soil Sci. Soc. Am. J. 51, 1173 1179. Pascual, J.A., Garcia, C., Hernandez, T., Moreno, J.L., Ros, M., 2000. Soil microbial activity as a biomarker of degradation and remediation processes. Soil Biol. Biochem. 32, 1877 1883. Paustian, K., 1994. Modelling soil biology and biochemical processes for sustainable agricultural research. In: Pankhurst, Z.E., Doube, B.M., Gupta, S.R., Grace, P.R. (Eds.), Soil Biota Management in Sustainable Farming Systems. CSIRO Information Services, Melbourne, pp. 182 193. Petersen, B.M., Olesen, J.E., Heidmann, T., 2002. A flexible tool for simulation of soil carbon turnover. Ecol. Model. 151, 1 14. Post, W.M., Pastor, J., Zinke, P.J., Stangenbergere, A.G., 1985. Global pattern of soil nitrogen storage. Nature 317, 613 616. Raubuch, M., Joergensen, R.G., 2002. C and net N mineralisation in a coniferous forest soil: the contribution of the temporal variability of microbial biomass C and N. Soil Biol. Biochem. 34, 841 849. Ross, D.J., Kelliher, F.M., Tate, K.R., 1999. Microbial processes in relation to carbon, nitrogen and temperature regimes in litter and a sandy mineral soil from a central Siberian Pinus sylvestris L. forest. Soil Biol. Biochem. 31, 757 767. Saiya-Corka, K.R., Sinsabaugha, R.L., Zakb, D.R., 2002. The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol. Biochem. 34, 1309 1315.

146

C. Fang et al. / Geoderma 129 (2005) 139146 Trumbore, S., 2000. Age of soil organic matter and soil respiration: radiocarbon constraints on belowground C dynamics. Ecol. Appl. 10, 399 411. Wang, W.J., Dalal, R.C., Moody, P.W., Smith, C.J., 2003. Relationships of soil respiration to microbial biomass, substrate availability and clay content. Soil Biol. Biochem. 35, 273 284. Wardle, D.A., 1998. Controls of temporal variability of the soil microbial biomass: a global-scale synthesis. Soil Biol. Biochem. 30, 1627 1637. Yang, H.S., Janssen, B.H., 2000. A mono-component model of carbon mineralization with a dynamic rate constant. Eur. J. Soil Sci. 51, 517 529.

Smith, P., Andre n, O., Brussaard, L., Dangerfield, M., Ekschmitt, K., Lavelle, P., Tate, K., 1998. Soil biota and global change at the ecosystem level: describing soil biota in mathematical models. Glob. Chang. Biol. 4, 773 784. Smolander, A., Kitunen, V., 2002. Soil microbial activities and characteristics of dissolved organic C and N in relation to tree species. Soil Biol. Biochem. 34, 651 660. Stenstrfm, J., Svensson, K., Johansson, M., 2001. Reversible transition between active and dormant microbial states in soil. FEMS Microbiol. Ecol. 36, 93 104. Thornley, J.H.M., Cannel, M.G.R., 1997. Temperate grassland response to climate change: an analysis using the Hurley Pasture Model. Ann. Bot. 80, 205 221.