Decomposition of
13
C-labelled plant material in a European 65±
40
8
latitudinal transect of coniferous forest soils: simulation of
climate change by translocation of soils
Pierre Bottner
a,*, Marie-Madeleine CouÃteaux
a, Jonathan M. Anderson
b, BjoÈrn Berg
c,
Georges BilleÁs
a, Tom Bolger
d, Herve Casabianca
e, Joan RomanyaÂ
f, Pere Rovira
fa
CEFE-CNRS, 1919 Route de Mende, 34293 Montpellier Cedex 5, France
b
Department of Biological Sciences, Hatherly Laboratories, University of Exeter, Prince of Wales Road, Exeter EX4 4PS, UK
c
Department of Forest Soils, Swedish University of Agricultural Sciences, P.O. Box 7001, S-750 07 Uppsala, Sweden
d
Department of Zoology, University of Dublin, Bel®eld, Dublin 4, Ireland
e
Service Central d'Analyse, CNRS, BP 22, 69390 Vernaison, France
f
Dept Biologia Vegetal, Universitat de Barcelona, 645 Diagonal, 08028 Barcelona, Spain
Accepted 27 September 1999
Abstract
Standard13C-labelled plant material was exposed over 2±3 yr at 8 sites in a north±south climatic gradient of coniferous forest soils, developed on acid and calcareous parent materials in Western Europe. In addition to soils exposed in their sites of origin, replicate units containing labelled material were translocated in a cascade sequence southwards along the transect, to simulate the eects of climate warming on decomposition processes. The current Atlantic climate represented the most favourable soil temperature and moisture conditions for decomposition. Northward this climatic zone, where the soil processes are essentially temperature-limited, the prediction for a temperature increase of 38C estimated a probable increase of C mineralisation by 20± 25% for the boreal zone and 10% for the cool temperate zone. Southward the cool Atlantic climate zone, (the Mediterranean climate), where the processes are seasonally moisture-limited, the predicted increase of temperature by 1±28C little aected the soil organic matter dynamics, because of the higher water de®cit. A signi®cant decrease of C mineralisation rates was observed only in the super®cial layers recognised in Mediterranean forest soils as `xeromoder' and subject to frequent dry conditions. In the deeper Mediterranean soil organic horizons (the mull humus types), representing the major C storage in this zone, C mineralisation was not aected by a simulated 28C temperature increase. The temperature eect is probably counteracted by a higher water de®cit.72000 Elsevier Science Ltd. All rights reserved.
Keywords:Decomposition; Carbon; Coniferous forests;13C-labelling; Climate change; North±south transect; Translocation; Organic matter; Car-bon mineralisation; Forest soils; Europe; Tracer techniques
1. Introduction
One of the key issues in climate change research is the future dynamics of organic carbon in soils which contains about two-thirds of the total organic C in terrestrial systems. Even small changes of the
mineralisation rates of these large soil pools could therefore have signi®cant eects on concentrations of atmospheric CO2. As yet there are few indications
as to whether soils will be net sources of CO2, since
climate warming increases mineralisation rates, or net sinks for C as a consequence of the CO2 eect on
plant litter production, quality and decomposition rates (CouÃteaux et al., 1991; Cotrufo et al., 1994). A number of dierent approaches have been used to
ob-Soil Biology & Biochemistry 32 (2000) 527±543
0038-0717/00/$ - see front matter72000 Elsevier Science Ltd. All rights reserved.
PII: S 0 0 3 8 - 0 7 1 7 ( 9 9 ) 0 0 1 8 2 - 0
www.elsevier.com/locate/soilbio
serve these trends which involve ®eld measurements, manipulative experiments and simulation models.
The net changes in the balances between C input to soils and mineralisation rates are generally too small to detect by direct measurements, because of the variability of the ¯uxes and pools. Using indir-ect evidence, a large current terrestrial CO2 sink in
the northern hemisphere, referred as `missing sink' was indicated (i) by atmospheric chemistry measurements: CO2 pressure gradients (Tans et al., 1990), CO2 13
C/12C ratio (Ciais et al., 1995) and O2concentration
(Keeling et al., 1996) and (ii) by analysis of climate variability during the last decades (Dai and Fung, 1993).
The eect of climate controls over soil C dynamics at geographical scales have been investi-gated using a number of dierent approaches. Soil respiration data have been extensively employed in empirically-based statistical models, to predict annual and global CO2emission from terrestrial soils
(Raich and Schlesinger, 1992) and to de®ne the spatial and temporal climate controls of soil respiration (Raich and Potter, 1995). Since a possible imbalance in the ecosystem C cycle arises from the diering re-sponses of production and decomposition to tempera-ture change, the mechanistic models are generally based on coupled production and decomposition sub-models. A relatively simple model developed by Town-send et al. (1992) describes the temperature eect on net ecosystem production using a linear function and an exponential function for response by soil respir-ation. More complex decomposition models partition the organic matter into multiple C and N pools with speci®c turnover rates (Jenkinson et al., 1991; Schimel et al., 1994). Production- and decomposition-submo-dels have been linked by the litter quality and plant detritus chemistry (C-to-N ratio and lignin content) and by the nitrogen cycle (the dynamics of N mineral-isation controlling N uptake by the plants). The spatial dimension of the decomposition models necessitated the integration of the geographical distribution of soil types and some essential intrinsic soil properties.
In our study 13C- and 15N-labelled standard plant material was exposed, at eight sites along a north± south climatic gradient of coniferous forest soils in Western Europe, which included boreal, Atlantic and Mediterranean climates. In addition, the soils with their labelled plant material were translocated from north to south according to a cascade procedure, in order to simulate a south to north climate shift. The objective was to investigate the decomposition pro-cesses in the climatic transect, where the current cli-matic spatial dierences were used as an analogue for expected climate change. This publication only pre-sents results for13C dynamics.
2. Materials and methods
2.1. The sites and humus types
Within each climatic zone, except for boreal, two sites were identi®ed (on acidic and calcareous parent materials; Fig. 1 and Table 1). In boreal coniferous forests the surface organic layers are generally of low pH irrespective of the base status of the underlying parent material. The complement of sites detailed in Table 1 included representatives of the major humus types developed under coniferous forest stands on well-drained soils in Western Europe. The series of humus types developed on acid soils included, from north to south: `mor' (Oh horizons at Vindeln and JaÈdraaÊs), acid `mull' (A1 horizons at Haldon, TheÂzan and Desert) and acid `xeromoder' (Oh at TheÂzan). The calcareous soils series comprised acid `mull' at Friston, `calcic mull' at La Clape (where the exchange capacity was saturated by Ca2+ without the presence of car-bonates), `calcareous mull' at Maials (Ca2+ saturated exchange capacity with presence of carbonates) and ®nally neutral `xeromoder' at la Clape and Maials.
Mor and xeromoder are Oh horizons where the or-ganic layer with a high C content, and high C-to-N ratio (Fig. 2) is developed on the surface of the min-eral soil, resulting from the slow turnover rates of low quality litters under temperature-limited conditions in the boreal region (mor) and under moisture limitation in the Mediterranean region (xeromoder). The mull soils are mainly developed under Atlantic and Mediter-ranean conditions where organic matter decomposing at higher rates is incorporated into the mineral soil, by faunal activity, forming stabilised organo-mineral com-plexes. On acid soils, the pH (H2O) values of mull are
5±6, irrespective of the climatic conditions (Fig. 2). In the calcareous soils sequence, the pH values, the Ca2+ saturation and the carbonate concentrations in the mull soils increase from north to south, indicating a decreasing capacity of dissolution and leaching of car-bonates from the organic horizon. At TheÂzan, La Clape and Maials, the Oh horizon (xeromoder) over-lies the A1 horizon (mull). This is a common situation under Mediterranean conditions (Fig. 2).
2.2.13C and15N soil labelling and ®eld incubation in cylinders
The soil was divided into pedological horizons (Fig. 2) de®ned by the distribution of organic matter in the pro®le. The material from each horizon was sieved (4 mm mesh) and thoroughly homogenised. The material from the horizons selected for labelling was air-dried in the laboratory before the labelled plant material was added to the soil. The moist materials from the unlabelled horizons were placed in increments
in plastic cylinders (inside dia 12 cm, length 30 cm) and packed down with a heavy metal ram to reconsti-tute a bulk density close to the ®eld value. Discs of 1 mm mesh polyester netting were placed between the horizons to facilitate sampling. The depth and mass of the horizons established for each experimental unit are given in Fig. 2.
The labelled plant material was produced by grow-ing wheat (`Florence Aurore', an old sprgrow-ing-wheat cul-tivar with low N requirements) over 4 months, in a
labelling chamber with facilities for maintaining tem-perature, radiation, moisture and CO2conditions, in a
nutrient solution with low 15N, P and K concen-trations, plus micro-nutrients, under a 13CO2-labelled
atmosphere. In order to obtain material with a high C-to-N ratio, only the stems and leaves were used in the experiment. The harvested plant material was air-dried, milled into 2±7 mm long ®brous particles and homogenised.
The labelled plant material was added separately to
Fig. 1. Location of the research plots on a climate and soils transect in Western Europe extending from latitude 658to 408. The arrows indicate
the north to south sequential translocation of acidic and calcareous soils to simulate the eects of projected patterns of climate change on soil processes.
each replicate sample (Table 2) of soil and mixed for 15 min. The labelled soil was then added to the cylin-ders on top of the unlabelled material and packed to the appropriate bulk density. The thickness of the labelled horizons ranged from 3 cm for the Oh layers to 4±5 cm for the A1 layers (Fig. 2). To complete the reconstituted pro®le, the soil surfaces were covered by litter or moss according the characteristics of the ®eld site. The units were then moistened with 200 ml deio-nised water. For each pro®le, 28±36 cylinders were installed (seven to nine sampling occasions and four replicates). At TheÂzan, La Clape and Maials, the Oh and A1 horizons were labelled separately (Fig. 2), so that the number of cylinders was doubled.
2.3. Soil translocation, cascade experiment
In addition to soils exposed at their site of origin, replicate units were translocated to simulate the pre-dicted eects of climatic changes on carbon dynamics. Within each soil series (acid and calcareous soils) the soils were transplanted from a northern site (the source site) to the next southern site (the host site) (Figs. 1 and 3). In order to preserve the physical and chemical environment of the labelled horizon, in each case the translocated soils comprised the labelled horizon and the unlabelled horizons above and below this layer, from the source site but the deeper (B) horizon was reconstituted using material from the host site. The untranslocated `control' soils are referred to below as the `native soils'. For the whole experiment, 704 cylin-ders were installed. The cylincylin-ders were randomly dis-tributed in the sites. After the ®rst year, the litterfall was removed from the cylinders and replaced by the litter fallen during this time in the source site. During the following years the litterfall in the cylinders was not controlled.
2.4. Sampling procedures and soils analyses
The cylinders were installed during spring and sum-mer 1993 for the acid soils and during winter 1993 and spring 1994 for the calcareous soils. Four replicate units were randomly sampled on seven (Vindeln), eight (JaÈdraaÊs) and nine (the other sites) occasions over 2 yr (Haldon and Friston), or over 3 yr (the other sites) up to March 1997.
After collection from the ®eld, the soil column was pushed out of the cylinders, and the horizons separ-ated at the polyester mesh disks (Fig. 2). The un-labelled horizons were air-dried. The un-labelled soil was either prepared immediately or stored over a maximum of 7 d at 48C. In either case, the moist soil was thoroughly mixed and subsampled for analysis of total C and 13C, microbial biomass C and 13C and organic matter fractionation.
Fig. 2. Structural composition of labelled and unlabelled horizons in the soil cylinders, and physical and chemical characteristics of the soils. At TheÂzan, La Clape and Maials both Oh and A1 horizons were labelled.
Fig. 3. Translocation between climate zones of humus types in the cascade series of acidic and calcareous soils.
P.
Bottner
et
al.
/
Soil
Biology
&
Biochemis
try
32
(2000)
527±543
2.5. C, N and mass spectrometry analysis
Since highly labelled plant material was added to the soils in small amounts, preparation methods were investigated to determine the sample homogen-eity required to reduce variation in results of mass spectrometry. The following procedures were carried out on the labelled horizons and on the soil ma-terials above and below this layer.
For the mineral soil samples (A1 horizons), about 60% of the initial mass remained after subsampling for microbial biomass (and inorganic N). This ma-terial was air-dried and homogenised. One-third was stored for organic matter fractionation and the remaining material was ground in a blender for 5 min. One-third of this ground material was ground again using a ball mill (Retsch MM2, 10 ml cups, 10 min) and then a third of this material was ground again to a ®nal ®ne powder using a liquid N freeze mill (Spex 6700 freezer/mill, 5 min). For the labelled Oh horizons (mor and xeromoder) the blender was replaced by a ultracentrifuge mill (Retsch ZM1).
Total C, and 13C isotopic ratios were measured at the Service Central d'Analyses of the CNRS, Solaize (France), using a CN elemental analyser (CNRS) coupled with a mass spectrometer (Finnigan delta S or MAT 252).
One analysis was generally carried out for each ®eld replicate, but 10±25 replicates were initially analysed (time `t0') according to humus types. This
was necessary for two reasons. Firstly, it was dicult to obtain homogeneous soil samples because the unde-composed labelled wheat material was initially resist-ant to grinding, and secondly, it was necessary to obtain very accurate initial values for isotope ratios, since the 13C remaining in soils during the ®eld ex-posure period was calculated in percent of the initial material.
The natural 13C isotopic ratio, measured in four replicates at each site before the installation of the experiment, varied from 1.081 to 1.083%. The 13C derived from added plant material was calculated, using the 13C isotopic enrichments: enrichment
atom%excess measured isotopic ratio ÿ
natural isotopic ratio 100: In highly labelled
exper-iments this formulation was preferable to d13C
-(Boutton, 1991). In Table 2, d13C - varied from +262 to +56 for the initial soil13C and from +67 to +5 for the ®nal soil 13C. In the ®gures the bares rep-resent the standard deviation for the four replicates. The comparison of data was performed using the test of Student (p value).
3. Results
3.1. Isotopic13C
The characteristics of the labelled material were: C40:220:2%;
13C isotopic ratio 10
:54020:013%;
N1:2820:02%
15N isotopic ratio 9
:73520:018%
and C-to-N ratio31:4: The added N in the labelled
plant material, as % of soil native total N, ranged between 0.8 and 3.4%. The added C in plant material, expressed as % of soil native organic C, ranged gener-ally from 1.5 to 3.4%. The initial isotopic ratios measured at t0 for the experiment ranged from 1.173
to 1.399%. The ®nal isotopic ratios measured on the last sampling occasion after 2±3 yr ®eld exposure ran-ged from 1.116 to 1.184% (Table 2). These ratios were signi®cantly dierent from 1.081±1.083% determined for the unlabelled soils sampled before the experiment (P< 0.01). Thus, because of the low N and high 13 C-labelling, the plant material could be added to the soil as a very small proportion of the total mass, that is without changing the chemical, physical and biological properties of the soil native organic matter and the tra-cer was suciently concentrated to be detected throughout the experiment.
3.2. Transfers of labelled C
In all cases the 13C isotopic ratios in the layers located directly above the labelled horizons were close to the natural ratios. Hence upwards transfers of the labelled-C (for instance by fungi) were negligible. The
13
C measured in the horizon located directly below the labelled one was also low, ranging from 2 to 7% of the initial 13C. The highest 13C leaching occurred in the Vindeln (boreal) soil of 4±7% of the initial 13C. The lowest values were observed in the acid Mediterra-nean soils with generally less than 3% of the initial label. Data for 13C in these adjacent horizons are not presented separately.
3.3.13C mineralisation rates
Fig. 4(a and b) shows the percentage 13C remaining in soils (sum of 13C remaining in the initially labelled horizon plus the 13C recovered in the horizons located directly under and above the initially labelled layer). For technical reasons, the installation of the exper-iment in the donor site for the native soil and in the host site for the translocated soil was generally not achieved exactly at the same date. The time scale is therefore shown as exposure days for both native and transplanted soils, rather than from the date on instal-lation. Fig. 4(a and b) illustrates the dynamics of 13C mineralisation assuming that (i) the leaching of labelled carbon below the layers analysed was
gible and (ii) 13C remaining in the pro®le can be bud-geted as the dierence between initial 13C and 13CO2
lost by respiration. The ®rst assumption is probably valid, since the amount of 13C translocated down the pro®le was low. The second assumption presupposes that there were no13C-bicarbonates and carbonates ac-cumulating in the soil from the 13CO2 released by the
soil respiration. This will not occur in acid and neutral soil but could occur in soils containing CaCO3. The
La Clape soil contained less than 1% carbonates but was Ca2+ saturated pH7:3). The
13
C measured in the A12 horizon (directly located below the labelled
horizon; Fig. 2) never exceeded 4%, indicating that
13
C immobilisation was probably negligible. In con-trast the Maials soil contained 40±42% carbonates in all horizons and showed unrealistic high 13C values (15±20%) in the below horizon. In this case 13CO2
may have been immobilised. The dierentiation of car-bonate-13C from organic-13C is necessary to clarify the CO2
-13
C sequestration. The results for this soil are therefore not presented in this paper.
3.4. Soils from the boreal zone
The relocation of soil from Vindeln to JaÈdraaÊs, i.e. from a north to a more south Scandinavian climate (Figs. 1 and 3), was accompanied by (i) an increase in mean annual air temperatures of 2.58C (averaged over 3 yr), (ii) an increase of 17% of the sum of mean daily temperatures greater than 08C and (iii) a mean annual precipitation increase of 23% (Table 3). At both sites, the water de®cit (PET-AET) was low and similar to the long-term values, except for the second year at JaÈdraaÊs.
At both Vindeln and JaÈdraaÊs, the experiment was installed in June 1993. In the native Vindeln soil, the total soil C remained relatively constant (Fig. 4a). When transplanted to JaÈdraaÊs, the total C decreased progressively by 20% and 13C remaining in the trans-located soil was 10% lower than the native soil (P< 0.05). During the ®rst year of incubation, the rapid in-itial decomposition phase was interrupted during the 6±7 winter months by temperatures falling below 08C. Consequently both the native and transplanted soils showed a stepwise pattern of13C depletion. This eect was not evident during the second (1994±1995) and third (1995±1996) winters.
The translocation of the JaÈdraaÊs soil from JaÈdraaÊs (boreal) to Haldon (Atlantic climate) corresponded over the 3 yr to a mean annual air temperature increase of 78C. Precipitation increased by a factor of two over this period. The summer water de®cit was low at both sites and of the same order of magnitude (<50 mm; Table 3) and was probably not a limiting factor for C mineralisation. The JaÈdraaÊs native soil was installed in June and the transplanted soil was
Ta
Fig. 4. (a). Total C and13
C in the boreal (Vindeln and JaÈdraaÊs) and in the Atlantic (Haldon and Friston) soils in their native and host sites. The soils at Vindeln, JaÈdraaÊs and Haldon are acidic while the Friston soils are developed on calcareous material. (b). Total C and13C in the Mediterranean soils in their native and host sites. The TheÂzan Oh and A1 horizons are acidic and the La Clape Oh and A1 horizons are developed on calcareous material. Values are means n4). Vertical bars indicate standard deviation.
P.
Bottner
et
al.
/
Soil
Biology
&
Biochemis
try
32
(2000)
527±543
Fig.
4
(
con
tinue
d
)
installed at Haldon only 3 months later. The stepwise temperature-linked 13C-curve was also clearly observed for the native soil during the ®rst winter period, but disappeared for this soil when transplanted under Atlantic conditions. Both sites showed a similar decrease in total C of about 15%. The translocation increased the 13C mineralisation by 5±10% (P< 0.05; Fig. 4a).
3.5. Soils from the Atlantic zone
In the acid soil sequence (Figs. 1 and 3), the Haldon soil (Atlantic climate) was transplanted to TheÂzan (wet Mediterranean). The soil was thus exposed to an increase in annual mean air temperature of 5.48C and a decrease in annual precipitation from 1505 to 731 mm throughout the experiment. The water de®cit also increased from 47 mm (with PET-AET > 0 over 3 months) at Haldon to 313 mm with 7 months water de®cit at TheÂzan during spring, summer and autumn (Table 3). The native soil was installed in September 1993 and the transplanted soil was installed 2 months later. The total C decreased by 15% of the initial total C for both soils over 3 yr (Fig. 4a). Translocation of Haldon soil to TheÂzan resulted in a slower rate of 13C decrease in the transplanted soil. During the initial and rapid decomposition phase, the amount of 13C in the translocated soil was 5±10% higher than in the native soil (P< 0.05 at samplings 2 and 3). During the slower decomposition phase, the mineralisation rates became comparable.
When the calcareous Friston soil (Atlantic climate) was transplanted to La Clape (wet Mediterranean) (Figs. 1 and 3) the soil was exposed to an increase in mean annual air temperature of 3.58C and a decrease in precipitation from 750 to 572 mm (Table 3). These values are comparable to long-term records but both sites experienced a dry summer during the second year of the experiment. The water de®cit increased from 111 to 281 mm and the dry months increased from 5 to 8.5 at La Clape. The third winter was at La Clape exceptionally wet with 1199 mm precipitation. Never-theless, the moisture eect of the second and third year on the 13C mineralisation rates was of little sig-ni®cance since, as shown in Fig. 4a, the pattern of 13C losses was already stabilised after the ®rst year. The native Friston soil was installed in March 1994 but the transplanted soil had already been installed at La Clape since January 1994. The total organic C content of the Friston soil decreased by 10±15% for both native and transplanted soils. The 13C curve of the translocated soil was generally higher by 5±10% com-pared to the native soil (0.1 >P> 0.05).
Hence, moisture de®cit limited 13C mineralisation in the translocated Haldon and Friston soils. In contrast to the soils maintained under boreal conditions, for
Ta
both native Atlantic climate soils (Haldon and Friston) and the boreal JaÈdraaÊs soil transplanted to Haldon, the generally favourable seasonal patterns of moisture and temperature resulted in steady and regular rates of
13
C mineralisation. The variability was particularly low for the native Haldon and Friston soils.
3.6. Soils in the Mediterranean zone
In the acid soils series, the xeromoder (Oh) and the acid mull (A1) of TheÂzan were transplanted from wet Mediterranean conditions to Desert de les Palmes (Figs. 1 and 3) which had the driest climatic conditions in the transect. This involved a (3 yr) mean annual precipitation decrease from 731 to 387 mm, an increase in moisture de®cit (PET-AET) from 313 to 453 mm yrÿ1; the number of dry months (PET-AET > 0) increased from 7 to 10 and the temperature increased from 15.5 to 16.58C (Table 3). Units at TheÂzan were installed in July 1993 and at Desert 3 weeks later. The curves for residual organic-C and 13C showed greater variation compared with results from of the Atlantic sites (Fig. 4b). This was probably the consequence of the heterogeneous spatial distribution of the Mediter-ranean vegetation in the sites, creating greater vari-ation in microclimate.
The more arid environment of the transplanted soils aected the pattern of total organic C and 13C losses from the Oh layer (Fig. 4b). During the ®rst year, total organic C was reduced by about 20% for the native soil and 10% for the transplanted soil and 13C by 55 and 45%, respectively (P< 0.05 at samplings 2 and 3). Over this ®rst year the Desert site was particu-larly dry with a water de®cit for 10 months compared to 5 months at TheÂzan. Over the remainder of the ex-periment, the curves for residual 13C were not signi®-cantly dierent (P > 0.1) for the two soil and stabilised at relatively high values. In contrast to the boreal soils where freezing markedly aected the 13C mineralisation curves, the dry summer eect of the Mediterranean soils was probably masked by the high variability of the data.
Results for the TheÂzan A1 horizon showed high variability for the same reasons considered for the Oh material. The curves for total organic C and 13C were similar for the native and transplanted soil, except on the ®rst sampling occasion (Fig. 4b).
When the calcareous La Clape soil was transplanted from a wet Mediterranean climate to dry Mediterra-nean conditions at Maials (Figs. 1 and 3), the soils changed from a mean annual precipitation of 781 to 381 mm yrÿ1. The temperature increased from 15.1 to 16.08C. Water de®cit increased from 282 (8 dry months) to 468 mm yrÿ1(9 dry months). As with the TheÂzan soil, the Oh and A1 horizons were investigated (Fig. 2). Simulating the natural ®eld pro®le, the Oh
horizon was separated from the underlying A1 horizon by a stone layer (St layer in Fig. 2). The experiment was installed at La Clape in January 1994 and at Maials in April.
During the ®rst spring and summer, conditions were extremely dry with 7±8 dry months and at Maials there were no decreases in Oh 13C from April (installa-tion) to September. At La Clape in Oh only 10±15% of the initial 13C was mineralised during this period. At Maials maximum rates of 13C mineralisation occurred during the ®rst wet autumn and winter (1994). During the summer of 1995, mineralisation of
13
C was again reduced. Thus Maials Oh showed a stepwise pattern of 13C losses controlled by seasonal alternate dry and wet periods while at La Clape the drought eects were attenuated and only manifested during the ®rst summer period.
The La Clape labelled A1 mull horizon was located in the mineral soil under the xeromoder horizon and the stony layer (Fig. 2). This buered the variability in moisture conditions at both sites. The dry summer conditions did not aect the 13C mineralisation (Fig. 4b). This soil, with basic pH and buered moist-ure conditions, showed high mineralisation rates result-ing in 65% 13C loss during the ®rst year. In the native and transplanted soils, the curves for total organic C and 13C were similar despite the comparatively low variability of the data.
3.7. Temperature eect on13C mineralisation and
stabilisation
Fig. 5 shows the residual 13C in the native and transplanted soils in relation to the mean annual air temperatures of the donor and host sites. The slopes of the lines indicate the temperature eect on 13C min-eralisation. The increase in soil temperatures produced by translocation had the largest eect (highest negative slope) on 13C mineralisation between Vindeln and JaÈdraaÊs, i.e. from north to south boreal conditions. The 13C mineralisation rates were enhanced over the 3 yr of decomposition as shown by signi®cant (P < 0.001) dierences in the slopes of V1, V2 and V3. The translocation from boreal to Atlantic conditions also produced an increase in 13C mineralisation, but the slopes are less steep and the temperature eect decreased from the ®rst (J1; P< 0.01) to the last year (J3; P< 0.05). The temperature increase had no sig-ni®cant eects when the Haldon soil was translocated to TheÂzan and the positive slope for H1 indicates a tendency P0:13 for
13
C mineralisation to decrease during the ®rst year. For the Friston soil transplanted to La Clape, the mineralisation of13C was signi®cantly reduced during the ®rst (P< 0.01 for F1) and second years (P< 0.01 for F2). Translocation within the Med-iterranean region had no eect on 13C mineralisation
or resulted after 3 yr in a decreased mineralisation rates of the La Clape Oh layer transplanted to Maials. For L(o)3,P< 0.05 and for L(a)3 P0:08:The
nega-tive slope of La Clape Oh after 1 yr (L(o)1) was transi-ent.
4. Discussion
4.1. Soils in the boreal region
Within the boreal zone, signi®cantly higher 13C losses (10%) occurred in the Vindeln soil transplanted to JaÈdraaÊs than in the native soil. The climate eect is con®rmed when both native soils are compared: the re-sidual 13C remaining in the native JaÈdraaÊs soil is by 20% (of the initial 13C) lower than in the native
Vin-deln soil. The mean annual air temperature calculated over the 3 yr of 0.68C in Vindeln and 3.18C in JaÈdraaÊs, is a realistic predictive ®gure of the northward climate shift in a 2CO2 concentration context. Thus, as
il-lustrated in Fig. 6, the southward translocation of the Vindeln soil to JaÈdraaÊs, decreased the 13C in the trans-planted soil in a proportion of 20±25% of 13C of the native soil. In other words, the expected northward warmer climate shift would increase the C mineralis-ation rate in the boreal forest soils by 20±25%.
The Q10 values for the 13C mineralisation rates,
de-rived from data in Fig. 5 (over 3 yr), ranged from 2.6 to 1.6 when the native and transplanted Vindeln soils were compared and from 1.6 to 1.4 when the native Vindeln and JaÈdraaÊs soil were compared. Nevertheless the temperature responses are also aected by the soil moisture regime. The mean water de®cit (PET-AET)
Fig. 5. Residual13C in soils after 1, 2 and 3 yr of exposure in relation to mean annual temperature (MAT) of donor (native soil) and host
(trans-planted soil) sites. V=Vindeln, J=JaÈdraaÊs, H=Haldon, F=Friston, L(o)=La Clape Oh horizon, L(a)=La Clape A1 horizon, T(o)=TheÂzan Oh horizon, T(a)=TheÂzan A1 horizon. Each soil is represented by three lines (year 1, 2 and 3); the left hand end of the lines indicates the
amount of13C remaining in the native soil; the right hand end of the line indicates the amount of13C remaining in the translocated soil. For
instance, for JaÈdraaÊs: the left end of lines J1, J2 and J3 indicates13
C remaining in the native JaÈdraaÊs soil (MAT 2.38C) after 1, 2 and 3 yr; the
right end of the line indicates the13
C remaining in the JaÈdraaÊs soil transplanted to Haldon (MAT 9.88C). Vertical bars indicate standard
devi-ation. For clarity, only the lines for years 1 and 3 are shown for the Mediterranean soils (La Clape and TheÂzan); for instance for La Clape Oh:
L(o)1 and L(o)3). Since the13C mineralisation curves of TheÂzan Oh and A1 were comparable (see text), data for the A1 horizon are not
pre-sented. The slopes of the lines indicate the eect on13C mineralisation of the dierence in annual temperature between the donor (native soil)
and host (transplanted soil) sites.
was 50 and 19 mm at Vindeln and JaÈdraaÊs, respect-ively (Table 3). Thus the drier regime in Vindeln could result in an overestimate of the calculated Q10 values.
However, since at both sites the water de®cit was low it may not have signi®cantly in¯uenced C mineralis-ation. Recently, KaÈtterer et al. (1998) calculated from literature data, that aQ10of 2 was adequate for a
tem-perature range from 5 to 358. For soils at temperatures below 58C, they found that the calculation using other temperature response functions than Q10 are probably
more adequate.
For the native and transplanted soils, the mineralis-ation pattern was clearly modi®ed by the long period over which the soils were frozen. This resulted in a stepwise pattern of 13C losses over the ®rst year with no signi®cant changes between October 1993 and June 1994 (Fig. 4a). At Vindeln this inactive winter period was followed by a substantial leaching of13C from the labelled horizon into the underlying layer as the soils thawed. This winter eect was not observed in years 2 and 3, probably because the responses of the more recalcitrant materials were masked by the variability. In a ®eld experiment of barley straw decomposition in Sweden (608N) AndreÂn and Paustian (1987) also
observed a similar pattern of mass losses. Raich and Schlesinger (1992), however, showed in boreal soils that CO2 evolution continue over the winter period.
Snow cover and the activity in deeper layers will prob-ably contribute to these dierences in responses.
4.2. Atlantic climate shift toward the boreal forest
The translocation of the JaÈdraaÊs soil to Haldon sig-ni®cantly increased 13C mineralisation rates through-out the experiment and the 13C mineralisation rates in the native Haldon soil were signi®cantly higher com-pared to the native JaÈdraaÊs soil (Fig. 5). The JaÈdraaÊs soil located at Haldon lost 20±25% more 13C than the same material in the parent site (Fig. 6). However, the temperature between the two locations increased from 3 to 108C, i.e. greater than the climate warming of 38C predicted for high latitudes. TheQ10 values determined
over the 3 yr for these soils ranged between 1.2 and 1.5. The summer water de®cit was low at both sites and of the same order of magnitude (<50 mm) and was probably not a major limiting factor for C miner-alisation. Thus, assuming a Q10 of 1.4, there would be
an estimated 6±7% increase in C mineralisation after
Fig. 6. Relative change in remaining13C resulting from transplantation (%). Vertical bars represent standard deviation. Year 1, 2 and 3=13C
balance after 1, 2 and 3 yr of ®eld exposure. For instance, Vindeln to JaÈdraaÊs=native Vindeln soil transplanted to JaÈdraaÊs. P. Bottner et al. / Soil Biology & Biochemistry 32 (2000) 527±543
the ®rst year of the JaÈdraaÊs soil for a 38C rise in tem-perature and a increase of 4% after 3 y. Thus a 38C increase in the JaÈdraaÊs soil had a substantially smaller eect than the same temperature increase in the Vin-deln soil, indicating that there were dierences in the temperature sensitivity of the organic matter at the two latitudes.
4.3. Soils in the warmer temperate regions
The mean temperature increased from 9.8 at Haldon to 158C at TheÂzan and from 11.9 at Friston to 168C at La Clape but the 13C mineralisation was not aected because the temperature eect was probably counter-acted by the increasing moisture de®cits down the transect (Fig. 6). Water de®cit signi®cantly reduced
13
C mineralisation during the ®rst 2 yr when the Fris-ton soil was translocated to La Clape and also for Haldon during the ®rst year. Thus the expected climate shift of wet Mediterranean climate toward the Atlantic zone would lower the decomposition rates of the tran-sient labile compounds during the initial mineralisation phases. The slow 13C mineralisation phases were not signi®cantly aected, either because the decomposition of the stabilised material was less sensitive to moisture regime (e.g. changes in the composition of the mi-crobial community, inducing functional shifts; Zogg et al., 1997) or the high variability masked the dierence between the treatments. In addition Pinol et al. (1995) observed that ®eld CO2 eux from Mediterranean
soils are not entirely explained by moisture and tem-perature conditions.
In western temperate Europe, with a doubling of at-mospheric CO2, a global warming of 1.1±2.48C is
pre-dicted with higher frequencies of seasonal and weather extremes. Summer precipitation is predicted to decrease in southern UK and potential evapotranspira-tion to increase in both winter and summer (CCIRG, 1996). Nevertheless, despite the lack of more precise predictions for moisture regime, the climate conditions of TheÂzan and La Clape compared to Haldon and Friston probably overestimate the eects of predicted climate shifts. Assuming roughly a linear relation between water de®cit and C mineralisation for the range of precipitation between the donor and host sites, a decrease of about 6±12 % in C mineralisation per 100 mm decline in rainfall is a realistic estimate. More precise predictions would be questionable; the most ®rm result is that the temperature eect is clearly counteracted by the moisture eect.
4.4. Eects of increased temperature and aridity in the wet Mediterranean zone
The translocation of soils by 2±38latitude, from the wet Mediterranean sites (TheÂzan and La Clape in
southern France) to the dry Mediterranean Spanish host sites (Desert and Maials), resulted in a mean air temperature increase over the 3 yr of 1.0 and 0.88C for TheÂzan to Desert and La Clape to Maials, respectively. The corresponding decrease in precipitation was 344 and 400 mm yrÿ1
and the increased water de®cits were 140 and 187 mm, respectively. The general circulation models predict a temperature increase of 1.3±1.98C in the Mediterranean with a doubling of atmospheric CO2 with longer periods of consecutive hot periods
during the dry seasons (Rambal and Ho, 1998). An essential characteristic of the Mediterranean soils is the deep distribution of the soil organic matter within the soil pro®le as a consequence of both deep rooting sys-tems and soil faunal animal activity: a strategy of plants and animals to survive during the dry season. Thus the soil organic matter quality (humus types) is strongly in¯uenced by the physical and chemical characteristics of the mineral soil.
With the exception of the La Clape Oh horizon during the ®rst year (Lo1 in Fig. 5) the host
environ-ment generally reduced 13C mineralisation rates in Oh and A1 as a consequence of moisture limitation over-riding temperature eects. However, the dierence between native and transplanted soil was really im-portant and signi®cant only for the La Clape Oh hor-izon (L(o)3, Fig. 5). The increasing moisture limitation substantially aected only the Oh layers (Fig. 6).
At La Clape, the Oh horizon was separated from the underlying A1 horizon by a stone layer of about 5 cm thickness. In Mediterranean soils, this frequently observed layer results from the residual accumulation of 2±7 cm dia stones after erosion of soil ®nes, when the primary Mediterranean forest was destroyed. After the more recent natural forest reinstalled, the xeromo-der (Oh) developed on the surface of the stone layer and was consequently subject to severe desiccation and ¯uctuating moisture regimes. Similar conditions lead-ing to the development of xeromoders are quite preva-lent in Mediterranean forests, especially on calcareous soils. The columns set up with the La Clape soils included this stone layer (Fig. 2) and probably contrib-uted to the larger residual 13C in the Oh horizon than in the A1 horizons for both the native and translo-cated systems.
While the Oh material at La Clape has developed on a soil recently renewed by erosion and recolonised by forest, the TheÂzan Oh is developed on a old stabil-ised `luvisol', representative of large areas in the Medi-terranean region. Here the clays and ®ne particle fractions have been weathered out of the topsoil into the B horizon during long pedogenesis periods, so that xeromoder horizon has developed on the surface of an impoverished, very permeable, residual, sandy and dry horizon (Bottner et al., 1995). Although the humus type (Oh) is similar, the pH is 5.2 for La Clape on
careous material and 4.3 for TheÂzan on acid sand ma-terial. The13C mineralisation rates in Oh were similar for the two soils, emphasising the dominant eects of moisture on decomposition processes in the top layers in this region.
The13C mineralisation characteristics of the TheÂzan A1 horizon (not shown in Fig. 5) were similar to those of the TheÂzan Oh horizon. The TheÂzan A1 horizon was also developed in the leached and extremely per-meable top mineral layer below the xeromoder (Fig. 2); so soil processes in this horizon were probably also moisture-limited for a signi®cant period of the year.
The La Clape A1 horizon is of special interest as it showed the highest mineralisation rates with more than 75% losses of 13C from both the native and translocated soils (Fig. 4b). The most likely reasons for this are that (i) the water draining rapidly through the Oh and stone layers is retained within this clay and loam horizon and moisture losses by evaporation are reduced by the mulching eects of the overlying materials and (ii) in this Ca2+. saturated soil the ac-tivity is stimulated by soil neutral pH (7.3). In this A1 horizon, the processes are not moisture-limited for extended periods, when desiccation limits decompo-sition of surface organic matter (Oh). The la Clape A1 horizon illustrates the high activity of the Mediterra-nean soil deep organic layers, where favourable tem-perature conditions meet buered moisture conditions lasting beyond the rain season.
4.5. The climate shift from Mediterranean to Atlantic: a key situation for transition of soils as carbon source or sink
The concave shape of the curves shown in Fig. 5 in-dicates a number of key features of the eects of cli-mate change on these soils. (1) The magnitude of the temperature eect decreased progressively from the northern boreal climate at Vindeln to the Atlantic cli-mate at Haldon. Then from Atlantic to Mediterranean regions the moisture limitation counteracts the eects of higher temperatures. (2) In the more temperature-limited situations (Vindeln to JaÈdraaÊs), the temperature eect persists over the 3 yr. When the temperature eect becomes less dominant (JaÈdraaÊs to Haldon) only the ®rst year decomposition is aected (the active de-composition phase). (3) Similarly, the water de®cit aects generally only the ®rst year decomposition i.e. H1 and F1 in Fig. 5. The lowering of 13C mineralis-ation persists over the 3 yr only under the driest con-ditions, i.e. La Clape Oh, (L(o)3 in Fig. 5). (4) The concave part of the centre of the Figure (the Haldon site with Haldon native soil and the soil transplanted from JaÈdraaÊs and the native Friston soil) illustrates that optimum combined temperature and moisture
conditions occur under the current Atlantic climate, and results in the highest 13C mineralisation rates.
The transition between the current Atlantic climate and wet Mediterranean climate (in the more general Holdridge life zone chart: the transition between cool temperate and warm temperate) is probably a key situ-ation, with an expected net stimulation of the C miner-alisation controlled by the predicted temperature increase to the north and a net slowdown controlled by the predicted water de®cit increase to the south. This is illustrated by Fig. 5: The ordinate of the north±south soils sequences follows asymmetrical con-cave shaped curves (year 1: V14J14H14F1; year 2: V2, 4J2, 4H2 4F2; year 3: V3,4J34H34 F3) indicating from north to south a temperature con-trolled decrease of C mineralisation from Vindeln to Haldon and Friston. Southward, beyond the Atlantic climate, despite the temperature increase, the C miner-alisation remains constant or tends to be slightly low-ered. The increased water de®cit from wet to dry Mediterranean climate, lowered the C mineralisation clearly in particularly unfavourable conditions, illus-trated by the xeromoders. The high and prolonged soil activity persists under Mediterranean conditions only under particular favourable microclimatic circum-stances, which were illustrated in this paper by the deep organic and moisture buered layers of the Medi-terranean soils (La Clape A1, i.e. L(a)3 in Fig. 5). The root litter derived from of the deeply distributed root system of the Mediterranean vegetation and the or-ganic matter incorporated by animals provides sub-strate for microbial activity.
5. Conclusion
The combination of (i) tracer techniques, (ii) latitu-dinal climatic gradient investigation and (iii) transloca-tion of dierent humus forms has provided a novel insight into the potential eects of climate change on decomposition processes and the dynamics of soil C pools. In the West European 65±408 latitudes, the most favourable temperature and moisture conditions occur under the current Atlantic climate. Northward this climate zone (the cool temperate and boreal cli-mate), where the soil processes are essentially tempera-ture-limited, the predicted temperature increase of 38C will probably enhance C mineralisation. Based on Q10
values derived from the comparison of native and transplanted soils, the calculation estimates an increase of the C mineralisation of about 10% for the cool tem-perate zone and of about 20±25% for the boreal zone. This estimation is based on the assumption that in these northern sites the dierence in moisture eect between native and host site is of small importance compared to the temperature eect. Southward the
Atlantic climate zone, where soil processes are season-ally moisture-limited, increased temperatures are likely to have little eects on soil organic matter dynamics, because of the higher water de®cit. A signi®cant re-duction of C mineralisation rates was shown only in the surface organic layers, morphologically recognised in Mediterranean forest soils as `xeromoder' and sub-ject to frequent dry conditions. The amount of C stored in this thin and patch-wise distributed organic surface horizon is unknown. In the deeper organic layers (the mull humus types) which constitute the main soil C pools in Mediterranean soils, microbial ac-tivity is maintained for longer into the dry seasons as a consequence of moisture storage. However a tem-perature increase of 28C did not signi®cantly aect C mineralisation in this layer because the eects of higher temperatures may have been counteracted by increased water de®cits.
Acknowledgements
This work was supported by the Environmental Research and Development Programme of the Com-mission of the European Community (Vamos pro-gramme). We are grateful to V. CouÃteaux, P. Jame, F. Picasso and P. Splatt for technical assistance with the project.
References
AndreÂn, O., Paustian, K., 1987. Barley straw decomposition in the ®eld: a comparison of models. Ecology 68, 1190±1200.
Bottner, P., CouÃteaux, M.M., Vallejo, V.R., 1995. Soil organic mat-ter in Medimat-terranean-type ecosystems and global climatic changes: a case study: the soils of the Mediterranean Basin. In: Moreno, J.M., Oechel, W.C. (Eds.), Global Changes and Mediterranean-Type Ecosystems. Springer, New York, pp. 306±325.
Boutton, T.W., 1991. Stable carbon isotopic ratios of natural ma-terial: Sample preparation and mass spectrometic analysis. In: Coleman, D.C., Fry, B. (Eds.), Carbon Isotopic Techniques. Academic Press, New York, pp. 155±171.
CCIRG, 1996. Review of the potential eects of climate change in
the United Kindom. Department of Environment, HMSO, London.
Ciais, P., Tans, P.P., Trollier, M., White, J.W.C., Francey, R.J.,
1995. A large northern hemisphere terrestrial CO2sink indicated
by the13C/12C ratio of atmospheric CO
2. Science 269, 1098±1102.
Cotrufo, M.F., Ineson, P., Rowland, A.P., 1994. Decomposition of
tree leaf litters grown under elevated CO2: eects of litter quality.
Plant and Soil 163, 121±130.
CouÃteaux, M.M., Mousseau, M., CeÂleÂrier, M.L., Bottner, P., 1991.
Increased atmospheric CO2 and litter quality: decomposition of
sweet chestnut leaf litter with animal food webs of dierent com-plexities. Oikos 61, 54±64.
Dai, A., Fung, I.Y., 1993. Can climate variability contribute to the
``missing'' CO2sink? Global Biogeochemical Cycles 7, 599±609.
Jenkinson, D.S., Adams, D.E., Wild, A., 1991. Model estimates of
CO2 emissions from soil in response to global warming. Nature
351, 304±306.
KaÈtterer, T., Reichstein, M., AndreÂn, O., Lomander, A., 1998. Temperature dependance of organic matter decomposition: a critical review using literature data analysed with dierent models. Biology and Fertility of Soils 27, 258±262.
Keeling, R.F., Piper, S.C., Heimann, M., 1996. Global and
hemi-spheric CO2sinks deduced from changes in atmospheric O2
con-centration. Nature 381, 218±221.
Pinol, J., Alcaniz, J.M., Roda, F., 1995. Carbon dioxide eux and
pCO2 in soils of three Quercus ilex montane forests.
Biogeochemistry 30, 191±215.
Raich, J.W., Potter, C.S., 1995. Global patterns of carbon dioxide emissions from soils. Global Biogeochemical Cycles 9, 23±36. Raich, J.W., Schlesinger, W.H., 1992. The global carbon dioxide ¯ux
in soil respiration and its relationship to vegetation and climate. Tellus 44B, 81±99.
Rambal, S., Ho, C., 1998. Mediterranean ecosystems and ®re: the threats of global change. In: Moreno, J.M. (Ed.), Large Forest Fires. Backhuys, Leiden, pp. 187±213.
Schimel, D.S., Braswell, B.H., Holland, E.A., Mckeown, R., Ojima, D.S., Painter, T.H., Parton, W.J., Townsend, A.R., 1994. Climatic, edaphic and biotic controls over storage and turnover of carbon in soils. Global Biogeochemical Cycles 8, 279±293. Tans, P.P., Fung, I.Y., Takahashi, T., 1990. Observational
con-straints on the global atmospheric CO2 budget. Science 247,
1431±1438.
Townsend, A.R., Vitousek, P.M., Holland, E.A., 1992. Tropical soils could dominate the short-term carbon cycle feedback to increased global temperature. Climatic Change 22, 293±303.
Zogg, G.P., Zak, D.R., Ringelberg, D.B., MacDonald, N.W., 1997. Compositional and functional shifts in microbial communities due to soil warming. Soil Science Society of America Journal 61, 475±481.
