Biotic and abiotic factors controlling soil respiration rates in
Picea abies
stands
Nina Buchmann*
Max-Planck-Institute for Biogeochemistry, P.O. Box 100164, D-07701 Jena, Germany
Accepted 17 May 2000
Abstract
The response of soil respiration to varying environmental factors was studied in four Picea abies stands (47-, 87-, 111- and 146-year old) during the 1998 growing season. While within-site variations of soil CO2eux (up to 1.6mmol CO2mÿ2sÿ1) were
larger than their diurnal variability (<0.25 mmol CO2 mÿ2 sÿ1), spatial variations within a site were smaller than seasonal
changes in soil respiration rates (up to 4.4mmol CO2mÿ2sÿ1). Highest within-site variability of soil eux was generally found
during the summer months when maximum ¯ux rates of 4±6mmol CO2mÿ2 sÿ1 were reached (coecient of variation 40%).
Soil temperatures (in the Of and Ohlayers, and Ahhorizon) showed a pronounced seasonal course, in contrast to soil moisture.
An exponential equation best described the relationships between soil temperature in the Of layer and soil CO2 eux r2
between 0.75 and 0.81). However, an Arrhenius type equation always resulted in lower r2 values (0.52±0.71). The Q
10 values ranged between 2.39 (146-year old stand) and 3.22 (87-year old stand), averaging 2.72 for the P. abies stands within the watershed. The removal of litter and organic layers generally aected soil CO2 eux negatively. In three of the fourP. abies
stands (47-, 87-, 146-year old stands), soil respiration rates were reduced by 10±20% after removal of the L and Of layer, and
by 30±40% after removal of the L and most of the Of and Ohlayers. Thus, mineral soil respiration seemed to contribute a
major fraction to the total soil CO2¯ux (>60%). Trenching shallow ®ne roots during collar insertion and mechanical inhibition
of root in-growth during the following months allowed ®ne root respiration to be separated from microbial respiration only in times of highest root growth. Microbial respiration seemed to dominate the respiratory CO2loss from the forest ¯oor (>70%).
The comparison of the annual soil CO2eux in the 47-year oldP. abiesstand (about 710 g C mÿ2yrÿ1) with annual litterfall
and root net primary productivity estimates supported this conclusion.72000 Elsevier Science Ltd. All rights reserved.
Keywords:Microbial respiration; Organic layer; Root respiration; Seasonality; Soil; Respiration;Q10 value
1. Introduction
Soil respiration is a major CO2¯ux within terrestrial
ecosystems as well as between the biosphere and the atmosphere (Schlesinger, 1977; Raich and Schlesinger, 1992; IPCC, 1996). Soil CO2 ¯uxes originate from
autotrophic root respiration and heterotrophic mi-crobial respiration in the rhizosphere and the bulk soil. Generally, between 50% and 80% of the nocturnal biosphere±atmosphere CO2 exchange, measured with
eddy covariance techniques, are due to soil CO2eux
(Lavigne et al., 1997). However, during the night, these measurements of net ecosystem CO2 exchange
are associated with the largest errors (Moncrie et al., 1997). Thus, detailed information on soil CO2 ¯uxes
and on factors that control these ¯uxes are needed to constrain the ecosystem carbon budget and to decide whether or not terrestrial ecosystems are carbon sinks or sources (Fan et al., 1995; Goulden et al., 1996; Lavigne et al., 1997; Lindroth et al., 1998). Further-more, climate and land-use change have the potential to enhance or reduce soil CO2 ¯uxes. Changes in
tem-perature and precipitation, and also shifts from forest to agricultural land-use or changing management
prac-0038-0717/00/$ - see front matter72000 Elsevier Science Ltd. All rights reserved. PII: S 0 0 3 8 - 0 7 1 7 ( 0 0 ) 0 0 0 7 7 - 8
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* Tel.: +49-3641-64-3721; fax: +49-3641-64-3710.
tices will aect soil respiration ¯uxes and therefore, the carbon budget of terrestrial ecosystems (Raich and Potter, 1995; IPCC, 1996).
Typically, soil CO2¯ux rates show large spatial and
temporal variations, both within and among sites, which are only partly due to methodological dier-ences (Raich and Nadelhoer, 1989; Hanson et al., 1993; Norman et al., 1997). Since soil respiration is a combined ¯ux from roots and microorganisms from dierent soil depths (organic surface layers and min-eral horizons), sevmin-eral factors and their interactions aect soil respiration rates. Soil temperature and soil moisture are among the most important factors con-trolling the CO2 ¯ux (Raich and Schlesinger, 1992;
Raich and Potter, 1995; Davidson et al., 1998). Root nitrogen concentrations, soil texture, substrate quantity and quality have also been shown to have an eect (Grant and Rochette, 1994; Randerson et al., 1996; Boone et al., 1998; Pregitzer et al., 1998). Great debate still exists on how to model the impact of these factors on soil respiration (e.g., Lloyd and Taylor, 1994; Thierron and Laudelout, 1996), and how the large variability in¯uences aggregation of soil CO2 eux
estimates for a watershed or a landscape (Kicklighter et al., 1994). Thus, although the variability of soil CO2
¯uxes and some of the underlying causes are well known, they still bear uncertainties that need to be resolved.
Since autotrophic and heterotrophic respiration will react dierently to changes in environmental con-ditions, it is crucial to get more insight into both com-ponents of soil respiration (Kirschbaum, 1995; Boone et al., 1998). However, the separation of root (includ-ing rhizosphere microorganisms) and microbial respir-ation under ®eld conditions is still dicult. So far, many dierent approaches have been used in situ, ran-ging from severe disturbances of a site to very speci®c requirements, e.g., changes in the carbon isotopic sig-nature of the two respiratory components (either due to a change of the photosynthetic pathway of the veg-etation or manipulations with isotope tracers). Auto-trophic respiration of intact roots has been measured with root cuvettes in the ®eld (Gansert, 1994) or with excised roots in the laboratory (Burton et al., 1998). Trenching (Fisher and Gosz, 1986; Bowden et al., 1993; Hart and Sollins, 1998; Boone et al., 1998), labeling with 14C, 13C or 18O (Horwath et al., 1994; Swinnen et al., 1994; HoÈgberg and Ekblad, 1996; Lin et al., 1999), inhibiting one respiratory component with speci®c inhibitors or herbicides (Helal and Sauer-beck, 1991; Nakane et al., 1996), and enhancing one component over the other (Bowden et al., 1993) have been used to separate root from microbial respiration. However, the ratio between the two respiration com-ponents is generally quite site-speci®c and varies between 1:9 and 9:1 (Hanson et al., 2000).
Natural disturbances (e.g., ®re, windthrow) or anthropogenic land-use changes (e.g., logging, agricul-tural cultivation, aorestation) often alter the soil pro-®le, thereby changing not only carbon stocks, but maybe also carbon ¯uxes (Schimel et al., 1997). The magnitude of change in soil CO2 eux is dependent
on whether or not litter and organic layers are removed, roots are disturbed or mineral soil horizons are exposed or mixed. However, only very limited in-formation is available about these aspects in forest ecosystems (Edwards and Sollins, 1973; Bowden et al., 1993; Mallik and Hu, 1997; Nakane et al., 1997; Boone et al., 1998; Thuille et al., 2000). Since forest management always involves some kind of site disturb-ance, this adds further uncertainty to modeled soil CO2¯ux estimates of managed forests.
In this study, spatial versus temporal variability of soil respiration was studied in four Picea abies stands during the 1998 growing season. Spatial variability was investigated at two dierent scales, within a site and within a watershed, using stands growing close to each other (less than 500 m apart). Temporal variability was addressed on a diurnal and a seasonal basis. Fur-thermore, the eects of ®ne root exclusion and organic layer removal on soil CO2¯ux rates was tested in
Nor-way spruce forests.
2. Materials and methods
2.1. Sites
Four Norway spruce stands (Picea abies(L.) Karst.) were chosen within the Lehstenbach watershed, at about 770 m elevation in the Fichtelgebirge, Northeast Bavaria, Germany (50808' N, 11852' E). The four stands were located close to each other (<500 m apart) and ranged in age from 47 to 146 years (Table 1). The higher LAI of the youngest stand was associated with a higher stand density compared to the oldest spruce stand (1018 and 363 trees haÿ1, respect-ively). The managed stands had almost no woody deb-ris and only a sparse understory with the grasses Deschampsia ¯exuosa and Calamagrostis villosa and the ericaceous dwarf shrubs Vaccinium myrtillus and V. vitis-idea. Forest ¯oor characteristics were quite similar, with litter layers (L) of about 1.2 cm, and with organic Of and Oh layers (Of = <70% ®ne organic
matter, plant material still recognizable; Oh = >70%
with sandy±loamy soil texture and low pH values (Dieenbach et al., 1997).
2.2. Measurements of soil CO2eux and organic layer
parameters
Soil respiration rates were measured monthly during the growing season of 1998 (April±October) using a soil respiration chamber (LI-6400-09; LiCor, Lincoln, Nebraska, USA) connected to a portable photosyn-thesis system (LI-6400). Four to ®ve PVC collars (10 cm long, 10 cm inside diameter) were inserted into the soil of each stand. Insertion depth was ca. 5±8 cm into the forest ¯oor. Shorter collars (3±5 cm long) were un-stable and tended to disturb the forest ¯oor. Although the soil disturbance during collar insertion generally results in initially high ¯uxes just after collar installa-tion, ¯uxes stabilize after 10±30 min (Norman et al., 1997). In accordance with most other studies, collars were installed at least 24 h prior to measurement. The soil respiration chamber was set on top of these col-lars, allowing an undisturbed measurement of soil CO2
¯ux rates. The protocol recommended by LiCor (LI-6400-09 manual) was changed to ®ve observations of 10mmol molÿ1change per measurement. Litter and or-ganic layer thickness (L, Of and Oh layers) as well as
soil temperatures in the Of and Oh layers and the Ah
horizon (at 5, 10 and 15 cm depths, respectively) were measured next to each PVC tube. Gravimetric soil water contents of the Of and Oh layers were
deter-mined with three replicates per measurement. The wet soil samples were weighed, then dried until weight con-stancy, and weighed again. Soil moisture is expressed as per cent dry weight.
2.3. The eect of ®ne root exclusion and organic layer removal on soil CO2eux
In each of the four spruce stands, some PVC collars established earlier in the growing season remained in the soil and soil CO2 eux was measured during the
following months. Thus, in October for example, soil collars were available that had been established in
April through October n1±5 per month since estab-lishment). This design was used to test whether tren-ching shallow ®ne roots (growing in the organic layers) during collar insertion and mechanical inhibition of root in-growth had an eect on current soil respiration rates. At the end of the experiment, collars were taken out and checked for root in-growth into the collar from below. However, no root in-growth was observed.
In July, August, and October 1998, nine additional collars were established in each stand. The litter and Of layers were carefully removed before the insertion
of three collars. For three other collars, the litter and most of both the Of and Oh layers were removed from
the mineral soil, and three undisturbed soil pro®les served as controls. Rare coarse roots (>1 mm diam-eter) within the organic layers were cut with a knife without disturbing the underlying mineral soil hor-izons. Soil CO2 eux was determined 24 h later. This
design allowed the organic layer respiration to be sep-arated from mineral soil respiration.
2.4. Statistics
Analyses of variance with a posteriori tests (Tukey's honestly signi®cant dierence (HSD) test, a0:05
were used to separate the means. Data were trans-formed when variances were not homogenous. Non-linear regression analyses were used to test the eect of collar establishment. Soil CO2 eux and temperature
data were pooled when the interaction term was not signi®cant at the a0:05 level. Correlation and
non-linear regression analyses were used to test the re-lationship between soil temperature, soil moisture and soil respiration (Eq. (1)). The Q10 values were calcu-lated according to Eq. (2). Residual analyses were per-formed to test the exponential regression (Eq. (1)) versus the Lloyd and Taylor (1994) Arrhenius type equation (Eq. (3)).
yb0e b1T 1
Q10e10b1 2
Table 1
Stand characteristics of fourP. abiesstands within the Lehstenbach watersheda
Site Age (yr) LAIb L (cm) Thickness of O
flayer (cm) Thickness of Ohlayer (cm)
Weidenbrunnen 47 10.4 1.320.3 5.120.4 3.620.8b
Weidenbrunnen3 87 NDc 1.520.1 4.820.7 4.220.7b
Weidenbrunnen2 111 ND 1.020.1 5.220.6 7.220.6a
Coulissenhieb 146 6.6 0.920.1 5.920.2 4.420.2b
a
Dierent letters within a column denote signi®cantly dierent thickness data (Tukey HSD test,a0:05). b
Leaf area index data provided by Martina Mund, Max-Planck Institute for Biogeochemistry, Jena, Germany. c
whereTis the soil temperature (8C).
yR10exp
308:56
1 56:02ÿ
1
Tÿ227:13
3
whereR10 is the soil respiration rate at 108C, and T is the absolute soil temperature (K). See Lloyd and Tay-lor (1994) for the derivation of the equation.
3. Results
3.1. Spatial versus temporal variability of soil respiration rates
Within-site spatial variations among soil collars were larger than the diurnal variability of soil respiration rates measured with the same collars during a day (Fig. 1). While within-site dierences of soil CO2eux
among replicated collars were up to 1.6mmol CO2mÿ2
sÿ1 (about 40% of maximum values, between 60% and 70% of minimum values), diurnal variations were less than 0.25 mmol CO2 mÿ2 sÿ1 (<10% of average
rates per collar). During the 10 h period, soil CO2
eux remained almost constant for all four collars, re¯ecting the time course of soil temperatures in the Oh layer (10 cm depth) more closely than those in the
Of layer (5 cm depth) (average change in temperature
of 0.5 vs. 1.48C).
In contrast, seasonal variations of soil respiration rates were greater than within-site spatial variations for the four Picea abies stands during the 1998 grow-ing season (Table 2). Whereas seasonal ¯uctuations of soil CO2 eux rates were as high as 4.4 mmol CO2
mÿ2 sÿ1 (111-year old stand), within-site spatial varia-bility was smaller, on average about 25% of the re-spective rates (coecient of variation, CV; Fig. 2). Highest within-site variability of soil respiration rates (about 40%) was generally found during the summer months (with one exception) although soil tempera-tures varied by less than 5% within each given site (not shown).
All spruce stands studied in the Lehstenbach water-shed showed the same seasonal trend in their soil CO2
eux P0:629 for the interaction term `site X
month'). Soil respiration rates increased during spring and summer, and reached maximum values of 4±6 mmol CO2mÿ2 sÿ1 in July and August P<0:001 for
`month' as main factor; Fig. 3). During fall (Septem-ber±October), soil respiration rates declined again, reaching values close to those in spring (April). Although soil CO2 eux did not dier signi®cantly
among the four P. abies stands within the watershed throughout the growing season P0:196 for `site' as
main factor), soil respiration rates in the 111-year old spruce stand tended to show higher rates than those in
Fig. 2. Seasonal course of the coecient of within-site variation for soil CO2 eux rates in fourP. abies stands. Collars were inserted into the soil 24 h before the measurements.
the other stands. Soil temperatures of the Of and Oh
layers and the Ah horizon (at 5, 10 and 15 cm depth)
showed the same pronounced seasonal course as the soil CO2 eux r0:93, r0:92, and r0:82,
re-spectively). In contrast, soil moisture of the Of layer
(Fig. 3), and also of the Oh layer (not shown) showed
a dierent pattern that did not explain a signi®cant
fraction of the within-watershed spatial variance in soil respiration rates r ÿ0:41 and r ÿ0:36,
respect-ively).
3.2. Relationships between soil temperature and soil respiration
An exponential equation (Eq. (1)) best described the relationships between soil temperature at various depths (in the organic layers and the Ah horizon) and
soil CO2eux r2 between 0.60 and 0.93 compared to
r2 between 0.53 and 0.81 for a linear ®t; Fig. 4). Soil temperatures in the four stands changed dierently during the growing season P<0:001 for the
inter-Table 2
Soil respiration rates (mmol CO2mÿ2sÿ1) in fourP. abiesstands in the Fichtelgebirge during the 1998 growing seasona
Month 47-year old 87-year old 111-year old 146-year old All stands
April 1.2320.09d 1.1720.12d 1.5520.17d 1.0820.12d 1.2420.06c May 2.9820.14b 2.5720.67bc 3.1520.18bc 2.6220.34bc 2.8220.17b June 2.6320.30bc 3.6120.30ab 3.4120.31bc 2.3020.14cd 2.9920.19b July 3.9720.39a 4.7420.76a 5.0721.03ab 4.6320.78a 4.5120.32a
August 4.1020.42a 4.35
20.41ab 5.93
20.87a 3.94
20.27ab 4.58
20.33a Septemberb 2.6020.17bc 2.6320.29bc 3.2620.30bc 2.3320.25cd 2.7120.21b October 1.6020.08cd 1.6320.09c 1.9520.23c 1.3720.18cd 1.6420.09c
aMeans and standard errors n5are given. Dierent letters within a spruce stand denote signi®cantly dierent soil respiration rates (Tukey HSD test,a0:05).
bCollars had been installed in the soil one week prior to measurements.
Fig. 4. Relationship between soil respiration rates and soil tempera-ture in the Oflayer at 5 cm depth for all fourP. abiesstands during the growing season of 1998. The exponential regression equations are given in Table 3. All collars were installed 24 h prior to measure-ment.
action term `sitemonth'), probably due to dierences in stand structure (see Table 1). This within-watershed spatial variability of soil temperatures required separ-ate regression analyses for the four P. abies stands within the watershed (Table 3). Comparingn,r2 andF values as well as residuals, best results were obtained with soil temperature in the Of layer (at 5 cm) as
inde-pendent variable. All relationships were highly signi®-cant P<0:0001 and explained between 75% and
81% of the variance in the soil respiration rates (using the T5 relationships). The Q10 values ranged between 2.39 (146-year old stand) and 3.22 (87-year old stand), averaging 2.72 for theP. abiesstands within the water-shed (Eq. (2)).
Furthermore, these exponential regressions were compared to the Arrhenius type equation (Lloyd and Taylor, 1994) where b0 is standardized to 108C, and the eective activation energy for respiration varies inversely with soil temperature (Eq. (3)). The overall ®t of the Arrhenius type equation to the four datasets generally resulted in lowerr2 values: 0.71 compared to 0.80 for the 47-year old stand, 0.68 compared to 0.81 for the 87-year old stand, 0.63 compared to 0.80 for the 111-year old stand, and 0.52 compared to 0.75 for the 146-year old stand. Furthermore, residual analyses showed no dierence between the equations. Thus, the (simpler) exponential equation with soil temperature at 5 cm depth (Of layer) was preferred (Eq. (1)).
3.3. Eect of ®ne root exclusion on soil respiration
Trenching shallow ®ne roots during collar insertion and subsequent mechanical inhibition of root in-growth aected soil respiration rates in all four stands of the watershed in the same way P0:75 for the
in-teraction term `site X months since installation'). Therefore, the four datasets were pooled. However, the eect of ®ne root exclusion could not be observed at all sampling dates during the 1998 growing season
Table 3
Relationships between soil respiration rates (mmol CO2 mÿ2 sÿ1) and soil temperatures (8C) measured in the Of and Ohlayers at 5 and 10 cm depth and in the Ahhorizon at 15 cm depth for fourP. abiesstands in the Fichtelgebirge during the 1998 growing season
Site yb0e b1T SEb0 SEb1 Q10 n F r2 P
47-year old y0:98e 0:088:T5 0.13 0.011 2.41 20 70.2 0.80 < 0.0001 y1:24e 0:085:T10 0.18 0.014 2.34 23 34.7 0.62 < 0.0001 y0:99e 0:109:T15 0.18 0.018 2.34 16 38.2 0.73 < 0.0001
87-year old y0:80e 0:117:T5 0.16 0.016 3.22 14 52.0 0.81 < 0.0001 y0:73e 0:141:T10 0.08 0.013 4.11 24 122.8 0.85 < 0.0001 y0:55e 0:166:T15 0.08 0.014 4.11 12 134.7 0.93 < 0.0001
111-year old y1:03e 0:105:T5 0.17 0.014 2.87 16 54.2 0.80 < 0.0001
y1:01e 0:119:T10 0.14 0.014 3.27 21 74.2 0.80 < 0.0001
y1:05e 0:119:T15 0.23 0.023 3.27 14 27.5 0.70 < 0.0001
146-year old y0:87e 0:087:T5 0.13 0.012 2.39 21 55.4 0.75 < 0.0001 y0:85e 0:103:T10 0.11 0.012 2.82 30 70.59 0.71 < 0.0001 y0:73e 0:117:T15 0.13 0.016 2.82 22 50.8 0.72 < 0.0001
(Fig. 5). Soil respiration rates, measured with collars inserted 24 h prior to measurement (i.e., 0 months since installation), diered signi®cantly from those measured with older collars (i.e., 1±6 months since installation) only in May and August. No eect was detectable in June, July or October. Soil CO2 eux
rates measured with newly installed collars were 20% (May) to 30% (August) higher than those measured with 1-month old collars, indicating the fraction of new root growth during May and August. However, whether roots had been excluded (i.e., collars had been installed) 1 month or longer did not have any eect on soil CO2 eux, supporting the observation that no
roots were growing into the collars from below. Thus, although root respiration in the upper organic layers must have been highest in May and August, microbial respiration seemed to dominate the respiratory CO2
loss from the forest ¯oor (>70%).
3.4. Eect of organic layer removal on soil CO2eux
Generally, the removal of the litter and organic layers aected the soil CO2 eux negatively (Fig. 6).
In three of the four P. abies stands, soil respiration rates were reduced by 10±20% after removal of the L and Of layers, and by 30±40% after removal of the L
and most of the Of and Oh layers (47-, 87-, 146-year
old stands). In two of the spruce stands, this reduction was signi®cant P0:042 for the 47-year old stand;
P0:030 for the 146-year old stand). Due to small
soil respiration rates in the 87-year old stand and therefore relatively large variations, this treatment eect was not evident in the 87-year old spruce stand P0:28). Within-site variability of the 111-year old
stand was much larger than for all the other stands, a trend already seen in the monthly measurements in July and August (see Table 2). Both ®ndings could be due to the higher presence of grass roots in the organic layer of the 111-year old stand the compared to the other stands. Consequently, no treatment eect could be detected P0:98). Since soil moisture and soil
temperatures, which had been determined inside the collars just after the ¯ux measurements, did not dier among the treatments P>0:6), mineral soil
respir-ation seemed to contribute a major fraction to the total soil CO2¯ux (>60%).
4. Discussion
4.1. Within-site variations
Within-site spatial variations in soil respiration rates were greater than the diurnal variations, but smaller than the seasonal variability within a site. Since about 80% of the variance in soil CO2 ¯uxes was explained
by changes in soil temperature, and because soil tem-peratures stayed fairly constant during the day, no diurnal ¯uctuations in soil respiration rates were detected in this study. However, as soon as daytime ¯uctuations of soil temperature increased, soil respir-ation rates responded (Witkamp, 1969; Ben-Asher et al., 1994; Bouma et al., 1997; diurnal changes of 10± 208C). In accordance with other studies (e.g., Hanson et al., 1993; Boone et al., 1998; Davidson et al., 1998), a distinct seasonal trend was observed with highest soil CO2 ¯ux rates as well as greatest coecients of
vari-ation during the summer months throughout the
watershed in this study. Generally, soil temperature alone was sucient to explain seasonal variations of soil and root respiration (this study; Burton et al., 1998; Gansert, 1994; Hanson et al., 1993). However, under certain conditions, soil CO2 eux could also be
constrained by precipitation or soil moisture, e.g., in arid ecosystems by low soil moisture (Conant et al., 1998) or in humid ecosystems by high soil moisture (Buchmann et al., 1997, 1998). Thus, although global models typically use soil temperature as well as soil moisture for large-scale soil CO2 eux estimates
(Kicklighter et al., 1994; Raich and Potter, 1995), other factors that are highly variable at a microscale such as litter quality or water availability might be re-sponsible for large within-site variations during sum-mer months (CV of 40%).
4.2. Temperature dependence and Q10values
There are still uncertainties associated with modeling the strong temperature dependence of soil respiration rates. While under some circumstances, linear or sinu-soidal regressions give good relationships between soil CO2 eux and soil temperature (Raich and
Schle-singer, 1992; Ben-Asher et al., 1994; Fan et al., 1995), most of the studies report exponential regression equations (e.g., Boone et al., 1998; Burton et al., 1998; Davidson et al., 1998; Fan et al., 1995; Raich and Pot-ter, 1995). However, some authors strongly rec-ommend an Arrhenius type equation that at least in one case (where the eective activation energy changed inversely with temperature) resulted in evenly distribu-ted residual variances across the entire temperature range (Lloyd and Taylor, 1994; Thierron and Laudel-out, 1996). In this study, all three functions (linear, ex-ponential, and Arrhenius type) were compared. Whereas linear and Arrhenius type functions gave much lower r2 values than those of the exponential function, the residual variances of exponential and Arrhenius type functions were similarly distributed along the soil temperature range from 28C to 178C for all four stands. Lloyd and Taylor (1994) argued that over a wider temperature range soil microbial popu-lations responsible for soil organic matter decompo-sition might change and that, therefore,Q10 values, the indicators of temperature sensitivity, might change as well. However, their temperature range was about 408C, more than twice the range found in this study. Thus, in this study, the relatively small temperature range might be responsible for the better ®t and simi-lar residual variances using the exponential function compared to the Arrhenius function.
The temperature sensitivity of soil CO2¯uxes within
the watershed varied between 2.4 and 3.2, well within the range of 2.0±3.9 generally given for bulk soil res-piration (Baldocchi et al., 1986; Davidson et al., 1998;
Hanson et al., 1993; Kicklighter et al., 1994; Raich and Schlesinger, 1992; Schleser, 1982). However, soil respiration is a combination of autotrophic and het-erotrophic respiration, and both can exhibit dierent Q10 values. Boone et al. (1998) reported signi®cantly higher Q10 values for root respiration (4.6) than for bulk soil respiration (3.5). However, soil organic mat-ter oxidation was shown to be the most responsive to increased temperatures in small `terracosms' (Lin et al., 1999). Nevertheless, under future climate scenarios with increasing temperatures, higher root respiration rates might result in a smaller soil carbon sink than anticipated (Kirschbaum, 1995; Boone et al., 1998).
4.3. Partitioning of soil CO2eux
The potential change in soil carbon ¯uxes due to increased temperatures will strongly depend on the ratio between root (including rhizosphere) and mi-crobial respiration. Whereas a few studies report higher contributions from root than from microbial respiration (Helal and Sauerbeck, 1992; Thierron and Laudelout, 1996), the microbial component seems to dominate the bulk soil CO2¯uxes in forest soils
(Han-son et al., 2000). In this study, microbial respiration dominated the total soil CO2 ¯ux by >70%. Similar
results with higher contributions from microbial than from root respiration were also observed by Kelting et al. (1998) who separated this microbial component even further (20% of total soil respiration was due to microbial respiration in the rhizosphere, 48% were due to microorganisms in the bulk soil). Killing the root system after clear-cutting followed by herbicide appli-cation (Nakane et al., 1996) as well as using stable car-bon and oxygen isotopes to separate the dierent respiratory ¯uxes (Lin et al., 1999), resulted in mi-crobial respiration rates that were between 50% and 70% of bulk soil respiration. Manipulating litter input, root presence and soil organic matter contents, Bow-den et al. (1993) estimated that only about 33% of total soil respiration was due to root respiration. Although all of these dierent experimental approaches have uncertainties, microbial respiration (not associated with the rhizosphere) appears to rep-resent the dominant fraction of total soil CO2eux in
a wide range of terrestrial ecosystems.
res-piration (33% vs. 67%), supporting the ®ndings with the small collars (<30% vs. >70%). Changes in soil respiration rates after long-term exclusion of roots can be the result of several mechanisms. Soil CO2 eux
might be reduced not only because the root component is lacking, but also because trenching prevents below-ground carbon input for microbial decomposition. Furthermore, soil CO2 ¯ux rates might change due to
a higher soil moisture regime as a result of restricted plant water uptake (Hart and Sollins, 1998). In this study, however, soil moisture remained the same, and during most of the growing season, the duration of root exclusion did not have an eect on soil CO2¯ux
rates, indicating that root respiration in the organic layer was only a minor component of bulk soil respir-ation.
The removal of litter and organic layers in this study generally resulted in a reduction in the soil res-piration rates that was less than 40% (Fig. 6). Thus, the major fraction of the respired CO2 originated not
from organic surface layers, but from mineral hor-izons, probably the Ah horizon (>60%). Similar
results were reported from a temperate deciduous for-est (Edwards and Sollins, 1973) (>60% of total soil respiration originated from deeper mineral horizons) and boreal Canadian and Japanese forests (Mallik and Hu, 1997; Nakane et al., 1997) (between 58% and 74% of the total soil respiration ¯ux originated from mineral soil horizons). Thus, any natural disturbance and land-use change that aects the composition of the soil pro®le will strongly aect soil CO2eux rates.
According to the results of this and others studies, such an eect will be larger if mineral soil horizons were disturbed.
4.4. Annual soil CO2¯ux
A comparison of annual soil CO2eux with annual
litterfall and root net primary productivity estimates supported the partitioning of total soil respiration in root and microbial respiratory ¯uxes. The annual soil CO2 eux for the 47-year old P. abies stand totaled
about 710 g C mÿ2 yrÿ1 (using the exponential equation given in Table 3 with daily averages of soil temperatures in the Of layer at 5 cm depth; data
pro-vided by C. Rebmann, Max-Planck-Institute for Bio-geochemistry, Jena, Germany). Separating this ¯ux into its microbial and root components resulted in >500 g C mÿ2yrÿ1(>70%) and <210 g C mÿ2yrÿ1 (<30%), respectively. Total annual above-ground lit-terfall (including wood) was about 240 g C mÿ2 yrÿ1 (data provided by the Bayreuth Institute for Terrestrial Ecosystem Research, Bayreuth, Germany); annual root net primary productivity of spruce was about 290 g C mÿ2 yrÿ1 (Mund et al., in preparation). Assuming (1) fast turnover rates of root biomass (Schlesinger, 1997),
(2) carbon losses due to soil respiration that are higher than the carbon input due to annual above-ground lit-terfall (Raich and Nadelhoer, 1989; Nadelhoer and Raich, 1992) and (3) negligible contributions from understory root respiration (see methods), 530 g C mÿ2 yrÿ1 are available for microbial respiration 240290 g C/m2 yrÿ1; spruce litter and root carbon inputs). Surprisingly, the soil respiration and litterfall data for this spruce stand fall perfectly within the 95% con®dence interval of the regression between both par-ameters reported by Nadelhoer and Raich (1992). Furthermore, this potential microbial respiratory car-bon loss of 530 g C mÿ2 yrÿ1 compares well to the value of >500 g C mÿ2 yrÿ1 estimated in this study. Furthermore, after accounting for the microbial frac-tion of bulk respirafrac-tion, the remaining 180 g C mÿ2 yrÿ1 710ÿ530 g C mÿ2 yrÿ1) should represent the root component of soil respiration. Again, this value compares well to the <210 g C mÿ2yrÿ1estimated for root respiration (see earlier).
5. Conclusions
The contribution to the uncertainty of regional or landscape estimates of annual carbon ¯uxes from small-scale, spatial variations of soil CO2 ¯uxes in a
watershed seems to be of minor importance. Despite the existence of high within-site variations at any given time, all four spruce stands followed the same seasonal trend, even though they varied in age and stand struc-ture. Variations in soil respiration could be explained using soil temperature only. However, major errors can arise in carbon models from assumptions about the relative contribution of root, microbial, organic and mineral soil CO2¯uxes. These assumptions are
es-pecially important after natural or anthropogenic dis-turbances (e.g., ®re, windthrow, logging), when carbon stocks have been lost, and physical soil parameters have been altered (e.g., depth and density of organic and mineral horizons). Here, microbial respiration may exceed the 70% reported from many ®eld sites, but unaccounted for in most models. Consequently, CO2 ¯ux rates, their response to increased soil
tem-peratures as well as the future potential for carbon sequestration in those soils might be strongly underes-timated in current models.
Acknowledgements
soil temperatures were collected by C. Rebmann, Max-Planck Institute for Biogeochemistry, Jena, Germany. Litterfall data were provided by the Bayreuth Institute for Terrestrial Ecosystem Research (BITOÈK, Bayreuth, Germany).
References
Baldocchi, D.D., Verma, S.B., Matt, D.R., Anderson, D.E., 1986. Eddy-correlation measurements of carbon dioxide eux from the ¯oor of a deciduous forest. Journal of Applied Ecology 23, 967± 975.
Ben-Asher, J., Cardon, G.E., Peters, D., Rolston, D.E., Biggar, J.W., Phene, C.J., Ephrath, J.E., 1994. Determining root activity distribution by measuring surface carbon dioxide ¯uxes. Soil Science Society of America Journal 58, 926±930.
Boone, R.D., Nadelhoer, K.J., Canary, J.D., Kaye, J.P., 1998. Roots exert a strong in¯uence on the temperature sensitivity of soil respiration. Nature 396, 570±572.
Bouma, T.J., Nielsen, K.L., Eissenstat, D.M., Lynch, J.P., 1997. Estimating respiration of roots in soil: interactions with soil CO2, soil temperature and soil water content. Plant and Soil 195, 221± 232.
Bowden, R.D., Nadelhoer, K.J., Boone, R.D., Melillo, J.M., Garrison, J.B., 1993. Contributions of above-ground litter, below-ground litter, and root respiration to total soil respiration in a temperate mixed hardwood forest. Canadian Journal of Forest Research 23, 1402±1407.
Buchmann, N., Guehl, J.M., Barigah, T.S., Ehleringer, J.R., 1997. Interseasonal comparison of CO2concentrations, isotopic compo-sition, and carbon dynamics in an Amazonian rainforest (French Guiana). Oecologia 110, 120±131.
Buchmann, N., Hinckley, T.M., Ehleringer, J.R., 1998. Carbon iso-tope dynamics in Abies amabilis stands in the Cascades. Canadian Journal of Forest Research 28, 808±819.
Burton, A.J., Pregitzer, K.S., Zogg, G.P., Zak, D.R., 1998. Drought reduces root respiration in sugar maple forests. Ecological Applications 8, 771±778.
Conant, R.T., Klopatek, J.M., Malin, R.C., Klopatek, C.C., 1998. Carbon pools and ¯uxes along an environmental gradient in northern Arizona. Biogeochemistry 43, 43±61.
Davidson, E.A., Belk, E., Boone, R.D., 1998. Soil water content and temperature as independent or confounded factors controlling soil respiration in a temperate mixed hardwood forest. Global Change Biology 4, 217±227.
Dieenbach, A., GoÈttlein, A., Matzner, E., 1997. In-situ soil solution chemistry in an acid forest soil as in¯uenced by growing roots of Norway spruce (Picea abies[L.] Karst.). Plant and Soil 192, 57± 61.
Edwards, N.T., Sollins, P., 1973. Continuous measurement of carbon dioxide evolution from partitioned forest ¯oor components. Ecology 54, 406±412.
Fan, S.M., Goulden, M.L., Munger, J.W., Daube, B.C., Bakwin, P.S., Wofsy, S.C., Amthor, J.S., Fitzjarrald, D., Moore, K.E., Moore, T.R., 1995. Environmental controls on the photosynthesis and respiration of a boreal lichen woodland: a growing season of whole-ecosystem exchange measurements by eddy-correlation. Oecologia 102, 443±452.
Fisher, F.M., Gosz, J.R., 1986. Eects of trenching on soil processes and properties in a New Mexico mixed-conifer forest. Biology and Fertilility of Soils 2, 35±42.
Gansert, D., 1994. Root respiration and its importance for the car-bon balance of beech seedlings (Fagus sylvaticaL.) in a montane beech forest. Plant and Soil 167, 109±119.
Goulden, M.L., Munger, J.W., Fan, S.M., Daube, B.C., Wofsy, S.C., 1996. Exchange of carbon dioxide by a deciduous forest: re-sponse to interannual climate variability. Science 271, 1576±1578. Grant, R.F., Rochette, P., 1994. Soil microbial respiration at
dier-ent water potdier-entials and temperatures: theory and mathematical modelling. Soil Science Society of America Journal 58, 1681± 1690.
Hanson, P.J., Wullschleger, S.D., Bohlman, S.A., Todd, D.E., 1993. Seasonal and topographic patterns of forest ¯oor CO2eux from an upland oak forest. Tree Physiology 13, 1±15.
Hanson, P.J., Edwards, N.T., Garten, C.T., Andrews, J.A., 2000. Separating root and soil microbial contributions to soil respir-ation: a review of methods and observations. Biogeochemistry 48, 115±146.
Hart, S.C., Sollins, P., 1998. Soil carbon and nitrogen pools and pro-cesses in an old-growth conifer forest 13 years after trenching. Canadian Journal of Forest Research 28, 1261±1265.
Helal, H.M., Sauerbeck, D., 1991. Short term determination of the actual respiration rate of intact plant roots. In: McMichael, B.L., Persson, H. (Eds.), Plant Roots and Their Environment. Elsevier Applied Science, London, NY, pp. 88±92.
HoÈgberg, P., Ekblad, A., 1996. Substrate-induced respiration measured in situ in a C3-plant ecosystem using additions of C4-sucrose. Soil Biology and Biochemistry 28, 1131±1138.
Horwath, W.R., Pregitzer, K.S., Paul, E.A., 1994.14Callocation in
tree±soil systems. Tree Physiology 14, 1163±1176.
IPCC, 1996. Climate Change 1995. The Science of Climate Change. Cambridge University Press, Cambridge, p. 572.
Kelting, D.L., Burger, J.A., Edwards, G.S., 1998. Estimating root respiration, microbial respiration in the rhizosphere, and root-free soil respiration in forest soils. Soil Biology and Biochemistry 30, 961±968.
Kicklighter, D.W., Melillo, J.M., Peterjohn, W.T., Rastetter, E.B., McGuire, A.D., Steudler, P.A., 1994. Aspects of spatial and tem-poral aggregation in estimating regional carbon dioxide ¯uxes from terrestrial forest soils. Journal of Geophysical Research 99, 1303±1315.
Kirschbaum, M.U.F., 1995. The temperature dependence of soil or-ganic matter decomposition, and the eect of global warming on soil organic matter. Soil Biology and Biochemistry 27, 753±760. Lavigne, M.B., Ryan, M.G., Anderson, D.E., Baldocchi, D.D., Crill,
P.M., Fitzjarrald, D.R., Goulden, M.L., Gower, S.T., Massheder, J.M.M., McCaughey, J.H., Rayment, M.B., Striegl, R.G., 1997. Comparing nocturnal eddy covariance measurements to estimates of ecosystem respiration made by scaling chamber measurements at six coniferous boreal sites. Journal of Geophysical Research 102, 28977±28985.
Lin, G., Ehleringer, J.R., Rygiewicz, P.T., Johnson, M.G., Tingey, D.T., 1999. Elevated CO2 and temperature impacts on dierent components of soil CO2 eux in Douglas-®r terracosms. Global Change Biology 5, 157±168.
Lindroth, A., Grelle, A., Moren, A., 1998. Long-term measurements of boreal forest carbon balance reveal large temperature sensi-tivity. Global Change Biology 4, 443±450.
Lloyd, J., Taylor, J.A., 1994. On the temperature dependence of soil respiration. Functional Ecology 8, 315±323.
Mallik, A.U., Hu, D., 1997. Soil respiration following site prep-aration treatments in boreal mixed wood forest. Forest Ecology and Management 97, 265±275.
Moncrie, J., Valentini, R., Greco, S., Seufert, G., Ciccioli, P., 1997. Trace gas exchange over terrestrial ecosystems: methods and per-spectives in micrometeorology. Journal of Experimental Botany 48, 1133±1142.
Nadelhoer, K.J., Raich, J.W., 1992. Fine root production estimates and belowground carbon allocation in forest ecosystems. Ecology 73, 1139±1147.
Nakane, K., Kohno, T., Horikoshi, T., 1996. Root respiration rate before and just after clear-felling in a mature, deciduous, broad-leaved forest. Ecological Research 11, 111±119.
Nakane, K., Kohno, T., Horikoshi, T., Nakatsubo, T., 1997. Soil carbon cycling at a black spruce (Picea mariana) forest stand in Saskatchewan, Canada. Journal of Geophysical Research 102, 28785±28793.
Norman, J.M., Kucharik, C.J., Gower, S.T., Baldocchi, D.D., Crill, P.M., Rayment, M.B., Savage, K., Striegl, R.G., 1997. A com-parison of six methods for measuring soil-surface carbon dioxide ¯uxes. Journal of Geophysical Research 102, 28773±28777. Pregitzer, K.S., Laskowski, M.J., Burton, A.J., Lessard, V.C., Zak,
D.R., 1998. Variation in sugar maple root respiration with root diameter and soil depth. Tree Physiology 18, 665±670.
Raich, J.W., Nadelhoer, K.J., 1989. Belowground carbon allocation in forest ecosystems: global trends. Ecology 70, 1346±1354. 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.
Raich, J.W., Potter, C.S., 1995. Global patterns of carbon dioxide emissions from soils. Global Biogeochemical Cycles 9, 23±36. Randerson, J.T., Thompson, M.V., Malmstrom, C.M., Field, C.B.,
Fung, I.Y., 1996. Substrate limitations for heterotrophs:
impli-cations for models that estimate the seasonal cycle of atmospheric CO2. Global Biogeochemical Cycles 10, 585±602.
Schimel, D.S., VEMAP Participants, Braswell, B.H. Continental scale variability in ecosystem processes: models, data, and the role of disturbance. Ecological Monographs. 67 (1997) 251±271. Schleser, G.H., 1982. The response of CO2 evolution from soils to
global temperature changes. Zeitschrift fuÈr Naturforschung 37a, 287±291.
Schlesinger, W.H., 1977. Carbon balance in terrestrial detritus. Annual Review of Ecology and Systematics 8, 51±81.
Schlesinger, W.H., 1997. Biogeochemistry. Academic Press, London, NY, p. 563.
Swinnen, J., van Veen, J.A., Merckx, R., 1994. Rhizosphere carbon ¯uxes in ®eld-grown spring wheat: model calculations based on
14C partitioning after pulse-labelling. Soil Biology and
Biochemistry 26, 171±182.
Thierron, V., Laudelout, H., 1996. Contribution of root respiration to total CO2eux from the soil of a deciduous forest. Canadian Journal of Forest Research 26, 1142±1148.
Thuille, A., Buchmann, N., Schulze, E.D., 2000. Carbon pools and soil respiration rates during deforestation, grassland use and sub-sequent spruce aorestation in the Southern Alps, Italy: a case study related to the Kyoto Protocol. Tree Physiology, in press. Witkamp, M., 1969. Cycles of temperature and carbon dioxide
