REGULAR ARTICLE

Carbon fluxes in coniferous and deciduous forest soils

Steve Wunderlich & Christoph Schulz &

Winfried Grimmeisen & Werner Borken

Received: 30 September 2011 /Accepted: 30 January 2012 /Published online: 3 March 2012# Springer Science+Business Media B.V. 2012

AbstractAims Our aims were to identify responsible factors forthe site-to-site variability in soil CO2 efflux and toassess the sources of soil CO2 of different forest typeson a regional scale.Methods Soil CO2 effluxes were measured over 1–4 years in four coniferous and three deciduous forestsof Bavaria, Germany, and related to climate, soil prop-erties and forest productivity. Total belowground car-bon allocation (TBCA) was assessed using soil CO2

effluxes and aboveground litterfall. Additionally, CO2

production of organic layers was examined over10 months under constant conditions in an incubationexperiment.Results Annual soil CO2 effluxes were not differentamong the forest sites, but predicted effluxes at agiven temperature of 10°C revealed some significantdifferences and correlated with the phosphorous stockof the organic layers. The incubation study indicated50% faster decomposition of organic layers from de-ciduous than from coniferous forests. TBCA related tosoil CO2 efflux was smaller in the deciduous than in

the coniferous forests. The ratio of TBCA to soil CO2

efflux was positively correlated with the C stock oforganic layers.Conclusions Our results suggest that marked differ-ences in site characteristics have little impact on soilCO2 effluxes at the regional scale, but the contributionof soil CO2 sources varies among the forest types.

Keywords Soil CO2 efflux . Temperate forests .

Litterfall . Belowground carbon allocation . Organiclayer

Introduction

The CO2 efflux of forest soils has been intensivelyinvestigated during the last decades as it represents amajor flux of the C cycle in forest ecosystems(Schlesinger and Andrews 2000). Numerous stud-ies focused on environmental variables controllingthe soil CO2 efflux on different temporal andspatial scales. The most important factors for sea-sonal and interannual variability are soil tempera-ture and soil moisture (e.g., Epron et al. 1999;Subke et al. 2003). In addition to climatic factors,Epron et al. (2004) discussed changes in stand biomassas a major factor of interannual variability of soil CO2

efflux in a beech dominated forest. Interannual variabil-ity of soil CO2 efflux also was closely related to patternsin basal increment of trees, a surrogate for forest pro-ductivity (Irvine et al. 2008).

Plant Soil (2012) 357:355–368DOI 10.1007/s11104-012-1158-y

Responsible Editor: Zucong Cai.

S. Wunderlich :W. Borken (*)Department of Soil Ecology, University of Bayreuth,95448 Bayreuth, Germanye-mail: werner.borken@uni-bayreuth.de

C. Schulz :W. GrimmeisenBavarian State Institute of Forestry,85354 Freising, Germany

In general, the variation of soil CO2 efflux amongforest types on different spatial scales results from inter-acting variables such as climatic conditions, forest pro-ductivity, litter quality, as well as chemical and physicalsoil properties. On a global scale, annual soil CO2 effluxis correlated with annual means of air temperature,precipitation and net primary production (NPP) (Raichand Schlesinger 1992). Annual aboveground litterfallexplained in part the variation of soil CO2 efflux amongforests across different biomes (Raich and Nadelhoffer1989; Davidson et al. 2002). The relationship betweengross primary production (GPP) and soil CO2 efflux inEuropean forests represents a direct link between CO2

fixation by photosynthesis and soil respiration (Janssenset al. 2001). By contrast, temperature is a less reliablevariable for the variation of soil CO2 efflux on theEuropean scale (Janssens et al. 2001).

On the regional scale, however, global or continen-tal relationships might be superimposed by individualsite characteristics. For instance, annual soil CO2 ef-flux in temperate Chinese forests was positively cor-related with both soil organic carbon content and fineroot biomass (Wang et al. 2006). In a Spanish pineforest, mean soil CO2 efflux along an elevation gradi-ent was correlated with the soil C and N stock (Inclánet al. 2010). At constant soil temperature, the C/Nratio, the total P content or organic C content of thetop soil largely account for the variability of soil CO2

efflux in different forest types (Borken et al. 2002;Rodeghiero and Cescatti 2005).

In many managed temperate forests with low soilfertility, thick organic layers represent an important Cstock with relatively short turnover times. The C stockand turnover of organic layers is controlled by a varietyof site-specific factors related to climate, soil properties,tree species/litter quality and forest management. Givensimilar climatic conditions and soil properties, Borkenand Beese (2005) reported higher rates of microbialrespiration in organic layers of pure beech and beechdominated stands than of pure spruce and spruce dom-inated stands. Because of fast turnover and dense rootsystems, thick organic layers emit considerable amountsof CO2 and make a major contribution to total soil CO2

efflux (Borken and Beese 2005; Peichl et al. 2010).Hence, the type of organic layers could also accountfor site-to-site variability of total soil CO2 efflux inforests.

Another reason for the variation of soil CO2 effluxamong different forest sites is possibly the varying

contribution of heterotrophic and autotrophic respira-tion (Subke et al. 2006). Heterotrophic respiration isgenerally defined as CO2 production from decompo-sition of soil organic matter and litter by heterotrophicorganisms whereas autotrophic respiration is oftensummarized as respiration of living roots, mycorrhizalfungi and rhizosphere microorganisms (Högberg andRead 2006; Trumbore 2006). Autotrophic respirationin the soil relies on the belowground translocation andavailability of assimilates by the plants. Under fieldconditions, however, permanent separation of thesesources is difficult without disturbance of the rootsystem or manipulation of the soil water regime (Han-son et al. 2000).

A simple approach by Raich and Nadelhoffer(1989) uses soil CO2 efflux and annual abovegroundlitterfall to assess the total belowground C allocation(TBCA). TBCA comprises all components of autotro-phic respiration (see above) and CO2 released bydecomposition of belowground litter (dead roots, my-corrhizal fungi and rhizosphere microorganisms). Thisapproach assumes steady-state condition for the Cstocks of organic matter, root biomass and microbialbiomass in the mineral soil and organic layer. Thesteady-state assumption is critical as even smallchanges in one of the total C stocks could affect thesoil CO2 efflux. Despite the uncertainties, this ap-proach provides a reliable estimate of TBCA whenthe forest is near steady-state and when measurementscover the interannual variation of soil CO2 efflux andaboveground litterfall (Davidson et al. 2002).

The objectives of our studies were (1) to identifythe responsible factors for the variability in soil CO2

efflux among different forests across Bavaria, Ger-many, (2) to assess the contribution of TBCA to soilCO2 efflux using input by aboveground litterfall, and(3) to determine the CO2 production of organic layersfrom these forest sites under constant temperature andmoisture conditions. We specifically analyzed the Cfluxes in terms of systematic differences between co-niferous and deciduous forests.

Materials and methods

Site characteristics

The seven forest sites are part of a long-term monitor-ing programme and are located in different climatic

356 Plant Soil (2012) 357:355–368

and geological regions of Bavaria, south-east Ger-many, at elevations of 406–1025 m a.s.l. (Table 1).Mean annual air temperature (MAT) ranges between5.5 and 8.2°C and mean annual precipitation (MAP)between 699 and 1357 mm. Norway spruce (Piceaabies, L.) is the main tree species at Ebersberg(EBE), Flossenbürg (FLO), Waldstein (WAL), andScots pine (Pinus silvestris, L.) at Altdorf (ALT). Thestands at Freising (FRE) and Mitterfels (MIT) are dom-inated by European beech (Fagus sylvatica, L.), where-as the stand Riedenburg (RIE) primarily consists ofSessile Oak (Quercus petrea, Liebl.). The age of theforests varies between 91 and 157 years.

The humus form of the coniferous stands is moder ormor-type with typically large stocks of C and N. Except

MIT (moder), the deciduous stands have mull humusform, storing much less C and N in the organic layerthan the coniferous forests. Different subtypes of Pod-zols and Cambisols as well as an Alfisol represent thevariation of soils types. Cation exchange capacity(CECeff) of the mineral soil from 0 to 30 cm depth(0 cm is defined as the interface between the organiclayer and the mineral soil) varies between 73 and231 μmolc g−1. Base saturation of 15–18% indicatescritical supply of K, Mg and Ca at ALT, EBE, FLOandMIT due to base poor bedrock and soil acidification.The latter is indicated by low pH (KCl) ranging from 2.9to 4.4 in the top soil.

Annual wood increment is largest at FRE, RIE(deciduous forests) and EBE (spruce forest) while

Table 1 Characteristics and soil properties of seven forest sites in Bavaria

Site ALT EBE FLO WAL FRE MIT RIE

Longitude 11° 19′ 11° 55′ 12° 24′ 11° 52′ 11° 39′ 12° 53′ 11° 46′

Latitude 49° 25′ 48° 07′ 49° 56′ 50° 08′ 48° 24′ 48° 59′ 48° 56′

Elevation (m a.s.l.) 406 540 840 770 508 1025 475

MAT (°C) 8.0 7.7 6.1 6.2 8.2 5.5 7.9

MAP (mm) 789 992 949 982 847 1357 699

Dominant treespecies

Pinussylvestris

Picea abies Picea abies Picea abies Fagussylvatica

Fagussylvatica

Quercuspetrea

Mean stand age (yr) 107 93 91 141 157 117 118

Soil type HaplicPodsol

HaplicAlfisol

HaplicPodsol

HaplicPodsol

EutricCambisol

DystricCambisol

EutricCambisol

Humus form Mor Moder Moder Mor Mull Moder Mull

Organic layer

Thickness (cm) 7.3 2.9 5.9 9.2 2.0 2.8 1.9

C stock (kg C m−2) 4.2 1.5 3.4 4.5 0.8 1.3 0.7

N stock (g N m−2) 126 56 151 210 28 55 23

P stock(g P m−2) 6.1 3.8 8.9 16.1 2.2 3.1 1.7

C/N ratio 33 27 23 22 28 24 29

C/P ratio 684 386 384 307 363 437 378

Mineral soil (0–30 cm)

Corg stock (kg C m−2) 5.1 6.6 9.6 8.0 2.9 16.0 7.3

Ntot stock (g N m−2) 250 342 395 502 276 915 584

Ptot stock (g P m−2) 48 75 83 104 107 285 116

C/N ratio 19 18 24 18 11 18 12

C/P ratio 126 85 130 79 38 57 68

CECeff (μmolc g−1) 73 86 123 146 115 134 231

BS (%) 16 15 15 35 44 18 91

pH (KCl) 3.1 3.3 2.9 3.6 3.6 3.1 4.4

CECeff effective cation exchange capacity; BS base saturation

Plant Soil (2012) 357:355–368 357

the lowest increment occurred in the nutrient-poorpine stand at ALT (Table 2). Accordingly, stock ofwood is largest at EBE, FRE, and RIE and is lowest atALT (Table 2). Medium stocks of wood are found atFLO, WAL, and MIT. Compared with mean stocks ofwood for respective tree species and stand ages inBavaria (Böswald 1996), stocks at ALT, FLO, WAL,and MIT were 25–38% lower whereas stocks at EBE,FRE, and RIE were 38–75% larger than the average.

Soil CO2 efflux

Soil CO2 efflux was measured following the closeddynamic chamber method combined with infrared gasanalyzers (IRGA) (Gas-Card, Edinburgh Instruments,UK and Li 820, Li-Cor Bioscience, USA). At WAL,nine PVC collars (inner diameter 49.5 cm, height20 cm) were inserted in the organic layer to a depthof about 5 cm on three subplots in the summer of2005. At the other six sites, three identical collars werepermanently installed per study site in the summer of2006. The collars were placed in areas with littleground vegetation. Green vegetation was regularlyclipped and removed from the collars during the grow-ing seasons before each CO2 measurement. A CO2

measurement was carried out by closing the collarwith an opaque lid which was connected to an IRGAvia two 6 mm polyamide tubes. A gas pump (NMP830 KNDC, KNF Neuberger GmbH, Germany) circu-lated headspace air in the closed chamber - IRGAsystem at a constant flow rate of 0.5 L min−1. Theincrease in CO2 concentration of chamber headspacewas measured for 3 to 10 min depending on season.The CO2 concentration was recorded every 10 s by adata logger (Messwert GmbH, Göttingen, Germany).Soil CO2 efflux of each chamber was calculated fromthe change in CO2 concentration per time unit,

headspace volume, headspace air temperature and at-mospheric pressure. For more details on the methodsee (Borken et al. 2006).

Soil CO2 efflux measurements were usually carriedout weekly-biweekly between 8:30 and 13:00 from thesummer of 2006 to January/February of 2011. Theforest stand at MIT was only measured between2006 and 2007 due to logistical problems. Annual soilCO2 effluxes (calendar year) were calculated separate-ly for each chamber by linear interpolation of weekly-biweekly measurements. However, annual soil CO2

efflux for MIT was calculated for 2007 by extrapolat-ing missing CO2 measurements of November andDecember 2007 using soil temperature and the esti-mated parameters of the Arrhenius equation of this site(see below). At EBE, FLO and FRE, missing winterlysoil CO2 effluxes were extrapolated in the same wayfor the period between January and March/April inrespective years. The time periods, for which CO2

effluxes were extrapolated, add up to 19% (2009,EBE), 26% and 37% (2009 and 2010, FLO), 27%(2009, FRE) and 25% (2007, MIT) of the respectiveyears. Because of technical problems, annual CO2

effluxes were not determined for EBE and FRE in2008. Missing winterly soil CO2 effluxes at EBE,FRE, MIT and FLO were predicted using the Arrhe-nius equation:

FCO2 ¼ A�e�Ea=ðR�TÞ ð1Þwhere A is the Arrhenius constant, Ea is the activationenergy (kJ mol−1), R is the universal gas constant(0.0083144 kJ mol−1 K−1), and T is the soil tempera-ture (K) at 10 cm depth. Moreover, the Arrheniusequation was used to calculate standardized soil CO2

efflux rates at a reference soil temperature of 10°C forstandardized comparison of soil CO2 effluxes from allsites. Diminished soil CO2 effluxes during dry periods

Table 2 Forest growth parameters of the study sites in 2009. Wood increment was calculated as the mean increment between 2004 and2009

Site ALT EBE FLO WAL FRE MIT RIE

Stand density (trees ha−1) 667 426 424 308 375 260 501

Mean stand DBH (cm) 23.0 49.8 35.8 41.8 36.7 38.1 30.5

Basal area (m2 ha−1) 27.4 82.8 42.6 42.2 39.7 29.6 36.5

Stock of wood (kg C m−2) 6.8 27.2 11.6 11.3 23.5 10.5 20.8

Wood increment(g C m−2 yr−1)

54 426 193 194 639 245 432

358 Plant Soil (2012) 357:355–368

in the growing seasons were excluded from the Arrhe-nius fitting. Dry periods were defined as periods of10 days or longer with precipitation ≤5 mm and meanair temperature of ≥10.0°C. Overall, between 0%(MIT) and 9% (FRE) of the measured CO2 effluxeswere removed. Soil temperature at 10 cm depth wasautomatically recorded by resistance thermometer(Pt100 sensor).

The accuracy of annual soil CO2 fluxes is restrictedby linear interpolation of weekly-biweekly measure-ments and by prediction of missing winterly measure-ments using the Arrhenius equation and soil temperatureat 10 cm depth. Due to diurnal and seasonal hysteresis ofsoil temperatures, soil temperature at 10 cm does notnecessarily display the optimum for the prediction ofsoil CO2 effluxes. Moreover, mean daily CO2 fluxes areonly approximately estimated by CO2 measurementsbetween 8:30 and 13:00.

Litterfall and total belowground carbon allocation

Aboveground litter was collected monthly in samplers(n08) with an area of 0.25 m2 (50×50 cm) and there-after separated into foliage, twigs and fruits. Afterdrying at 60°C, the litter fractions were weighed,ground and C contents were measured using an ele-mentar analyzer (NA 1500, Carlo Erba, Italy). Dryweights of each litter factions were multiplied by thecorresponding C content and summed to total annualC input by litterfall per m−2. Assuming soil C poolswere near steady state, total belowground carbon allo-cation (TBAC in g C m−2 yr−1) was estimated usingthe carbon budget approach by Raich and Nadelhoffer(1989):

TBCA ¼ FCO2 � LF ð2Þwhere FCO2 is the mean annual soil CO2 efflux(g C m−2 yr−1) and LF is the mean annual litterfall(g C m−2 yr−1). At steady state, TBCA is equivalent tothe sum of rhizosphere respiration and root litter de-composition. Because of a hurricane in January 2007elevated litterfall rates of 2006/2007 at EBE and WALwere excluded from the TBCA approach.

CO2 production of organic layers

In a laboratory experiment, CO2 production of undis-turbed organic layers from all study sites were

measured in a climate chamber at a constant tempera-ture of 20°C over a period of 301 days. For thispurpose, four undisturbed soil columns were takenfrom each study site in May or June of 2007. Poly-acrylic cylinders (inner diameter 17.1 cm, height20 cm) were carefully driven into the forest floor usinga sampling device. After clipping of green vegetationand removal of mineral soil, the organic layers werestored at +5°C for 4 weeks and then repeatedly irri-gated with deionized water up to field capacity beforeCO2 measurements. Irrigation caused no leaching los-ses of dissolved organic carbon (DOC) as the cylin-ders were sealed at the bottom. Hereafter, the cylinderswere installed in an automated and ventilated mes-ocosm system that allowed up to four CO2 mea-surements per mesocosm per day by an IRGA(BINOS 100-4P, Fisher-Rosemount). Water lossesof organic layers by continuous ventilation werecompensated by irrigation with deionized waterevery second week using a syringe with a fine-spraying nozzle. The amount of irrigated waterwas obtained from the mass loss of individualmesocosms due to weighing. For technical detailsand operation of the automated mesocosms systemsee Muhr et al. (2008).

According to the field study, the CO2 productionwas calculated from the linear increase in CO2 con-centration in the headspace of individual mesocosms.The mean daily CO2 production for each mesocosmwas calculated from repeated CO2 measurements perday. Cumulative CO2 production rates over 301 dayswere obtained by summing daily CO2 production ratesand by linear interpolation of missing periods.

After incubation, final C stock of each mesocosmwas determined from the sum of dry weights (dried at60°C) of individual organic horizons multiplied bytheir organic C contents. Initial C stocks were calcu-lated from the sum of final C stocks and cumulativeCO2 production rates. The relative loss of C by min-eralization (in %) was calculated as the ratio of cumu-lative CO2 production after 301 days to the initial Cstock.

Statistical analysis

Mean and standard error of interpolated annual soilCO2 effluxes were calculated from 3 replications perforest site. In case of WAL, the 9 chambers weregrouped in 3 subplots which were treated as replicates

Plant Soil (2012) 357:355–368 359

(n03). One way analysis of variance on rank trans-formed data and post-hoc testing using Tukey’s testwere performed to analyze (1) the site-to-site variationof annual soil CO2 efflux, cumulative CO2 productionas well as relative C loss of organic layers, and (2) theinterannual variability of annual soil CO2 efflux. TheArrhenius equation (1) was applied by linear regressionof log-transformed mean daily soil CO2 efflux rates (n03) and the reciprocal of soil temperatures (1/T in K) at10 cm depth. CO2 efflux rates at 10°C were predictedfor each forest site using the regression equations.Slopes and elevations of the regression lines and pre-dicted soil CO2 efflux rates at 10°C were tested fordifferences among the forest sites by employing a pro-cedure for comparing more than two regression linesincluding multiple comparisons (Tukey’s test) (Zar2010). The 95% confidence interval of predicted soilCO2 efflux at 10°C was calculated based on the uncer-tainty of the linear regression equation (Helsel andHirsch 2002). To test for differences between the conif-erous and deciduous forest stands, the Mann–Whitney-U-test was performed on data of annual soil CO2 efflux(n03), annual aboveground litterfall, TBCA and cumu-lative CO2 production as well as relative C loss of organiclayers. Linear correlation analysis was applied to identifyresponsible parameters for the variability of mean annualCO2 effluxes among coniferous and deciduous forests ordifferent humus forms. Statistical analyses based onmulti-year estimates of soil CO2 effluxes comprised someuncertainties because CO2 efflux at MIT was only mea-sured in 2007. All statistics were computed in SYSTAT12.0.8 (Systat Software, Inc., USA) except the compar-isons of predicted soil CO2 efflux rates at 10°C amongthe forest sites.

Results

Variability of soil CO2 effluxes

Soil CO2 effluxes and soil temperatures at 10 cm depthgenerally followed a typical seasonal pattern at allsites with maxima during summer and minima inJanuary or February (Fig. 1). A long-lasting droughtperiod in the spring of 2008 reduced the CO2 efflux atALT, a site characterized by a sandy soil texture andrelatively small water storage capacity. Naturaldrought periods also had severe effects on the CO2

efflux at RIE, the site with the lowest precipitation.

CO2 effluxes steadily declined in the summer of 2008and 2009 despite elevated temperature. The amount ofprecipitation during the summer months was reducedby about 60% compared to 2007 and 2010. The othersites received more precipitation and were barely af-fected by natural drought periods.

Interannual variability of soil CO2 effluxes wasrelatively small and not significant (p00.23–0.60) al-though mean annual temperature steadily decreased(p00.042) at all sites (except FLO, p00.17) by 1.4–2.2°C from 2007 to 2010 (Table 3). Maximum annualCO2 effluxes occurred only at ALT, WAL and RIE in2007, the warmest and wettest year of these sitesduring the study period. In contrast, the smallest an-nual CO2 effluxes at ALT, EBE, FLO and WAL weremeasured in 2010, by far the coldest year.

Annual soil CO2 effluxes ranged from 487 to758 g C m−2 yr−1 in the coniferous forests and from547 to 715 g Cm−2 yr−1 in the deciduous forests over theentire study period (Table 3). There were no systematicdifferences between coniferous and deciduous forests.The differences within a tree species were of the samemagnitude as among different tree species. For example,the smallest annual soil CO2 effluxes generally occurredin the spruce stand at FLO. Despite similar climaticconditions and a similar soil type, mean CO2 effluxwas 140 g C m−2 yr−1 lower at FLO than at WAL.

Overall, mean annual soil CO2 effluxes were statisti-cally not different among the sites. Neither climaticparameters nor soil or stand properties (Tables 1 and 2)were correlated with annual soil CO2 effluxes of theforest sites.

Using the Arrhenius equation, soil temperatureexplained a large portion of the temporal variabilityin soil CO2 efflux as presented for the pine stand atALT (Fig. 2). The regression was slightly strongerwithout soil CO2 effluxes at dry conditions (r200.89)compared to the regression with all soil CO2 effluxes(r200.86). In the other stands, the r2 of the Arrheniusfitting (without dry periods) varied between 0.75(RIE) and 0.87 (FLO) (not shown). The Arrheniusequation was further used to predict soil CO2 effluxesat a reference soil temperature of 10°C for comparisonof the study sites. Predicted soil CO2 effluxes variedbetween 65 and 100 mg C m−2 h−1 in the coniferousforests and between 69 and 79 mg C m−2 h−1 in thedeciduous forests (Fig. 3a), but again there were nosystematic differences between coniferous and decid-uous forests. The greatest predicted CO2 efflux for the

360 Plant Soil (2012) 357:355–368

spruce forest at WAL coincided with an extraordinari-ly large P stock of 16.1 g m−2 in the organic layer ofthis site (Table 1). Positive correlations were obtainedbetween predicted soil CO2 effluxes at 10°C and the Pstock of the Oe horizon (Fig. 3b, y011.6 x+51.3, r200.77, p00.009) or the total P stock of the organic layer(not shown, r200.72, p00.016). The relationship wasstronger when the two forest stands with mull humus(FRE, RIE) were excluded from the regression(Fig. 3b, y016.9 x+35.4, r200.96, p00.003).

Litterfall and total belowground carbon allocation(TBCA)

Across all years, annual litterfall rates ranged from 111to 667 g C m−2 yr−1 in the coniferous stands and from206 to 447 g C m−2 yr−1 in the deciduous stands(Fig. 4). Annual litterfall was exceptionally great in

the spruce stands at EBE and WAL in the period of2006/07 due to a hurricane in January 2007. Elevatedlitterfall was also observed in the beech stands at FREin 2006/07 and 2009/10 and at MIT in 2009/10 as aresult of intensive fruit production (mast years). With-out these exceptional years, mean annual litterfall wasgreatest in the oak forest at RIE and smallest in thespruce stand at FLO. Overall, mean annual litterfallwas significantly (p00.034) greater in deciduous for-ests than in the coniferous forests.

TBCA was greatest in the pine stand at ALT(513 g C m−2 yr−1) and lowest in the oak stand atRIE (255 g C m−2 yr−1) (Fig. 5a). The ratio of TBCAto soil CO2 efflux was largest in the coniferous standsvarying between 65 and 75%. Deciduous forestsexhibited smaller TBCA/soil CO2 efflux ratios of42–56%. The TBCA/soil CO2 efflux ratio was posi-tively correlated with the C stock of the organic layers

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Fig. 1 Mean (±SE) soil CO2 efflux (filled triangles) and soil temperature at 10 cm depth (open circles) at the study sites from June 2006to February 2011

Plant Soil (2012) 357:355–368 361

(y00.0072 x+45.0, r200.84, p00.004) (Fig. 5b). Inother words, the relative C flux into the root systemincreased with the C stock of the organic layer. Fur-thermore, the TBCA/soil CO2 efflux ratio was nega-tively correlated with mean annual wood increment(y0−0.05x+77.4, r200.58, p00.048) (Fig. 5c).

CO2 production of organic layers

CO2 production of organic layers exponentially de-creased over the entire incubation period of 301 days(Fig. 6). Biweekly wetting events often caused short-

term pulses in CO2 production of different intensity.Initial CO2 production rates ranged from 67 to115 mg C m−2 h−1 in coniferous forests (Fig. 6a) andfrom 64 to 88 mg C m−2 h−1 in deciduous forests(Fig. 6b). The slopes of the CO2 production curves weredifferent for the organic layers from the coniferous forestsand resulted in varying final CO2 production rates. Incontrast, organic layers from deciduous forests exhibitedonly minor differences in final CO2 production rate.

Cumulative CO2 production over 301 days variedbetween 207 and 331 g C m−2 for coniferous forestsand between 145 and 234 g C m−2 for deciduous

Table 3 Soil CO2 efflux (± SE),mean air temperature (T) andprecipitation (P) at the studysites for individual years from2007 to 2010 and their meansover the entire investigationperiod

n.d. not determined

Site Year CO2 efflux T P(g C m−2 yr−1) (°C) (mm)

ALT 2007 758±70 8.1 986

2008 652±60 7.6 612

2009 672±83 7.1 869

2010 643±75 5.9 821

Mean 681±41 7.2 822

EBE 2007 551±89 7.9 988

2008 n.d. 7.8 939

2009 619±109 7.6 996

2010 519±84 6.6 1089

Mean 562±46 7.5 1003

FLO 2007 514±55 6.8 1050

2008 542±72 6.4 803

2009 582±87 6.5 833

2010 487±34 4.9 984

Mean 530±32 6.2 917

WAL 2007 717±63 7.2 1265

2008 658±65 6.9 957

2009 683±59 6.6 972

2010 618±50 5.2 1084

Mean 670±19 6.5 1070

FRE 2007 622±112 8.8 876

2008 n.d. 8.2 792

2009 715±108 7.9 808

2010 690±179 6.8 884

Mean 669±31 7.9 840

MIT 2007 547±54 6.5 1683

RIE 2007 704±92 8.4 879

2008 615±99 8.0 558

2009 548±102 7.7 775

2010 560±76 6.7 786

Mean 607±29 7.7 749

362 Plant Soil (2012) 357:355–368

forests (Fig. 7). The largest cumulative CO2 productionrate was found for the thick organic layer from WAL,whereas the shallow organic layers from FRE and RIEhad the smallest cumulative CO2 production rates. Theinitial C stock of organic layers explained 87% of thecumulative CO2 production (Fig. 7, y00.047x+101,r200.87, p00.006). The N and P stock of the organiclayers were also significantly correlated (N stock: r200.79, p00.008; P stock: r200.67, p00.024) with cumu-lative CO2 production (not shown). Cumulative C lossesin relation to the initial C stocks were 7 to 9% for theconiferous forests and 11 to 13% for the deciduousforests (Fig. 8). With the exception of EBE und RIE,cumulative C losses were significantly (p<0.01) greaterfor the deciduous forests than for coniferous forests.

Discussion

Variability of soil CO2 effluxes

Annual soil CO2 effluxes of 487 to758 g C m−2 yr−1 atour study sites are within the lower range of soil CO2

effluxes in temperate forests (Subke et al. 2006). Weattribute this level to the relatively low temperatureregimes at our sites. Maximum interannual differencesof 93 to 156 g C m−2 yr−1 point to the relevance ofclimatic factors for the seasonal variation of soil CO2

effluxes at the individual sites. Some sites exhibitedmaximum CO2 effluxes in the warm year of 2007 andminimum CO2 effluxes in the cold year of 2010.Although soil temperature explained 75 to 89% oftemporal variation in CO2 efflux, annual CO2 effluxesdid not always follow the decrease in mean annualtemperature between 2007 and 2010. Extendeddrought periods as in spring 2008 have likely counter-acted the effect of elevated temperature on CO2 efflu-xes. Reduced water availability frequently limits therespiration in organic layers and reduces thereby theannual CO2 efflux of forest soils (Borken et al. 2006;Muhr and Borken 2009). The potential of severedrought stress, however, is constrained under the givenclimatic conditions at our study sites.

The site-to-site variability of annual soil CO2 efflu-xes was generally small and not significant. Exclusionof soil temperature by prediction of soil CO2 effluxesat 10°C revealed some significant differences amongthe forest sites. It is interesting that the soil organic Cstock, aboveground litter production or forest produc-tivity did not explain the variability at our sites as

Soil temperature [°C]

-5 0 5 10 15 20

CO

2 ef

flux

[mg

C m

-2 h

-1]

0

50

100

150

200

Fig. 2 Arrhenius function applied to mean soil temperature at10 cm depth and mean soil CO2 effluxes of the pine stand atALT. The solid line refers to all CO2 effluxes (filled and opentriangles) whereas the dashed line excludes CO2 effluxes mea-sured at dry conditions (open triangles)

a

bc b b bc

dcd

b

P stock in the Oe horizon [g P m-2]

1 2 3 4

CO

2 ef

flux

at 1

0 °C

[mg

C m

-2 h

-1]

50

60

70

80

90

100

Mor/ModerMull

ALT EBE FLO WAL FRE MIT RIE

CO

2 ef

flux

at 1

0 °C

[mg

C m

-2 h

-1]

0

30

60

90

120

150 a

Fig. 3 a Soil CO2 efflux at 10°C at the study sites predicted fromthe Arrhenius function and b its relationship to the P stock in theOe horizon. Error bars represent the 95% confidence interval of the

predicted soil CO2 efflux. Different letters indicate significantdifferences of predicted soil CO2 effluxes at α00.05

Plant Soil (2012) 357:355–368 363

reported for other studies (e.g., Davidson et al. 2002;Inclán et al. 2010; Janssens et al. 2001; Raich andNadelhoffer 1989). It seems that these factors are ofminor importance on the regional scale with moderategradients in climate. The sole positive correlation withthe P stock of the organic layers indicates that soil CO2

efflux is partly controlled by the P availability in thesoil. In a previous study, Borken et al. (2002)explained the variability of the soil CO2 efflux in sixtemperate forests with the soil P content. As an essen-tial nutrient of all organisms, phosphate limits not onlythe productivity of trees in temperate forests (Plassardand Dell 2010; Prietzel et al. 2008), but also theactivity and biomass of microorganisms in forest soils(Achat et al. 2010). The P availability is not inevitablycorrelated with the P stock, but it is the result of manyfactors like inorganic and organic forms and the solu-bility of inorganic P minerals. The close relationshipof gross P and gross C mineralization (Achat et al.2010) suggests that the P stock of organic layers is ofrelevance for the P availability in acid forest soils. Incontrast to organic P compounds, P minerals are ofminor importance in acid forest soils as the solubilityof P minerals is small at low pH (Blackwell et al.2010). Hence, the P stock of organic layers couldaffect the soil CO2 efflux directly by the biodegrad-ability of organic matter and by the activity of fineroots and mycorrhiza. Because P availability is limitedin most acid forest soils, trees may compensate for Pdeficiency by forming a dense root system and sym-biosis with mycorrhiza. The thin organic layers (mull)of the deciduous forest stands at FRE and RIE are,however, of minor importance for the P availability inthe soil. Here, the largest part of the P turnover takesplace in the mineral soil. In the other forest stands with

moder or mor, the P stock in the organic layer isassociated with soil CO2 efflux. Given the stock andrelatively fast turnover of organic matter, moder ormor play an important role for both the P and C cyclein respective coniferous and deciduous forests.

ALT EBE FLO WAL FRE MIT RIE

Litte

rfal

l [g

C m

-2 y

r-1]

0

200

400

600

800 2006/07 2007/082008/09 2009/10

Fig. 4 Annual aboveground litterfall at the study sites fromApril to March of the following calendar year

C stock of organic layer [g C m-2]

0 1000 2000 3000 4000 5000

TB

CA

/CO

2 ef

flux

[%]

20

40

60

80

100

Coniferous forestDeciduous forest

Wood increment [g C m-2 yr-1]

0 200 400 600 800

TB

CA

/CO

2 ef

flux

[%]

20

40

60

80

100

a

b

c

ALT EBE FLO WAL FRE MIT RIE

Car

bon

flux

[g C

m-2 y

r-1]

0

200

400

600

800

1000

Deciduous forestConiferous forest

Fig. 5 a Mean (±SE) aboveground litterfall from 2006–2010(hatched bars) and total belowground C allocation (TBCA, un-hatched bars) at the study sites. Relationships between theTBCA/soil CO2 efflux ratio (%) and b the C stock in the organiclayers and c the mean annual wood increment

364 Plant Soil (2012) 357:355–368

CO2 production of organic layers

Soil CO2 effluxes of our forest sites were not correlat-ed with the C stock of the organic layers. Neverthe-less, the linear increase of cumulative CO2 productionwith increasing initial C stocks of the incubated or-ganic layers suggests that the organic layers played aprominent role in the site-to-site variability of soil CO2

effluxes. Based on this linear relationship, organiclayers of spruce and pine forests produce more CO2

by mineralization than those of beech and oak forests.C stocks of organic layers are generally greater underspruce and pine than under oak, beech and birch(Gärdenäs 1998; Borken et al. 2011), indicating thedegradability of litter under field conditions.

Besides the quantity of the C stock, cumulativeCO2 production was additionally affected by the qual-ity of organic matter. Relative C losses of the organic

layers were about 50% greater for the deciduous for-ests than for the coniferous forests. Surprisingly, thedifferences in C losses were small within the twogroups given the variation in the humus form andnutrient contents. In agreement with our finding,Borken and Beese (2005) reported faster turnover ofthe organic layer in a beech stand (5.5 years) than in anadjacent spruce stand (20.6 years). They found inter-mediate turnover times for the organic layers frommixed beech-spruce stands. However, initial decayrates of litter may strongly vary among tree speciesand do not reflect the CO2 production of respectiveorganic layers. A comparison of litter from 14 treespecies revealed no systematic differences in the decayrate between coniferous and deciduous tree species(Hobbie et al. 2006). Klotzbücher et al. (2011) foundeven greater initial decomposition rates for fresh

EBEFLOWAL

ALT

Time period [d]

0 50 100 150 200 250 300

CO

2 pr

oduc

tion

[mg

C m

-2 h

-1]

0

20

40

60

80

100

120 aMIT RIE

FRE

Time period [d]

0 50 100 150 200 250 300

CO

2 pr

oduc

tion

[mg

C m

-2 h

-1]

0

20

40

60

80

100

120 b

Wetting pulses Wetting pulses

Fig. 6 CO2 production of organic layers from a coniferous forests and b deciduous forests incubated at 20°C over 301 days. Arrowspoint to wetting pulses often observed during the incubation after addition of water to compensate water losses

Initial C stock [g C m-2]

1000 2000 3000 4000 5000

Cum

ulat

ive

CO

2 pr

oduc

tion

[g C

m-2 3

01 d

-1]

100

200

300

400

Coniferous forestDeciduous forest

Fig. 7 Relationship between mean (±SE) cumulative CO2 pro-duction rates over 301 days and the initial organic C stock oforganic layers

a

ALT EBE FLO WAL FRE MIT RIE

Loss

of C

[%]

0

4

8

12

16

20 Coniferous forest Deciduous forest

bb b

a

ab

ab

Fig. 8 Mean (±SE) percentage C loss by mineralization referredto initial organic C stock in the organic layer from seven forestsites over 301 days. Different letters indicate significant differ-ences in mean percentage C losses at α00.05

Plant Soil (2012) 357:355–368 365

spruce litter than for fresh beech litter, and similarrates at later stages of decomposition. According toHobbie et al. (2006), differences in microbial litterdecomposition of various tree species is primarilyassociated with the lignin content and secondarily withthe Ca content of litter. Klotzbücher et al. (2011)argued that the degradation of lignin during differentstages of litter decomposition is controlled by theavailability of easily decomposable C compounds.

Aboveground litterfall and total belowground carbonallocation

Mean aboveground litterfall of 160 to 352 g C m−2

yr−1 at our sites (Fig. 5a) corresponds to respectivelitterfall rates of other temperate forests (Raich andNadelhoffer 1989). Annual litterfall was significantlygreater in the deciduous forests than in the coniferousforests, which is in line with other studies (Liu et al.2004; Reich et al. 2005). The difference in annuallitterfall between deciduous and coniferous forests atour sites is associated with differences in the P and Navailability in the mineral soils as indicated by the C/Nand C/P ratio. Given the higher nutrient contents ofbeech and oak litter (not shown), the deciduous forestsoils received more litter of better quality.

We assumed that the organic C stock of the forestsoils is near steady-state on a multi-annual scale. Thisassumption was made because annual accumulation ofsoil organic C in undisturbed and mature forests ismostly small and not detectable by measuring Cfluxes. For example, a mean accumulation rate of only4–8 g C m−2 yr−1 was estimated for the organic layerof the spruce forest at WAL (Schulze et al. 2009).S imi la r ly, smal l accumula t ion ra tes of 2–7 g C m−2 yr−1 were reported for a mixed deciduousforest (Gaudinski et al. 2000) and 12–13 g C m−2 yr−1

for spruce forests (Ågren et al. 2008). In single years,however, the soil C stock may considerably differfrom steady-state conditions due to reduced orenhanced C input or C output. Such deviations oftenoccur as a result of extreme climatic events as thehurricane in January 2007 that more than doubled thelitter input at EBE and WAL.

Exclusion of these exceptional litter input rates indi-cates that TBCA of deciduous forests (255–331 g C m−2 yr−1) is significantly smaller (p00.034)than TBCA of coniferous forests (367–513 g C m−2 yr−1).We postulate that the deciduous forests require less fine

roots including ectomycorrhizal symbionts, and thusless assimilates, for the acquisition of nutrients.The rapid decay of organic matter and fast cyclingof nutrients in the organic layer minimize the costfor nutrient acquisition in many deciduous forests.Conversely, the need for assimilates by the rootsystem for nutrient acquisition is greater in nutrient-poorsoils. Our results are supported by the findings of Osto-nen et al. (2011) who found an increasing ectomycor-rhizal biomass in spruce stands with decreasing Navailability. Ectomycorrhizal fungi are crucial for thenutrition uptake of forest trees growing on nutrient-poor soils as they exploit nutrient resources which arenot accessible for roots.

The largest TBCA occurred at ALT, the sitewith the smallest soil N and P stock and woodincrement. Interestingly, TBCA was also large atWAL, a site with relatively good nutrient supply.In addition to the exceptional litter input, the hur-ricane could have potentially disturbed the soilCO2 efflux in the following years. In the yearbefore the hurricane, however, the soil CO2 effluxamounted to 670 g C m−2 yr−1 (Muhr and Borken2009) which is consistent with the mean CO2

efflux between 2007 and 2010. Perhaps, the soilC budget of the soil is not in steady-state and the mineralsoil act as a net C source through enhanced mineraliza-tion of soil organic matter. Such an imbalancewould explain the large contribution of heterotro-phic respiration to soil CO2 efflux as indicated by radio-carbon signatures of released CO2 (Muhr and Borken2009).

The TBCA/soil CO2 efflux ratios were relativelysmall in our deciduous forests (42–56%) whereas therespective ratios of the coniferous forests (65–75%)were in the range of other studies. An analysis of manyforest types across different biomes revealed meanTBCA/soil CO2 efflux ratios of 70–80% (Raich andNadelhoffer 1989). A systematic difference betweendeciduous and coniferous was not reported so faralthough individual sites differ from this mean range(Bowden et al. 1993; Davidson et al. 2002; Borkenand Beese 2005; Sulzman et al. 2005). The smallTBCA/soil CO2 efflux ratios of our deciduous forestspossibly reflect the relatively good nutrient supply atthese sites. As mentioned before, large nutrient stocksin the mineral soil and fast cycling of nutrients throughdecomposition of leaf litter minimize the cost for themaintenance of the fine root system and mycorrhizal

366 Plant Soil (2012) 357:355–368

fungi. In the coniferous forests, nutrient cycling bylitter decomposition is rather slow and organic matteraccumulates to thick organic layers during successionof the forests. The relationships between the ratio ofTBCA to soil CO2 efflux and the C stock of theorganic layers or wood increment highlight the rele-vance of nutrient availability for belowground Callocation.

Conclusion

Despite the differences in climate, nutrient stocks andproductivity, soil CO2 effluxes were not statisticallydifferent among the forest sites, suggesting that forestsoil CO2 efflux is relatively robust on a regional scalewith small gradients in temperature and precipitation.Exclusion of temperature as a dominant factor ofbiological processes emphasizes the relevance of Pstock and vertical P distribution for soil C cycling atour sites. Our results suggest that the C costs for Pacquisition by roots und soil microorganism increasewith increasing P stock in the organic layer. Accordingto the partitioning approach, the increase in soil CO2

efflux is attributable to an elevated total belowgroundC allocation in coniferous forest soils with thick or-ganic layers. Hence, these coniferous forests havehigher C costs for the acquisition of P and othernutrients than deciduous forests with thin organiclayers. In conclusion, our empirical findings are re-stricted considering the methodological limitationsand the possible correlation of soil CO2 efflux withconfounding variables. Particularly, the relationshipbetween P stock and the soil CO2 efflux need to beverified by systematic investigations.

Acknowledgements The monitoring programme was finan-cially supported by the European Union under the contract No2152/2003 (Forest Focus) until 2006 and afterwards under No614/2007 (LIFE+). We like to thank, Alfred Schubert, DanielWeindl, Dr. Uwe Blum and the team of the Central Laboratoryfrom the Bayerische Landesanstalt für Wald und Forstwirtschaft,Freising, for the comprehensive preparation and chemical anal-ysis of litter and soil samples of the forest sites. Measurements atthe Waldstein were financially supported by the program 562‘Soil processes under extreme meteorological boundary condi-tions’ of the Deutsche Forschungsgemeinschaft (DFG). Weappreciate the contribution of Tim Froitzheim for the laboratoryincubation of organic layers and of Dr. Jan Muhr for providingsoil CO2 effluxes at the Waldstein for the years 2006 and 2007.

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