Soil respiration and soil carbon balance in anorthern hardwood forest ecosystem

T.J. Fahey, G.L. Tierney, R.D. Fitzhugh, G.F. Wilson, and T.G. Siccama

Abstract: Soil C fluxes were measured in a northern hardwood forest ecosystem at the Hubbard Brook ExperimentalForest to provide insights into the C balance of soils at this long-term study site. Soil CO2 emission (FCO 2

) was esti-mated using a univariate exponential model as a function of soil temperature based on 23 measurement dates over5 years. Annual FCO 2

for the undisturbed northern hardwood forest was estimated at 660 ± 54 g C·m–2·year–1. Low soilmoisture significantly reduced FCO 2

on three of the measurement dates. The proportion of FCO 2derived from the forest

floor horizons was estimated empirically to be about 58%. We estimated that respiration of root tissues contributed about40% of FCO 2

, with a higher proportion for mineral soil (46%) than for forest floor (35%). Soil C-balance calculations,based upon evidence that major soil C pools are near steady state at this site, indicated a large C flux associated withroot exudation plus allocation to mycorrhizal fungi (80 g C·m–2·year–1, or 17% of total root C allocation); however, un-certainty in this estimate is high owing especially to high error bounds for root respiration flux. The estimated propor-tion of FCO 2

associated with autotrophic activity (52%) was comparable with that reported elsewhere (56%).

Résumé : Les flux de carbone dans le sol ont été mesurés dans un écosystème forestier de feuillus nordiques à la forêtexpérimentale de Hubbard Brook pour améliorer nos connaissances du bilan du carbone dans les sols de cette stationoù sont menés des travaux de recherche à long terme. Les émissions de CO2 du sol (FCO 2

) ont été estimées à l’aided’un modèle exponentiel univarié en fonction de la température du sol basée sur des mesures prises à 23 dates diffé-rentes pendant 5 ans. La valeur annuelle de FCO 2

pour une forêt de feuillus nordiques non perturbée a été estimée à660 ± 54 g C·m–2·an–1. Une faible teneur en eau du sol a significativement réduit la valeur de FCO 2

pour trois des datesoù des mesures ont été prises. Le pourcentage de FCO 2

provenant des horizons organiques a été estimé empiriquementà environ 58 %. Les auteurs ont estimé qu’environ 40 % de la valeur de FCO 2

provenait de la respiration des racinesavec une plus forte proportion dans le sol minéral (46 %) que dans la litière (35 %). Les calculs de bilan du carbonedans le sol, basés sur des indices que les principaux pools de carbone du sol sont presque à l’état d’équilibre danscette station, indiquent qu’il y a un important flux de C associé à l’exsudation racinaire en plus de l’allocation auxchampignons mycorhiziens (80 g C·m–2·an–1, ou 17 % de l’allocation totale de C aux racines). Cependant, cette estima-tion comporte une grande incertitude particulièrement à cause de la marge d’erreur élevée pour le flux de CO2 relié àla respiration des racines. La proportion estimée de la valeur de FCO 2

associée à l’activité autotrophe (52 %) est com-parable à celle rapportée ailleurs (56 %).

[Traduit par la Rédaction] Fahey et al. 253

Introduction

Carbon plays a critical role in ecological interactions, be-cause it is fundamentally linked to ecosystem energetics andto the cycles of water and mineral nutrients. An upsurge ofinterest in C biogeochemistry has been stimulated by therole of CO2 and CH4 as greenhouse gases. Among the larg-est C fluxes in terrestrial ecosystems is the emission of CO2from the soil surface, often equated with total soil respira-tion (TSR; Raich and Schlesinger 1992). The relative ease ofmeasuring TSR in the field, together with its importance in

the local and global C cycle, explains the large number ofrecent studies reporting TSR in forests (Raich and Schlesinger1992; Valentini et al. 2000). At the outset, however, wepoint out that equating soil CO2 emission with actual TSR isinexact, because some of the CO2 produced in the soil mayleave the site in the form of dissolved inorganic carbon(Kling et al. 1992); hence, throughout this report we utilizethe abbreviation FCO2

in reference to CO2 flux from the soilsurface.

In many forest regions where environmental conditions re-strict the rate of litter decomposition or the distribution of

Can. J. For. Res. 35: 244–253 (2005) doi: 10.1139/X04-182 © 2005 NRC Canada

244

Received 27 April 2004. Accepted 27 September 2004. Published on the NRC Research Press Web site at http://cjfr.nrc.ca on18 February 2005.

T.J. Fahey.1 Department of Natural Resources, Cornell University, Ithaca, NY 14853, USA.G.L. Tierney. Department of Environmental and Forest Biology, SUNY College of Environmental Science and Forestry, 305 IllickHall, Syracuse, NY 13210, USA.R.D. Fitzhugh. Department of Plant Biology, University of Illinois, 505 South Goodwin Avenue, 265 Morrill Hall, Urbana, IL61801, USA.G.F. Wilson. Hubbard Brook Research Foundation, 16 Buck Road, Hanover, NH 03755, USA.T.G. Siccama. Yale School of Forestry and Environmental Studies, Greeley Lab, 370 Prospect Street, New Haven, CT 06511, USA.

1Corresponding author (e-mail: tjf5@cornell.edu).

soil fauna, thick organic horizons have accumulated on themineral soil surface. This observation applies especially tothe soil orders Spodosols and Histosols, which are widelydistributed at high latitudes, and also to Inceptisols and Enti-sols and to other climatic regions (Vogt et al. 1995). Carbontransformations are different in organic horizons than in min-eral soil horizons because of the protection of organic matterfrom microbial degradation in the presence of soil minerals(Tisdale and Oades 1982). Partitioning soil C fluxes betweenorganic and mineral soil horizons is an important challengefor improving our understanding of C biogeochemistry inmany forest ecosystems. Northern hardwood forests of north-eastern United States and eastern Canada typically exhibitthick surface organic horizons with a very high density offine roots (Fahey and Hughes 1994). At the Hubbard BrookExperimental Forest (HBEF) where the present study wasconducted, nearly half of the fine root (<1 mm) biomass andabout 80% of root phosphorus uptake in the northern hardwoodforest is concentrated in the forest floor horizons (Yanai1992; Fahey and Hughes 1994).

Annual C fluxes in and out of the forest floor in theHBEF in the form of litterfall (Gosz et al. 1972), throughfall(Lovett et al. 1996), root growth and turnover (Tierney et al.2001; Tierney and Fahey 2002), heterotrophic respiration(Bohlen et al. 2000), and leaching (Johnson et al. 2000) havebeen measured in detail. Together with studies of forest pro-ductivity and nutrient cycling (Whittaker et al. 1974; Likensand Bormann 1995), these measurements provided a valu-able framework for investigating soil respiration in the HBEF.The goal of the present study was to improve understandingof the C balance in northern hardwood forest soils by quanti-fying soil C fluxes at the HBEF. Our specific objectives were(1) to measure FCO2

and litterfall at a suite of representativesites in and around the experimental watersheds at the HBEFand (2) to partition FCO2

between the forest floor and min-eral soil horizons and between root and heterotrophic respi-ration for the HBEF.

Methods

Study areasHubbard Brook Experimental Forest is a 30-km2 forested

watershed in central New Hampshire (43°56′N, 71°45′W)that has been intensively studied for more than 40 years

(Likens and Bormann 1995). The vegetation is dominated bynorthern hardwood forest comprising predominantly Ameri-can beech (Fagus grandifolia Ehrh.), sugar maple (Acer sac-charum Marsh.), and yellow birch (Betula alleghaniensisBritt.). At the highest elevations in the HBEF, the forest iscomposed of red spruce (Picea rubens Sarg.), balsam fir(Abies balsamea L.), and paper birch (Betula papyriferaMarsh.). Forest age structure is dominated by cohorts thatoriginated following heavy cutting in about 1915 (Likens1985). Canopy height decreases steadily with increasing ele-vation from about 26 m at 400 m to about 16 m at 800 m.The climate is humid continental, with mean temperatures of–9 °C in January and 18 °C in July and with annual precipi-tation of 140 cm evenly distributed through the year (Baileyet al. 2003). A deep snowpack usually develops in Decem-ber and melts in April and prevents significant soil freezingin most years (Fitzhugh et al. 2003). The soils are predomi-nantly highly acidic Spodosols (Typic Haplorthods andFragiorthods) developed on basal till with a thick organichorizon (mean = 70 mm) overlying the mineral soil. Addi-tional details about the HBEF can be found at the HubbardBrook Ecosystem Study website (http://www.hubbardbrook.org).

The present study was conducted primarily at a suite ofintensive research plots (0.5 ha each) in and around thegauged experimental watersheds (Bear Brook (BB) and wa-tershed 1 (W1)) on the south-facing slope of the HubbardBrook valley. The forests and soils of these intensive plotswere representative of the variation exhibited across the top-ographic-elevation gradient in these watersheds as describedby Johnson et al. (2000). Six of the plots were located innorthern hardwood forest, and two plots at the upper eleva-tion were dominated by spruce – fir – paper birch forest (Ta-ble 1). Soils in the latter two plots differed markedly; siteW1-4 occurred on ledges and the soil was a lithic Hemistwhereas site BB-4 had deeper Haplorthod soil. Among thesix northern hardwood plots, typic Haplorthod soils predom-inated except at site W1-3, where a typic Dystrochrept soiloccurred on bouldery glacial till.

Additional measurement sites for the present study in-cluded another typical northern hardwood stand located at500 m elevation between experimental watersheds 4 and 5where fine root dynamics have been quantified (Tierney andFahey 2001, 2002). Size of the coarse woody debris pool(RCWD) was measured in watershed 6 (W6), the biogeochem-

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Fahey et al. 245

PlotElevation(m)

Slope angle(%)

Dominanttree speciesa

Surfacerockiness (%)

Forest floorthickness (cm)

BB-1 525 12 AB–YB–SM 11.0 7.0BB-2 585 15 SM–AB–YB 7.9 4.7BB-3 800 8 AB–YB–SM 10.4 7.0BB-4 790 5 PB–RS–BF 5.8 9.8W1-1 560 6 SM–AB–YB 8.6 6.9W1-2 650 17 AB–SM–YB 6.8 8.9W1-3 750 27 AB–YB–SM 33.8 7.8W1-4 770 10 RS–BF–PB 39.5 10.0

aListed in order of abundance: AB, American beech (Fagus grandifolia Ehrh.); BF, balsam fir (Abies balsamea L.); PB,paper birch (Betula papyrifera Marsh.); RS, red spruce (Picea rubens Sarg.); SM, sugar maple (Acer saccharum Marsh.); andYB, yellow birch (Betula alleghaniensis Britt.).

Table 1. Characteristics of eight study plots in the Hubbard Brook Experimental Forest, New Hampshire,where field measurements were conducted.

ical reference watershed (Likens et al. 1998). Finally, treemortality and deposition of deadwood to the ground weremeasured in permanent plots in northern hardwood forest lo-cated adjacent to intensive plots BB-1, BB-2, and BB-3.

Field measurementsSoil CO2 emission (FCO2

) was measured using a LI-CORsoil respiration chamber (model LI-6000-09) (LI-COR Bio-sciences, Lincoln, Nebraska) and LI-6200 infrared gas ana-lyzer (LI-COR Biosciences, Lincoln, Nebraska) (Norman etal. 1992). Twelve permanent soil collars were positionedrandomly in each plot; the collars minimized disruption ofthe forest floor during measurements while maintaining atight seal. Measurements were conducted on 23 dates duringthe snow-free season (May–November) over 5 years (1998–2002), for a total of 2100 flux measurements. Precautionswere taken to reduce bias in these measurements of FCO2(Davidson et al. 2002). The CO2 concentration was mea-sured in the ambient air adjacent to the collar. Then, thechamber was placed over the collar and allowed toequilibrate for about 1 min. Over the interval of three or fourflux readings, the concentration of CO2 in the headspace ofthe chamber spanned a range from about 40 µmol·mol–1 be-low to about 60 µmol·mol–1 above the ambient atmosphericconcentration near the soil surface, and the average of thesethree or four readings was used. Soil temperature was mea-sured to ±0.5 °C at 5 cm soil depth using a soil probe foreach reading. For a few dates when instrument failure oc-curred, soil temperature data were derived from thermistormeasurements made in association with a soil-freezing study,as detailed by Hardy et al. (2001).

Fine litterfall was measured with a random array of 12 littertraps constructed from dairy crates (trap size = 0.096 m2).Litterfall was collected in late summer (late August), imme-diately following leaf fall (early November), and in springsoon after snowmelt (early May) from 1992 to 1997 in thefour BB plots (Table 1). Litterfall samples were sorted bycomponent (leaves, twigs, fruits, etc.), dried to constant massat 70 °C, and weighed to ±0.01 g. Coarse litter (mostlybranches >2 cm diameter) was collected using five randomlylocated 4.0-m2 quadrats in these plots that were cleared ofwoody litter each year (1994–1997), and the litter was driedto constant mass and weighed to ±0.1 g. In 1978 and 1995,the mass of coarse woody debris (CWD) was measured onW6 using the line intercept method (Warren and Olsen 1964;Van Wagner and Wilson 1976). Six random 100-m transectswere measured and stratified by elevation zone. Details ofthe procedure are described in Tritton (1980). Tree mortality,standing dead, and deadfall were quantified every 2 yearsbetween 1991 and 2001 in 400 permanent plots (10 m ×25 m, each) located between 500 and 750 m elevation in andadjacent to sites BB1, BB2, and BB3. Each tree (≥10 cmDBH) in these plots was measured for species and DBH andclassified as live, standing dead, or fallen. The biomass oflive and dead trees was estimated using allometric equationsdeveloped for the site (Whittaker et al. 1974; Siccama et al.1994). Literature estimates of decay rates of CWD for theHBEF (Arthur et al. 1993) and of standing dead trees in an-other eastern deciduous forest (Onega and Eickmeier 1991)were used to estimate C fluxes from these pools.

Respiration of detached fine roots was measured by acuvette method using the LI-COR respiration chamber andLI-6200 infrared gas analyzer. Fine roots (<1 mm diameter)were collected in a mixed northern hardwood forest locatedin the lower valley of the HBEF at 250 m elevation. Cleanroot samples weighing 0.5 to 2.0 g dry mass were obtainedseparately for forest floor and mineral horizons by gentlywashing the samples under stream flow to remove soil andorganic debris. Samples and chamber atmosphere were keptmoist with tissue paper and misting; also, samples weresealed in the chamber by placing them on a plastic base cap.Measurements were conducted after a 15-min delay to mini-mize respiration due to injury response, and measurementswere completed within 30 min of sample excavation. Rootrespiration measurements were made in late spring, midsum-mer, and autumn 1998. Air temperature in the chamber wasmaintained within 3 °C of ambient soil temperature by ad-justing the time of measurements through the season (e.g.,midsummer measurements were made at dawn). Althoughroot respiration measurements were conducted at atmo-spheric rather than soil CO2 concentrations, recent resultssuggest that measurement CO2 concentration does not sig-nificantly affect tree-root respiration (Burton and Pregitzer2002).

We employed an empirical approach in the field to distin-guish soil respiration in the organic horizons from that inmineral soil by inserting a metal plate horizontally into thesoil (Thierron and Laudelout 1996). These measurementswere conducted in the lower hardwood zone plot adjacent toour minirhizotron site at the HBEF (Tierney and Fahey2002). First, we measured FCO2

using the same approach asdescribed above. Next, a small trench was excavated adja-cent to the FCO2

measurement plot and a sheet steel barrier,about 10 times larger in area than the LI-COR respirationchamber, was inserted horizontally at the organic–mineralsoil interface. Because the barrier caused a change in theCO2 gradient within the organic horizon owing to the elimi-nation of CO2 flux from underlying mineral soil, we allowedan interval of time to elapse before measuring CO2 effluxfrom the organic horizon. The necessary interval was deter-mined empirically in four test cases by frequently repeatedmeasurements, which indicated that about 1 h was sufficientto reach a new steady-state flux (Fig. 1). Subsequently, weused the mean of two to three measurements taken about 1 hafter emplacement of the barrier to estimate forest floorrespiration flux. Fine root and total forest floor mass weremeasured for cores collected from the locations of thesemeasurements. A total of 19 measurements was made on16 May, 6 July, and 3 October 1998.

Analysis and calculationsTo scale the collar measurements of TSR to the plot and

watershed scale, we assumed that FCO2was zero for loca-

tions where boulders or bedrock intersected the soil surfaceand for the area covered by tree-root crowns. The area ofboulder cover in each plot was measured using the line inter-cept method (Canfield 1941). Transects were laid out at reg-ular intervals, and the length intersected by boulders andledges was recorded for 500–1000 m of transect in each plot(Table 1). All values of FCO2

reported herein have been cor-rected for coverage values of rock and tree root crowns.

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246 Can. J. For. Res. Vol. 35, 2005

We estimated average annual FCO2for the two lower hard-

wood zone sites in the untreated watershed (BB-1 and BB-2;Table 1) using the best-fit relationship between soil tempera-ture and FCO2

emission. Linear regression was used to de-velop a univariate exponential function model:

F TCO2

e= β β0

1

where FCO2is soil CO2 emission (µmol·m–2·s–1), β0 and β1

are constants obtained by least squares, and T is soil temper-ature at 5 cm depth. For each sample date, the mean of 12respiration measurements in each plot was used. These mod-els were then applied to long-term, daily mean soil tempera-ture values (1959–1997) collected with thermistors in anearby location at the HBEF (Bailey et al. 2003;http://www.hubbardbrook.org). Although soil CO2 emissionsbeneath the winter snowpack were not included in our re-gression models, field measurements in late November andDecember 1998 at lower hardwood plots were similar tothose predicted by the regression model (0.56–0.98 versus0.64 µmol·m–2·s–1).

A similar approach was taken for fine root respiration.Separate regression models were developed for forest floorand mineral soil fine roots. Long-term soil temperature val-ues for 8 cm depth were applied to equations for forest floorroot respiration equations and those for 15 cm depth formineral soil roots (Bailey et al. 2003). Fine root respirationflux was calculated as the product of long-term average fineroot biomass and fine root respiration rate. Propagation oferror in these estimates was derived by Monte Carlo simula-tions using the statistical distributions for root biomass andrespiration.

For a broader interpretation of patterns of FCO2and soil C

balance across the HBEF landscape, we analyzed data for alleight plots (Table 1). Interpretation of these values was com-plicated by two “treatment” effects: (1) all the sites on W1were treated with a calcium silicate mineral (wollastonite) infall 1999 (Fiorentino et al. 2003) and (2) three sites (BB-3,W1-2, W1-3; Table 1) were severely damaged by an intenseice storm in January 1998 (Rhoads et al. 2002; the lower

hardwood sites were minimally affected by this event). Amixed model (SAS Proc Mixed; SAS Institute Inc. 1996)was employed because of the unbalanced sampling designand to account for the random effects associated with thepermanent sampling collars and years of sampling. Fixed ef-fects in the model included measured soil temperature (5 cmdepth), plot, “treatment” (Ca addition and (or) ice damage),and soil moisture content. Soil moisture was not measureddirectly; however, daily soil water content was estimated us-ing the forest hydrology simulation model, BROOK 90(Federer 1995), which was developed and validated at thisstudy area. The model was run both for the study period(1997–2002) and for long-term (1966–2003) using meteoro-logic data collected at the site (Bailey et al. 2003).

Results

The flux of CO2 from the soil surface (FCO2) varied sea-

sonally as a weak exponential function of soil temperature(Fig. 2), with Q10 values ranging from 2.05 to 2.92 acrossthe plots (Table 2). The mean summer maximum FCO2

valueacross all eight plots and 5 years of measurement was5.25 µmol·m–2·s–1 and always corresponded with the highestannual soil temperatures. The overall mean and median valuesacross all measurements were 2.65 and 2.56 µmol·m–2·s–1,respectively. The results of the mixed model indicated thatthe effects of collar location within stands (i.e., local spatialvariation) and year were highly significant (p < 0.001), andthe rankings of FCO2

values for individual collar locationswere highly consistent across observation dates. In the over-all mixed model, estimated volumetric soil water contentalso significantly affected FCO2

(p < 0.001). Severe droughtconditions on three of the sample dates (21–22 August 2001;15 August and 10 September 2002) were associated with de-

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Fahey et al. 247

Fig. 1. Temporal changes in soil CO2 emission following inser-tion of a barrier to exclude CO2 flux from mineral soil, ex-pressed as a percentage of pretreatment flux. Lines representfour separate trials.

Fig. 2. Flux of CO2 from the soil surface for eight forest stands(Table 1) in the Hubbard Brook Experimental Forest, NewHampshire, in relation to measured soil temperature (5 cmdepth). Each data point represents the mean of 12 measurementsin each stand and the line represents the best-fit exponentialfunction.

pressed FCO2. Omitting these three dates eliminated any sig-

nal of a soil drought effect; in fact, for this subset of data amarginally significant (p = 0.09) reduction of FCO2

wasassociated with high water content. Finally, no effects ofice-storm damage or Ca treatment could be detected (p =0.40).

For purposes of soil C-budget calculations we utilized theexponential function models based on soil temperature fortwo untreated and minimally damaged lower hardwood sites(BB-1 and BB-2; Tables 1, 2). An estimate of uncertaintywas obtained on the basis of confidence intervals around theQ10 values from the mixed models (Table 2). Long-term av-erage soil temperature data (1959–1998) from a forested plotadjacent to these sites were used to calculate annual FCO2

.The three dates for which TSR was depressed by low soilmoisture were omitted from the data set for calculating annualFCO2

. Instead, we applied the hydrologic model, BROOK90(Federer 1995), to 37 years of hydrometeorologic data fromthe site to determine over the long-term the number of dayson which soil moisture content was below the clear thresh-old causing TSR depression; this was 4.4 days/year. Forthose days, the measured TSR was only 57% as high as thevalue predicted by the regressions on soil temperature. Theannual average TSR calculated from soil temperature alonewas reduced, accordingly, by 5 g C·m–2·year–1 to account forsevere drought effects. The resulting long-term estimatedTSR for the lower hardwood zone at the HBEF was 660 ±54 g C·m–2·year–1.

Based upon 19 measurements for which forest floor respi-ration was measured following insertion of a mineral soilbarrier, the proportion of FCO2

associated with forest floorhorizons was 64.6% (±3.2% SE). This percentage was notsignificantly different between the three measurement dates(16 May (75%), 6 July (65%), and 3 October (60%)). Thetrend towards higher values in May probably reflected de-layed warming of deeper soil layers. The proportion of totalfine root biomass (to 25 cm soil depth) that occurred in theforest floor for all these samples (225 g·m–2 or 49.4%) wasslightly higher than that previously observed in the samenorthern hardwood forest at the HBEF (44%; Fahey andHughes 1994). Similarly, the average organic matter content

of the forest floor for these samples (5.84 kg·m–2) wasslightly higher than the forest-wide average (5.41 kg·m–2;Johnson et al. 1995). These results suggest that the metalbarrier was inserted into the soil at a slightly greater depththan is used for our routine separation of forest floor andmineral soil at the HBEF (Federer 1982; Yanai et al. 1999).

Respiration rate of fine roots (<1 mm diameter) rangedfrom 0.23 to 5.61 nmol·g–1·s–1 and increased exponentiallywith temperature for both forest floor and mineral soil roots(Fig. 3). Respiration rates were much higher for forest floorthan mineral soil fine roots, although Q10 values were simi-lar (2.93 and 3.06, respectively).

Long-term fine litterfall flux (mostly foliage, twigs, andfruits) averaged 369 g·m–2·year–1 (±13 SE) in the lowerhardwood zone plots (BB-1 and BB-2) for 1992–1997. Aver-age coarse litterfall flux (branches >2 cm diameter) was30 g·m–2·year–1, but high spatial and annual variation re-duced the precision of this estimate; for example, across6 years of collection a twofold range in this flux was ob-served. The mass of CWD in W6 did not change signifi-cantly between 1978 (1.09 ± 0.22 kg·m–2) and 1995 (0.94 ±0.09 kg·m–2). Over 10 years of measurement (1991–2001),tree mortality added an average of 0.224 kg·m–2·year–1 ofcoarse woody biomass to the pools of standing dead andCWD in the forest west of W6. The estimated biomass ofstanding dead trees exhibited negligible changes over the 10-year interval (1.09 to 1.07 kg·m–2), and about 0.14 kg·m–2 ofwoody biomass was transferred from standing dead to theCWD pool, annually.

Discussion

Our estimate of annual FCO2for the lower hardwood zone

forest at the HBEF (660 ± 54 g C·m–2·year–1) is similar

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248 Can. J. For. Res. Vol. 35, 2005

Site β0 β1 Q10 (CI)Annual C flux(g C·m–2·year–1)

BB-1 0.776 0.094 2.57 (2.46, 2.68) 679BB-2 0.864 0.081 2.25 (2.15, 2.35) 657BB-3 0.567 0.107 2.92 (2.79, 3.05) 564BB-4 0.908 0.106 2.88 (2.78, 2.98) 801W1-1 0.981 0.079 2.20 (2.10, 2.30) 726W1-2 0.917 0.078 2.18 (2.05, 2.31) 673W1-3 0.868 0.072 2.05 (1.94, 2.16) 601W1-4 0.721 0.084 2.32 (2.20, 2.44) 541

Note: Annual CO2–C flux from the forest floor calculated from modelsapplied to long-term average soil temperature (Bailey et al. 2003).

Table 2. Coefficients of univariate exponential models predictingFCO 2

from soil temperature (5 cm depth) and consequent Q10

(with 95% confidence intervals (CI)), all parameters estimatedwith a mixed model using SAS Proc Mixed (SAS Institute Inc.1996).

Fig. 3. Respiration of detached fine roots (<1 mm diameter) in anorthern hardwood forest at the Hubbard Brook ExperimentalForest, New Hampshire, in relation to measurement temperature.Closed circles are for forest floor roots and open boxes for min-eral soil roots, with best-fit exponential functions indicated.

to that for global temperate deciduous forest (647 ± 51 gC·m–2·year–1) reported by Raich and Schlesinger (1992).Goreau (1981) estimated FCO2

for the snow-free period(8 months) in northern hardwood forest at the HBEF at670 g C·m–2, somewhat higher than the current estimate as-suming that an additional 60–70 g C·m–2·year–1 was emittedbeneath the winter snowpack. However, Goreau’s valuewould be comparable with that calculated for another hard-wood site, W1-1 (726 g C·m–2·year–1; Table 2). The range ofestimated annual FCO2

across the experimental watersheds(541–801 g C·m–2·year–1; Table 2) is similar to thatacross six forest stands at nearby Harvard Forest (530–870 gC·m–2·year–1; Davidson et al. 1998), but lower than for fourbroadleaf deciduous forests to the south in Tennessee (740–930 g C·m–2·year–1; Hanson et al. 1993).

Values of FCO2depended strongly on soil temperature,

with Q10 averaging 2.4 ± 0.1 based on plot-level means(Table 2). These Q10 values are within the range observedacross the world’s terrestrial biomes (1.3–3.3; Raich andSchlesinger 1992) but lower than those values observed atthe Harvard Forest (3.4–5.6; Davidson et al. 1998). Part ofthis difference may be attributed to the greater depth of soiltemperature measurements for the Harvard Forest (10 cm)than the present study (5 cm). The Q10 value is also highlysensitive to the method of calculation (Xu and Qi 2001), andour mixed model based upon individual collars resulted inhigher Q10 values (Q10 = 2.7 ± 0.1) than those values in theapproach using plot-level means.

Our statistical analysis indicated significant reductions inFCO2

during severe droughts in late summer 2001 and 2002(early August to mid-September). The levels of volumetricsoil water content predicted by the hydrologic model,BROOK 90 (Federer 1995), during these periods occurredon only 1.2% of the days for a 37-year period of simulation.Several other studies have reported that severe soil droughtreduces FCO2

in temperate broadleaf forest ecosystems(Hanson et al. 1993; Epron et al. 1999; Borken et al. 2002),though the confounding effects of temperature and moistureare notoriously difficult to separate (Davidson et al. 1998).Edwards (1975) and Davidson et al. (1998) have reported areduction of FCO2

at high soil water content, similar to theweak trend in our study; this trend may be attributed in partto physical effects on diffusion.

Significant spatial and annual variability in FCO2were ob-

served across the study area. The between-plot differencescould not be attributed to either Ca treatment or ice-stormdamage because of many intervening factors. Although FCO2tended to decline with increasing elevation (Tables 1, 2), thistrend cannot be regarded as evidence for a simple pattern.Moreover, differences between the conifer-dominated plotsat high elevation and the northern hardwood forest at lowerelevations were not consistent, as one of the spruce–fir–birchplots had the lowest and the other had the highest estimatedannual FCO2

among all the sites (Table 2). More clear wasthe effect of high rock-fragment content (at W1-3 and W1-4;Table 1) in reducing FCO2

on ledges and bouldery sites.We acknowledge potential sources of error in the mea-

surement of FCO2. In a field comparison, Janssens et al.

(2000) observed large differences among four methods ofmeasurement, with the LI-COR chamber yielding much

lower flux estimates than another chamber design, whichmatched the results of Le Dantec et al. (1999). Both studiesattributed the disagreement to differences in air movementwithin the chamber and suggested that the LI-COR chamberused in our study more accurately represented field condi-tions. Most recently, Davidson et al. (2002) indicated thatwhen suitable precautions are taken, underestimates of FCO2with the LI-COR chamber may not be severe. Nevertheless,we emphasize that caution should be exercised in the inter-pretation of FCO2

values in the present study.

Evaluating soil carbon balance at HBEFThe long-term measurements from the HBEF provide an

opportunity to evaluate FCO2in the framework of the soil

and ecosystem carbon balance. For simplicity, in the follow-ing analysis we assume carbon concentration in plant detri-tus is 50% of dry mass. It appears that the detrital pools of Cin the 90-year-old forest at the HBEF are near steady state.For example, the CWD pool on W6 did not change signifi-cantly between 1978 and 1995, although recent changes as-sociated with the intense ice storm of 1998 (Rhoads et al.2002) are likely. Similarly, the biomass of standing deadtrees remained nearly constant from 1991 to 2001. Periodicremeasurements of forest floor organic matter content in themature forest at the HBEF (Yanai et al. 1999) indicate thatover the period 1976 to 2002 the size of this C storage pooldid not change significantly. However, to detect a change atα = 0.05 with the sampling intensity used, the pool size wouldneed to have changed by 23%; hence, a change in organic Ccontent of the forest floor as large as 26 g C·m–2·year–1 cannotbe ruled out (Fahey et al. 2005). Similarly, it is impossible todetect changes in the large mineral soil C pool (Johnson etal. 1995), but for the following analysis we assume that bothof these soil pools currently are at steady state. We presentthe soil C balance in units of kg·m–2·year–1 (Fig. 4) in recog-nition of the low precision and high uncertainty in thesepool-size changes and in some of the flux estimates (e.g., to-tal root allocation and root respiration).

Soil carbon inputsCarbon flux in litterfall, excluding CWD, averaged 198 g

C·m–2·year–1 for the lower hardwood zone over 5 years ofmeasurement. This flux includes our best estimate forbranch litter (15 g C·m–2·year–1), which remains the largestsource of uncertainty in fine litterfall flux because of its epi-sodic nature, associated with unusual weather events (e.g.,ice storms; Rhoads et al. 2002). A relatively small amount ofC is added to the soil surface in the form of canopythroughfall (4.5 g C·m–2·year–1; Lovett et al. 1996), so thattotal C flux to the soil surface (excluding CWD) totals about0.20 kg C·m–2·year–1 (Fig. 4). Annual C flux to the CWDpools from tree mortality averaged 112 g C·m–2·year–1 forthe period 1991–2001. Although this represents a relativelylarge flux of C, its role in our soil C-balance calculations islimited because we avoided locations with obvious CWD inour measurements of TSR. A small fraction of CWD eventu-ally becomes indistinguishable from forest floor, and we es-timate the flux to this highly decayed wood pool to be about0.02 kg C·m–2·year–1. The remainder of C losses from thispool (0.09 kg·m–2·year–1) would be to heterotrophic respira-

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tion (Fig. 4). These observations indicate that CO2 flux fromdecaying wood is about 12% of total carbon flux from soil(i.e., 0.66 + 0.09 = 0.75 kg C·m–2·year–1) at the HBEF. Thisproportion is considerably higher than for an old-growthponderosa pine (Pinus ponderosa Laws.) stand in central Or-egon (about 4% to 5%; Law et al. 2001), probably reflectingprimarily a much lower decay rate of CWD in western coni-fer forests than in eastern deciduous forests (Harmon et al.1986).

Total C allocation to roots (TRA) in forests where majorbelowground C pools are at or near steady state has beenestimated frequently as the difference between FCO2

andaboveground litterfall (Raich and Nadelhoffer 1989). The re-sulting estimate of TRA for Hubbard Brook is about 0.46 kgC·m–2·year–1. This estimate of TRA is comparable withthose for other temperate deciduous forests summarized byRaich and Nadelhoffer (1989).

Soil carbon outputsCarbon fluxes out of the forest floor and mineral soil

occur primarily as CO2, and our empirical measurementsprovide a basis for apportioning these fluxes between auto-trophic and heterotrophic respiration and between forestfloor and mineral soil horizons. We applied the empiricalmodels for fine root respiration derived from our detachedroot measurements (Fig. 3) to the long-term average soiltemperature data (Bailey et al. 2003) and fine root biomassdata (Tierney and Fahey 2001) to estimate respiratory C fluxfor forest floor and mineral soil roots. Annual fine root

(<1 mm diameter) respiration for the forest floor horizonswas estimated to be 118 g C·m–2·year–1 and for the mineralsoil, 90 g C·m–2·year–1. The uncertainty in these estimateswas calculated by Monte Carlo simulation using the statisti-cal distributions for the regression functions of root respira-tion and for fine root biomass. The standard deviationsfor these estimates were relatively large (±44 and ±38 gC·m–2·year–1 for forest floor and mineral soil, respectively),reflecting high variation in both root respiration rates andfine root biomass. For comparison, we applied the regres-sion equations of Burton et al. (1998) developed for sugarmaple in Michigan using measured values of root N concen-trations (Fahey and Arthur 1994) and long-term soil temper-ature and moisture values (Bailey et al. 2003). The resultingestimates were higher: 163 g C·m–2·year–1 for forest floorand 123 g C·m–2·year–1 for mineral soil. These results dem-onstrate that fine root respiration is a key source of uncer-tainty in soil C budgeting.

An additional source of autotrophic respiration is woodyroots, but no measurements of woody root respiration havebeen conducted at the HBEF. We derived woody root respi-ration estimates from the output of a simulation model(PnET-II) that has been developed and validated for theHBEF (Aber et al. 1995). Total root respiration for theHubbard Brook forest predicted by the model was 0.26 kgC·m–2·year–1, which by difference leaves about 0.05 kgC·m–2·year–1 associated with woody roots (>1 mm diameter).This flux was apportioned between forest floor and mineralsoil in proportion to biomass (Fahey et al. 1988). In sum, our

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250 Can. J. For. Res. Vol. 35, 2005

Fig. 4. Soil carbon budget for a northern hardwood forest at Hubbard Brook Experimental Forest, New Hampshire. Boxes indicatepool sizes in kg C·m–2. Arrows indicate flux densities in kg C·m–2·year–1. Legends adjacent to arrows identify the flux process repre-sented; for example, the flux of 0.25 kg C·m–2·year–1 from the forest floor organic matter pool indicates heterotrophic respiration, andtotal soil heterotrophic respiration is the sum of forest floor plus mineral soil respiration (0.25 + 0.15 = 0.40). The flux of 0.10 fromthe coarse woody debris pool (RCWD) is our best estimate of CO2 emission from CWD; this value would be added to TSR (which ex-cluded CWD) to obtain total CO2–C emission (0.66 + 0.10 = 0.76).

current best estimate for root respiration flux from forestfloor is 0.14 kg C·m–2·year–1 and for mineral soil, 0.12 kgC·m–2·year–1 (Fig. 4). Again, we emphasize that these esti-mates must be regarded as tentative, particularly given theuncertainty about the accuracy of field measurements of fineroot respiration (Bouma et al. 1991) and the lack of directmeasurements of woody root respiration. Future attempts atsoil C budgeting should focus on this source of uncertainty.

Our empirical approach indicated that 64.6% ± 3.2% ofsoil CO2 emission was associated with forest floor horizons.We applied this value to our best estimate of FCO2

for thelower hardwood zone (0.66 kg C·m–2·year–1) to apportionthis flux between forest floor and mineral soil. However, wefirst applied a small correction in recognition of the observa-tions indicating that separation of forest floor and mineralsoil differed slightly between our standard soil coring meth-ods and the emplacement of our metal barrier (i.e., higherforest floor mass and fine root biomass were noted for thelatter). Based on the proportional difference for these obser-vations, we reduced our estimate of the proportion of soilCO2 flux from the forest floor to 58%, and this value is usedin our budget calculations (Fig. 4). Gaudinski et al. (2000)apportioned TSR between surface and subsoil horizons usinga 14C-age approach in a broadleaf deciduous forest in Mas-sachusetts and concluded that about 63% of TSR was attrib-uted to O + A + Ap soil horizons. The apparent proportion ofTSR per unit soil C in subsoil horizons in their study wasmuch higher than at the HBEF, probably illustrating bothhigher proportions of subsoil TSR associated with roots andlower amounts of highly recalcitrant mineral soil C at theHarvard Forest than at the HBEF.

Hydrologic transport contributes significantly to C fluxthrough soils at the HBEF (Johnson et al. 2000). Carbontransport from forest floor to mineral soil has been quanti-fied using lysimeters (Johnson et al. 2000) at about 30 gC·m–2·year–1, about 88% in dissolved organic form (DOC).Most of the DOC is retained within the mineral soil by ad-sorption and coprecipitation with Fe and Al (McDowell andWood 1984), with only about 4 g C·m–2·year–1 leaching belowthe Bs horizon (Fahey et al. 2005). Additional deep leachingin the form of dissolved inorganic C results from dissolutionof respiratory CO2, a flux that usually has been ignored inestimates of net ecosystem carbon exchange (Raich andSchlesinger 1992). Based on soil solution measurements, thisflux is estimated at 4 g C·m–2·year–1 (Fahey et al. 2005), fora total hydrologic output of 8 g C·m–2·year–1.

Internal soil C fluxesIn the lower hardwood zone, fine root biomass (to 25 cm

depth) averaged 548 ± 26 g·m–2 over 5 years of measure-ment (Tierney and Fahey 2002). Fine root production andturnover have been estimated for the lower hardwood zoneat the HBEF on the basis of both minirhizotron estimates ofroot longevity and 14C measurements of root age (Tierneyand Fahey 2002). These methods converged on a fine rootturnover rate of 0.35 year–1. Hence, carbon flux associatedwith fine root turnover is about 0.10 kg C·m–2·year–1. Coarseroot turnover has not been measured directly at the HBEF(nor to our knowledge in any forest). We estimated this fluxby assuming that the ratio of aboveground to belowgroundwoody biomass equals the ratio of aboveground to

belowground woody detrital C flux. The resulting value isabout 0.02 kg C·m–2·year–1. Both fine- and coarse-root turn-over were apportioned between the forest floor and mineralsoil in proportion to biomass (Fahey et al. 1988; Fig. 4).

Another significant C input to soil from plants is associ-ated with root exudation, rhizodeposition, and allocation tomycorrhizal fungi (rhizosphere carbon flux (RCF)), but di-rect measurements of RCF are not available. We employed amass-balance approach to provide an estimate of RCF(Fig. 4): TRA is about 0.46 kg C·m–2·year–1, root turnover isabout 0.12 kg C·m–2·year–1, and root respiration is about0.26 kg C·m–2·year–1; hence, by difference C flux to exuda-tion plus mycorrhizal fungi is about 0.08 kg C·m–2·year–1

(Fig. 4). This RCF estimate would increase the proportion ofFCO2

attributed to autotrophic activity to 52%, comparablewith the estimate of 56% for Scots pine (Pinus sylvestris L.)forest in Sweden (Högberg et al. 2001). Phillips and Fahey(2005) estimated RCF by extrapolating measurements of 10-year-old saplings of sugar maple and yellow birch using a13C pulse-labelling approach; their estimate ranged from 5.9%to 12.3% of net C assimilation, which would extrapolate to53–111 g C·m–2·year–1. These values are in the same rangeas estimates for other plants, including trees (Norton et al.1990; Butler et al. 2004). Nevertheless, we emphasize thatour estimate of RCF is subject to high uncertainty. Errors inany of the flux estimates that contribute to our mass-balancecalculation could significantly alter the RCF estimate. Forexample, estimates of fine root turnover in northeastern de-ciduous forest based upon 14C age measurements are consid-erably lower than our estimate (Gaudinski et al. 2001). If Cflux via root mortality is lower than our estimate, then a pro-portionally higher RCF would be indicated.

These empirical measurements and mass-balance calcula-tions allow us to estimate the proportion of soil respirationattributed to live root tissues; overall this value is about 40%with a substantially higher proportion for mineral soil (slightlyover 45%) than forest floor (35%) as would be expected be-cause of litterfall C inputs to the forest floor. Although awide range has been reported for the proportion of soil res-piration attributed to roots, recent studies have suggestedvalues of about 40% to 50% across a range of forests (Hansonet al. 1993, 2000; Nakane et al. 1996; Lee et al. 2003).

The consistency of our budgetary mass-balance estimatescan be evaluated by calculating all the fluxes separately forforest floor and mineral soil horizons (Fig. 4). Utilizing thevalues described above appears to yield reasonably consistentmass balances under the assumption that all the major poolsare near steady state. We include an estimate of particulate Cflux from forest floor to mineral soil (0.01 kg C·m–2·year–1,or 4% of detrital input to the forest floor), a flux that to ourknowledge never has been measured. This tentative soil Cbudget for the northern hardwood forest at the HBEF alsohelps to illustrate the principal constraints on our under-standing of forest ecosystem C fluxes. Our calculations arebased on observations and assumptions that indicate the netecosystem exchange of C at the HBEF is near zero: (1) liveforest biomass (Likens et al. 1998) and CWD have remainednearly constant for the past 20 years; (2) any changes in for-est floor C content have been less than 26 kg C·m–2·year–1

(Yanai et al. 1999); and (3) changes in mineral soil C poolsprobably have been minor (Johnson et al. 1995), though they

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have not been measured. Although our estimates of C allo-cation to roots and to exudation and mycorrhizal fungi mustbe regarded as tentative, they provide an independent confir-mation of the probable magnitude of these fluxes in foresttrees that is consistent with other approaches (Norton et al.1990; Högberg et al. 2001).

Acknowledgements

This research was supported by a grant from the NationalScience Foundation, Long-Term Ecological Research Pro-gram. For their assistance on the research, the authors thankWyatt Hartman, Marian Hovencamp, Rich Phillips, Jess Tabolt,Jacquelyn Wilson, Cindy Wood, and Brian Zimmer.

References

Aber, J.D., Ollinger, S.V., Federer, C.A., Reich, P.B., Goulden,M.L., Kicklighter, D.W., Melillo, J.M., and Lathrop, R.G. 1995.Predicting the effects of climate change on water yield and for-est production in the northeastern U.S. Clim. Res. 5: 207–222.

Arthur, M.A., Tritton, L.H., and Fahey, T.J. 1993. Dead bole massand nutrients remaining 23 years after clear-felling of a northernhardwood forest. Can. J. For. Res. 23: 1298–1305.

Bailey, A.S., Hornbeck, J.W., Campbell, J.L., and Eagar, C. 2003.Hydrometeorological database for Hubbard Brook ExperimentalForest: 1955–2000. USDA For. Serv., Northeast. Res. Stn., Gen.Tech. Rep. NE-305.

Bohlen, P.J., Groffman, P.M., Driscoll, C.T., Fahey, T.J., andSiccama, T.G. 2001. Plant-soil-microbial interactions in a north-ern montane hardwood forest. Ecology, 82(4): 965–978.

Borken, W., Xu, Y-J., Davidson, E.A., and Beese, F. 2002. Site andtemporal variation of soil respiration in European beech, Nor-way spruce, and Scots pine forests. Global Change Biol. 8:1205–1216.

Bouma, T.J., Mielsen, K.L., Eissenstat, D.M., and Lynch, J.P. 1991.Estimating respiration of roots in soil: interactions with soilCO2, soil temperature and soil water content. Plant Soil, 195:221–232.

Burton, A.J., and Pregitzer, K.S. 2002. Measurement carbon diox-ide concentration does not affect root respiration rates of ninetree species in the field. Tree Phys. 22: 67–72.

Burton, A.J., Pregitzer, K.S., Zogg, G.P., and Zak, D.R. 1998.Drought reduces root respiration in sugar maple forests. Ecol.Appl. 8: 771–778.

Butler, J.L., Bottomley, P.J., Griffith, S.M., and Myrold, D.D. 2004.Distribution and turnover of recently fixed photosynthate in rye-grass rhizospheres. Soil Biol. Biochem. 36: 371–382.

Canfield, R.H. 1941. Application of the line-intercept method insampling range vegetation. J. For. 39: 388–394.

Davidson, E.A., Belk, E., and Boone, R.D. 1998. Soil water con-tent and temperature as independent or confounded factors con-trolling soil respiration in a temperate mixed hardwood forest.Global Change Biol. 4: 217–227.

Davidson, E.A., Savage, K., Verchot, L.V., and Navarro, R. 2002.Minimizing artifacts and biases in chamber-based measurementsof soil respiration. Agric. For. Meteorol. 113: 21–37.

Edwards, N.T. 1975. Effects of temperature and moisture on car-bon dioxide evolution in a mixed deciduous forest floor. SoilSci. Soc. Amer. J. 39: 361–365.

Epron, D., Farque, L., Lucot, E, and Badot, P.M. 1999. Soil CO2efflux in a beech forest: dependence on soil temperature and soilwater content. Ann. For. Sci. 56: 221–226.

Fahey, T.J., and Arthur, M.A. 1994. Further studies of root decom-position following harvest of a northern hardwood forest. For.Sci. 40(4): 618–629.

Fahey, T.J., and Hughes, J.W. 1994. Fine root dynamics in a north-ern hardwood forest ecosystem at Hubbard Brook ExperimentalForest, NH. J. Ecol. 82: 533–548.

Fahey, T.J., Hughes, J.W., Pu, M., and Arthur, M.A. 1988. Root de-composition and nutrient flux following whole-tree harvest ofnorthern hardwood forest. For. Sci. 34: 744–768.

Fahey, T.J., Siccama, T.G., Driscoll, C.T., Likens, G.E., Campbell,J., Johnson, C.E., Aber, J.D., Cole, J.J., Fisk, M.C., Groffman,P.M., Hamburg, S.P., Holmes, R.T., Schwarz, P.A., and Yanai,R.D. 2005. The biogeochemistry of carbon at Hubbard Brook.Biogeochemistry. In press.

Federer, C.A. 1982. Subjectivity in the separation of organic hori-zons in the forest floor. Soil Sci. Soc. Amer. J. 46(5): 1090–1093.

Federer, C.A. 1995. BROOK90: a simulation model for evapora-tion, soil water and streamflow. Version BROOK90 [computerprogram]. USDA Forest Service, Durham, New Hampshire.

Fiorentino, I., Fahey, T.J., Groffman, P.M., Eagar, C., Driscoll,C.T., and Siccama, T.G. 2003. Initial responses of phosphorusbiogeochemistry to calcium addition in a northern forest ecosys-tem. Can. J. For. Res. 33: 1864–1873.

Fitzhugh, R.D., Driscoll, C.T., Groffman, P.M., Tierney, G.L.,Fahey, T.J., and Hardy, J.P. 2003. Soil freezing and the acid-basechemistry of soil solutions in a northern hardwood forest. SoilSci. Soc. Am. J. 67: 1897–1908.

Gaudinski, J.B., Trumbore, S.E., Davidson, E.A., and Zheng, S.2000. Soil carbon cycling in a temperate forest: radiocarbon-based estimates of residence times, sequestration rates and parti-tioning of fluxes. Biogeochemistry, 51: 33–69.

Gaudinski, J.B., Trumbore, S.E., Davidson, E.A., Cook, A.C.,Markewitz, D., and Richter, D.D. 2001. The age of fine-root car-bon in three forests of the eastern United States measured by ra-diocarbon. Oecologia, 129: 420–429.

Goreau, T.J. 1981. Biochemistry of nitrous oxide. Ph.D. thesis,Harvard University, Cambridge, Mass.

Gosz, J.R., Likens, G.E., and Bormann, F.H. 1972. Nutrient con-tent of litter fall on the Hubbard Brook Experimental Forest,New Hampshire. Ecology, 53(5): 769–784.

Hanson, P.J., Wallschleger, S.D., Bohlman, S.A., and Todd, D.E.1993. Seasonal and topographic patterns of forest floor CO2efflux from an upland oak forest. Tree Physiol. 13: 1–15.

Hanson, P.J., Edwards, N.T, Garten, C.T., and Andrews, J.A. 2000.Separating root and soil microbial contributions to soil respira-tion: a review of methods and observations. Biogeochemistry,48: 115–146.

Hardy, J.P., Groffman, P.M., Fitzhugh, R.D., Henry, K.S., Welman,T.A., Demers, J.D., Fahey, T.J., Driscoll, C.T., Tierney, G.L.,and Nolan, S. 2001. Snow depth manipulation and its influenceon soil frost and water dynamics in a northern hardwood forest.Biogeochemistry, 56: 151–174.

Harmon, M.E., Franklin, J.F., Sollins, P., Gregory, S.V., Lattin,J.D., Anderson, N.H., et al. 1986. Ecology of coarse woody de-bris. Adv. Ecol. Res. 15: 133–302.

Högberg, P., Nordgren, A., Buchmann, N., Taylor, A.F.S., Ekblad,A., Högberg, M.N., Nyberg, G., Ottoson-Lofvenius, M., andRead, D.J. 2001. Large-scale forest girdling shows that currentphotosynthesis drives soil respiration. Nature, 411: 789–792.

Janssens, I.A., Kowalski, A.S., Longdoz, B., and Ceulemans, R.2000. Assessing forest soil CO2 efflux: an in situ comparison offour techniques. Tree Physiol. 20: 23–32.

© 2005 NRC Canada

252 Can. J. For. Res. Vol. 35, 2005

Johnson, C.E., Driscoll, C.T., Fahey, T.J., Siccama, T.G., andHughes, J.W. 1995. Carbon dynamics following clearcutting of anorthern hardwood forest. In Carbon forms and functions in for-est soils. Edited by W.W. McFee and J.M. Kelly. American Soci-ety of Agronomy, Madison, Wisconsin. pp. 463–488.

Johnson, C.E., Driscoll, C.T., Siccama, T.G., and Likens, G.E.2000. Element fluxes and landscape position in a northern hard-wood forest watershed-ecosystem. Ecosystems, 3: 159–184.

Kling, G.W., Kipphutt, G.W., and Miller, M.C. 1992. The flux ofCO2 and CH4 from lakes and rivers in the arctic Alaska. Hydro-biologia, 240: 23–36.

Law, B.E., Thornton, P.E., Irvine, J., Anthoni, P.M., and Van Tuyl,S. 2001. Carbon storage and fluxes in ponderosa pine forests atdifferent developmental stages. Global Change Biol. 7: 755–777.

Le Dantec, V., Epron, D., and Dufrêne, E. 1999. Soil CO2 efflux ina beech forest: comparison of two closed dynamic systems. PlantSoil, 214: 125–132.

Lee, M., Nakane, K, Nakatsuba, T., and Koizumi, H. 2003. Sea-sonal changes in the contribution of root respiration to total soilrespiration in a cool-temperate deciduous forest. Plant Soil, 255:311–318.

Likens, G.E. 1985. The lake ecosystem. In An ecosystem approachto aquatic ecology: mirror lake and its environment. Edited byG.E. Likens. Springer-Verlag New York Inc., New York. pp. 337–344.

Likens, G.E., and Bormann, F.H. 1995. Biogeochemistry of a for-ested ecosystem. 2nd ed. Springer-Verlag New York Inc., NewYork. pp. 159.

Likens, G.E., Driscoll, C.T., Buso, D.C., Siccama, T.G., Johnson,C.E., Lovett, G.M., Fahey, T.J., Reiners, W.A., Ryan, D.F., Mar-tin, C.W., and S.W. Bailey. 1998. The biogeochemistry of cal-cium at Hubbard Brook. Biogeochemistry, 41: 89–173.

Lovett, G.M., Nolan, S.S., Driscoll, C.T., and Fahey, T.J. 1996.Factors regulating throughfall flux in a New Hampshire forestedlandscape. Can. J. For. Res. 26: 2134–2144.

McDowell, W.H., and Wood, T. 1984. Podzolization: soil processescontrol dissolved organic carbon concentrations in stream water.Soil Sci. 137: 23–32.

Nakane, K., Kohno, T., and Horikoshi, T. 1996. Root respirationrate before and just after clear-felling in a mature, deciduous,broad-leaved forest. Ecol. Res. 11: 111–119.

Norman, J.M., Garcia, R., and Verma, S.B. 1992. Soil surface CO2fluxes and the carbon budget of a grassland. J. Geophys. Res.97: 18 845–18 853.

Norton, J.M., Smith, J.L., and Firestone, M.K. 1990. Carbon flowin the rhizosphere of ponderosa pine seedlings. Soil Biol. Biochem.22: 449–455.

Onega, T.L., and Eickmeier, W.G. 1991. Woody detritus inputs anddecomposition kinetics in a southern temperate deciduous forest.Bull. Torrey Bot. Club, 118: 52–57.

Phillips, R.P., and Fahey, T.J. 2005. Patterns of rhizosphere carbonflux in sugar maple (Acer saccharum) and yellow birch (Betulaallegheniensis) saplings. Global Change Biol. In press.

Raich, J.W., and Nadelhoffer, K.J. 1989. Belowground carbon allo-cation in forest ecosystems: global trends. Ecology, 70: 1346–1354.

Raich, J.W., and Schlesinger, W.H. 1992. The global carbon diox-ide flux in soil respiration and its relationship to vegetation andclimate. Tellus, 44B: 81–99.

Rhoads, A.G., Hamburg, S.P., Fahey, T.J., Siccama, T.G., Hane,E.N., Battles, J.J., Cogbill, C., Randall, J., and Wilson, G.F.2002. Effects of a large ice storm on the structure of a northernhardwood forest. Can. J. For. Res. 32: 1763–1775.

SAS Institute Inc. 1996. SAS/STAT software: changes and en-hancements through release 6.12. Version 6.12. [computer pro-gram]. SAS Institute Inc., Cary, N.C.

Siccama, T.G., Hamburg, S.P., Arthur, M.A., Yanai R.D., Bormann,F.H., and Likens, G.E. 1994. Corrections to allometric equationsand plant tissue chemistry for Hubbard Brook Experimental For-est. Ecology, 75(1): 246–248.

Thierron, V., and Laudelout, H. 1996. Contribution of root respira-tion to total CO2 efflux from the soil of a deciduous forest. Can.J. For. Res. 26: 1142–1148.

Tierney, G.L., and Fahey, T.J. 2001. Evaluating minirhizotron esti-mates of fine root dynamics in a northern hardwood forest. Plantand Soil 229(2): 167–176.

Tierney, G.L., and Fahey, T.J. 2002. Fine root turnover in a north-ern hardwood forest: a direct comparison of the radiocarbon andminirhizotron methods. Can. J. For. Res. 32: 1692–1697.

Tierney, G.T., Fahey, T.J., Groffman, P.M., Hardy, J.P., Fitzhugh,R.D., and Driscoll, C.T. 2001. Soil freezing alters fine root dynam-ics in a northern hardwood forest. Biogeochemistry, 56: 175–190.

Tisdale, J.M., and Oades, J.M. 1982. Organic matter and water-stable aggregates in soils. J. Soil Sci. 33: 141–163.

Tritton, L.M. 1980. Dead wood in the northern hardwood forestecosystem. Ph.D. thesis, Yale University, New Haven, Connecticut.

Valentini, R., Matteucci, G., Dolman, A.J., Schulze, E.-D.,Rebmann, C., Moors, E.J., et al. 2000. Respiration of the maindeterminant of carbon balance of European forests. Nature, 404:861–864.

Van Wagner, C.E., and Wilson, A.L. 1976. Diameter measurementin the line intersect method. For. Sci. 22: 230–232.

Vogt, K.A., Vogt, D.J., Brown, S., Tilley, J.P., Edmonds, R.L., Sil-ver, W.L., and Siccama, T.G. 1995. Dynamics of forest floor andsoil organic matter accumulation in boreal, temperate, and tropi-cal forests. In Carbon and nitrogen cycling in European forestecosystems. Edited by E.D. Schulze. Ecological Studies 142,Springer, Berlin. pp. 159–178.

Warren, S.G., and Olsen, P.F. 1964. A line intersect technique formeasuring logging waste. For. Sci. 10: 267–276.

Whittaker, R.H., Bormann, F.H., Likens, G.E., and Siccama, T.G.1974. The Hubbard Brook ecosystem study: forest biomass andproduction. Ecol. Mongr. 44: 233–252.

Xu, M., and Qi, Y. 2001. Spatial and seasonal variations of Q10 de-termined by soil respiration measurements at a Sierra Nevadaforest. Global Biogeochem. Cycles, 15: 687–697.

Yanai, R.D. 1992. The phosphorus budget of a 70-year-old north-ern hardwood forest. Biogeochemistry, 17: 1–22.

Yanai, R.D., Siccama, T.G., Arthur, M.A., Fereder, C.A., andFriedland, A.J. 1999. Accumulation and depletion of base cationin forest floors in the northeastern United States. Ecology, 80:2774–2787.

© 2005 NRC Canada

Fahey et al. 253