Agricultural and Forest Meteorology 139 (2006) 344360 www.elsevier.

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Footprint-adjusted net ecosystem CO2 exchange and carbon balance components of a temperate forest
Miklos T. Nagy 1, Ivan A. Janssens, Jorge Curiel Yuste 3, Arnaud Carrara 2, Reinhart Ceulemans *
University of Antwerp, Department of Biology, Research Group of Plant and Vegetation Ecology, Universiteitsplein 1, B-2610 Wilrijk, Belgium Received 24 August 2005; received in revised form 4 August 2006; accepted 7 August 2006

Abstract We combined eddy covariance measurements of CO2 exchange with a suite of ecological methods to construct the carbon balance of a mixed coniferousdeciduous forest in northern Belgium. The CO2 ux measurements were footprint-corrected to eliminate all uxes originating from outside of the study site, and the ecological measurements were up-scaled by weighting the main vegetation types by their relative contribution to the footprint of the CO2 ux measurements. The footprint-corrected annual net ecosystem exchange (NEE) was much lower than previously published u*-corrected NEE. Annual NEE ranged from 1.1 to 1.1 t(C) ha1 year1, and the forest ecosystem was a moderate CO2 sink with a mean annual rate of 0.3 t(C) ha1 year1 over the investigated period (19972002). In 20012002, the mean NEE was 1.0 t(C) ha1 year1. However, despite this net CO2 sink, the forest was losing carbon because carbon export via wood harvesting amounted to 1.2 t(C) ha1 year1. Also in 20012002, gross primary productivity (GPP) calculated from the eddy covariance data was estimated to be 10.4 t(C) ha1 year1. Thus, of the photosynthetically absorbed CO2, 90% was offset by respiration by plants and heterotrophs. The net primary production (NPP) in the effectively contributing forest ecosystem amounted to 5.55.8 t(C) ha1 year1. Therefore, the NPP/GPP ratio was slightly higher than the previously assumed xed ratio of 0.47. These results highlight the importance of including management-related carbon uxes and of applying footprint corrections in carbon-balance studies. # 2006 Elsevier B.V. All rights reserved.
Keywords: Carbon balance; Net ecosystem exchange; Footprint corrections

1. Introduction The increasing atmospheric CO2 concentration and subsequent climate change have drawn the attention of
* Corresponding author. Tel.: +32 3 820 2256; fax: +32 3 820 2271. E-mail address: Reinhart.Ceulemans@ua.ac.be (R. Ceulemans). 1 Present address: University College Dublin, School of Biology and Environmental Science, Beleld, Dublin 4, Ireland. 2 Present address: Fundacion CEAM, Parque Tecnologico, Calle Charles R. Darwin, Paterna (Valencia) SP-46980, Spain. 3 Present address: University of California-Berkeley, Ecosystems Science Division, Department of Environmental Science Policy and Management, 137 Mulford Hall, Berkeley, CA 94720-3114, USA. 0168-1923/$ see front matter # 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.agrformet.2006.08.012

scientists worldwide on the carbon cycle. Hence, many studies aim to determine the carbon balance of terrestrial ecosystems at local to global scales, and to predict changes herein under different climatic conditions (Prentice et al., 2001). The net carbon balance of an ecosystem is the result of several carbon ows that act simultaneously, but often respond in contrasting ways to changes in environmental factors (Goulden et al., 1996). Moreover, spatial differences in species composition, age, and management practices contribute to the complexity and make the interpretation as well as the spatial and temporal up-scaling very difcult.

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The eddy covariance technique offers an independent and useful tool to complement chamber-based CO2-ux measurements. This technique, originally proposed by Swinbank (1951), allows measuring the net ecosystem CO2 exchange (NEE) between ecosystems and the atmosphere directly (Desjardins, 1985; Verma et al., 1986; Baldocchi et al., 1988; Falge et al., 2001). The eddy covariance technique became widely applied only in the second half of the 1990s; therefore the length of most long-term data sets averages around 7 or 8 years (Valentini et al., 2000). When NEE, chamber-based CO2-ux measurements, and eld measurements of biomass growth, litter production, etc. are assessed simultaneously, the carbon balance of an ecosystem can be determined in great detail. Moreover, the constructed carbon balance becomes more reliable, because these independently collected measurements provide mutual constraints. However, before eddy covariance-based uxes can be compared to up-scaled ecological measurements, two major difculties have to be overcome: (1) The eddy covariance measurements must originate from the ecosystem under investigation. (2) We have to be able to correctly identify the surface area that is actually measured by the eddy covariance technique. This area is commonly referred to as footprint and changes with wind direction, wind speed and stability (Schmid, 1997). An accurate comparison of eddy covariance and other ecological measurements thus requires both footprint correction of the eddy ux data set (to exclude all uxes originating from outside of the ecosystem under study) and up-scaling of the ecological measurements in different areas proportional to their relative contribution to the footprint of the eddy covariance system. The eddy covariance technique can be deconvoluted into its main contributing uxes: gross primary productivity (GPP) and total ecosystem respiration (TER; Falge et al., 2002; Carrara et al., 2004). Waring et al. (1998) reported that in forest ecosystems net primary productivity (NPP) is proportional to GPP (approximately 50%). However, in their study, gross primary productivity was not measured but estimated indirectly. Although the assumption of a constant NPP to GPP ratio has been applied in stand growth-models with promising results (e.g., Battaglia and Sands, 1997; Landsberg and Waring, 1997), other studies questioned kela and Valentine (2001) suggested this assumption. Ma that a signicant decline in the NPP to GPP ratio with tree size or age seems highly probable, especially in

even-aged forests. Other ecosystem models suggested that the NPP to GPP ratio is not constant, but is conned to a narrow range (Thornley and Cannell, 2000). Nonetheless, all of these studies agreed that the assumption of a xed NPP to GPP ratio needs verication (or rejection) in studies where both NPP and GPP are measured independently within the same ecosystem. Previous analyses of the 6 years long eddy covariance dataset (Carrara et al., 2004) suggested that this study site uctuated between a negligible CO2 sink and a moderate CO2 source, but these analyses were not footprintcorrected nor compared with independent ecological measurements. The main objectives of this study are therefore: (1) to construct a detailed footprint-adjusted carbon balance of a mixed, temperate forest ecosystem for the period 20012002; and (2) to test the hypothesis of a constant NPP to GPP ratio, by comparing eddy covariance-based GPP estimates with independent NPP estimates scaled-up to the same footprint area. 2. Materials and methods 2.1. Site description The study site is a mixed coniferous/deciduous forest located in Brasschaat in the Belgian Campine region (518180 3300 N, 48310 1400 E). The site is a level-II observation plot of the European ICP-Forests network (International Cooperative Programme on Assessment and Monitoring of Air Pollution Effects on Forests in the ECE-Region, UNEP-UN/ECE) and is also part of the CARBOEUROPE ux towers network (Valentini et al., 2000). The landscape is a coastal plain at a mean elevation of 16 m and is almost at (slope <0.3%). The climate is temperate maritime with a mean annual temperature of 9.8 8C and 750 mm of annual precipitation. The soil is loamy sand, moderately wet, with a distinct humus and iron B-horizon (Baeyens et al., 1993), and is classied as Umbric Regosol (FAO classication; Roskams et al., 1997). A clay layer lies below the upper sandy layer at a depth of 1.52 m. Due to this clay layer, the site has poor drainage, and groundwater depth usually is between 1.2 and 1.5 m (Baeyens et al., 1993). A more detailed description of the physical and chemical description of the soil is available (Janssens et al., 1999; Neirynck et al., 2002). This relatively small (150 ha) forest consists of many mono-specic patches of different coniferous and deciduous species, with a variety of under storey species as well. Scots pine (Pinus sylvestris L.) covering about 80% of the coniferous plots and pedunculate oak (Quercus robur L.) also covering 80% of the deciduous

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plots, are the dominant over storey species. The undergrowth is dominated by black cherry (Prunus serotina Ehrh.), rhododendron (Rhododendron ponticum L.) and grass (Molinia caerulea L. Moench). A more complete description of the forest, with vegetation composition of the various patches has been previously published (de Pury and Ceulemans, 1997; Janssens et al., 2000). The forest stands in the investigated area were relatively even-aged and had similar characteristics. The Scots pine stands were all planted in 1929 and were characterized by a mean stand density of 361 trees ha1, mean tree height of 21.4 m, mean diameter at breast height (DBH) of 0.29 m and mean stem basal area of 24 m2 ha1. The pedunculate oak stands were slightly younger (planted in 1936) and had a mean stand density of about 310 trees ha1, mean tree height of 17.2 m, mean DBH of about 0.24 m and stem basal area of 14 m2 ha1 (Curiel Yuste et al., 2005b; Xiao et al., 2003). The area-weighted maximum leaf area index (LAI) for the entire forest, including both over and under storey LAI was about 3 m2 m2 (Gond et al., 1999). This managed forest is bordered by urban area on the north and west, and by rural area (mostly forested terrain) on the south and east sides (Fig. 1). The shortest fetch (about 500 m) to the measuring tower is in the western sector and a larger fetch (1000 m) is toward the east side. The main wind direction at the site is

southwest, the roughness length of the forest is about 1 m and the zero plane displacement is 19.2 m (Carrara et al., 2003). 2.2. Instrumentation and measurements The net carbon dioxide exchange between the forest ecosystem and the atmosphere was calculated from turbulence measurements on top of a 40 m tall ux tower located in the experimental forest (Fig. 1) using the eddy covariance technique. The instrumentation on the ux tower included a three-dimensional sonic anemometer (Model SOLENT 1012R2, Gill Instruments, Lymington, UK) for wind speed, wind direction and temperature measurements, and an infrared gas analyzer (IRGA) (Model LI-6262, LI-COR Inc., Lincoln, NE, USA) for CO2 concentration measurements. The data were logged at 20.8 Hz and uxes were computed in real time using the EDISOL software (Moncrieff et al., 1997) and stored as half-hourly values. More detailed information can be found in Carrara et al. (2003, 2004). Continuous meteorological measurements were carried out with additional instruments on top of the tower. The measured parameters were global radiation (pyranometer, Kipp and Zonen, type CM6B, Delft, The Netherlands), net radiation (REBS 07, Seattle, WA, USA), photosynthetically active radiation (PAR quantum

Fig. 1. Aerial photo of the surroundings around the eddy covariance tower. ( ) Indicates the location of the tower, () indicates the administrative border of the forest, (- - -) indicates the approximate border of the wind sectors.

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sensor, JYP-1000, SDEC, Tours, France), precipitation (tipping-bucket rain gauge, Didcot DRG-51, Didcot Instrument Co. Ltd., Abingdon, UK), relative humidity and temperature (psychrometer, Didcot DTS-5A, Abingdon, UK). The measured data were stored as half-hourly means on a data logger (Campbell CR 10, CSI, Logan, UT, USA). Temperature in the soil was measured at 2 and 9 cm depth (Didcot DPS-404, Abingdon, UK). More details about the instruments and methods can be found in Overloop and Meiresonne (1999), Kowalski et al. (2000), and Carrara et al. (2003). 2.3. NEE calculations

2.4. Footprint analysis and database correction Our footprint calculation is based on the work of Rebmann et al. (2005). In that study, the results of the footprint calculations were associated with the quality assessment of turbulent ux data. Rebmann et al. (2005) provided for each of the investigated CARBOEUROFLUX sites three two-dimensional matrices corresponding to three different stability classes: stable conditions (j > 0.0625), neutral conditions (0.0625 < j < 0.0625) and unstable conditions (j < 0.0625). The stability parameter j was calculated as: j zm d L (1)

The calculation of eddy covariance uxes and the processing of data correction were made according to the guidelines of the standard EUROFLUX methodology (Aubinet et al., 2000). The calculations and ux analyses for the forest over the period 19972002 were carried out and discussed in detail in two earlier publications (Carrara et al., 2003, 2004). In these papers, however, data were not selected based on a footprint analysis.

where zm is the observation height (42 m), d the zero plane displacement (20 m) and L is the Obukhov-length (Wyngaard et al., 1971). The grid cells of the matrices represent 150 m 150 m squares surrounding the tower and the value of each cell shows its relative contribution to the total ux (Rebmann et al., 2005). The three footprint maps for our study site are shown in Fig. 2. It is obvious from these

Fig. 2. Spatial contribution to the total ux in case of different quality classes of turbulent ux data as: stable conditions, when j > 0.0625; neutral conditions, when 0.0625 > j > 0.0625; unstable conditions, when 0.0625 > j. j is the stability parameter of the atmospheric conditions. The corrected footprint was obtained by applying differently strict thresholds for j in different wind sectors (see Section 2).

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graphs, that under stable conditions the majority of the uxes originate from outside of the studied area, while under unstable conditions uxes originate from within the forest boundaries. Thus, we selected our data set as follows: The surroundings around the ux tower were divided into 12 wind sectors (about 308 range each) (Fig. 1). In a few sectors all data were rejected either because of an insufcient fetch or an undesired vegetation type (e.g. grassland, or recently afforested area; Table 1). In each of the remaining wind sectors all data obtained under stable conditions were rejected. In these sectors, different j thresholds were applied according to the fetch in that direction. Where the fetch was large enough, also uxes obtained under neutral conditions were maintained. Where the fetch was intermediate, the j threshold was set at 0 (Table 1). Where sector borders split a matrix cell, the matrix values were divided proportionally to the area of the matrix cell within each wind sector. The use of different j thresholds depending on available fetch and vegetation composition modied both the footprint and the ux data set, and the resulting uxes were more representative for the investigated forest. We were afraid that eliminating data obtained under stable conditions would induce a systematic bias, but we did not observe substantial association between weather patterns and stability. Hence, we assume that this lter induced no systematic bias in the data. 2.5. Gap lling and annual NEE The gap lling method applied on this j-modied data set was based on the gap lling procedures recommended by Falge et al. (2001). The data set of each year was separated into two-monthly periods (JanuaryFebruary; MarchApril; . . .) and nonlinear regressions tted to the data. Daytime and nighttime data were analyzed separately.

Daytime data were sorted in 5 8C-wide temperature classes and light response functions were evaluated using a modied form of the MichaelisMenten equation (Michaelis and Menten, 1913), with the same modication as in Carrara et al. (2003): F NEE a 0 Rg F RE;day 1 Rg =1000 a0 Rg =F GPP;opt (2) where F NEE is the daytime ux (mmol CO2 m2 s1), a0 the ecosystem quantum yield (mmol CO2 J1), Rg global radiation (W m2), F GPP,opt the optimum gross primary production (mmol CO2 m2 s1) at a Rg value of 1000 W m2 and F RE,day is the ecosystem respiration during the daytime (mmol CO2 m2 s1). To evaluate the temperature response of nighttime CO2 uxes, we tted the following exponential function to the data: F RE;night r 0 ebT (3)

where F RE,night is the nighttime respiration (mmol CO2 m2 s1), b the tted temperature sensitivity parameter, T air temperature (8C) and r0 is the ecosystem respiration (mmol CO2 m2 s1) at 0 8C. Gaps of more than 2 weeks long were lled using non-linear regressions (with T for F RE,night and with Rg for F NEE) created from 6 years pooled data of the same period of other years. The annual rate of net carbon ecosystem exchange (NEE) (t(C) ha1 year1) was calculated from the gap lled half hourly CO2 ux data F NEE and F RE,night (mmol m2 s1). 2.6. Total ecosystem respiration Total ecosystem respiration (TER) was estimated based on the assumption that dark respiration during nighttime and daytime follow the same temperature response. Nighttime respiration responses to air

Table 1 Criteria for dismissing CO2 ux data in different wind sectors of the forest Wind sector 0298 302098 2102408 2413008 3013328 3333598 Criterium of applied data No data j < 0.0625 j<0 No data j < 0.0313 No data Reasons Extensive grassland in the sector Moderately short fetch (600 m) Less than 500 m fetch and undesired vegetation Moderately short fetch (600 m) Extensive grassland in the sector

Criteria were determined on the basis of the stability parameter (j) of the CO2 ux data, as well as on the vegetation type and the available fetch in each sector.

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temperature were tted in two-monthly periods. The temperature response was determined from the parameters of Eq. (3), and the daytime half-hourly mean air temperature was then substituted into the equation to obtain the daytime respiration ux. Annual TER (TER) was nally obtained as: T ER
6 X Rnighttime Rdaytime k k 1

(4)

where Rnighttime and Rdaytime are the two-monthly sums of nighttime and daytime respiration values, respectively, and k indicates a bimonthly period. Because our objective was to compute the carbon balance for the 20012002 period, TER values for 2001 and 2002 were computed separately and subsequently averaged. 2.7. Gross primary production Annual rate of gross primary production (GPP = GPP) was obtained from the equation: GPP T ER N EE (5)

by the geographic distribution of vegetation types. As the relative occurrence of different wind directions and wind speed varied seasonally and inter-annually, also the vegetation measured by our eddy covariance system varied seasonally and inter-annually (Table 2). For a more reliable assessment of the ecosystem represented by our data set, we therefore computed the effectively contributing ecosystem in which the contribution of the different vegetation types varied seasonally and inter-annually. This effectively contributing ecosystem method was applied to determine not only the vegetation composition of the ecosystem represented by the eddy ux data set, but also for the spatial upscaling of all other ecological measurements. 2.10. Net primary production, litter fall, biomass Detailed inventories of standing biomass were made in one representative oak and one representative Scots pine stand in the winters of 20002001 and of 20032004. We assume that these plots were representative for all other pine and oak plots. Because all other plots were of similar age and the soil is relatively homogeneous, this assumption was not unreasonable. Because oak and Scots pine represented the vast majority of the over storey composition, we further assumed that all other deciduous or coniferous species had similar growth rates. The estimate of the carbon stored in the standing biomass reported in the carbon balance represents the calculated winter 2001/2002 condition. Thus, the deciduous species were calculated without foliage biomass, and both oak and pine biomass were calculated with ne root biomass measured and repo no pka rted for February 2003 in both stand types (Ko et al., 2005). Annual net primary production (NPP) was calculated by combining changes in standing biomass, litter fall and ne root productivity over the period concerned. Productivity of stems was determined with two different methods: (1) by establishing allometric relationships between stem biomass and diameter at breast height (DBH; Curiel Yuste et al., 2005a). The difference in standing stem biomass between repeated forest inventories (2000, 2001, 2003) was then assumed as stem NPP. (2) with species-specic growth tables (Jansen et al., 1996). These yield tables are empirical tables used by forest managers to estimate aboveground wood volume and current wood increment in standing forests. As soil and other environmental factors determine productivity of a forest tree species at a specic location, several yield classes (ranging from optimal to

GPP for the reconstructed carbon balance was calculated as the mean of the GPP values of 2001 and 2002. 2.8. Effect of footprint correction on NEE An earlier NEE estimate was produced for this forest over the 19972002 period by Carrara et al. (2003, 2004), where uxes were not discarded based on footprint criteria, but on a friction velocity (u*) threshold of 0.2 m s1. The difference between this earlier and our current NEE estimate was analyzed statistically as follows. Two-monthly NEE values were calculated for both u*- and footprint-corrected uxes. Daytime and nighttime NEE were addressed separately. Differences between the u*- and footprint-corrected data sets were tested for signicance with a t-test at the P < 0.05 level. 2.9. The effectively contributing ecosystem (footprint weighted) The forest ecosystem surrounding an eddy ux tower is hardly ever perfectly homogeneous. Species composition and leaf area index usually differ in different areas around the tower. Therefore, the ecosystem that is effectively inuencing the eddy covariance system is determined by turbulence characteristicsand

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Table 2 Annual and seasonal variation in the vegetation composition of the footprint-weighted ecosystem Over storey Under storey Annual variation 1997 1998 1999 2000 2001 2002 Seasonal variation Months 12 Months 34 Months 56 Months 78 Months 910 Months 1112 Pinus sylvestris Other coniferous Quercus robur Other deciduous Grass P

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Prunus Rhodo Molinia Org. lay. Total Prunus Molinia Org. lay. Total Prunus Rhodo Endemic Org. lay. Total Prunus Org. lay. Total 31.6 32.7 30.0 35.0 29.4 29.1 39.8 32.3 29.7 31.2 33.0 25.3 6.1 4.8 4.5 4.8 4.5 4.3 3.2 4.8 4.8 4.8 4.8 6.0 4.4 10.9 8.9 10.7 8.8 10.8 11.2 7.1 10.0 11.5 11.5 9.2 10.7 11.0 10.7 10.2 9.7 9.4 9.7 9.6 6.6 9.6 9.8 9.5 9.8 12.4 9.7 59.3 56.6 54.8 58.0 54.5 54.2 56.7 56.7 55.8 57.0 56.9 54.3 54.4 2.6 2.4 2.9 2.0 2.7 3.6 2.3 2.6 2.5 2.3 2.8 3.5 3.1 0.5 0.3 0.7 0.5 0.7 0.5 0.4 0.5 0.7 0.6 0.4 0.5 0.6 9.8 10.7 10.7 9.4 11.1 12.5 9.9 10.7 11.1 11.7 9.7 10.9 11.8 13.0 13.4 14.2 11.9 14.6 16.5 12.6 13.7 14.4 14.6 12.9 14.9 15.5 8.1 8.6 8.6 9.3 7.6 7.3 10.1 8.2 7.6 7.6 9.6 7.1 7.4 1.6 1.5 2.0 1.5 2.0 1.9 1.5 1.7 2.0 1.8 1.6 1.9 2.0 2.4 2.8 2.0 2.9 2.2 2.2 3.7 2.6 1.7 1.4 2.8 2.8 2.2 8.9 10.2 10.3 10.5 10.5 8.8 9.7 9.8 9.5 8.0 10.4 11.7 9.6 21.0 23.1 22.9 24.2 22.3 20.2 25.0 22.3 20.8 18.8 24.4 23.6 21.2 0.8 0.8 0.7 0.9 0.6 0.6 1.1 0.7 0.6 0.7 0.9 0.4 0.6 3.8 3.5 5.0 2.5 4.9 6.1 2.6 3.8 4.8 4.4 3.8 5.9 5.5 4.6 4.3 5.8 3.4 5.5 6.7 3.6 4.6 5.4 5.1 4.7 6.3 6.1 2.1 2.6 2.4 2.5 3.2 2.4 2.1 2.8 3.7 4.5 1.2 0.9 2.8 100 100 100 100 100 100 100 100 100 100 100 100 100

Mean 20012002 29.3

All values are in % of total. The footprint-weighted ecosystem was calculated by weighting the vegetation composition of every wind sector (combining over storey and under storey) with the proportion of data originating from each particular sector.

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extremely poor) have been developed for each species. Yield classes are tree species-specic at a given site and can be determined from stand age, mean DBH and mean height. Current aboveground wood increment can then be estimated from the empirical yield table. This results in a fairly correct estimation of the current wood increment rate of even-aged stands, in particular in the case of middle-aged forests. For branch NPP, we also applied allometric relationships (Curiel Yuste et al., 2005a) to determine the change in standing biomass, and summed this with the measured ne- and coarse branch litter fall. Aboveground litter fall (leaves, cones and branches) was measured from January 2001 until December 2003 (Curiel Yuste et al., 2005a). We used the average of the 3 years results for the carbon balance. Foliage NPP was calculated differently for pine and oak. In pine, NPP of needles was estimated from allometric relationships between current-year needles and DBH (Xiao et al., 2003), and the stand inventory data. Foliage in oak was estimated directly from the foliage litter fall during 20012003 (Curiel Yuste et al., 2005a). Coarse root NPP was estimated with allometric relationships between coarse root biomass and DBH (Curiel Yuste et al., 2005a) and repeated forest inventories (2000, 2001, 2003). Fine root NPP was estimated by repeated root no pka et al., 2005, for detailed coring (see Ko description of methodology). Belowground litter production was assumed equal to ne root NPP. Then, NPP for the over storey was calculated by weighting the oak and Scots pine NPP according to their relative contribution to the effectively contributing ecosystem. For the main under storey tree species (Prunus and Rhododendron), biomass, NPP and litter production were estimated as follows: for Rhododendron, we applied the estimates of Nadezhdina et al. (2003) measured at the same site. For Prunus, a similar allometric relationship between component biomass and diameter at breast height (DBH) was applied as for oak (Curiel Yuste et al., 2005a). 2.11. Soil carbon content and soil respiration Carbon stores in the organic surface layer and in the mineral soil (up to 30 cm deep) were determined in 2003, separately for the oak and the pine stands (Curiel Yuste et al., 2005a). As samples were taken only until 30 cm depth, the soil carbon stores reported here are underestimated (see Curiel Yuste et al., 2005a for more

detailed information about organic layers and mineral soil content). Soil CO2 efux was measured during 2001 at monthly intervals with a closed dynamic system and an IRGA (CIRAS-1, PP SYSTEMS, Hitchin, Herts, UK) in nine plots representative for the forest composition (different associations of canopy/under storey vegetation; 10 collars per plot; Curiel Yuste et al., 2005b). The vegetation types were determined by the combination of the over storey and under storey species, and corresponded to the vegetation types that were used to determine the effectively contributing ecosystem. A more detailed description of the methods and results are given by Curiel Yuste et al. (2005b). 2.12. Thinnings, wood export, slash inputs and decomposition Wood export was quantied from the annual timber selling reports of the local forest station (detailed for each management unit in the forest). The remaining slash was estimated from the allometric relations established to determine standing biomass. For the under storey (which was systematically removed) slash inputs were estimated by multiplying the cleaned areas (also annually reported for each management unit) with our estimate of standing biomass. Decomposition of this remaining slash was estimated with an exponential decay model applying different parameters for woody tissues and foliage/ne roots (Janssens et al., unpublished results): RSD BC eka (6)

where RSD is the respiration from slash decomposition (t(C) ha1 year1), BC is the carbon content of the remaining slash, k is the decomposition parameter and a is the time passed since the slash started to decompose (year). The applied values for the decomposition parameter k were 0.12 for stumps, 0.22 for branches and coarse roots, 0.25 for pine and rhododendron foliage and ne roots, and 0.35 for oak and Prunus foliage and ne roots, respectively (decomposition parameters were obtained by averaging parameter values of a range of studies; Berg, 1984; McClaugherty et al., 1984; Berg and Staaf, 1987; Berg et al., 1993; Liski et al., 2002). Respiration originating from slash decomposition was determined for each plot separately (t(C) ha1 year1) and subsequently scaled-up to the effectively contributing forest ecosystem as described earlier.

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Table 3 Equations and methods used to obtain the components of the carbon balance Carbon ux Net ecosystem exchange (NEE) Net ecosystem production (NEP) Total ecosystem respiration (TER) Gross primary production (GPP) Standing biomass Soil carbon Net primary production (NPP) Methods/equations Measured eddy covariance uxes and footprint correction =NEE Extrapolation of footprint-corrected nighttime eddy covariance uxes =TER + NEP Measured in dominant vegetation types (stand inventories and allometric relationships and root coring) and up-scaled by footprint-weighted ecosystem Measured in dominant vegetation types and up-scaled by footprint-weighted ecosystem 1. Change in woody biomass determined from measured stem growth and allometric relationships + measured aboveground litter production + ne root production and up-scaled by footprint-weighted ecosystem 2. Wood production determined with yield tables + measured above-ground litter production + ne root production and up-scaled by footprint-weighted ecosystem =GPP NPP Litter traps and up-scaled by footprint-weighted ecosystem =Fine root production and up-scaled by footprint-weighted ecosystem Forest management reports and up-scaled by footprint-weighted ecosystem Wood export data combined with allometric relationships to determine non-harvested biomass of removed trees and up-scaled by footprint-weighted ecosystem Slash production and decomposition model and up-scaled to footprint-weighted ecosystem Measured vegetation types and up-scaled by footprint weighted ecosystem =TER RSoil RSD =RA Raboveground =RSoil RRoot

Autotrophic respiration (RA) Above-ground litterfall Below-ground litter production Wood export Slash production Slash decomposition (RSD) Soil respiration (RSoil) Above-ground respiration (Raboveground) Root and mycorrhizal respiration (RRoot) Organic matter decomposition (RH)

See Section 2 for a more detailed description of methods.

2.13. Estimation of other components in the carbon balance Missing components in the carbon balance were calculated as follows: Autotrophic respiration (RA) RA GPP N PP (7) Aboveground autotrophic respiration (Raboveground) Raboveground T ER RSoil RSD (8)

of the carbon balance components is presented in Table 3. 3. Results and discussion 3.1. Modied eddy ux dataset and effectively contributing ecosystem The main result of applying the footprint criteria was that under unstable atmospheric conditions 97% of the remaining ux data originated from within the investigated forest. Under neutral conditions this percentage was lower (91%), but overall no less than 95% of the remaining ux data originated from within the investigated forest. Thus, we conclude that the reported CO2 uxes are representative for the investigated forest. The vegetation composition of the effectively contributing ecosystem varied annually and seasonally (Table 2). However, the temporal variation in the vegetation type contributing to the uxes was not large, because the different vegetation types were distributed fairly evenly throughout the forest. Averaged over all years, conifers covered 70.2% of the area in the effectively contributing ecosystem; deciduous species 27.3%, while 2.5% of the area in the effectively

where RSoil is soil CO2 efux and RSD is the CO2 ux originating from slash decomposition. Belowground autotrophic respiration (root + mycorrhizal respiration; RRoot) RRoot RA Raboveground (9) Decomposition of soil organic matter (SOM) equals heterotrophic respiration (RH) RH RSoil RRoot (10)

For all uxes the units are t(C) ha1 year1. For reasons of clarity a synoptic overview of the methods and approaches applied to obtain the values

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contributing ecosystem was not covered by trees (grasses or lanes). 3.2. Biomass and soil carbon pools Overall, Scots pines stored 83.7 t(C) ha1 in their biomass, pedunculate oaks 76.0 t(C) ha1 and the under storey biomass was 5.3 t(C) ha1. Thus the biomass of the effectively contributing ecosystem amounted to 84.6 t(C) ha1 (Fig. 3). The soil carbon content in the effectively contributing ecosystem was calculated to be 134.3 t(C) ha1 (Fig. 3), but this estimate is limited to the upper 30 cm. Oak stands contained much less carbon (92.2 t(C) ha1) than the pine stands (150.8 t(C) ha1; Curiel Yuste et al., 2005a). This higher soil carbon content in the Scots pine stands was expected given the recalcitrance of pine litter to decay, and the reduced heterotrophic activity in the more acid environment (Curiel Yuste et al., 2005a). 3.3. NEE estimates Annual NEE was estimated from the footprintcorrected and gap-lled database (Table 4). A considerable inter-annual variation in NEE was observed between 1997 and 2002, in agreement with many other ux sites across the world (Baldocchi et al., 2001). Annual NEE showed a much stronger correlation with TER (R2 = 0.89) than with GPP (R2 = 0.65). Hence, inter-annual differences in TER probably contribute most to the observed interannual variation in NEE. The highest (=most positive) NEE was obtained in 2000 (+1.1 t(C) ha1 year1) and the lowest in 2002 (1.1 t(C) ha1 year1). The positive NEE in 2000 might be a consequence of the intensive thinning in the previous year, of the short length of the growing season relative to the other years or of high respiration
Fig. 3. Carbon balance and carbon uxes in the investigated Scots pine/pedunculate oak mixed forest during the 20012002 period. All values are in t(C) ha1 year1. Abbreviations: NEP, net ecosystem production; GPP, gross primary production; TER, total ecosystem respiration; NPP, net primary production; RA, autotrophic respiration; SOM, soil organic matter. Values within square brackets refer to indirectly calculated estimations (see text), or give an indication of the range of accuracy. Values indicated with an asterisk (*) are affected by the use of yield tables rather than inventories.

rates related to temperature and rainfall anomalies (Carrara et al., 2003). The average NEE over the 6 year period was 0.3 t(C) ha1 year1, indicating a small net CO2 uptake by the forest ecosystem. The carbon balance depicted in Fig. 3 gives values averaged over 20012002. During this period the mean NEE was 1.0 t(C) ha1 year1 (note that NEP = NEE).

Table 4 Annual rates of the measured net ecosystem exchange (NEE), nighttime respiration (Rnighttime) and the calculated daytime respiration (Rdaytime), total ecosystem respiration (TER), gross primary production (GPP) for the 6 years investigated period Years 1997 1998 1999 2000 2001 2002 Mean S.D. C.V. (%) NEE (g(C) m2 year1) 94.4 10.4 13.5 107.4 94.9 108.7 27.8 85.9 Rnighttime (g(C) m2 year1) 416.1 496.1 527.5 524.7 395.3 347.6 451.2 75.3 16.7 Rdaytime (g(C) m2 year1) 648.2 724.9 740.1 767.6 623.0 506.5 668.4 86.8 14.5 TER (g(C) m2 year1) 1064.3 1221.0 1267.6 1292.3 1018.3 854.1 1119.6 170.8 15.3 GPP (g(C) m2 year1) 1158.7 1210.6 1254.1 1184.9 1113.2 962.8 1147.4 102.1 8.9

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Fig. 4. Bimonthly net ecosystem exchange (NEE) of carbon during daytime (round symbols) and nighttime (square symbols) in u*-corrected total ecosystem (open symbols) and footprint-corrected forest ecosystem (solid symbols). The values in the graph were calculated as the average of the bimonthly values in the same bimonthly periods of the 6 years. Signicance between the bimonthly data sets of the same periods between u*- and footprint-corrected NEE estimation is indicated by asterisks: ****P < 0.0001; ***P < 0.001; **P < 0.01; *P < 0.05; and n.s., not signicant.

The comparison of our footprint-corrected NEE to the earlier u*-corrected NEE estimate indicated some interesting differences (Fig. 4). The footprint-based NEE consistently showed much lower annual values (i.e. towards higher sequestration), while the inter-annual variation remained similar. The difference between the 6year-mean NEE estimates by the u*- and footprintcorrected data sets was 1.2 t(C) ha1 year1, and the forest ecosystem turned out to be a small net CO2 sink (NEE = 0.3 t(C) ha1 year1) after footprint-correction, in contrast with the u*-based estimate, which indicated a net CO2 source of 0.9 t(C) ha1 year1. Some further analyses were made to understand what exactly determined the difference in NEE between both approaches. Two-monthly daytime and nighttime NEE values obtained with u* and footprint correction were compared (Fig. 4). Daytime NEE values did not show consistent differences between u*-corrected dataset. Daytime meteorological conditions were usually unstable; therefore, rejecting only a limited amount of ux data obtained under occasionally stable conditions did not cause a strong effect on the daytime ux. The difference between u*- and footprint-corrected NEE values was, however, larger for nighttime conditions (1.1 t(C) ha1 year1), with a 19% decrease in NEE in the footprint-corrected dataset compared to the u*-corrected dataset. This originates from the facts that (1) during nighttime, stable and neutral conditions

were dominant, and (2) the footprint lter rejected more data than the u* lter. Hence, the difference between both approaches was much larger than during daytime. It is also obvious from Fig. 2 that the majority of the ux data measured during stable conditions represented the areas neighbouring the forest, including the town of Brasschaat, rural urban areas and parks. Combustion from domestic heating and trafc in the town of Brasschaat probably increased nighttime CO2 efux. Similarly, the typically more active deciduous vegetation in the surrounding parks (Curiel Yuste et al., 2005a) and common application of fertilizer and wood-chips (soil cover) in gardens are also likely to have produced higher nighttime CO2 efux in the areas surrounding the forest. The stronger discrepancy between the two ltering approaches during winter nights (when heating was most pronounced) suggests that the u* lter may not have excluded all of the high uxes from the neighbouring areas (Fig. 5). Thus, both u*- and footprint-corrected NEE represented the forest ecosystem well during daytime, but during nighttime the footprint-corrected NEE represented the forest better. 3.4. Total ecosystem respiration The measured annual nighttime respiration, the calculated annual daytime respiration and TER values are presented in Table 4. Annual TER ranged from

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Fig. 5. Annual net ecosystem exchange of carbon (NEE) in the u*-corrected total ecosystem ux ( ) and in the effectively contributing forest ecosystem ( ).

8.5 t(C) ha1 year1 in 2002 to 12.9 t(C) ha1 year1 in 2000 with an average of 11.2 t(C) ha1 year1 over the 6-year period. The highest value corresponds to a year characterized by a short growing season, relatively high temperatures and following substantial thinnings (Carrara et al., 2003). Our 6-year mean TER is slightly higher than the mean TER of the 18 EUROFLUX forests included in the review by Janssens et al. (2001; mean: 10.4 t(C) ha1 year1; range: 6 1 16 t(C) ha year1). In comparison with other Scots pine-dominated forests, the TER values obtained in this study are higher than in more northern pine stands, where TER ranged between 6.2 and 9.1 t(C) ha1 year1 in southern Finland (Kolari et al., 2004) and between 5.7 and 6.4 t(C) ha1 year1 in northern Finland (Wang et al., 2004). In contrast, our values were somewhat lower than the TER of 13.4 t(C) ha1 year1 measured in a Scots pine forest in the Netherlands that experienced more similar climatic conditions (Valentini et al., 2000). The 20012002 mean TER used in the carbon balance was 9.4 t(C) ha1 year1 (Fig. 3). This value is substantially lower than the 6-year-mean, because 2001 and 2002 were characterized by the lowest TER of the entire period. 3.5. Gross primary production The highest GPP value (12.5 t(C) ha1 year1) was obtained in 1999, the year before the thinning, and the lowest (9.6 t(C) ha1 year1) in 2002 (Table 4). In

contrast to TER, our mean GPP value for the 6 years (11.5 t(C) ha1 year1) was lower than the mean GPP value of the EUROFLUX forests (13.4 t(C) ha1 year1; Janssens et al., 2001). This contrasting difference explains the very small NEE at our site. The low GPP is probably related to the relatively high age of the pine trees that dominated the footprint area, as well as to the ongoing thinnings (canopy not completely closed). Nonetheless, our mean GPP of 11.5 t(C) ha1 year1 was well within the reported ranges for forest GPP of 3.0 to 34.4 t(C) ha1 year1 (Waring et al., 1998) and 7.022.0 (Janssens et al., 2001). In comparison with our results, a higher annual GPP of 15.5 t(C) ha1 year1 was calculated from NEE and TER from a single year eddy covariance measurement in a 80-year-old Scots pine stand in the Netherlands (Valentini et al., 2000). Similar values for GPP were reported for the southern Finnish pine forests (Kolari et al., 2004), where GPP ranged between 9.3 and 10.7 t(C) ha1 year1. Wang et al. (2004) found that GPP varied from 7.3 to 9.9 t(C) ha1 year1 in pine forests in northern Finland. These lower GPP values are, of course, expected given the typical negative relation between GPP and latitude (Waring et al., 1998). The GPP value of 20012002 was 10.4 t(C) ha1 year1, and it must be noted that GPP in these 2 years was the lowest of the 6 years of measurements (1997 2002). Therefore, the GPP value depicted in the carbon balance (Fig. 3) is around 10% lower than the average of the entire period.

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3.6. Net primary production The annual mean NPP in the period 20012003 was 4.1 t(C) ha1 year1 in the Scots pine stands and 8.9 t(C) ha1 year1 in the oak stands (Curiel Yuste et al., 2005a). We further estimated a NPP of 0.6 t(C) ha1 year1 in the under storey vegetation. Thus the NPP used for the carbon balance of the effectively contributing ecosystem amounted to 5.8 t(C) ha1 year1. The explanation for the more than double NPP in oak as compared to pine might be in the soil nutrient availability. Several observations indicated that soil organic matter accumulated at higher rates under pines than under oaks (Curiel Yuste et al., 2005a). Curiel Yuste et al. (2005a) therefore hypothesized that more nutrients were being immobilized in soils under pine than under oak, and that the pines were exhibiting an age-related decline in productivity due to nutrient limitation. The observed accumulation of organic matter resulted from the poor decomposability of the pine litter. In the oak stands, litter is less recalcitrant to decay and soil acidity is less severe; hence organic matter appears not to be accumulating and nutrients are recycled. This probably explains why NPP was much higher in the oaks than in the pines and why oaks allocated a much smaller proportion of NPP to ne root growth (Curiel Yuste et al., 2005a). From the yield tables we predicted stem and branch wood production as 3.8 m3 ha1 year1 in the Scots pine stands. This value contrasts with the 1.8 m3 ha1 year1 estimated with the inventory approach. For pedunculate oak, in contrast, yield tables predicted a much lower wood increment than the inventory approach (respectively, 6.5 and 15.5 m3 ha1 year1). When we recalculated NPP with the above-mentioned values of aboveground wood increment, the rate of NPP in the effectively contributing forest ecosystem was reduced from 5.8 to 5.5 t(C) ha1 year1. Hence, we are reporting both inventory- and yield table based estimates of NPP in the carbon balance (Fig. 3). 3.7. Litter and slash inputs Measured above-ground and below-ground litter production amounted to an annual mean carbon ux of 3.9 t(C) ha1 year1 in the Scots pine and 4.0 t(C) ha1 year1 in the pedunculate oak stands over the 20012003 period. We estimated an additional 0.5 t(C) ha1 year1 litter production from the under storey vegetation. The total carbon ux via litter in the footprint-corrected ecosystem was thus 4.3 t(C) ha1 year1.

Fig. 6. Schematic illustration of the calculation of net biome productivity (NBP). The width of the arrow reects the magnitude of the carbon ux. GPP, gross primary productivity; NPP, net primary productivity; NEP, net ecosystem productivity (equals minus net ecosystem exchange). All values are in t(C) ha1 year1.

Some stands within the footprint area were thinned and the under storey removed during the past and recent decades. We took these thinnings into account, as the decomposition of the remaining slash could be a signicant component of TER. Calculations, based on the reported thinnings and on allometric relations, showed a wood carbon export of 1.2 t(C) ha1 year1 from the ecosystem by timber sales and 0.5 t(C) ha1 year1 remaining as above- and belowground slash during the 20012002 period. The modelled decomposition of the total slash inputs during the previous 21 years (Janssens et al., unpublished results) suggested a mean carbon efux of 0.5 t(C) ha1 year1 over the 20012002 period (Fig. 3; 0.6 and 0.5 t(C) ha1 year1 in the 2 years, respectively). Summation of the exported carbon and the NEE produces an estimate of the net biome productivity (NBP; Fig. 6). During the 20012002 period, the forest absorbed 1.0 t(C) ha1 year1 as CO2 from the atmosphere, but lost 1.2 t(C) ha1 year1 as wood carbon. Thus, the forest site had a negative NBP, implying that the ecosystem was losing carbon (0.2 t(C) ha1 year1). 3.8. Soil CO2 efux Soil CO2 efux of the effectively contributing ecosystem was 5.8 t(C) ha1 year1 (Curiel Yuste et al., 2005b). This value was slightly less than the mean of 67 t(C) ha1 year1 reported by Raich and Schlesinger (1992) for temperate forests and of 6.6 t(C) ha1 year1 reported by Janssens et al. (2001) for the EUROFLUX forests. The contribution of soil respiration to TER tended to vary seasonally, with minimum contributions during summer (less than 50% of TER) and maximum contributions during winter (about 94% of TER). We hypothesized that the observed changes in the contribution of soil respiration to TER were a result of the antagonistic growth patterns of

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shoots and roots caused by seasonal changes in carbon allocation, the larger seasonal changes in foliar biomass than in root biomass, and the differences in soil and air temperature (Curiel Yuste et al., 2005b). 3.9. Carbon accumulation in biomass and soil Based on the two inventories, we calculated that biomass was increasing at a rate of 4.9 t(C) ha1 year1 in the pedunculate oak stands and of 0.2 t(C) ha1 year1 in the Scots pine stands. Biomass of the under storey of the ecosystem was estimated to increase by 0.1 t(C) ha1 year1. These results suggested that the total net biomass in the effectively contributing ecosystem increased at a rate of 1.5 t(C) ha1 year1 (excluding harvest). When biomass increases were based on yield table estimates, the rate of biomass increment was 1.2 t(C) ha1 year1 in the effectively contributing ecosystem (excluding harvest). Given that almost 1.7 t(C) ha1 year1 was removed from the biomass compartment as wood export or slash, the biomass carbon pool was declining by 0.20.6 t(C) ha1 year1. The carbon balance of the effectively contributing ecosystem further suggested no change in soil carbon content when NPP was calculated from the results of the inventory measurements. Both litter- and slash inputs (4.3 and 0.5 t(C) ha1 year1) were in balance with their decomposition rates (4.3 and 0.5 t(C) ha1 year1, respectively). When growth was estimated with yield tables, however, we calculated a small increment in soil carbon (0.4 t(C) ha1 year1). Curiel Yuste et al. (2005a) did observe C sequestration in the soil of the pine stands, but unfortunately did not measure in the other vegetation types. Thus, the forest ecosystem was losing 0.2 t(C) ha1 year1 (see discussion about NBP above) and this decline concealed a loss of biomasscarbon of 0.20.6 t(C) ha1 year1 and a gain in soil carbon of 00.4 t(C) ha1 year1. 3.10. Other component uxes Other components in the carbon balance model were determined from simple equations as described in Section 2. Two rates were obtained for several of the missing components. These two rates represented carbon uxes when NPP was estimated either from inventory results or from yield tables. Total autotrophic respiration was estimated as 4.64.9 t(C) ha1 year1. Of this total, aboveground autotrophic respiration consumed the largest fraction (3.0 t(C) ha1 year1), and root-mycorrhizal respiration the smallest: 1.6 1.9 t(C) ha1 year1 (Fig. 3).

Heterotrophic respiration (RH) associated with the decomposition of soil carbon (excluding the decomposition of slash) was estimated as 3.94.3 t(C) ha1 year1. 3.11. Discussion of accuracy To close the carbon balance, calculations were made in the same order as the results presented above. As measurement and scaling errors were thus propagated, the individual autotrophic and heterotrophic respiratory components were the most uncertain elements of the carbon balance. We have no data to validate these uxes, nor information about their accuracy. An alternative approach to test the validity of the ux estimates in our carbon balance is to compare uxes that should be of similar magnitude or whose ratios are often assumed to be relatively conservative. For instance, the fact that the measured litter inputs and calculated decomposition rates were of similar magnitude, despite the fact that they were obtained independently, suggests that either the values in the carbon balance are reliable, or that both are incorrect. The ratio of soil CO2 efux to total ecosystem respiration (0.62) was also very conservative and close to the average ratio observed among the EUROFLUX forests (0.63; Janssens et al., 2001). The ratio of root respiration to soil CO2 efux was estimated at 27% when NPP was calculated from allometric relations and 33% when the NPP calculation was based on yield tables. Landsberg and Gower (1997) reported that the average contribution of root respiration to total soil CO2 efux was 45% in forests, but the estimates ranged widely from 22% (Tate et al., 1993) to 90% (Thierron and Laudelout, 1996). More recently, Bond-Lamberty et al. (2004) reported global trends in the contributions of roots and heterotrophs to soil CO2 efux. When applied to our site, their regressions predict root respiration to be 2.15 t(C) ha1 year1 (we estimated 1.61.9), and heterotrophic respiration to be 3.4 t(C) ha1 year1 (we estimated 3.94.3). Although our estimate of root respiration thus appears too low, it is well within the ranges reported both by Landsberg and Gower (1997) and Bond-Lamberty et al. (2004). Another approach to check the accuracy of the estimated values of the component uxes in our carbon balance is based on the assumption that respiration of the different plant parts should be more or less proportional to their NPP. For example, the ratio of aboveground to belowground NPP (1.97 and 1.76 depending on the method) was very similar to the ratio of aboveground to belowground autotrophic respiration

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(1.93 and 1.57 for both methods to determine NPP). Also the ratio of NPPaboveground to Raboveground (1.15 and 1.03, respectively, for the two NPP estimates) was similar to the ratio of NPPbelowground to RRoot (1.13 and 0.92, respectively, for the two NPP estimates). These consistent results further increased condence in the validity of our carbon balance uxes. The observation of Waring et al. (1998) that NPP was approximately proportional to GPP (0.47 0.04 (S.D.)) in 12 contrasting forest ecosystems allows a great simplication of forest growth models. However, as these authors calculated respiration and GPP in an indirect way, their observation remains a hypothesis that should be tested and veried by independent growth and respiration measurements (Waring et al., 1998; Medlyn and Dewar, 1999). In our study growth was measured directly and GPP was calculated independently. It should, however, be noted that the GPP estimate of a specic year (using the generally applied method for eddy covariance studies) is not independent from the NPP of the previous years. The calculation of GPP is based on the measurement of TER, yet a substantial fraction of TER originates from the decomposition of the previous years litter fall. Therefore, comparing mean NPP to mean GPP over a longer measurement period is a better reection of the NPP/GPP ratio. When the mean NPP from the inventory measurements of the 3 years period (20012003), i.e. 5.8 t(C) ha1 year1 was compared to the mean GPP over 6 years (19972002), i.e. 11.5 t(C) ha1 year1, the ratio was 0.51, a result that supports the hypothesis of Waring et al. (1998). When the NPP calculation based on yield tables (5.5 t(C) ha1 year1) was compared to the 6 years mean GPP, the NPP/GPP ratio changed to 0.475, which agreed almost perfectly with the 0.47 prediction of Waring et al. (1998). 4. Conclusions Application of a footprint correction to eddy covariance CO2 ux data in a relatively small forest reduced NEE by 1.2 t(C) ha1 year1 in comparison to a u* correction, and shifted the NEE of the forest from positive to negative (0.3 t(C) ha1 year1). These footprint-corrected NEE data were combined with a footprint-weighted ecological study and management information to construct a complete carbon balance representative for the forested ecosystem. Despite being a net CO2 sink, the forest was losing carbon due to intensive thinnings and subsequent export of wood. Our presented carbon balance further

describes the main carbon processes in a predominantly old and even-aged Scots pine ecosystem, where the declining growth process is accompanied by a low carbon sequestration in the biosphere. Our results tended to support the predicted 0.47 ratio between NPP and GPP, even when these components were measured independently in a forest ecosystem. Volumes and rates in the carbon balance presented in this study may differ from those in other ecosystem types, but the similar footprint correction applied to eddy covariance data, ecological measurements, and management information makes the carbon balance reported in this study relevant to better understand and quantify carbon ows in forests. Acknowledgements This research was nancially supported by the ECs Fourth (EUROFLUX contract ENV4-CT95-0078) and Fifth (CARBOEUROFLUX contract EVKL-CT-199900032) Framework Programs. The authors acknowledge the Division of Forests & Green Areas of the Ministry of the Flemish Community for access to the forest site, the Institute for Forestry and Game Management (IFG) and forest ranger M. Schuermans for logistic support. We are also grateful to F. Kockelbergh (UA), N. Calluy (UA) and Y. Buidin (IFG) for technical assistance. M.T. Nagy was supported by a grant from the UA-Research Council (call 2003) during his sojourn at the University of Antwerpen. This study also contributes to the GCTE Core Project of the International Geosphere Biosphere Programme (IGBP). References
., Moncrieff, J., Foken, Aubinet, M., Grelle, A., Ibrom, A., Rannik, U T., Kowalski, A.S., Martin, Ph., Berbigier, P., Clement, R., Elbers, nwald, T., Morgenstern, K., Pilegaard, K., J., Granier, A., Gru Rebmann, C., Snijders, W., Valentini, R., Vesala, T., 2000. Estimates of the annual net carbon and water exchanges of forests: the EUROFLUX methodology. Adv. Ecol. Res. 30, 113175. Baeyens, L., Van Slycken, J., Stevens, D., 1993. Description of the Soil Prole in Brasschaat. Internal Research Paper. Institute for Forestry and Game Management, Geraardsbergen, Belgium, pp. 17. Baldocchi, D.D., Hicks, B.B., Meyers, T.P., 1988. Measuring biosphereatmosphere exchange of biologically related gases with micrometeorological methods. Ecology 69, 13311340. Baldocchi, D.D., Falge, E., Gu, L., Olson, R., Hollinger, D., Running, S., Anthoni, P., Bernhofer, C., Davis, K., Fuentes, J., Goldstein, A., Katul, G., Law, B., Lee, X., Mahli, Y., Meyers, T., Munger, W., Oechel, W., Paw, U.K.T., Pilegaard, K., Schmid, H.P., Valentini, R., Verma, S., Vesala, T., Wilson, K., Wofsy, S., 2001. FLUXNET: a new tool to study the temporal and spatial variability of

M.T. Nagy et al. / Agricultural and Forest Meteorology 139 (2006) 344360 ecosystem-scale carbon dioxide, water vapour and energy ux densities. Bull. Am. Meteorol. Soc. 82, 24152434. Battaglia, M., Sands, P., 1997. Modelling site productivity of Eucalyptus globulus in response of climatic and site factors. Aust. J. Plant Physiol. 24, 831850. Berg, B., 1984. Decomposition of root litter and some factors regulating the process. Soil Biol. Biochem. 16, 609617. Berg, B., Staaf, H., 1987. Release of nutrients from decomposition of white birch leaves and Scots pine needle litter. Pedobiology 30, 5563. Berg, B., McClaugherty, C.A., Johansson, M.-B., 1993. Litter mass loss rates in late stages of decomposition at some climatically and nutritionally different pine sites. Long-term decomposition in a Scots pine forest. VIII. Can. J. Bot. 71, 680692. Bond-Lamberty, B., Chuankuan, W., Gower, S.T., 2004. A global relationship between heterotrophic and autotrophic components of soil respiration? Global Change Biol. 10, 17561766. Carrara, A., Kowalski, A.S., Neirynck, J., Janssens, I.A., Curiel Yuste, J., Ceulemans, R., 2003. Net ecosystem CO2 exchange of mixed forest in Belgium over 5 years. Agric. For. Meteorol. 119, 209 227. Carrara, A., Janssens, I.A., Curiel Yuste, J., Ceulemans, R., 2004. Seasonal changes in photosynthesis, respiration and NEE of a mixed temperate forest. Agric. For. Meteorol. 126, 1531. Curiel Yuste, J., Konopka, B., Janssens, I.A., Coenen, K., Xiao, C.W., Ceulemans, R., 2005a. Contrasting net primary productivity and carbon distribution between neighbouring stands of Quercus robur and Pinus sylvestris. Tree Physiol. 25, 701712. Curiel Yuste, J., Nagy, M., Janssens, I.A., Carrara, A., Ceulemans, R., 2005b. Soil respiration in a mixed temperate forest and its contribution to total ecosystem respiration. Tree Physiol. 25, 609619. de Pury, D.G.G., Ceulemans, R., 1997. Scaling-up carbon uxes from leaves to stands in a patchy coniferous/deciduous forest. In: Mohren, G.M.J., Kramer, K., Sabate, S. (Eds.), Impacts of Global Change on Tree Physiology and Forest Ecosystems. Kluwer Academic Publishers, Dordrecht, pp. 263272. Desjardins, R.L., 1985. Carbon dioxide budget of maize. Agric. For. Meteorol. 36, 2941. Falge, E., Baldocchi, D., Olson, R.J., Anthoni, P., Aubinet, M., Bernhofer, C., Burba, G., Ceulemans, R., Dolman, H., Granier, A., Gross, P., Grunwald, T., Hollinger, D., Jensen, N.O., Katul, G., Keronen, P., Kowalski, A.S., Ta Lai, C., Law, B.E., Meyers, T., Moncrieff, J., Moors, E., Munger, J.W., Pilegaard, K., Rannik, U., Rebmann, C., Suyker, A., Tenhunen, J., Tu, K., Verma, S., Vesala, T., Wilson, K., Wofsy, S., 2001. Gap lling strategies for defensible annual sums of net ecosystem exchange. Agric. For. Meteorol. 107, 4369. Falge, E., Baldocchi, D., Tenhunen, J., Aubinet, M., Bakwin, P., Berbigier, P., Bernhofer, C., Burba, G., Clement, R., Davis, K.J., Elbers, J.A., Goldstein, A.H., Grelle, A., Granier, A., Guomundsson, J., Hollinger, D., Kowalski, A.S., Katul, G., Law, B.E., Malhi, Y., Meyers, T., Monson, R.K., Munger, J.W., Oechel, W., Paw, K.T., Pilegaard, K., Rannik, U., Rebmann, C., Suyker, A., Valentini, R., Wilson, K., Wofsy, S., 2002. Seasonality of ecosystem respiration and gross primary production as derived from FLUXNET measurements. Agric. For. Meteorol. 113, 5374. Gond, V., de Pury, D.G.G., Veroustraete, F., Ceulemans, R., 1999. Seasonal variation in leaf area index, leaf chlorophyll, and water content; scaling-up to estimate fAPAR and carbon balance in a multilayer, multispecies temperate forest. Tree Physiol. 19, 673 679.

359

Goulden, M.L., Munger, J.W., Fan, S.M., Daube, B.C., Wofsy, S.C., 1996. Measurements of carbon storage by long-term eddy correlation: methods and a critical assessment of accuracy. Global Change Biol. 2, 169182. Jansen, J.J., Sevenster, J., Faber, P.J., 1996. Opbrengsttabellen voor belangrijke boomsoorten in Nederland (Yield tables for important tree species in the Netherlands). IBN Report 221, IBN-DLO, Wageningen, pp. 4245 and 7782 (in Dutch). Janssens, I.A., Sampson, D.A., Cermak, J., Meiresonne, L., Riguzzi, F., Overloop, S., Ceulemans, R., 1999. Above- and below-ground phytomass and carbon storage in a Belgian Scots pine stand. Ann. For. Sci. 56, 8190. Janssens, I.A., Meiresonne, L., Ceulemans, R., 2000. Mean soil CO2 efux from a mixed forest: temporal and spatial integration. In: Ceulemans, R.J.M., Veroustraete, F., Gond, V., Van Rensbergen, J.B.H.F. (Eds.), Forest Ecosystem Modeling, Upscaling and Remote Sensing. SPB Academic Publishing, The Hague, The Netherlands, pp. 1933. Janssens, I.A., Lankreijer, H., Matteucci, G., Kowalski, A.S., Buchmann, N., Epron, D., Pilegaard, K., Kutsch, W., Longdoz, B., nwald, T., Montagnani, L., Dore, S., Rebmann, C., Moors, E.J., Gru ., Morgenstern, K., Clement, R., Oltchev, S., Grelle, A., Rannik, U Gumundsson, J., Minerbi, S., Berbigier, P., Ibrom, A., Moncrieff, J., Aubinet, M., Bernhofer, C., Jensen, N.O., Vesala, T., Granier, A., Schulze, E.-D., Lindroth, A., Dolman, A.J., Jarvis, P.G., Ceulemans, R., Valentini, R., 2001. Productivity overshadows temperature in determining soil and ecosystem respiration across European forests. Global Change Biol. 7, 269278. Kolari, P., Pumpanen, J., Rannik, U., Ilvesniemi, H., Hari, P., Berninger, F., 2004. Carbon balance of different aged Scots pine forests in Southern Finland. Global Change Biol. 10, 11061119. no pka, B., Curiel Yuste, J., Janssens, I.A., Ceulemans, R., 2005. Ko Comparison of ne root dynamics in Scots pine and Pedunculate oak in sandy soil. Plant and Soil 276, 3345. Kowalski, A.S., Overloop, S., Ceulemans, R., 2000. Eddy uxes above a Belgian, Campine forest and their relationship with predicting variables. In: Ceulemans, R.J.M., Veroustraete, F., Gond, V., Van Rensbergen, J.B.H.F. (Eds.), Forest Ecosystem Modeling, Upscaling and Remote Sensing. SPB Academic Publishing, The Hague, The Netherlands, pp. 317. Landsberg, J.J., Gower, S.T., 1997. Applications of Physiological Ecology to Forest Management. Academic Press, San Diego. Landsberg, J.J., Waring, R.H., 1997. A generalised model of forest productivity using simplied concepts of radiation-use efciency, carbon balance and partitioning. For. Ecol. Manage. 95, 209228. Liski, J., Perruchoud, D., Karjalainen, T., 2002. Increasing carbon stocks in the forest soils of western Europe. For. Ecol. Manage. 169, 159175. kela , A., Valentine, H.T., 2001. The ratio of NPP to GPP: evidence Ma of change over the course of stand development. Tree Physiol. 21, 10151030. McClaugherty, C.A., Aber, J.D., Melillo, J.M., 1984. Decomposition dynamics of ne roots in forested ecosystems. Oikos 42, 378386. Medlyn, B.E., Dewar, R.C., 1999. Comment on the article by R.H. Waring, J. Landsberg and M. Williams relating net primary production to gross primary production. Tree Physiol. 19, 137 138. Michaelis, L., Menten, M.L., 1913. Die Kinetik der Invertin Wirkung. Biochemische Zeitschrift 49, 333. Moncrieff, J.B., Massheder, J.M., de Bruin, H., Elbers, J., Friborg, T., Heusinkveld, B., Kabat, P., Scott, S., Soegaard, H., Verhoef, A., 1997. A system to measure surface uxes of momentum, sensible

360

M.T. Nagy et al. / Agricultural and Forest Meteorology 139 (2006) 344360 Roskams, P., Sioen, G., Overloop, S., 1997. Meetnet voor de intensieve monitoring van het bosecosysteem in het Vlaamse Gewest resultaten 19911992. Communications of the Institute for Forestry and Game Management, Ministry of the Flemish Community (in Dutch), pp. 191. Schmid, H.P., 1997. Experimental design for ux measurements: matching scales of observations and uxes. Agric. For. Meteorol. 87, 179200. Swinbank, W.C., 1951. The measurement of vertical transfer of heat and water vapour by eddies in the lower atmosphere. J. Atmos. Sci. 8, 135145. Tate, K.R., Ross, D.J., OBrien, B.J., Kelliher, F.M., 1993. Carbon storage and turnover, and respiratory activity, in the litter and soil of an old-growth southern beech (Nothofagus) forest. Soil Biol. Biochem. 25, 16011612. Thierron, V., Laudelout, H., 1996. Contribution of root respiration to total CO2 efux from the soil of a deciduous forest. Can. J. For. Res. 26, 11421148. Thornley, J.H.M., Cannell, M.G.R., 2000. Modelling the components of plant respiration. Ann. Bot. 85, 5567. Valentini, R., Matteucci, G., Dolman, A.J., Schulze, E.-D., Rebmann, C., Moors, E.J., Granier, A., Gross, P., Jensen, N.O., Pilegaard, K., Lindroth, A., Grelle, A., Bernhofer, C., Grunwald, T., Aubinet, M., Ceulemans, R., Kowalski, A.S., Vesala, T., Rannik, U., Berbigier, P., Loustau, D., Gudmundsson, J., Thorgeirsson, H., Ibrom, A., Morgenstern, K., Clement, R., Moncrieff, J., Montagnani, L., Minerbi, S., Jarvis, P.G., 2000. Respiration as the main determinant of carbon balance in European forests. Nature 404, 861865. Verma, S.B., Baldocchi, D.D., Anderson, D.E., Matt, D.R., Clement, R.J., 1986. Eddy uxes of CO2, water vapour and sensible heat over a deciduous forest. Boundary-Layer Meteorol. 36, 7191. ki, S., Zha, T.S., Peltola, H., 2004. Component Wang, K.-Y., Kelloma carbon uxes and their contribution to ecosystem carbon exchange in a pine forest: an assessment based on eddy covariance measurements and an integrated model. Tree Physiol. 24, 1934. Waring, R.H., Landsberg, J.J., Williams, M., 1998. Net primary production of forests: a constant fraction of gross primary production? Tree Physiol. 18, 129134. , O.R., Izumi, Y., 1971. Local free convection, Wyngaard, J.C., Cote similarity and the budgets of shear stress and heat ux. J. Atmos. Sci. 28, 11711182. Xiao, C.-W., Curiel Yuste, J., Janssens, I.A., Roskams, P., Nachtergale, L., Carrara, A., Sanchez, B.Y., Ceulemans, R., 2003. Above- and belowground biomass and net primary production in a 73-year-old Scots pine forest. Tree Physiol. 23, 505516.

heat, water vapour and carbon dioxide. J. Hydrol. 188189, 589 611. Nadezhdina, N., Tatarinov, F., Ceulemans, R., 2003. Leaf area and biomass of Rhododendron under story in a stand of Scots pine. For. Ecol. Manage. 187, 235246. Neirynck, J., Van Ranst, E., Roskams, P., Lust, N., 2002. Impact of decreasing through fall depositions on soil solutions chemistry at coniferous monitoring sites in northern Belgium. For. Ecol. Manage. 160, 127142. Overloop, S., Meiresonne, L., 1999. Basiskarakteristieken van het proefvlak Brasschaat, domeinbos de Inslag. Communications of the Institute for Forestry and Game Management, Ministry of the Flemish Community 1, pp. 1121 (in Dutch). Prentice, I.C., Farquhar, G.D., Fasham, M.J.R., Goulden, M.L., Heimann, M., Kheshi, H.S., Le Quere, C., Scholes, R.J., Wallace, D.W.R., Archer, D., Ashmore, M.R., Aumont, O., Baker, D., Battle, M., Bender, M., Bopp, L.P., Bousquet, P., Caldeira, K., Ciais, P., Cramer, W., Dentener, F., Enting, I.G., Field, C.B., Holland, E.A., Houghton, R.A., House, J.I., Ishida, A., Jain, A.K., Janssens, I.A., Joos, F., Kaminski, T., Keeling, C.D., Keeling, R.F., Kicklighter, D.W., Kohfeld, K.E., Knorr, W., Law, R., Lenton, T., Lindsay, K., Maier-Reimer, E., Manning, A., Matear, R.J., McGuire, A.D., Melillo, J.M., Meyer, R., Mund, M., Orr, J.C., Piper, S., Plattner, K., Rayner, P.J., Sitch, S., Slater, R., Taguchi, S., Tans, P.P., Tian, H.Q., Weirig, M.F., Whorf, T., Yool, A., 2001. The carbon cycle and atmospheric carbon dioxide. In: Houghton, J.T., Ding, Y., Griggs, D.J., Noguer, M., van der Linden, P.J., Xiaosu, D. (Eds.), Climate Change 2001. The Scientic Basis. Contribution of Working Group I to the Third Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, pp. 183237. ckede, M., Foken, T., Aubinet, M., Aurela, M., Rebmann, C., Go Berbigier, P., Bernhofer, C., Buchmann, N., Carrara, A., Cescatti, nA., Ceulemans, R., Clement, R., Elbers, J.A., Granier, A., Gru ` nkova ` , K., Heinesch, B., Knohl, A., wald, T., Guyon, D., Havra Laurila, T., Longdoz, B., Marcolla, B., Markkanen, T., Miglietta, F., Moncrieff, J., Montagnani, L., Moors, E., Nardino, M., Ourci ., Rotenberg, E., Sedlak, P., val, J.M., Rambal, S., Rannik, U Unterhuber, G., Vesala, T., Yakir, D., 2005. Quality analysis applied on eddy covariance measurements at complex forest sites using footprint modelling. Theor. Appl. Clim. 80, 121141. Raich, J.W., Schlesinger, W.H., 1992. The global carbon dioxide ux in soil respiration and its relationship to vegetation and climate. Tellus 44B, 8199.