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Agriculture, Ecosystems and Environment 139 (2010) 336–345

Contents lists available at ScienceDirect

Agriculture, Ecosystems and Environment

journa l homepage: www.e lsev ier .com/ locate /agee

he net biome production of full crop rotations in Europe

.L. Kutscha,∗, M. Aubinetb, N. Buchmannc, P. Smithd, B. Osbornee, W. Eugsterc, M. Wattenbachd,. Schrumpf f, E.D. Schulze f, E. Tomelleri f, E. Ceschiag, C. Bernhoferh, P. Béziatg, A. Carrara i,

. Di Tommasi j, T. Grünwaldh, M. Jonesk, V. Magliulo j, O. Marloie l, C. Moureauxb, A. Olioso l,.J. Sanz i, M. Saunderse, H. Søgaardm, W. Ziegler f

Johann Heinrich von Thünen-Institut, Institute for Agricultural Climate Research, Braunschweig, GermanyUnit of Biosystem Physics, Faculté Universitaire des Sciences Agronomiques, Gembloux, BelgiumETH Zurich, Institute of Plant, Animal and Agroecosystem Sciences, Dept. of Agricultural and Food Sciences, Zurich, SwitzerlandInstitute of Biological and Environmental Sciences, School of Biological Sciences, University of Aberdeen, Cruickshank Building, St Machar Drive, Aberdeen, AB24 3UU Scotland, UKSchool of Biology and Environmental Science, University College Dublin, Belfield, Dublin 4, IrelandMax-Planck-Institute for Biogeochemistry, Jena, GermanyCESBIO, UMR 5126 – CNES-CNRS-UPS-IRD, 18 Avenue Edouard Belin, 31401 Toulouse cedex 9, FranceTechnische Universität Dresden, Department of Meteorology, Tharandt, GermanyFundación CEAM, c/Charles Darwin 14, Parque Tecnológico, 46980 Paterna, SpainCNR Institute for Agricultural and Forest Systems, Via Patacca 85, 80056 Ercolano, Napoli, ItalySchool of Natural Sciences, Department of Botany, Trinity College Dublin, Dublin 2, IrelandINRA, UMR 1114 INRA-UAPV, Domaine Saint Paul, Site Agroparc, F-84914 Avignon, FranceDepartment of Geography and Geology, University of Kopenhagen, Oster Voldgade 10, DK-1350 Copenhagen, Denmark

r t i c l e i n f o

rticle history:eceived 20 July 2009eceived in revised form 22 July 2010ccepted 27 July 2010vailable online 24 August 2010

eywords:arbon budgetddy covariancearvestrganic fertilizerood practice guidelinesgriculture

a b s t r a c t

Data sets of biometeorological measurements of ecosystem CO2 flux, combined with harvest and manuredata from several European cropland were integrated to provide an assessment of the carbon budget.Sites encompassed different climatic regions and contrasting crop rotations. The influence of differentcrops and management practices was also assessed to identify some of the major factors contributingto the cropland carbon balance. Since crops are rotated and cropping periods do not always follow thecalendar year, net ecosystem production (NEP) as well as net biome production (NBP) sums of full croprotations or of at least 4 years of longer-term crop rotations and of monocultures were used. In a secondanalysis NBP sums were correlated to soil properties. Finally, the data were combined with additionaldata to derive a mean annual GHG balance for the European cropland sites under consideration.

Five crop rotations and two monocultures were integrated over 4 years. During 4 years the averageannual NEP was −240 ± 113 g C m−2 y−1. On average, 382 ± 117 g C m−2 y−1 were harvested, where asaverage carbon inputs by manure and seeding was 47 ± 51 g C m−2 y−1. The average NBP of the sevensites under consideration was estimated to be a carbon loss of 95 ± 87 g C m−2 y−1. The full GHG balanceof the considered sites was estimated to be 160 g C m−2 y−1 in CO2-equivalents.

These results challenge current good practice guidelines that predict neutral carbon budgets for systemswhere the inputs of manure and crop residues are of comparable magnitude to those associated with

the sites examined in this study. Ongoing humus loss in spite of good practice is mainly related to soilswith high carbon concentrations which are not in equilibrium but may also be a result of already ongoingclimate change. A modification in the good practice guidelines to increase carbon inputs may be required.

Results from a representativeness analysis suggest that more than 50 sites are necessary for a Europeancropland flux network to adequately represent the variability of climate, soil and management within

hus,e me

the European continent. Tuncertainty intrinsic in th

∗ Corresponding author at: Max-Planck-Institute for Biogeochemistry, Hans-nöll-Str. 10, 07745 Jena, Germany.

E-mail address: wkutsch@bgc-jena.mpg.de (W.L. Kutsch).

167-8809/$ – see front matter © 2010 Elsevier B.V. All rights reserved.oi:10.1016/j.agee.2010.07.016

the uncertainties due to the network design are currently bigger than theasurement method.

© 2010 Elsevier B.V. All rights reserved.

1. Introduction

The specific properties of agricultural practice require anadopted scientific approach for the estimation of carbon or fullgreenhouse gas balances of individual cropland ecosystems as well

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W.L. Kutsch et al. / Agriculture, Ecosys

s the generalization of any findings from these efforts. Due to dif-erences in crops, cropping systems and agricultural practices thedoption of site-specific approaches for estimating the full green-ouse gas balance may often be required (Osborne et al., 2010). Notnly does this limit any generalisations, but it also confounds anynterpretation of the causes for differences in greenhouse gas emis-ions and carbon sequestration. Two differences between croplandsnd forests or other less managed ecosystems are important:

1) In croplands, lateral fluxes, associated with harvesting and theapplication of organic fertilizer/manure can severely influencethe ecosystem carbon budget. However, this transfer of organiccarbon across ecosystem boundaries is not quantified by theeddy covariance method (Baldocchi et al., 1988; Aubinet et al.,2000) that has become the standard approach to quantify CO2fluxes at any given site (Smith et al., 2010). Thus, additionalefforts to measure lateral carbon fluxes are necessary to quan-tify net biome production (NBP) from net ecosystem exchange(NEE) as measured using eddy covariance techniques.

2) Crop rotations are important elements of agricultural manage-ment in many regions of Europe. Since cropping and fallowperiods are irregular and seldom follow the calendar year andsince different crops and related agricultural practices result indifferent carbon inputs into the soils, a realistic carbon bud-get for agricultural ecosystems under crop rotation can only bederived when at least a full rotation is considered.

Crop rotations are often considered an important way tonhance carbon sequestration and increase the sustainability ofgro-ecosystems, although this will depend on the type and com-lexity of the rotation used (West and Post, 2002). The inclusion oflegume in the rotation is more likely to result in a build up of soilrganic carbon, whilst reducing the dependence on nutrient inputs.n contrast, large carbon losses are likely with root crops, such asugar beet or where almost all of the crop is removed at harvest,s is the case for maize grown for silage (Osborne et al., 2010). Thisgain makes generalisations difficult and argues for a more com-rehensive assessment of the impact of different rotations on netiome productivity.

For the first time, comprehensive data sets of ecosystem CO2ux measurements from several EU cropland sites encompassingifferent climatic regions and contrasting crop rotations were madevailable by the CarboEurope-IP cropland project, allowing a com-rehensive synthesis of the results. The current study complementshat of Eugster et al. (2010) who focused on the influence of sin-le events and management practices on respiration, Moors et al.2010) who quantified gross and net primary production and har-est losses for single cropping periods and Ceschia et al. (2010)ho derived full annual greenhouse gas balances, in order to pro-

ide an assessment of the greenhouse gas budgets of contrastingropland sites in Europe over that are associated with full cropotations.

. Material and methods

.1. General approach

Data obtained from sites belonging to the CarboEurope-IP net-ork were used to derive net biome production (NBP) based on

ddy covariance measurements of net ecosystem exchange (NEE)

upplemented with ancillary data on the main lateral carbon fluxes,pecifically, harvest and manure. Since crops are rotated and crop-ing periods do not always follow the calendar year, the usual

anuary to December annual flux estimate cannot be used to deriveepresentative annual estimates of NBP and NEP. For this reason,

nd Environment 139 (2010) 336–345 337

we derived NBP sums of full crop rotations or of at least 4 years oflonger-term crop rotations and of monocultures to derive estimatesthat are representative of the particular agricultural practice aswell as encompassing inter-annual variability. In a second step weattempted to analyse the calculated NBP sums, and in the third andfinal steps the data were combined with the results from Ceschiaet al. (2010) to derive a mean annual GHG balance for the Europeancropland sites under consideration.

2.1.1. Net ecosystem production (NEP) measurementsNEP was derived from eddy covariance measurements at all

sites. The application of this technique in agriculture is described indetail by Smith et al. (2010). The turbulent and storage CO2 fluxeswere calculated for 30 min intervals using standard CarboEuropesoftware (Mauder et al., 2008) and, thereafter, underwent standarddata processing within the CarboEurope database that includedquality checks, u*-filtering and gap-filling (Reichstein et al., 2005;Papale et al., 2006; Moffat et al., 2007). The resulting, so-called‘Level 4 ecosystem flux data’ comprised a full data set of half-hourlyfluxes and these were integrated over the full 4-year-period toderive NEP. The Level 4 data processing also generates derived vari-ables allowing for flux partitioning into gross primary production(GPP) and ecosystem respiration (Reco), which were also integratedfor the full crop rotations.

2.1.2. Net biome production (NBP)Net biome production (NBP) was calculated as the integral over

the 4 years of the relevant carbon fluxes for the croplands underconsideration (see also Buchmann and Schulze, 1999; Chapin et al.,2006). Here, we used a simplified approach (Eq. (1)) that ignoredthe ‘minor’ terms of the fully integrated NBP (see Smith et al., 2010;Osborne et al., 2010):

NBP = NEP − F − H + I (1)

where F is carbon lost by fires, H is carbon removed by harvest, I isinputs by organic fertilizer such as manure or slurry.

Carbon fluxes to the ground water as dissolved or particu-late organic, or inorganic carbon, volatile organic compounds,methane fluxes and carbon lost by soil erosion as detailed else-where (Osborne et al., 2010) were not considered. Since harvestedmaterial was removed from the site and most of the trans-locatedC was respired as CO2 over short time periods, the NBP reflects thelong-term load of CO2 to the atmosphere.

2.1.3. Full green house gas balancesEmissions that result from field operations were finally added

to the NBP to calculate the full greenhouse gas (GHG) balance overcrop rotations. We used the average emissions for fuel, fertilizerand machinery (32 g C m−2 y−1 in CO2-equivalents) and additionalN2O emissions due to agricultural practices (33 g C m−2 y−1 in CO2-equivalents) calculated by Ceschia et al. (2010).

2.1.4. Output/input ratios at field and farm levelOutput/input ratios (O/I) at field level are a measure of the effi-

ciency of agricultural practice. The full GHG balance is divided bythe export of carbon with harvested products. If the ratio is 1 the fullamount of harvest is already balanced by emissions and no net gainis in the field products. A value of 2 means an efficiency of 50%, orthat half of the exported carbon is already balanced by emissionsand only the other half can be accounted for as net relief for theatmosphere. This value is particularly important for the evaluation

of biofuel.

The farm gate balance is another O/I ratio that simply relates theenergy or carbon equivalents that enter and leave the farm via thefarm gate (e.g. Kutsch et al., 2008a). It is easy to derive but ignoreshumus losses and N2O emissions. Therefore, it has to be seen more

338 W.L. Kutsch et al. / Agriculture, Ecosystems and Environment 139 (2010) 336–345

Table 1Average annual values of gross primary productivity (GPP), ecosystem respiration (Reco), net ecosystem production (NEP), harvest, organic inputs and net biome production(NBP) of the sites under consideration.

Site GPP (g C m−2 y−1) Reco (g C m−2 y−1) NEP (g C m−2 y−1) Harvest (g C m−2 y−1) Organic inputsa (g C m−2 y−1) NBP (g C m−2 y−1)

Avignon −1176 1019 −157 272 −5 110Klingenberg −1228 1081 −147 511 −113 251Gebesee −1184 897 −287 465 −122 56Lonzée −1490 1029 −461 483 −23 −1Oensingen −1576 1387 −189 261 −54 18Carlow −807 644 −163 246 −5 78Risbyholm −1262 989 −273 437 −5 159Borgo Cioffib −1624 1280 −344 815 −86 385Suecab −1268 616 −652 357 −5 −300

Averagec −1246 ± 248 1006 ± 222 −240 ± 113 382 ± 117 −47 ± 51 95 ± 87

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a Including organic manure and imported carbon by seeds.b These sites were not included in the averaging.c Average ± standard deviation between sites.

s a measure of economic efficiency of the farm than a measure oflimate change mitigation in agriculture.

.2. Sites

The CarboEurope cropland network comprised 17 sites whereddy covariance measurements were conducted. Out of these, thereere six sites with a crop rotation and three sites with monocul-

ures that provided enough data (at least 4 years) to be used forhis study. Since many aspects of the sites are described in detailn other contributions to this special issue, maps by Eugster et al.2010) and Moors et al. (2010), descriptions of the crop rotations byeschia et al. (2010) and Moors et al. (2010), only a brief descriptionf the sites, that will focus on management and soil properties, isresented here. A list of all the sites is available in Osborne et al.2010). Soil properties of the sites are summarized in Table 1.

.2.1. Full crop rotation sites and sites with long-term cropotations.2.1.1. Avignon, France. The Avignon ‘crane’ site (‘Flux and Remoteensing Observation Site’) at the INRA Research Center near Avi-non, France has crops that are typical for the region, such as durumheat, corn, sunflower, soybean and sorghum, grown on a silty clay

oam soil. Irrigation is performed when required using an irriga-ion ramp, ensuring a complete and even coverage of the field inh. The region is characterized by a typical Mediterranean climateith mean annual temperature of 14 ◦C and mean annual precipi-

ation of 683 mm. The soil is a Calcaric Fluvisol (FAO) with averagearbon concentration of 13.3 g kg−1 and a C/N-ratio of 9.6 in theain footprint area.

.2.1.2. Gebesee, Germany. The station in Gebesee is located in thehuringian Plain in Germany. The area is in the lee of a low moun-ain range and receives only 500–550 mm of annual precipitationith a mean annual temperature of 7.9 ◦C (Anthoni et al., 2004).

he soil is classified as Chernozem (FAO) with a silty clay loamexture (∼30% clay) of granular structure. Total soil organic car-on concentration was 21 ± 1 g C kg−1 in 2001 in the 0–40 cm soil

ayer (Anthoni et al., 2004) and total carbon stock down to 60 cmepth was 131.2 ± 14.2 t C ha−1 (Schrumpf, pers. comm.). The siteas intensively managed until the 1990s and then subsequentlyodified to re-establish soil organic matter that was lost during

he period of intensive cultivation. Deep ploughing was omitted or

educed in some years. In addition, organic carbon was increasedy additions of manure and increasing retention of plant residues.

.2.1.3. Klingenberg, Germany. The Klingenberg Agricultural Sta-ion is located in Saxonia, Germany. The climate is subo-

ceanic/subcontinental with mean annual precipitation of 850 mmand a mean annual temperature of 7.3 ◦C. The soil is a Gleysoil (FAO)which has been drained for agricultural purposes; the organic soilhorizon (Ap) was identified as a medium clayey loam with a meanthickness of 0.2 m. Within the B horizon, mainly slightly sandy clay(Ts2) and clayey sandy loam (Lts) were observed. The mean val-ues of C concentration in horizons Ap and B are 42.6 g C kg−1 and2.9 g C kg−1, respectively (Schrumpf, pers. comm.). The total soilcarbon stock up to 60 cm depth is 97 t C ha−1 and the mean C/N-ratio is 13 (Schrumpf, pers. comm.). In the period between harvestand sowing of the new crop, the site is left mainly as fallow coveredby re-growing weeds or volunteers seedlings left over after harvest.Mineral fertilizer and herbicides were applied several times a year.Organic fertilizer was applied in August 2004 and October 2006.

2.2.1.4. Lonzée, Belgium. The study site at Lonzée is about 45 km SEof Brussels. The climate is temperate maritime with a mean annualtemperature of ∼10 ◦C, with an annual precipitation of ∼800 mm.The soil is a Luvisol (FAO classification) composed of 18–22% clay,5–10% sand and 68–77% silt. Manure has not been applied since1996. The depth of tillage was 30 cm. The soil carbon concentrationin the Ap horizon is 10.8 g kg−1. Total soil carbon stock up to 60 cmdepth is 63.2 t C ha−1 (Schrumpf, pers.comm.). The land has beencultivated for more than 70 years.

2.2.1.5. Oensingen, Switzerland. The Swiss cropland site at Oensin-gen is managed by a regional farmer. The documented crop rotationsince 1994 (see Dietiker et al., 2010) shows a typical 4-year cyclewith either rape or potatoes in one of the years, and barley orwheat in the three other years, which typically leads to full croprotation periods of 8–12 years. The current crop rotation periodwas started in 2000 (for 1997–1999 temporary grassland wasincluded in the crop rotation). The management follows the regula-tions of the Swiss Integrated Pest Management system (IP-Suisse,http://www.ipsuisse.ch). The climate is temperate humid with amean annual precipitation of 1100 mm and an annual mean tem-perature of 8.1 ◦C. The soil is a Eutri-Stagnic Cambisol (FAO) thathas developed on clayey alluvial deposits down to a depth of 1.6 m(Alaoui and Goetz, 2008). The soil contains 28 g C kg−1 organic mat-ter in the top soil layer (0–0.25 m depth) and a pH of 5.5. The soiltexture is a silty clay with 43.0% clay, 47.5% silt and 9.5% sand inthe top layer (Alaoui and Goetz, 2008). The total soil carbon stockis 128 t C ha−1 (0–70 cm depth). Due to a hail event potatoes were

not harvested in 2006.

2.2.2. Monoculture sites with 4 years of measurements2.2.2.1. Carlow, Ireland. The Oak Park cropland site near Carlow,Ireland is part of a long-term conventional cropping system with a

W.L. Kutsch et al. / Agriculture, Ecosystems and Environment 139 (2010) 336–345 339

Fig. 1. Fingerprints of net ecosystem production (NEP) from nine European cropland sites. Red and orange colours mean net carbon dioxide release from the ecosystem tothe atmosphere, while yellow, green and blue means net uptake of CO2 by the ecosystem. The graph (as the subsequent graphs) follows meteorological conventions withnegative numbers meaning net uptake of CO2 by the ecosystem and positive numbers net release of CO2. ‘R’ means re-growth of the crop from lost seeds during harvest.

340 W.L. Kutsch et al. / Agriculture, Ecosystems a

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by high daytime uptake during spring and early summer. Spring

ig. 2. Cumulative net ecosystem production (NEP, above) and net ecosystem car-on budget (NBP, below) from eight European cropland sites that were measureduring the observation period between 2004 and 2007.

ontinuous crop of Spring Barley (Hordeum vulgare) cropping. Cli-ate is maritime with a mean annual temperature of 9.4 ◦C and

n annual precipitation of 823 mm. The soil is a Eutric Cambisol.verage carbon concentration in the top soil is 22.8 g kg−1.

.2.2.2. Risbyholm, Denmark. The Risbyholm experimental site isocated in an agricultural area in central Zealand, Denmark. Theddy correlation equipment is located in a drained bog with His-osol soil type. The organic C concentration of the top soil is5.1 g C kg−1 while the total carbon content is 38.8 g C kg−1. Theeld is part of a slightly undulating landscape covered by glacialeposits (Weichsel). The monthly mean temperature varies from0.1 ◦C in January to 16.3 ◦C in July. The annual precipitation is80 mm with an annual potential evapotranspiration of 490 mm.he field has been cultivated for more than 20 years. For the ordi-ary grain crops the soil is ploughed down to a depth of 25 cm,arrowing and sowing is carried out in one step.

.2.2.3. Borgo Cioffi, Italy. This site is located in a 18 ha agricul-ural field in the middle of Piana del Sele, Italy, a river plainhat comprises the largest flatland area of the Campania region.he alluvial plain in Piana del Sele was re-claimed for agricul-ure after the Second World War. The mean annual temperatures 15.5 ◦C with an annual rainfall of 900 mm, mostly concentratedrom September through April, with a summer dry spell typical ofsouthern mediterranean climate. Alfalfa was continuously grown

rom 1998 to 2003, then a maize monoculture combined with fen-el (2003/2004, 2005/2006, 2006/2007) or rye-grass (2004/2005,

007/2008) as winter crops. Irrigation was performed during theummer by means of a centre pivot system and manure–slurrypplications were done regularly during the alfalfa monoculturend occasionally during the maize monoculture.

nd Environment 139 (2010) 336–345

The parent rock of the soil (sandy–clay type) is carbonate,but most of the material has an alluvial origin, derived from thenearby Sele River. Average particle-size distribution is 43:36:21(clay:sand:silt) but highly variable, so that the texture varies fromclay to sandy clay. The soil contains 15 ± 5 g C kg−1 in the 0–40 cmsoil layer and is classified as a Calcic Kastanozem Skeletic (WRB,2006). The water table depth may be as shallow as 1 m during thewintertime while it is about 5–6 m during the summer. Since theinfluence of these high fluctuations in water table on soil CO2 effluxwas unclear, the site was not considered in the average NBP values.

2.2.2.4. El Saler-Sueca, Spain. The flux site “El Saler-Sueca” islocated inside the protected wetland area “La Albufera NaturalPark” within a large rice paddy field area (ca. 15,000 ha). The cli-mate is Mediterranean sub-arid with dry and warm summers, withno or low excess of water in winter. The mean annual temperatureand precipitation in the area are 17.9 ◦C and 550 mm, respectively.The soil is a Gleysol. Soil depth is at least 2 m. The top soil layer(0–30 cm) is loamy, contains 37.6 g C kg−1.

The site history indicates continuous paddy rice cultivation as amonoculture for 150–200 years and representative of the paddyrice fields of this area. The whole “Albufera” paddy rice area isvery homogeneous in terms of timing (crop period, flooding peri-ods) and management. Management is determined by rice farmingpractices that did not change significantly for about 200 years,apart from mechanisation and use of fertilizers, pesticides and her-bicides. Fields are drained from March to April, flooded in earlyMay for sowing, and drained again in August for rice harvest inearly-mid September. Fields are flooded for the winter period(November–February) in late October after partial burning of strawresidues (the burning practice did not take place at the flux-towerpaddy field in 2006 and in 2007). Since the emissions by burningas well as expected methane emissions were not fully accountedfor, only an incomplete balance of this site can be presented and,therefore, was not considered in the average NBP values.

3. Results

Those sites which were measured during the period between2004 and 2007 were used to derive full 4-year budgets of netecosystem production (NEP) and net biome production (NBP). Thepatterns of NEP observed (Fig. 1) show that the seasonal varia-tions in croplands are much more irregular and fluctuate morethan those of many natural ecosystems with continuous vegeta-tion cover (not shown). Only the monocultures (Risbyholm, Carlow,Borgo Cioffi and Sueca) show a more regular pattern. The fluxes arehighly regulated by management and resulting differences in cropgrowth and development. At some sites (e.g. Lonzée and Gebeseebetween summer 2005 and spring 2006 or Avignon between sum-mer 2006 and spring 2007) long periods of net carbon losses occurduring fallow periods. Regular cover-cropping to improve the car-bon budget of the sites examined in this study (see Osborne et al.,2010) is practised only at few sites (Oensingen and Borgo Cioffi).At some sites the re-growth of the crop from seeds left over afterharvest together with weed establishment resulted in short peri-ods with net carbon uptake during the daytime (marked with ‘R’ inFig. 1).

The different crop species have specific ‘fingerprints’: wintercereals show small uptake during late autumn and winter followed

cereals, maize, potatoes and peas show small periods of intenseuptake during late spring and summer. Sugar beet crop has anextended growing season with a remarkable uptake until harvestin autumn.

W.L. Kutsch et al. / Agriculture, Ecosystems and Environment 139 (2010) 336–345 341

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ig. 3. (a) Total ecosystem respiration as obtained from the Level 4 data (Reco) and nrought to the site by organic fertilizers plotted against gross primary production (Gf the 4 years observation period between 2004 and 2007. (b) Net biome productiooint symbolizes the sum of the 4 years observation period between 2004 and 200

The data for the five crop rotations and the four monocul-ures were integrated over 4 years (Fig. 2, Table 1). However, theve crop rotations and two of the monocultures were used toerive averages, while the sites El Saler and Borgo Cioffi werexcluded due to the reasons explained in the site descriptions.uring 4 years the average NEP of the considered sites was960 ± 452 g C m−2 (Fig. 2a). This results in average annual NEP of240 ± 113 g C m−2 y−1.

The NBP was calculated from the NEP and the lateral fluxes fromarvest and organic fertilizer. On average, 1528 ± 468 g C m−2 werearvested. The respective average annual losses associated witharvest were 382 ± 117 g C m−2 y−1. Thus, harvest losses exceededEP by more than 60%. Manure, applied at Gebesee, Lonzée, Oensin-en, Klingenberg summed up to 167 ± 204 g C m−2 (mean annualnputs over all sites: 42 ± 51 g C m−2 y−1 + 5 g C m−2 y−1 for seeds).

vignon, Carlow and Risbyholm did not receive organic inputs apart

rom an average input of 5 g C m−2 y−1 due to seeds as calculatedy Ceschia et al. (2010). Thus, the average carbon inputs were7 ± 51 g C m−2 y−1.

ig. 4. Schematic representation of the various components of the mean annual carbonnnual value from 4 years of measurements at each site. Two sites of the original ensemn g C m−2 y−1 or g C-equiv. m−2 s−1 when other greenhouse gases are involved. Uncertanformation from other studies is shown without uncertainties.

on yield (Ynet) calculated as carbon removed from the site by harvest minus carbonr five crop rotation and two monoculture sites. Each data point symbolizes the sum) related to soil organic carbon concentration in the top soil of each site. Each data

On average, including all seven sites under consideration, therewas a loss of 380 ± 348 g C m−2 during the 4 observation years(mean annual NBP: 95 ± 87 g C m−2 y−1). The highest losses werefound at Klingenberg (overall NBP: 1004 g C m−2, mean annualNBP: 251 g C m−2 y−1) and Risbyholm (overall NBP: 636 g C m−2,mean annual NBP: 159 g C m−2 y−1), followed by Avignon (over-all NBP: 440 g C m−2, mean annual NBP: 110 g C m−2 y−1), Carlow(overall NBP: 312 g C m−2, mean annual NBP: 78 g C m−2 y−1), Gebe-see (overall NBP: 224 g C m−2, mean annual NBP: 56 g C m−2 y−1),and Oensingen (overall NBP: 72 g C m−2, mean annual NBP:18 g C m−2 y−1). Lonzée (overall NBP: −4 g C m−2, mean annual NBP:−1 g C m−2 y−1) was neutral, while only the Sueca site was an appar-ent sink with −1195 g C m−2 in 4 years, which results in an averageannual NBP of 298 g C m−2 y−1 (not considered in the average).The biggest source, Borgo Cioffi (overall NBP: 1669 g C m−2, mean

annual NBP: 417 g C m−2 y−1), was also not considered in the aver-age.

Another way to examine the impact of the different Europeancrop rotations on ecosystem carbon dynamics is to correlate ecosys-

balance of the croplands under consideration. The data were compiled as meanble (Borgo Cioffi and Sueca) were excluded from this average. Fluxes are depictedinties are derived as standard deviation between sites from this study. Additional

342 W.L. Kutsch et al. / Agriculture, Ecosystems and Environment 139 (2010) 336–345

Table 2Representativeness of the dataset in terms of crops. Number of site years of crop species are compared to their proportion in the EU 27 cropping area and production.

Crop Site years all Site years in average* EU 27 area(1) EU 27 Production(2)

n % n % % in 2007 %

Wheat 10 27.8 10 41.7 27.9 25.6Barley 7 19.4 7 29.2 15.3 11.4Rye 0 0.0 0 0.0 3.0 1.3Maize 5 13.9 1 4.2 9.2 11.3Rice 4 11.1 0 0 0.5 0.6Sugar Beet 2 5.6 2 8.3 2.1 22.5Oil Seed Rape 2 5.6 2 8.3 7.5 3.2Potatoes 2 5.6 2 8.3 2.5 11.4

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ources: (1)FAO stat (http://faostat.fao.org/default.aspx); (2)eurostat (http://epp.euro

em respiration (Reco) derived from the eddy data and net yieldharvested biomass – organic fertilizer brought to the field) withross primary production (GPP). The slopes of the correlation linesere 0.806 (Reco) and 0.302 (net yield), respectively, which means

hat on average the losses were about 110% of the carbon gainedy photosynthesis (Fig. 3a) and the sites are net emitters.

Carbon losses from the ecosystem (positive NBP) were corre-ated with the carbon concentrations in the topsoils (Fig. 3b). Borgoioffi and Sueca are shown in Fig. 3b but were not considered inhe correlation. Oensingen deviated from the correlation mainlyecause the potatoes grown in 2006 were not harvested after aail event. Avignon had relatively high losses despite low carbononcentration in the topsoil.

The average annual carbon and GHG balance of seven Europeanrop sites (Fig. 4) was also determined using data presented byeschia et al. (this issue) and Moors et al. (2010). The full GHG bal-nce sites was estimated to be 160 g C m−2 y−1 in CO2-equivalents.elated to the exported carbon, this means an O/I ratio of 2.4 equiv-lent to ∼42% of the harvested carbon being ‘lost’ by GHG emissionselated to its agricultural production.

For estimating the average farm gate balance the farms wereonsidered as pure cash crop entities with an internal cycling of2 g C m−2 y−1 taken from the harvest as manure. Under this con-iderations the O/I ratio was 9.2, a value that is very close to thatound by Kutsch et al. (2008a) for farms producing only cash cropsn Northern Germany.

. Discussion

The results of this analysis of eddy covariance-based assess-ents of NEP and NBP over several years of crop rotations or ofonocultures indicate carbon losses from all of these agricultural

ites, most of which have been converted to croplands manyecades ago. On average, these sites have received organic inputss organic fertilizers or crop residues have been retained, of aimilar order of magnitude to those recommended through goodractice guidelines for farmers in several countries (Defra, 2000;DLUFA, 2004; Fachstelle Bodenschutz, 2007; FRCA et al., 2008;eProft and Bodson, 2009). However, at sites with high carbononcentrations in the topsoil, in particular, those inputs seem noto be sufficient for a maintaining a balanced agriculture.

If the results reported here are representative for all EU crop-ands, this result may be surprising, since cropland soils in Europe

ould be expected to be close to equilibrium with respect toarbon, as they have been managed as croplands for many years

nd good practice has largely been applied. Recent modellingtudies have suggested that European cropland soils are closeo equilibrium, being either a small source (Smith et al., 2005;ondeau et al., 2007) or a small sink (Gervois et al., 2008; Schulzet al., 2009, 2010; Ciais et al., 2010). However, before we can

12.5 27.5 12.8

100 100 100

c.europa.eu/portal/page/portal/publications/eurostat yearbook).

make any comparison with pan-European modelling studies orassert that European croplands are losing carbon, the uncertaintyassociated with the estimates reported here, and whether theyare generally representative of European croplands, needs to beexamined (see also Osborne et al., 2010).

4.1. Measurement uncertainty – are the estimated carbon lossesdifferent from zero?

Uncertainties in NEP measurements by means of eddy covari-ance arise from a number of systematic as well as random errorsthat have been discussed extensively (Hollinger and Richardson,2005; Richardson and Hollinger, 2005; Loescher et al., 2006;Richardson et al., 2006; Van Gorsel et al., 2007; Aubinet, 2008;Finnigan, 2008; Lasslop et al., 2008). Random errors associated witheddy covariance measurements are not significant at an annualscale as the annual sums are based on more than 15,000 half-hourlyflux estimates. In contrast, systematic and selective systematicerrors are significant. The highest uncertainties are likely associ-ated with night time fluxes (Goulden et al., 1996; Aubinet et al.,2000) due to low turbulence and advection effects. However, ifnight time flux underestimation is especially important in tall forestecosystems or in complex terrain affected by advection (Aubinet,2008; Kutsch et al., 2008b) it is expected to be less critical in crop-land systems, as they have much lower and more homogeneouscanopies and are generally located in flat terrain. Earlier studieson crops estimated the night time flux error to be of the orderof some tens (0–50) of g C m−2 y−1 (Falge et al., 2001; Moureauxet al., 2006, 2008), reaching 100 C m−2 y−1 in two cases (Falge et al.,2001; Anthoni et al., 2004). This systematic bias may however beremoved by applying the so-called u* correction (Aubinet et al.,2000; Gu et al., 2005). However, this correction is based on sev-eral approximations so that a residual uncertainty remains after itsapplication. The main causes of uncertainty are due to the determi-nation of the filtering threshold or to the choice of the gap-fillingalgorithms. Few studies quantify this uncertainty at crop sites.Moureaux et al. (2008) estimated the former at 10 g C m−2 y−1 atLonzée and Falge et al. (2001) found the latter to vary among threesites from 30 to 40 g C m−2 y−1. In Béziat et al. (2009), NEP uncer-tainty due to measurement random errors and to long gaps in thedata set were estimated to range between ±18 g C m−2 y−1 for sun-flower at Auradé and ±42 g C m−2 y−1 for triticale and maize atLamasquère. Another uncertainty arises from the choice of the inte-gration period. With different integration periods Aubinet et al.

(2009) and Prescher et al. (2010) calculated slightly higher NBPvalues for Lonzée and Klingenberg, respectively.

We expect higher uncertainties associated with the quantifica-tion of the lateral fluxes. At some sites (e.g. Klingenberg and BorgoCioffi) removal of harvested products was taken from the farmer’s

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ook keeping, whereas at other sites (e.g. Lonzée and Gebesee)ctual measurements of NPP and harvested material were takenAnthoni et al., 2004; Aubinet et al., 2009; Béziat et al., 2009).ubinet et al. (2009) showed that the uncertainty in NPP estimatesue to biomass sampling amounted to 10–90 g C m−2, i.e., compa-able to those affecting eddy covariance measurements. Béziat et al.2009) also found larger uncertainties for NBP than for NEP, whichere mostly related to uncertainties in C removal by harvest and

n C inputs as organic fertilisation. Carbon inputs associated withrganic manures were consistently calculated from the informationrovided by farmers. Therefore, it is difficult to quantify the uncer-ainties with any degree of accuracy. Aubinet et al. (2009) quotedn overall error of ±140 g C m−2 for 4 years of a crop rotation, whichight be exceeded for some of the sites presented in the current

tudy. Nevertheless, it is important to note that almost all crop rota-ion sites in Fig. 2 behave as sources. The question arises whetherhis fact, as well as the general trend shown in Fig. 3, is statisticallyignificant.

Using standard statistics, there is only weak evidence that NBPiffers from zero at the cropland sites used in this study (two-sided-test, p = 0.237). If we hypothesize that croplands are a net carbonource (i.e., NBP >0), then the statistical uncertainty is still p = 0.119one-sided t-test). The question, however, remains whether theroplands used in this analysis can be considered a random butepresentative sample of the European ensemble of croplands (seeollowing section). If we question this assumption made by the t-est and simply use a normal distribution fitted to the available NBPata from all sites to quantify our statistical uncertainty, then ourypothesis that European croplands are a net carbon source cannote established statistically (p = 0.289).

.2. How representative are the sites examined?

Even though the sites under consideration represent some ofhe most important European crops and cropland areas and cover

any of the typical management practices, it is clear that a few eddyovariance sites can neither represent the diversity of agriculturalractice nor soil or climatic variability. It has to be considered thathe two biggest sources that were used in the averaging, Klingen-erg (drained Gleysol) and Risbyholm (drained Histosol) representwo soils with a high organic matter content, which might be over-epresented in this study compared to the majority of cropland soilsn Europe. The two sites with lower soil organic matter content,ebesee (depleted Chernozem) and Lonzée (Luvisol), which mighte more representative of the larger EU cropland area, showeduch lower carbon losses. However, even at Gebesee the goal of

arbon sequestration or at least a neutral carbon balance was notchieved in spite of the farmer’s efforts with supplementary organicanure and increased residue incorporation.In terms of crop representativeness, a comparison with Euro-

ean crop production (Table 2; Eurostat, 2008) shows that ourataset is quite representative for winter wheat and maize, butverestimates rice and barley, while sugar beet and potatoes arender-represented. Thus, the budgets calculated only for the cropotations might be more representative.

Statistically, the representativeness of the cropland sites net-ork can be shown by a very simple approximation of the required

ample size based on the required precision if we assume each yearo be an independent sample and NPP to be normally distributed.

e can use the following equation by Zar (1998) to determine the

umber of samples required:

=s2 · t2

˛(2),(n−1)

d2(2)

nd Environment 139 (2010) 336–345 343

where n represents the sample size; s2 is the sample variance; tis the two-tailed critical value for Student’s t and d is the half-width of the desired confidence interval. If we define the standarddeviation of the sample as the spatial variability of the mean crop-land annual carbon budget of Europe we are able to determine itfrom remote sensing based approaches like the Terra-MODIS NPPproduct (Running et al., 2004; Heinsch et al., 2006; Turner et al.,2006). The sample standard deviation of the 2000–2004 mean is95.7 g C m−2 y−1. A trial and error process with progressively moreaccurate estimations can be used to set the t value. In our case aconfidence interval commensurate to the above-described uncer-tainties of 50 g C m−2 y−1 with a confidence level of 95%, would leadto a network size of 59 sites. This value is far greater than the actualnetwork size. This suggests that the cropland flux network mightnot adequately represent the variability of climate, soil and man-agement within the European continent and the uncertainties dueto the network design are currently bigger than the uncertaintyintrinsic in the measurement method.

Our results confirm an earlier study of the average croplandNBP made by Janssens et al. (2003) who estimated a carbon lossof 90 ± 50 g C m−2 y−1. However, this work contradicts more recentstudies based on modelling and carbon inventories that resulted inan almost neutral balance for European agriculture (Gervois et al.,2008; Ciais et al., 2010).

4.3. Comparison of apparent losses reported here with lossesestimated by other methods

4.3.1. Stocktaking methodsThe average humus losses for winter wheat without organic

manure and complete removal of straw should be 28 g C m−2 y−1

according to the German consulting agency (VDLUFA, 2004),whereas we calculated losses of 178 g C m−2 y−1 as the average for10 site years in our study. Oil seed rape lost 109 g C m−2 y−1 onaverage although the straw was left on one site. Maize apparentlylost on average about 430 g C m−2 y−1 although organic fertil-izers were applied. Full crop rotations lost, on average, about95 ± 87 g C m−2 y−1, even though the average inputs from manure(around 47 ± 51 g C m−2 y−1) and residues were close to the ratesadvised by good practice guidelines.

The large differences between the estimates here and thosegiven in the good practice guidelines may be partly explained by thedifferent approaches used. Whereas the VDLUFA (2004) estimatesare based on long-term experiments with repeated stocktakingof soil organic matter, our results may reflect more the currentweather/climatic conditions that might not be representative oflonger cropping periods. On the other hand, flux measurementsmay detect changes earlier and may thus perform as an early-warning system. While the flux-based approach presented herehas, as discussed, a number of uncertainties, the biggest uncer-tainty of repeated stocktaking is due to the difficulties of detectinga small change in a large pool (e.g. Rodeghiero et al., 2009). Nev-ertheless, also some studies that use the stocktaking approachsupport our observation that agricultural soils with higher soilorganic carbon content are not balanced and loose carbon (e.g.Bellamy et al., 2005; Saby et al., 2008; Stevens and van Wesemael,2008).

4.3.2. Modelling methodsWhen comparing the present results with modelled estimates,

uncertainty in the modelled estimates also need to be considered.Sources of uncertainty reported in Smith et al. (2005) included alack of knowledge of how much increased production is offset byincreased decomposition in a warmer climate, and uncertainty overthe contribution of technological changes (management, cultivars,

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44 W.L. Kutsch et al. / Agriculture, Ecosys

tc.) on increasing carbon stocks. Other uncertainties arise fromhe steady state assumption: many models use a spin-up run athe beginning of a model run in order to bring soil carbon poolso equilibrium. Smith et al. (2005) as well as Gervois et al. (2008)sed a nominal equilibrium date of 1900 and the model was runorward from then, with results reported in Ciais et al. (2010) for990–1999. The 10,000 years model spin-up with an average agri-ultural practice by Gervois et al. (2008) resulted in an averagequilibrium carbon stock of about 56 t C ha−1 which is lower thanhe average stocks observed in this study. It is perhaps not surpris-ng therefore that these studies did not predict any further lossesetween 1901 and 2000, since sites with higher carbon stocks thatay be far from equilibrium were ignored as they had a shorter

gricultural history than the assumed ten millenia.Similarly, different models use different assumptions about

ield/productivity change over the 20th Century, (see Gervois et al.,008; Smith et al., 2005) and the range of crops considered by theodels differs greatly with just two crops considered by ORCHIDEE

Gervois et al., 2008), 12 by LPJmL (Bondeau et al., 2007) and genericrop inputs only considered by RothC (Smith et al., 2005). Otherifferences include the implementation of land use change duringhe 20th Century and the legacy effects of such change. Given theact that all models used almost the same spin-off procedure andather limited additional information on soils, it is not surprising,hat three models used by Schulze et al. (2009, 2010) and Ciais et al.2010), arrive at rather similar estimates for the annual carbon fluxrom croplands ranging from a small sink of 15 ± 15 g C m−2 y−1

ver the period 1990–1999 estimated using ORCHIDEE (Gervoist al., 2008), through a non-significant sink of 1.7 g C m−2 esti-ated using LPJmL (Bondeau et al., 2007), to a small source of7.6 g C m−2 y−1 estimated using RothC (Smith et al., 2005). Thencertainties associated with the modeled estimates of Europeanropland carbon flux are at least as large as those described in thistudy.

. Conclusions

Despite the uncertainties discussed above, we can concluderom this integrated data-oriented approach that, on average, theuropean croplands under consideration in this study appear tooose carbon, even though the farmers at some of the sites imple-

ented practices such as humus management with low tillage,rganic fertilizer input, inter-cropping and increased straw residueeturn that are considered to enhance carbon sequestration.

Information from the sites with a high soil carbon concentrationuggest that cropping on soils with high carbon contents may resultn hotspots of carbon losses. This fact challenges the equilibriumresumption that is used in many models. In addition, it showshat soils with high carbon concentration und agriculture shoulde targeted in efforts to reduce cropland emissions, while effortsn other soils should focus on sequestering carbon by building upoil organic matter.

We cannot conclude from this study whether the managementf European croplands is, in general, appropriate for humus con-ervation, or whether humus could still be lost in spite of goodractice as a result of already ongoing climate change. The latterould require a change in the good practice guidelines to increase

arbon inputs or to further reduce carbon to account for such arend.

As far as the uncertainty in the fluxes are concerned, it appearshat two factors will push cropland soil carbon in an unfavourable

irection: climate change will likely result in increased mineral-

zation rates, particularly during warmer winters, and efforts toitigate climate change by substitution of fossil fuels with biomass

rom agriculture could result in less residues available for carbonnput into agricultural soils.

nd Environment 139 (2010) 336–345

Acknowledgments

We would like to thank our technical staff and the farmersfor giving us access to their fields and for the time they spentgiving us information concerning management. This work wasmade possible through the support of the CARBOEUROPE-IP (GOCE-CT-2003-505572) European FP7 Program, the French Ministry incharge of Environment (GICC programme), the Centre Nationalde la Recherche Scientifique (CNRS), the Institut National des Sci-ences de l’Univers (INSU), the Région Midi-Pyrénées Council andthe EPA (Ireland) through the CCFLUX project. Foundation CEAMhas been supported by the programs CONSOLIDER-INGENIO 2010(GRACCIE), BALANGEIS (SUM2006-00030-C02) and CARBORED-ES(CGL2006-14195-C02-01). Pete Smith is a Royal Society-WolfsonResearch Merit Award holder.

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