Soil Respiration in European Grasslands in Relation to Climate

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Soil Respiration in European Grasslands in Relation to Climate

UKPMC Funders GroupAuthor ManuscriptEcosystems. Author manuscript; available in PMC 2010 October 7.Published in final edited form as: Ecosystems. 2008 December; 11(8): 1352–1367. doi:10.1007/s10021-008-9198-0.

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Soil Respiration in European Grasslands in Relation to Climate and Assimilate SupplyMichael Bahn1,*, Mirco Rodeghiero2, Margaret Anderson-Dunn3, Sabina Dore4, Cristina Gimeno5, Matthias Drösler6, Michael Williams7, Christof Ammann8, Frank Berninger9, Chris Flechard8, Stephanie Jones3, Manuela Balzarolo4, Suresh Kumar7, Christian Newesely1, Tibor Priwitzer10, Antonio Raschi11, Rolf Siegwolf12, Sanna Susiluoto10, John Tenhunen6, Georg Wohlfahrt1, and Alexander Cernusca11Institute

of Ecology, University of Innsbruck, Sternwartestr. 15, 6020 Innsbruck, Austria 2Centro di Ecologia Alpina-Fondazione Edmund Mach, 38040 Viote del Monte Bondone, Trento, Italy 3Centre for Ecology and Hydrology Edinburgh, Bush Estate, Penicuik, Midlothian EH260QB, United Kingdom 4Department of Forest Science and Environment, University of Tuscia, Via S.Camillo de Lellis, Viterbo 01100, Italy 5Fundación Centro de Estudios Ambientales del Mediterráneo, Parque Tecnológico C/ Charles R. Darwin 14, Paterna, Valencia 46980, Spain 6Department of Plant Ecology, University of Bayreuth, Universitätsstraße 30, Bayreuth 95440, Germany 7Department of Botany, School of Natural Science, Trinity College, University of Dublin, Dublin 2, Ireland 8Federal Research Station for Agroecology and Agriculture, Reckenholzstr. 191, Zürich 8046, Switzerland 9Department of Forest Ecology, University of Helsinki, Latokartanonkaari 7, P.O. BOX 27, Helsinki 00014, Finland 10National Forest Centre-Forest Research Institute, Zvolen 960 92, Slovakia 11Consiglio Nazionale delle Ricerche, Via Giovanni Caproni, Firenze 50145, Italy 12Paul-ScherrerInstitute, Villigen PSI 5232, Switzerland

AbstractSoil respiration constitutes the second largest flux of carbon (C) between terrestrial ecosystems and the atmosphere. This study provides a synthesis of soil respiration (Rs) in 20 European grasslands across a climatic transect, including ten meadows, eight pastures and two unmanaged grasslands. Maximum rates of Rs (Rsmax), Rs at a reference soil temperature (10°C; Rs10) and annual Rs (estimated for 13 sites) ranged from 1.9 to 15.9μmol CO2 m 2 s 1, 0.3 to 5.5μmol CO2 m 2 s 1 and 58 to 1988 g C m 2 y 1, respectively. Values obtained for Central European mountain meadows are amongst the highest so far reported for any type of ecosystem. Across all sites Rsmax was closely related to Rs10. Assimilate supply affected Rs at timescales from daily (but not necessarily diurnal) to annual. Reductions of assimilate supply by removal of aboveground biomass through grazing and cutting resulted in a rapid and a significant decrease of Rs. Temperature-independent seasonal fluctuations of Rs of an intensively managed

pasture were closely related to changes in leaf area index (LAI). Across sites Rs10 increased with mean annual soil temperature (MAT), LAI and gross primary productivity (GPP), indicating that assimilate supply overrides potential acclimation to prevailing temperatures. Also annual Rs was closely related to LAI and GPP. Because the latter two parameters were coupled to MAT, temperature was a suitable surrogate for deriving estimates of annual Rs across the grasslands studied. These findings contribute to our understanding of regional patterns of soil C fluxes and highlight the importance of assimilate supply for soil CO2 emissions at various timescales.

Soil Respiration in European Grasslands in Relation to Climate

Keywords

soil CO2 efflux; temperature; moisture; gross primary productivity; leaf area index; soil carbon; landuse

Introduction

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Soil respiration is the major source of CO2 released by terrestrial ecosystems and constitutesthe second largest flux of carbon between ecosystems and the atmosphere (Raich and

Schlesinger 1992). Current global estimates indicate that soils emit 68–80 Pg C per year (Raichand Potter 1995; Raich and others 2002), which exceeds emission rates from fossil fuel

combustion by a factor of more than 10 (Schlesinger and Andrews 2000). In view of a growinginterest concerning the role of ecosystems in the terrestrial carbon cycle and its feedbacks toclimate change, increasing numbers of studies have explored soil respiration in relation toenvironmental factors and across bioclimatic gradients. Whilst soil respiration (Rs) has beenwell characterized for a range of forest ecosystems (for example, recent syntheses for

bioclimatic transects by Janssens and others 2001; Kane and others 2003; Reichstein and others2003; Hibbard and others 2005; Rodeghiero and Cescatti 2005), comparatively little is knownfor grasslands.

Depending on definition, grasslands cover 20–40% of the land surface. In Europe, grasslandsplay an important role in areas where climate and topography restrict a highly productive useof crops. Therefore, grasslands are frequent in mountain areas of Central, Southern and EasternEurope and the uplands at higher latitudes. There is limited evidence that soil CO2 efflux fromgrasslands may be about 20% higher than that from comparable forest stands (Raich andTufekcioglu 2000). Unfortunately, however, most annual estimates of soil CO2 efflux fromtemperate grasslands date back to the 1970s (compare reviews by Raich and Schlesinger1992; Raich and Potter 1995), when primarily static-chamber methods were applied, whichhave been shown to underestimate Rs rates when fluxes are high (for example, Norman andothers 1997). Recent estimates for annual Rs in grasslands based on dynamic chambers arelargely restricted to seasonally dry, C4 dominated grasslands in North and South America (forexample, Luo and others 1996; Bremer and others 1998; Davidson and others 2000; Wan andLuo 2003). These grassland systems are mostly unfertilized and prone to extended periods ofwater stress, and may therefore exhibit lower rates of Rs than could be expected, for example,for managed grasslands in temperate climates. Up to now no comparative study on Rs is

available for temperate grasslands across a latitudinal transect. Thus, it is an aim of the presentpaper to provide an overview of soil CO2 efflux from differently managed and unmanagedtemperate grasslands along a climatic gradient. We explore the hypotheses that with increasingmean annual temperature (1) annual soil CO2 efflux increases in the absence of extendeddroughts and (2) soil respiration at a reference temperature decreases, indicating a temperatureacclimation of respiratory processes (as suggested by recent studies by Janssens and others2003 and Rodeghiero and Cescatti 2005).

A second objective of this study is to analyze possible effects of assimilate supply on Rs attimescales from diurnal to annual. A number of recent studies have shown that assimilatesupply may strongly affect Rs. Temperature-independent diurnal variations of Rs under treeshave been suggested to result from changes in photosynthesis (Tang and others 2005; Baldocchiand others 2006; Liu and others 2006). An interruption of the transport of assimilates to thesoil by tree girdling results in a substantial decrease of soil CO2 efflux (Högberg and others2001). Likewise, reductions in assimilate supply by shading and/or clipping have been shownto reduce grassland Rs (for example, Craine and others 1999; Wan and Luo 2003; Bahn andothers 2006). Estimates of the temperature sensitivity of Rs are often confounded by

Soil Respiration in European Grasslands in Relation to Climate

unidentified processes of substrate supply (compare reviews by Davidson and others 2006;Davidson and Janssens 2006). At an annual timescale Rs in forests is closely related to grossprimary productivity (GPP) and leaf area index (LAI) (Janssens and others 2001; Reichsteinand others 2003; Hibbard and others 2005), indicating a coupling between the amounts ofCO2 assimilated by forest canopies and released from the soil. We expected that, similarly, ingrasslands soil respiration responds to assimilate supply (1) at the diurnal scale, rates at a giventemperature being higher during daytime than at night, (2) at the daily to weekly scale in relationto grassland management (cutting and grazing), and (3) at the annual scale in relation to GPPand LAI.

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Methods

Sites

The sites were studied within the EU-Framework Program 5 projects CarboMont (Cernuscaand others 2008) and GreenGrass (Soussana and others 2007) and cover a latitudinal transectfrom 41 °90′ N to 67°72′ N and an altitudinal range from 50 m (Carlow, Ireland) to almost2000 m a.s.l. (Stubai, Austrian Alps) (Table 1), mean annual air and soil temperatures rangingfrom 1.0 to 10.1°C and from 3.3 to 11.8°C, respectively. Mean annual precipitation rangesfrom 500 to 1760 mm. Grasslands include meadows that are fertilized and cut at least twice ayear (intensive use; Oensingen 2, Stubai 1), lightly used meadows that are unfertilized orslightly fertilized, cut once a year and are mostly grazed during short periods late in the season(all other meadows), a fertilized intensive pasture that is cut for silage and is grazed extensivelyfrom then onwards (Carlow), moderately grazed pastures, abandoned and natural (unmanaged)grassland. For details on site characteristics refer to Table 1.

Soil Respiration Measurements

The two major systems used in this study were the LI 6400-09 soil respiration chamber

combined with a LI 6400 IRGA (Li-Cor, Lincoln, NE, USA) and the upgraded SRC-1 chamberin combination with an IRGA of the same company (EGM 1, 2 and 4, CIRAS-1) (PPSystems,Hitchin, Herts, UK) (Table 1). On several occasions these two systems were cross-compared(October 2002, Stubai Valley; April 2004, Innsbruck; August 2004, Seebodenalp; September2004, Monte Bondone; summer 2005, Viterbo), indicating a good agreement (on the averageless than 5% difference) between the systems applied on the same collars. At the Berchtesgadensites a manually operated closed system (home-made system as described by Velthof andOenema 1995, combining a chamber with a vent with IRGAs (Li-800 and Li-6262, Licor,Lincoln, NE, USA) was applied (compare also Pumpanen and others 2004). At Polana a home-made chamber was attached to an infrared gas analyzer (Li 6250, Li-Cor, USA). At Alinya andat the Stubai sites in addition to the closed chamber systems home-made open systems wereinstalled. For measurements, all chambers were placed on collars, which had been inserted intothe soil at least 24 h prior to measurement (Bahn and others 2008). Aboveground vegetationwas removed from inside the collars before measurements were started. In parallel to soilrespiration measurements soil temperature (using soil temperature probes) and soil moisture(using TDR probes) were recorded.

Additional Site Parameters

Continuous half-hourly means of soil temperature and moisture were obtained with

microclimate stations using soil thermocouples and TDR sensors. Soil carbon stocks weremeasured on at least nine cores per sites, except at Värriö where fewer large soil monolithswere excavated. Sieved and root-free soil samples were analyzed for C using elementalanalyzers. Leaf area index and standing biomass and were measured from samples cut at thesoil surface. Leaf area was determined using leaf area meters. For biomass estimates sampleswere oven-dried at 70–80°C. Gross primary productivity was estimated from eddy covariance

Soil Respiration in European Grasslands in Relation to Climate

measurements, as described by Wohlfahrt and others (2008) and Gilmanov and others(2007).

Annual Totals of Soil Respiration

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Annual totals of soil respiration were estimated by applying the following functions, which

were fitted against the measured values.

(1)

where Rs denotes soil respiration rate (μmol CO2 m 2 s 1); a, b and k are fitting parametersand Ts

is soil temperature (°C) (compare Rodeghiero and Cescatti 2005).

(2)

where Rs10 is the soil respiration rate at 10°C and Eo is the activation energy (Lloyd and Taylor1994, Eqn. 1).

For the sites Alinya, Monte Bondone and Carlow inclusion of soil water content as a separateparameter resulted in a distinctly better model fit; therefore, a Gompertz function (Janssens

and others 2003) was added to Eqn. 2:

where a and b are fitting parameters and Ms is the soil moisture (relative volumetric soil watercontent, %).

A nonlinear estimation least squares method (STATISTICA, StatSoft, Inc., 2005) was used tofit the models and derive model parameters. For estimating the generalization error of theapplied models (Eqs. 1, 2, 3), and testing their performance, we applied a holdout validationmethod (Shao 1993). For each site the original dataset was separated in two datasets called the“training set” and the “testing set”. The testing set was selected by randomly sampling 20% ofthe original data, according to their temperature frequency distribution. The remaining 80% ofthe data belonging to the training set was used for model fitting and to derive the modelparameters with a nonlinear estimation least square method (STATISTICA, Statsoft, Inc.,2005). We preferred the holdout validation method to a more complex k-fold cross validation(Shao 1993), because the datasets were large enough to allow for extraction of 20% of the data,leaving at the same time enough data for model fitting (more than 21; Table 2). Table 2

summarizes the model parameters and r2, as well as linear regression statistics of the validation.At all sites residuals of predicted versus observed values of Rs were plotted against Ms, r2values of the linear regressions are reported in Table 2. The models (1)–(3) were comparedwith respect to r2, mean absolute error (MAE) and model efficiency (ME) (compare forexample, Medlyn and others 2005;Richardson and Hollinger 2005), and the best performingmodel was selected for estimating annual totals of soil respiration for each site (Table 2).Annual soil CO2 efflux was calculated as the sum of single half-hourly fluxes obtained frommodel outputs based on continuously recorded soil temperature and moisture data. There areseveral approaches to estimating the uncertainty of modelled annual totals of fluxes, includingMonte Carlo and bootstrap simulations (Richardson and Hollinger 2005). We decided to adopta simpler approach, which is more conservative than the ones mentioned above and thus likelyprovides comparatively higher uncertainty estimates. We binned the data to equally sized Ts

Soil Respiration in European Grasslands in Relation to Climate

Bahn et al.UKPMC Funders Group Author ManuscriptResults

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classes. For each class the average and the 95% confidence interval of Rs were calculated,which were each used for parameterizing the equation previously applied for the site (compareLavigne and others 1997) and calculating annual Rs and its confidence interval as describedabove. Following this approach the uncertainty estimate for a selected site (Stubai 1) isapproximately five times higher (11.2%, Table 2) than when applying a bootstrap analysis(2.2%), and about half the value when the bootstrap analysis is combined with a Monte Carlosimulation (assuming a Gaussian uncertainty of 20%) of soil temperature (24%).

Rates of soil respiration at a reference temperature of 10°C ( 2Rs s 1 (Table 1) and increased with increasing mean annual soil temperature, C content10) ranged from 0.25 to 5.49μmol mof the upper soil layers, peak leaf area index and annual gross primary productivity across sites(Figure 1A–D). Maximum Rs exceeded 14 μmol m 2 s s 1 for a number of Central Europeansites, reaching values of up to 15.9 μmol m 2 s 1 on warm summer days (Table 1, Figure 2).Across sites maximum Rs rates were not correlated with associated soil temperatures, butgenerally increased with increasing Rs) based on the pooled data sets and calculated for a common temperature range (at10 of a site (Figure 2A, B). The temperature sensitivityof Rs (Q105 cm depth) from 10 to 15°C ranged from 2.0 to 4.9 and was not related to mean annual soiltemperature (r2 = 0.01; not shown).

Soil moisture constrained Rs at higher soil temperatures at most sites. This is reflected by thelogistic model, whose sigmoid shape levels Rs at higher Ts when limitations due to low soilmoisture are frequent, and the Lloyd and Taylor model combined with a Gompertz-function,which modifies the temperature response of Rs in relation to soil moisture. Reductions of Rsby low soil moisture were most pronounced at the Spanish site Alinya, which—with theexception of the northernmost site Värriö—was characterized by the lowest amounts of annualprecipitation (Table 1). Two time series illustrate the course of Rs at Alinya during two summerperiods immediately before and after short rainfall events. In July 2003 Rs was low and itsdiurnal variation was minor until after a rain event when soil moisture increased from less than10 to more than 20 vol%. After a short time lag following the rain pulse soil CO2 efflux doubledand then followed a distinct diurnal pattern (Figure 3A). As soil moisture dropped below 10vol% during the subsequent days, Rs was again reduced to values occurring before the rain,with a decreasing response to Ts fluctuations. In June 2004, soil moisture never decreased toless than 20 vol%, and an increase in soil moisture after rain did not alter Rs rates and theirresponse to Ts (Figure 3B).

The temperature response of Rs was not only influenced by thresholds of soil moisture, butvaried under non-limiting water supply in the course of the day. This was particularly obviouson clear days, when a hysteresis effect occurred, which became more apparent when relatingsoil CO2 efflux to temperature at increasing soil depth (Figure 4A–C). When related to a givenTs at 1 cm soil depth Rs was higher in the late afternoon as compared to the morning hours(Figure 4A), whereas in relation to a given Ts at deeper soil layers Rs was highest duringmorning hours and lowest at night (Figure 4B–C). On a cloudy day at a given Ts at 1 cm eveningand early night-time values of Rs were slightly higher than during the rest of the day (Figure4D), whereas no clear temperature response and temperature-independent pattern of Rs wereobserved in relation to temperatures at deeper soil layers (Figure 4E–F).

At a daily to weekly timescale land use affected Rs and its response to Ts. At Monte BondoneRs of clipped plots was reduced by approximately 10% relative to adjacent unclipped plots,and recovered after about 2 weeks (data not shown). At Amplero clipping resulted in a reductionof Rs by more than 50% at two periods during August, and by almost 30% later in the season,whereas it caused an increase in soil temperature during all periods (Figure 5). Additional

Soil Respiration in European Grasslands in Relation to Climate

grazing caused a further significant reduction of Rs only in late August (Figure 5). At Carlowa silage cut early in the season followed by subsequent extensive grazing resulted in distinctseasonal fluctuations of LAI, which explained much of the variation of observed versuspredicted Rs values, as based on the seasonal relationship between Ts and Rs (Figure 6).

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Annual soil CO2 efflux from the grasslands ranged from 58 to 1988 g C m 2 y 1 (Table 2), theaverage being 1108 g C m 2 y 1. The highest values were found for meadows in the Alps(Oensingen, Stubai Valley, Monte Bondone), the lowest occurred at the northernmost site inFinland (Värriö). The uncertainty of the annual estimates was 9–25% for most sites, but ashigh as 40 to almost 90% for three sites in different parts of the European transect (Table 2).Across sites annual Rs was closely related to mean annual Ts (Figure 7A). Without the twoMediterranean sites (Amplero, Alinya), whose annual totals were distinctly below the

regression line, r2 of the regression increased from 0.81 to 0.92 (P < 0.001). Across sites annualRs increased with increasing soil C content in the upper soil layers (r2 = 0.65; not shown) andpeak leaf area index (Figure 7B, without values for Auchencorth Moss r2 = 0.77), and was verywell correlated with gross primary productivity (Figure 7C), but exhibited no relationship withpeak aboveground biomass (r2 = 0.02; not shown).

Land use of the grasslands studied was generally related to mean annual soil temperature(Figure 7A), which decreased from meadows (mean annual Ts across sites 9.5 ± 0.6°C) topastures (8.3 ± 0.7°C), and the natural grasslands (5.1 ± 1.8°C). Thus it is not possible toseparate effects of land use on annual Rs from those related to temperature. Average annualRs pooled for meadows, pastures and natural grasslands was 1520 ± 151, 865 ± 155 and 293± 236 g C m 2 y 1, respectively.

Discussion

Soil Respiration in Relation to Climate and Site Productivity

Raich and Schlesinger (1992) and Raich and Potter (1995) showed that at a global scaletemperature is the single best predictor of annual Rs in the absence of water stress. Morerecently, several authors have pointed out that a consideration of productivity (for example,gross primary productivity, GPP) or surrogates of productivity (for example, peak leaf areaindex, LAI) improves predictions of annual Rs of forests (Janssens and others 2001; Reichsteinand others 2003; Hibbard and others 2005), especially in cases when GPP does not increaseconsistently with temperature (Janssens and others 2001). Dornbush and Raich (2006) havedemonstrated for central Iowa grasslands that, in contrast, aboveground net primaryproductivity (ANPP) is less suited for predicting intra-annual variations of Rs than soiltemperature.

All these observations are well supported by our data. We found that across sites annual Rswas closely related to GPP and LAI (Figure 7C, D). At the same time peak standing biomass,a proxy for ANPP, did not explain intersite variations of annual Rs. This, however, was notunexpected, as peak standing biomass underestimates productivity in grasslands that are cutmore than once a year or that are intensively grazed, and it likely overestimates productivityin unmanaged sites. Moreover, estimates of site productivity from aboveground biomass maybe strongly biased, as they ignore belowground productivity as well as dying and decomposingbiomass. Mean annual Ts was a very good predictor of annual Rs across sites, except for thetwo Mediterranean mountain grasslands, which exhibited distinctly lower annual Rs thanexpected from its relationship to mean annual Ts. For these two cases proxies or direct measuresof soil moisture (compare Table 2; Figure 3) would need to be included in models accountingfor the variability of Rs at larger scales (Raich and others 2002; Reichstein and others 2003).The fact that the slope of the temperature–respiration relationship of the grasslands studied(Figure 7A) was best described by a power rather than a linear (Raich and Schlesinger 1992)

Soil Respiration in European Grasslands in Relation to Climate

function may be explained by the fact that land use changed from pastures to more productive,fertilized meadows as annual temperatures increased.

There is some disagreement between studies on whether (Smith 2003; Rodeghiero and Cescatti2005) or not (Janssens and others 2003; Reichstein and others 2003) soil C content influencesRs. Rodeghiero and Cescatti (2005) suggested that a lack of standardized protocols for soil Csampling and a confusion of the terms concentration and content may obscure a possiblerelationship of soil C content and respiration. Our data indicate an increase in annual Rs withsoil C content in the uppermost soil layers. It should, however, be noted that sites with highsoil C content were also characterized by higher productivity. The degree to which soil effluxis coupled to soil C content may be largely determined by the proportions of labile versusrecalcitrant C (Gu and others 2004; Davidson and Jansssens 2006), as well as priming effectson soil organic matter decomposition through fresh organic C from litter-fall and root exudation(Kuzyakov 2002; Pendall and others 2003; Subke and others 2004), which may be coupled toshort-term assimilate supply as related to gross primary productivity.

Soil respiration at a reference temperature (Rsref) has often been used as an input for temperaturedependent models of Rs and as a key parameter for comparing Rs across bioclimatic transects(Janssens and others 2003; Reichstein and others 2003; Hibbard and others 2005; Rodeghieroand Cescatti 2005). Our study indicates that Rsref is also well suited for predicting maximumrates of Rs occurring across sites (Figure 2B). Recently some authors interpreted an observeddecrease of Rsref with increasing mean annual temperature along bioclimatic transects as anindication of acclimation of the respiration of roots and microorganisms (Janssens and others2003; Rodeghiero and Cescatti 2005). This interpretation is not supported by our results, whichshow that Rsref increases with mean annual Ts (Figure 1A). As Rsref increased with site

productivity (GPP, LAI) across all these mentioned studies (compare also Reichstein and others2003; Hibbard and others 2005) it appears that site productivity rather than acclimation to amean annual temperature determines Rsref, indicating that substrate supply overrides potentialacclimation.

Magnitude of Grassland Soil Respiration and Its Significance for Partitioning EcosystemCarbon Fluxes

Soil CO2 efflux varied considerably across the grasslands studied. Peak values, as regardsinstantaneous maximum flux rates, rates at a reference temperature and annual totals, wereamongst the highest reported in the literature (Table 3). Especially Central European meadowsexhibited distinctly higher rates and annual totals of soil CO2 efflux than has previously beendocumented for most forests and grasslands (Table 3). These meadows are characterized bycomparatively high Ts during summer coupled with only minor restrictions due to low soilmoisture, by fertilization and, in consequence, by a comparatively high peak leaf area indexand gross primary productivity. Comparatively low values of CO2 efflux of less than 1 μmolm 2 s 1 during winter were compensated by very high respiration rates during summer (up to14–16 μmol m 2 s 1) yielding annual totals in the range of 1743–1988 g C m 2 y 1 (Tables 1,2). For a lightly grazed grassland on the Tibetan plateau a similarly high annual soil CO2 effluxwas estimated (Cao and others 2004, Table 3).

Attempts to quantify soil CO2 emissions at scales from ecosystems to the globe (Raich andSchlesinger 1992; Raich and Potter 1995; Schlesinger and Andrews 2000; Raich and others2002) rely very much on the accuracy of estimates of annual totals and their underlyingparameters. However there is still a considerable uncertainty in such estimates (for example,Hibbard and others 2005; this study), which may result from inevitable tradeoffs betweentemporal and spatial data coverage (Savage and Davidson 2003), the large amount of abioticand biotic drivers and their interactions that may vary, and often co-vary, in the course of theyear (for example, Davidson and others 2006) and interannually (Raich and others 2002) and

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Soil Respiration in European Grasslands in Relation to Climate

the vast diversity of C substrates and enzymes, which so far constrain mechanistic approachesto modelling soil respiration (Davidson and Janssens 2006). Such uncertainties not only reducethe value of estimates of the magnitude of individual fluxes, but also limit their usefulness forpartitioning ecosystem carbon fluxes. A particularly critical aspect concerning estimates ofecosystem CO2 component fluxes is related to systematic differences between differentmethods. This is a major constraint when, for example, relating absolute values of annual Rs(based on chamber measurements) to those of GPP (derived from eddy covariance

measurements) (Table 1, Figure 7D). Generally, chamber-based estimates of fluxes (as mostlyapplied for soil respiration measurements) tend to yield distinctly (20–40%) higher values thanthose based on eddy covariance measurements (for example, Goulden and others 1996;Lavigne and others 1997; Drewitt and others 2002; Bolstad and others 2004; Wohlfahrt andothers 2005a). There are a number of major reasons for these discrepancies. These include: (1)differences in spatial sampling/footprint area (Lavigne and others 1997; Drewitt and others2002; Davidson and others 2002); (2) overestimation of dynamic chamber-based fluxesthrough underpressure created in chamber headspace by surface wind (Bain and others2005); (3) underestimation of EC-based respiration fluxes through advection or insufficientturbulence/mixing at night (Goulden and others 1996; Lavigne and others 1997). (4) Daytimerespiration rates may be overestimated when extrapolating from EC-based nighttime datarespiration fluxes due to a neglected reduction of leaf respiration in light (Atkin and others1997; Amthor and Baldocchi 2001; Wohlfahrt and others 2005b). (5) Daytime respiration ratesextrapolated from nighttime data usually do not account for possible temperature-independenteffects on Rs (Tang and others 2005; Liu and others 2006; this study, but see discussion below).Therefore, care should be taken when using soil respiration data based on chamber

measurements for partitioning ecosystem, regional or global fluxes of CO2, which are basedon different methodologies.

Soil Respiration and Short-Term Changes in Assimilate Supply

In recent years it has become increasingly evident that soil respiration is closely related tocanopy photosynthesis at various timescales. As discussed above, GPP and its surrogate LAIare generally well correlated with annual Rs. Also at the seasonal timescale we observed in anintensively managed pasture that the residuals of the temperature–respiration relationshipcould be well explained by changes in LAI (Figure 6). Likewise, Reichstein and others(2003) found that across a range of forest ecosystems residual Rs (based on a model usingtemperature and precipitation as a predictor) was closely related to LAI. Bremer and Ham(2002) found for an intensively grazed Konza prairie that LAI needed to be considered to obtainrealistic estimates of annual Rs. Our cutting and grazing experiments indicate that removal ofthe leaf mass may result in a significant reduction of Rs (Figure 5) and its temperature

sensitivity. This is in agreement with observations from tallgrass prairies and a pasture on theTibetan plateau (Bremer and others 1998;Johnson and Matchett 2001;Wan and Luo 2003;Caoand others 2004). In contrast, it has also been observed that soil warming following clippingmay override effects of reduced assimilate supply and lead to an increase in Rs (Bahn and others2006). However, when corrected for such temperature effects Rs is consistently reduced byclipping within 1–2 days (Wan and Luo 2003;Bahn and others 2006; this study), which isarguably the effect of a lack of assimilate supply by photosynthesis.

These findings strongly favor the view of a close short-term coupling of photosynthesis andRs. Evidence also comes from isotopic studies demonstrating that in forests Rs is largely drivenby freshly produced photosynthates and that time-lags for the isotopic signal from treephotosynthesis to appear in Rs are in the range of 1–10 days (Ekblad and Högberg 2001;Bowling and others 2002; Ekblad and others 2005; Steinmann and others 2004). It remains,however, somewhat speculative to what extent Rs is affected by photosynthesis at a diurnaltimescale. Recently, it has been shown that temperature-independent diel variations of Rs occur,

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Soil Respiration in European Grasslands in Relation to Climate

which have been interpreted as modulating effects of photosynthesis (Tang and others 2005;Baldocchi and others 2006; Liu and others 2006). Our results indicate, similarly, that there isa diurnal hysteresis in the temperature–Rs relationship (Figure 4). However, especially onsunny days the pattern changes depending on the soil depth at which temperature is measured(Figure 4A–C). Such a diel hysteresis, which can also be depicted by the residuals of observedversus predicted values of the temperature–respiration relationship (Liu and others 2006), maybe determined by a number of factors that produce a time lag between the rate of CO2 fluxemitted from the soil and the Ts at a given depth, the most predominant ones being (1) shiftsin phase and amplitude of soil temperature with depth, (2) diurnal changes of soil moistureclose to a critical threshold value, (3) time lags between CO2 production in various soil layersand the diffusion of CO2 out of the soil (which may be more relevant when soil moisture ishigh) and (4) possible effects of diurnal changes in the supply of newly produced

photosynthates on root and rhizosphere respiration. In the case of Figure 4 soil moisture isunlikely to have determined the observed hystereses (compare Figure 3 and section “Results”).However, it is not possible to clearly separate potential effects of progressive changes in Tsand of photosynthesis. Even when assuming (1) a constant basal respiratory activity and (2) aconstant temperature response across all soil layers as well as (3) no short-term effects ofphotosynthesis on soil respiration, a diurnal hysteresis in the relationship between soil

temperature at any fixed depth and soil respiration would occur, because shifts in phase andamplitude of soil temperature with depth during the day create time lags in the relationship(Reichstein and others 2005). However, it is likely that respiratory activity and its temperatureresponse are not evenly distributed in the soil, being higher in soil layers with high root activityand lower in deeper soil layers where little or no rhizosphere priming of the soil organic matterdecomposition occurs (for example, Boone and others 1998; Kuzyakov 2002; Pendall andothers 2003; Fontaine and others 2004). In that case effects will be much more confoundedand preclude a clear interpretation of an apparent diurnal relationship of canopy photosynthesisversus soil respiration (as described for example, by Tang and others 2005). A way forward inunderstanding the short-term coupling between canopy photosynthesis and Rs would be tomonitor diurnal changes in CO2 production in the main rooting horizon together with theassociated Ts and moisture, together with canopy photosynthesis, and/or to carry out factorialmanipulation experiments including isotopic pulse labelling.

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Conclusions

This study provides the first synthesis of soil respiration in temperate (mostly mountain)grasslands along a climatic transect, documenting that soil CO2 efflux from Central Europeanmeadows is amongst the highest so far reported for any type of ecosystem. The study indicatesthat in and across grasslands soil respiration is closely related to assimilate supply for timescales from daily (but not necessarily diurnal) to annual. Across sites Rs10increased with meanannual soil temperature (MAT), LAI and gross primary productivity (GPP) indicating thatassimilate supply overrides potential acclimation to prevailing temperatures. Also annual Rswas closely related to LAI and GPP. Because the latter two parameters were coupled to MAT,temperature was a suitable surrogate for deriving estimates of annual Rs across the grasslandsstudied. Thus, our study contributes to an understanding of regional patterns of soil C fluxes,and highlights the importance of assimilate supply as a major driver of soil CO2 emissions andthe necessity of future work examining more explicitly a direct short-term coupling betweencanopy photosynthesis and soil respiratory fluxes.

Acknowledgments

The study was funded by the EU FP5 projects CarboMont (EVK-2001-00125) and GreenGrass (EVK-2001-00105);data analysis was supported by the Austrian National Science Fund (FWF) project P18756-B16. We acknowledgeassistance in data collection by Nadine Pfahringer, Anton Pallua, Anton Stefan Schwarz, Robert Bajo, ChristianSkublics, Yuelin Li and Silvia Baronti.

Soil Respiration in European Grasslands in Relation to Climate

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Figure 1.

Soil respiration at a reference temperature (10°C) in relation to A mean annual soil temperature(r2 = 0.69, P < 0.001), B soil C content in the uppermost 20–25 cm of the soil (r2 = 0.50, P <0.05), C peak leaf area index (r2 = 0.55, P < 0.01) and D annual gross primary productivity(r2 = 0.88, P = 0.001). Meadows (▲), pastures (●), unmanaged Northern grasslands (◇).

Soil Respiration in European Grasslands in Relation to Climate

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Figure 2.

Maximum rates of soil respiration in relation to 2A the associated soil temperature and B soilrespiration at a reference temperature (10°C) (r = 0.87, P < 0.001). Meadows (▲), pastures(●), unmanaged Northern grasslands (◇). Error bars denote standard deviations obtained forthe highest spatially replicated soil respiration rates (n = 3–9) recorded at a single point of time.

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Figure 3.

Soil respiration (◆), soil temperature (dashed line) and soil moisture (solid line) before andafter rainfall during summer periods in A 2003 and B 2004 at Alinya. Bars indicate the timingand the amount rainfall. Soil respiration was measured using a continuous system on fivecollars, which were changed on DOY 206 in 2003, as indicated by different symbols. Note thedifferent scales in A and B.

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Figure 4.

Diurnal changes of soil respiration (Rs) in response to temperature at 1, 3 and 10 cm soil depthon a clear (18 June 2004; A–C) and a subsequent cloudy day (19 June 2004; D–F) at Alinya.Consecutive hourly means have been connected by lines, inserts indicate time of the day. Forfurther details on the time course of soil respiration, soil temperature and soil water contentrefer to Figure 3B.

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Figure 5.

Effects of clipping and grazing on A soil CO2 efflux and B soil temperature at Amplero duringthe summer of 2004 (for each treatment n = 9).

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Figure 6.

Residuals of observed minus predicted values of soil respiration at Carlow in relation to

seasonal values of leaf area index (LAI) in 2003 (r2 = 0.70, P < 0.001, when excluding the datapoint indicated with an open symbol from the regression).

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Figure 7.

Annual soil respiration in relation to 2A mean annual soil temperature (r2 = 0.81, P < 0.001),B peak leaf area index (r = 0.74, P < 0.001) and C annual gross primary productivity (r2 =0.94, P < 0.001). Meadows (▲), pastures (●), unmanaged Northern grasslands (◇).

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