Carbon budgets in fertile silver birch (Betula pendula Roth) chronosequence stands

Ecological Engineering 77 (2015) 284–296

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Carbon budgets in fertile silver birch (Betula pendula Roth) chronosequence stands Mats Varik a, * , Mai Kukumägi b , Jürgen Aosaar a , Hardo Becker a , Ivika Ostonen b , Krista Lõhmus b , Veiko Uri a a b

Department of Silviculture, Institute of Forestry and Rural Engineering, Estonian University of Life Sciences, Kreutzwaldi 5, 51014 Tartu, Estonia Department of Botany, Institute of Ecology and Earth Sciences, University of Tartu, Lai 40, 51005 Tartu, Estonia

A R T I C L E I N F O

A B S T R A C T

Article history: Received 12 May 2014 Received in revised form 19 January 2015 Accepted 25 January 2015 Available online xxx

Carbon (C) budgets were compiled for silver birch chronosequence stands by synthesizing the above- and belowground C pools and fluxes with the aim to assess the impact of age on stand C sequestration and cycling. The fine root (d < 2 mm) biomass, production, turnover rate and longevity of 13-, 32- and 45-year-old silver birch stands were determined by the ingrowth core method. Fine root production after the third year from the installation of cores was 0.89, 1.44 and 1.31 t ha
1 year
1 in the pole, middle-aged and premature silver birch stands, respectively. Soil respiration (Rs) was measured during the two growing seasons of 2010 and 2011; the trenching method was used to estimate the contribution of heterotrophic respiration (Rh) to total soil respiration. Soil temperature was the driving environmental factor of the temporal variation of Rs and Rh. Stand age affected significantly respiration rates. Annual Rs was 6.2, 9.7 and 8.2 t C ha
1 and annual Rh was 2.97, 4.21 and 3.61 t C ha
1 in the pole, middle-aged and premature silver birch stands, respectively. The annual contribution of Rh to Rs was similar in each stand ranging from 0.43 to 0.48. Total annual net primary production (NPP) of the ecosystems of 7.4, 7.9 and 8.5 t C ha
1 year
1 was estimated in the pole, middle-aged and premature stands. After balancing the C input and output fluxes in the silver birch stands of different development stages, it appeared that they all acted as effective C sinks. Net ecosystem production (NEP) was 4.4, 3.7 and 4.9 t C ha
1 year
1 in the pole, middle-aged and premature stands, respectively. In the premature stand the second layer of the spruce contributed significantly to the increased C input. The annual organic C input into the soil through above- and belowground litter occurred to be of the same magnitude as C loss via annual heterotrophic respiration. Thus, annual increment of woody biomass in fertile silver birch stands reflects annual organic C sequestration in the ecosystem. Among the studied stands, estimated NEP values were the lowest in the middle-aged stand and the highest in the oldest stand, indicating non-linear relationship between stand NEP and stand age. ã 2015 Elsevier B.V. All rights reserved.

Keywords: Carbon fluxes Fine root production Soil respiration Heterotrophic respiration C sequestration

1. Introduction Quantification of the ecosystem carbon budget (ECB), i.e. estimation of all carbon (C) storages and fluxes, is crucial for understanding of the functioning of the ecosystem and its C sequestration capacity. Carbon cycling is directly related to changing climate and anthropogenic or silvicultural management (Schimel et al., 2001; Heimann and Reichstein, 2008; Wu et al., 2013; Verlinden et al., 2013; Walle et al., 2007). In the light of the

* Corresponding author. Tel.: +372 731 3112/53 432 592. E-mail address: [email protected] (M. Varik). http://dx.doi.org/10.1016/j.ecoleng.2015.01.041 0925-8574/ ã 2015 Elsevier B.V. All rights reserved.

Kyoto Protocol, transparent reporting and monitoring of carbon sinks is required (IPCC, 2003). Efforts have been made to report the data of organic C accumulation and C balance at the country level in several countries; also governments are requested to report C pool changes in forests (e.g. LULUCF). Among them, belowground C should be taken into account (Brunner et al., 2013). Belowground biomass is still often the inadequately or discordantly estimated part of the C budget of forest ecosystems, despite the fact that belowground biomass, including the fine roots, may be crucial contributor to the C cycle (Jackson et al., 1997; Gill and Jackson, 2000; Yuan and Chen, 2010, 2012). Fine root production and turnover can account for 8–75% of global annual net primary production (NPP) in forested ecosystems (Keyes and Grier, 1981;

M. Varik et al. / Ecological Engineering 77 (2015) 284–296

Fogel, 1985; Nadelhoffer and Raich, 1992; Persson, 1992; Gower et al., 1996; Vogt et al., 1996; Jackson et al., 1997; Gill and Jackson, 2000; Helmisaari et al., 2002), being one of the main pathways through which C enters the soil (Vogt, 1991). Thus, accurate estimation of fine root production and turnover are essential for ultimate understanding of C and nutrient cycling in terrestrial ecosystems, which allows to improve and refine C budget models (Woodward and Osborne, 2000; Ostonen et al., 2005; Yuan and Chen, 2010; Finér et al., 2011; Brunner et al., 2013; Li et al., 2013). However, fine root production, morphology and biomass dynamics are complex processes that vary spatially and temporally and are greatly influenced by forest type, site quality, climate, soil nutrient status and properties, stand age, etc. (Nadelhoffer and Raich, 1992; Eissenstat and Yanai, 1997; Jackson et al., 2000; Makkonen and Helmisaari, 2001; Block et al., 2006; Jones et al., 2009; Hodge et al., 2009; Rosenvald et al., 2011; Finér et al., 2011; Yuan and Chen, 2012). Soil respiration (Rs) comprises a large part of forest ecosystem carbon fluxes, accounting for up to 80% of total ecosystem respiration (Janssens et al., 2001; Davidson et al., 2006). Soil respiration is divided into autotrophic (Ra) and heterotrophic (Rh) sources: Ra is closely linked to the supply of photosynthetic products and Rh is derived from above- and belowground litter which is decomposed by soil microorganisms (Epron et al., 1999; Ryan and Law, 2005; Cisneros-Dozal et al., 2006; Subke et al., 2006). Temperature and soil moisture are the main climatic factors controlling temporal variation of soil respiration (Raich and Schlesinger, 1992; Davidson et al., 1998; Luo and Zhou, 2006). Both, Ra and Rh are thought to respond differently to climatic conditions (Boone et al., 1998; Högberg et al., 2001). Thus, estimation of these components separately would provide a better knowledge of the carbon budget of ecosystems (Hanson et al., 2000; Subke et al., 2006). The relative contribution of Ra to Rs can vary greatly, from 10% to 90%, although the variability depends on the type of the ecosystem, season of the year and the measurement technique (Hanson et al., 2000). The trenching method is widely used for separating Ra and Rh components of Rs, although it has various limitations. Neglecting the decomposition of detached roots and increased soil water content in trenched plots leads to overestimation of Rh. On the other hand, lack of fresh inputs of above- and belowground litter leads to underestimation of Rh (Epron et al., 1999; Epron, 2009). Therefore, several corrections should be considered while estimating the contribution of Rh to Rs, but still very few studies have taken them into account. Forest age plays an important role in determining the distribution of ecosystem carbon fluxes, pools and sequestration (Pregitzer and Euskirchen, 2004), but relevant findings are contradictory. Total Rs has been found to increase (Wiseman and Seiler, 2004) or decrease (Saiz et al., 2006) with stand age; also non-linear responses (Wang et al., 2002; Tang et al., 2009) have been reported. Furthermore, partitioning between Rh and Ra can also change with stand age (Bond-Lamberty et al., 2004b; Saiz et al., 2006; Ma et al., 2014). There is still substantial uncertainty regarding the effect of stand age on soil CO2 efflux; however, to construct long-term models, it is crucial to understand the impact of stand age on forest carbon dynamics in association with changing climate (Tang et al., 2009). Soil respiration depends also on the composition of tree species of forests but pertinent studies of silver birch stands are still scarce in the literature. Silver birch is a fast-growing, light-demanding and early successional pioneer species, which can colonize open areas soon after clear-cut or forest fire, preferring fertile mesic sites (Hynynen et al., 2010). Economically and ecologically, silver birch is the most important deciduous tree species in Northern and Eastern Europe (Krüssmann, 1976; Evans, 1984). The proportion of birch in the total volume of the growing stock is 16%, 11%, 14% and 28% for

285

Finland, Sweden, Russia and Latvia, respectively (Hynynen et al., 2010). In Estonia, the total growing stock of birch stands is 120 million m3, which accounts for 26.3% of the total volume of the growing stock of forests (Yearbook Forest, 2011). Studies of C budgets on the ecosystem scale can help to understand the ecological processes and driving forces of the C cycle (Fang et al., 2007). However, such studies are still quite scarce, especially those addressing silver birch, which makes the present study actual and relevant. Our first results from the study of chronosequent fertile silver birch stands (Uri et al., 2012; Varik et al., 2013) demonstrated that the woody biomass of trees was the main C sink of which a significant share (up to 28%) was accumulated in the belowground part of the stand (Varik et al., 2013). For a more comprehensive understanding of C cycling in silver birch stands, fine root dynamics (production, mortality and turnover) and soil respiration in relation of the microbiology background along a chronosequence of silver birch stands were examined in this study. On the basis of the earlier results of studies conducted at the same sites (Uri et al., 2012; Varik et al., 2013), we hypothesized that: (1) the annual C efflux from the soil through the soil heterotrophic respiration is of the same magnitude as the annual C input into the soil through aboveground and belowground litter, which explains stable C content in the soil of chronosequent silver birch stands; (2) fine root production as well as soil heterotrophic respiration increase with stand age; and (3) silver birch stands growing at fertile sites act as carbon sinks irrespective of stand age. The objectives of this study were: (1) to assess fine root biomass production, turnover rate and longevity in a chronosequence of silver birch stands; (2) to analyse the effect of stand age on soil respiration and heterotrophic respiration; and (3) to compile C budgets for silver birch stands of pole, middle-age and premature stages. 2. Materials and methods The study was carried out in a chronosequence of silver birch stands in Estonia (Table 1). The stands were growing in an Oxalis site type with fertile, acidic and well drained soils (Lõhmus, 1984). Three different stages of stand development were represented: pole, 13-year-old (Kambja); middle-aged, 32-year-old (Alatskivi 2) and premature, 45-year-old (Erastvere). All studied stands had regenerated naturally and grew in a plain landscape. Study sites are described in detail in Uri et al. (2007, 2012),),Rosenvald et al. (2013) and Varik et al. (2013). 2.1. Estimation of above-ground production A detailed description of estimation of aboveground biomass and production as well of understorey production were published in Uri et al. (2012). Dimension analysis (Bormann and Gordon, 1984; Uri et al., 2007) was used for assessment. The annual production of the foliage was assumed to have entered the soil through leaf litter; the aboveground litter flux was estimated on the basis of litter traps (Uri et al., 2012), except 13-year-old stand, where original data was used. In the Erastvere stand, the homogeneous second layer of spruce was growing, and the biomass and production of spruces were estimated. The second layer of spruce is very typical for the silver birch stands growing on fertile sites. The average height of spruces formed roughly half of the birches (Table 1). In our earlier studies the second layer of spruces, was not considered. The diameter of all spruces growing in the sample plot was measured (D1,3) as well as the height of 11 trees. The stem volume of second layer was calculated by using Eq. (1).

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Table 1 Characteristics of the studied silver birch chronosequent stands. The topsoil characteristics of the studied stands are presented as average values for the upper 10 cm soil layer (Uri et al., 2012). Kambja

Age, year Location

13 58 30 N 27 10 N 5.0 7670 5.8 10.9 20.1 1.49 0.98 15.2 72.0 5.4 Sandy loam Albeluvisol

Stand area, ha Stand density, trees ha
1 Average diameter D1,3, cm Average height, m Basal area, m2 ha
1 Corg, % Ntot, g kg
1 C:N P AL-solublea , mg kg
1 pHKCl Texture class Soil type a

Alatskivi 2

32 58 370 N 27 20 E 0.7 3210 10.8 17.0 29.2 3.08 2.27 13.6 13.1 3.9 Sandy loam Gleyic Umbrisol

Erastvere Birch

Spruce 2nd layer

45 57 80 N 26 560 E 0.6 940 20.1 25.6 29.8 2.26 1.40 15.8 20.7 4.6 Sandy loam Albeluvisol

37

0.6 1824 11.9 13.5 20.1

Original data, AL: ammonium lactate.

V ¼ GHF;

(1) 3


1

2


1

where V is stem volume (m ha ), G is basal area (m ha ), H is average height (m), and F is form factor. For recalculation of stem volume to stem mass, the density value of 427 m3 kg
1 was used (Lõhmus, 1987). For modelling of the proportions of different biomass fractions, the corresponding data of an earlier study, conducted in a 40-year-old spruce stand on a similar soil (Ostonen et al., 2005; Lõhmus, 1987) were employed. For rough estimation of annual stem volume increment, mean annual increment (MAI) was used. For needle net primary production (NPP), the annual needle litter flux was taken as an estimate. For the biomass of the branches, the branch/stem biomass ratio (%) for the 40-year-old stand (Lõhmus, 1987), equal to 9.7%, was used. For branch NPP, the branch/stem NPP ratio (calculated from NPP data for the 40-year-old stand according to Ostonen et al., 2005), equal to 0.14 was multiplied by the branch biomass of second-layer spruces. It was assumed that the fine root/needle NPP ratio was similar for the fertile 40-year-old stand (Ostonen et al., 2005) and for the second-layer spruces in the Erastvere stand. The carbon pools for different fractions of the stands were calculated by using mass and C concentration (Uri et al., 2012; Varik et al., 2013) for a particular fraction. 2.2. Estimation of belowground production The belowground biomass in the 32-year-old stand was estimated on the basis of the excavated root system (Varik et al., 2013). For calculation of belowground biomass in the pole and premature silver birch stands, a root-shoot (leafless) ratio of 21% was used as this ratio was found at stand ages of 8 and 32 years at Oxalis sites (Uri et al., 2007; Varik et al., 2013). For estimation of the NPP of the coarse root (d  2 mm) fraction, the NPP/biomass ratio for the aboveground woody part was extrapolated for the belowground part (except for the fine root fraction) (Aosaar et al., 2013). Fine root production was estimated by ingrowth cores (d = 40 mm, mesh size 6 mm) (Ostonen et al., 2005), which were installed systematically in random transect groups all over the stands: in Kambja, in April 2005; in Alatskivi 2 and Erastvere, in April 2009. The ingrowth cores (altogether 315, i.e. 105 per stand) were gradually filled with the sieved root-free soil of local origin (from the non-forested area adjacent to the studied stand) and installed into the upper soil layer to a depth of 30 cm. Totally, 243 ingrowth cores were extracted during the growing seasons 2005–2007 and 2009–2011: 8 samplings per study stand

and 10–15 cores from different transect groups per sampling. Sampling was carried out three times per vegetation period, in June, August and October or November throughout whole study period for all stands. The extracted cores were placed in plastic bags and transported to the laboratory and stored at
18  C until processing, as described in detailed in Varik et al. (2013) and Aosaar et al. (2013). The production and turnover rate of the fine roots were calculated by balancing the living and dead root biomass compartments according to the decision matrix of Fairley and Alexander (1985). Fine root NPP was calculated on the basis of the third year data of the ingrowth cores from October 2007 to October 2008 in the 13-year-old stand and from October 2010 to October 2011 in the 32-year-old and in 45-year-old stands. Fine root turnover rate was calculated by dividing fine root NPP (g m
2 year
1) by mean fine root biomass (g m
2) in the third growing season according to McClaugherty et al. (1982). Mean fine root biomass was estimated as the average of live root biomass during the sampling time interval; the third year ingrowth core biomass data were considered to be representative of the actual fine root pool. Fine root longevity (year
1) was calculated as the reciprocal of root turnover rate. For calculation of the C flux into the soil through fine root litter, an average C concentration of 51.4% was used (Varik et al., 2013). 2.3. Soil respiration and heterotrophic respiration measurements Soil respiration was partitioned into heterotrophic and autotrophic respiration by the trenching approach (treatments: control and trenching). Trenching was carried out in each stand in August 2009: 5 PVC cylinders (inner diameter 20 cm, length 60 cm) in Alatskivi and Kambja and 4 cylinders in Erastvere were inserted in the soil by pushing them to a depth of 50 cm. Trenching precluded autotrophic respiration of the tree roots; the belowground parts of understorey as well as all aboveground vegetation were carefully removed from the inside of the trench with minimum soil disturbance and the trenched plots were kept free of the live vegetation throughout the study. Trenching to a depth of 50 cm is sufficient as the main share of tree fine root biomass is located in the upper 0–20 cm soil layer: 76% and 80% in Kambja and Alatskivi stands, respectively (Uri et al., 2007; Varik et al., 2013). The distance between each trenching cylinder was approximately 5–6 m. Collars for Rs measurements were installed at approximately 50 cm from the trenched plots. Soil respiration rates were

M. Varik et al. / Ecological Engineering 77 (2015) 284–296

measured monthly from June to November 2010 and from May to November 2011 using the closed dynamic chamber method (PP SystemsSRC-1 chamber (volume 1170 cm3, enclosed soil surface are 78 m2) with gas analyser CIRAS-2 (Differential CO2/H2O Infrared Gas Analyzers)). Soil respiration is measured when a chamber of known volume is placed on the soil and the rate of increase in CO2 within the chamber is monitored. The CO2 concentration is measured every 8 s, and a quadratic equation fitted to the relationship between the increasing CO2 concentration and elapsed time. Five collars (inner diameter 10 cm, height 5 cm) were installed in the control area and the other 5 in adjacent trenched cylinders to a soil depth of 1–2 cm. Soil temperature (Ts,  C) was measured simultaneously with soil respiration in the control and trenched treatments using an attached soil temperature probe STP-1 (PP Systems International, Inc., USA) inserted at a depth of 5 cm. Volumetric soil moisture (%) was also measured at a depth of 5 cm using a HH2 Moisture Meter Version 2 (Delta-T Devices Ltd., UK). In addition, soil temperature (model 1425, Technologies, Inc., USA) and soil moisture (Watermark soil moisture sensor 6450WD, Technologies, Inc., USA) were measured every hour at a depth of 10 cm in each stand and the data was stored with a data logger (WatchDog 1425, Spectrum Technologies, Inc., USA) during the growing seasons of 2010 and 2011. Multiple stepwise regression analysis was performed to evaluate relationships between respiration flux (Rs or Rh) and environmental variables (Ts, soil moisture) as follows: ððT
10Þ=10Þ

Flux ¼ R10 Q 10 s

aebSWC

(2)

where R10 is respiration rate at temperature 10  C, Q10 represents the relative increase of respiration with temperature increase to 10  C, a and b are coefficients, SWC is soil volumetric water content (%), Ts is soil temperature ( C). For the snow-free season, Rs and Rh fluxes were modelled for all stands using monthly mean Ts values calculated from continuous Ts measurements according to the data from the loggers: ððT
10Þ=10Þ

Flux ¼ R10 Q 10 s

(3)

To develop models (2 and 3), data from July 2010 to June 2011 was used; data from July 2011 was excluded because of severe drought. The annual fluxes of Rs and Rh for the carbon budget were calculated from the model for the year 2010. Soil temperatures outside the growing season were calculated using the regressions between stand soil temperature and soil temperature measured in the experimental area of free air humidity manipulation of forest ecosystems (FAHM) (Kupper et al., 2011) (R2 > 0.97) for all study stands. The trenching method used influences environmental conditions inside the PVC cylinders. Soil moisture content increases due to eliminated water uptake and transpiration by plants; as insertion of cylinders cuts off tree roots, the value of the CO2 efflux from the decomposing detached roots has to be subtracted from the Rh value (Epron, 2009); simultaneously, fine root growth and litter production are interrupted and Rh is underestimated accordingly. Considering this, we applied correction for differences in SWC and corrections which take into account root exclusion effects.

287

Correction for increased SWC was calculated as follows: for actual Rh measurements inside the cylinders, model (2) was developed; thereafter, the values of SWC inside the cylinders were replaced by the values of ambient SWC. Replacement was only done for measurements in the case of which the mean values of SWC inside and outside the cylinders were statistically different. Correction for the decomposition of detached roots, which causes overestimation of Rh, was calculated for the root fractions d < 2 mm and 2  d < 5 mm only. The share of thicker roots within the cylinders is expected to be small and their decomposition is very slow (Palviainen et al., 2010; Palviainen and Finér, 2012). Fine root decomposition experiments for the above fractions were carried out in Kambja; remaining mass Mt at time t (year) as the fraction of the absolute initial amount M0 of detached roots was described by the following equation: Mt ¼ e
kt M0

(4)

In Kambja, k values for the root fractions d < 2 mm and 2  d <5 mm were 0.18 and 0.24, respectively (V. Uri data not shown). For the other stands, an approximate k value of 0.20 was used according to Lõhmus et al. (1995) and according to unpublished data of K. Lõhmus and H.-S. Helmisaari. Fine root biomass (d < 2 mm) was estimated in the current study (Table 2). The biomass of the 2  d <5 mm root fraction was estimated in the 32 year-old stand, for the other stands it was calculated using d < 2 mm biomass and biomass ratio of the 2  d <5 mm to the d < 2 mm fraction (B2–5/B<2). According to Varik et al. (2013), this ratio depended strongly on stand age for chronosequent silver birch stands: B2
5 ¼
0:0086x þ 1:2939 B<2

(5)

R2 = 0.9997, P < 0.0001 Correction for the suppressed input of soil organic matter due to fine root mortality was applied for tree roots; the lack of fresh root litter inputs may decrease Rh. The fine root litter input was estimated by multiplying fine root biomass by turnover rate; thereafter, Eq. (4) was applied to estimate mass loss during per year. Also aboveground litter of the understorey inside the cylinders was eliminated, which caused underestimation of Rh; it was assumed to decompose during one year. Corrected Rh for each stand was calculated as follows: Rhcorrected ¼ Rhmeasured
SWCcor
root decompositioncor þ FR turnovercor þ AG understorey littercor

(6)

where corrections (cor) for soil water content (SWC), decomposition of the detached roots, suppressed fine root (FR) turnover and missing aboveground (AG) litter of the understorey have been taken into account. We did not measure the fluxes of Rs and Rh for the season with the snow cover (December–March), however, wintertime Rs and Rh fluxes were estimated by adding 5% to the modelled respiration fluxes (wintertime soil CO2 flux accounts for <5% of the corresponding values for the snow-free season) (K. Soosaar, personal communication based on eddy covariance measurements in a South-Estonian forest).

Table 2 Fine root (d < 2 mm) dynamics in the studied stands. Stand

Age

NPP, t ha
1 year
1

Mean biomass, t ha
1

Turnover rate, year
1

Longevity, year

Kambja Alatskivi 2 Erastvere

13 32 45

0.89 1.44 1.31

1.35 1.95 2.57

0.66 0.74 0.51

1.52 1.35 1.95

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2.4. Compiling of the C budget The carbon budget for silver birch stands of different ages were compiled by synthesizing our earlier (Uri et al., 2012; Varik et al., 2013) and original results from the same chronosequence stands. The NPP was calculated by summing the annual increments of the aboveground ecosystem compartments (trees of the first and the second layers, the understorey) and the increment of the belowground ecosystem compartments (coarse root system, fine roots, the roots of the herbaceous understorey). The C accumulation in woody biomass and in the herbaceous understorey as well as the C flux from aboveground litter was estimated in an earlier study (Uri et al., 2012). The belowground biomass and C accumulation in the belowground part of silver birch stands were estimated in Varik et al. (2013). The foliage produced in each measurement year was assumed to have entered the soil in the form of annual litter. The total litter flux was included in calculations for all of the studied stands. The estimate net ecosystem production (NEP) was obtained by subtracting heterotrophic respiration (Rh) from NPP. The NEP was calculated as NEP = NPP
Rh (Lambers et al., 2008), the export, import and oxidation fluxes (Lovett et al., 2006) were considered to be negligible. The NEP > 0, implies a net transfer of C from the atmosphere into the forest ecosystem (C sink), and NEP < 0 implies a net transfer of C from the forest ecosystem into the atmosphere (C source). The NEP represents the rate at which carbon is accumulated in the ecosystem, being a main parameter used to characterize forest carbon sequestration (Chapin et al., 2006; Waring and Running, 2007). Carbon losses were estimated as heterotrophic respiration (Rh). Autotrophic respiration was calculated by subtracting heterotrophic respiration from total soil respiration. The flux of dissolved organic carbon (DOC) leaching was not considered, however, according to our results from Free Air Humidity Manipulation experiment (Kupper et al., 2011) (the data not shown), C leaching is a negligible flux in young silver birch stands. In the case of the premature stand (Erastvere) also original data of the second spruce layer was taken into account.

2.5. Microbiological methods Soil samples for microbiological analysis were taken in all stands with a soil corer (Ø 2 cm) from the 0 to the 10 cm layer in October 2013. Three composite samples were formed per stand; for a composite sample, 10 subsamples were randomly collected. Fresh soil samples were sieved (d < 2 mm) to obtain the fine earth fraction (Lõhmus et al., 2006). Soil samples were used for measurements of microbial biomass C and dehydrogenase activity. Cross contamination of samples was carefully avoided at sampling and at sample processing. The substrate induced respiration (SIR) method was applied in order to evaluate metabolically active microbial biomass in the soil (Kukumägi et al., 2014). The SIR was determined via the Oxitop1 manometric system (Oxitop1, WTW), which allows to determinate sample oxygen consumption. Fifty grams of fieldmoist soil was amended with glycose (0.5 g per 100 g soil) and incubated in a closed vessel at 22  C in the dark for 24 h. The principle of the operation was based on the measurement of the pressure difference in the closed vessel system. During respiration, produced CO2 was bound to an absorber (soda lime pellets), and microbial oxygen consumption resulted in a pressure drop. The quantity of oxygen consumption per gram of dry soil was calculated according to a recommended procedure (Platen and Wirtz, 1999) and microbial biomass carbon (mg C per g of dry soil) was calculated using the following formula: 1 mg O2 g
1 h
1 = 28 mg biomass C g
1 (Beck et al., 1996).

Dehydrogenase activity was measured using [2-(p-iodophenyl)-3-(p-nitrophenyl)-5-phenyl tetrazoliumchloride] solution (INT). Samples were incubated for 2 h at 40  C in the dark. Reduced iodonitrotetrazolium formazan (INTF) was extracted with dimethylformamide and ethanol, and measured photometrically at 464 nm (von Mersi, 1996). 2.6. Calculations and data analysis The Statistica 7.1 software (StatSoft, Inc., 2005) was employed to perform all statistical analyses; the level of significance a = 0.05 was accepted in all cases. The normality of variables was checked using Lilliefors’ and Shapiro–Wilk’s tests on datasets. The Rs data were log-transformed to normalize for statistical analysis. The effects of treatment (trenching, control), stand age and sampling time (month) on Rs, Ts and soil moisture (SWC) were examined using repeated measures ANOVA (P < 0.05). T-test was used to identify significant differences. 3. Results 3.1. Fine root dynamics Fine root production (FRP) increased significantly from the pole to the premature stage. Regarding seasonal dynamics, fine root production demonstrated a similar pattern in the middleaged and premature stands. Fine root growth started in spring and the increase of fine root biomass in the ingrowth cores was very intensive during the first half of the summer (Fig. 1). However, this growth was modest in the pole stand. Fine root biomass reached maximum values in mid-summer and started to decrease thereafter. Seasonal patterns for the middle-aged stand and the premature stand were similar throughout the study period, which can evidently be explained by similar weather conditions since the ingrowth cores in these stands had been installed at the same time. 3.2. Soil respiration 3.2.1. Seasonal dynamics of respiration rates and soil microclimate in ambient and trenched conditions The seasonal dynamics of soil temperature (Ts) was very similar in each stand ranging from 5.1  0.3 to 17.7  0.4  C in the pole stand; from 4.1  0.4 to 17.0  0.3  C in the middle-aged stand and from 5.3  0.2 to 17.6  0.3  C in the premature stand throughout both study years. Trenching did not affect Ts (P > 0.05). In the control plots, soil moisture fluctuated markedly throughout the growing season ranging from 9.4  0.31% to 40.7  1.01% in the pole and middle-aged stands and from 6.8  0.48% to 24.3  0.15 in the premature stand (Fig. 3). On average, trenching increased soil moisture by 23–30% in all stands during the two study years, which is a direct consequence of root exclusion (P < 0.05). The seasonal dynamics of Rs and Rh in three stands showed a similar pattern following the changes in Ts. Respiration rates increased in spring, peaked in summer, and declined in autumn (Fig. 2). The decline in respiration rates in all stands in July in 2011 is probably related to very low soil moisture content at that time. Trenching decreased respiration rates significantly (P < 0.05). When integrated for each season (June–November 2010 and May–November 2011) respiration rates in trenched plots were on average 36% lower in both study years. The Rs and Rh were strongly correlated with Ts in all stands. Across stands of different ages, Ts alone explained 67–89% of the variation in respiration rates in the control and trenched plots. Soil

M. Varik et al. / Ecological Engineering 77 (2015) 284–296

289

4 Kambja 13-year-old Alatskivi 32-year-old

Fine root biomass, t ha-1

3

Erastvere 45-year-old

2

1

0 Summer Autumn Year I

Winter

Spring Summer Autumn

Winter

Spring Summer Autumn

Year II

Winter

Year III

Fig. 1. Seasonal dynamics of the fine root (d < 2 mm) biomass of silver birch in different study periods; 2005–2007 in Kambja; 2009–2011 in Alatskivi and Erastvere.

temperature and soil moisture together explained as much as 86–93% of the temporal variation in the trenched plots. 3.2.2. Stand age effect on soil respiration rates Stand age had a significant effect on the soil CO2 efflux (ANOVA, P < 0.05). Among all data sets, mean Rs in the pole stand was significantly lower than in the middle-aged and the premature stand (2.55  0.12 mmol CO2 m
2 s
1 versus 4.06  0.21 and 4.04  0.26 mmol CO2 m
2 s
1, respectively) (t-test, P < 0.05). Mean Rh was the lowest in the pole stand (1.54  0.07 mmol CO2 m
2 s
1) and the highest in the premature stand (3.08  0.18 mmol CO2 m
2 s
1). Among the three stands, the premature stand had the lowest mean Ts. A significant difference was revealed between the pole and the premature stand (t-test, P < 0.05), however, the difference between mean Ts was only 0.5  C. Among the control plots the driest soil was in the premature stand (15  0.8%) compared with the pole and the middle-aged stand (23  1.0% and 26  1.5%, respectively) (t-test, P < 0.05). A similar trend was observed in trenched conditions. The large contribution of the second layer of spruce in the premature stand probably diminished seasonal variation in soil moisture regime. Moreover, the contrasting differences between the control and trenched conditions occurring in the younger stands were not found in the premature stand (Fig. 3c). 3.2.3. Modelled annual Rs and Rh fluxes Modelled annual C respired from the control plots was 6.2– 9.7 t C ha
1 year
1, with the highest values in the middle-aged stand. Modelled and corrected annual Rh was 3.0–4.2 t C ha
1 year
1, with the highest value in the middle-aged stand (Table 3). When integrated over time from July 2010 to June 2011, the relative contribution of modelled Rh to modelled Rs was almost half of the latter in each stand, being 0.48 in the 13-year-old stand, 0.43 in the 32-year-old stand and 0.44 in the 45-year-old stand. The temperature sensitivity (Q10 value) of Rs was 2.4  0.08, 2.4  0.17 and 2.9  0.09 in the 13-, 32-, and 45-year-old stands, respectively. Q10 values of Rh increased with stand age, 1.9  0.08, 2.1  0.10 and 3.0  0.09, respectively. Basal respiration (R10 mmol CO2 m
2 s
1) of Rs and Rh increased with stand age; R10 of Rs was 2.0  0.05, 3.3  0.08 and 3.5  0.05 in 13-, 32-, and 45-year-old stand, R10 of Rh was 1.2  0.04, 2.1  0.05 and 2.6  0.04, respectively.

3.3. Carbon budgets in chronosequence silver birch stands Net ecosystem production (NEP) values differed along the chronosequence of the silver birch stands. Average sequestration in the ecosystem, i.e. NEP was around 3.7–4.9 t C ha
1 year
1, indicating that silver birch stands acted as effective carbon sinks at fertile sites (Table 3). The current annual increment and hence accumulation of C in the trees was of the same magnitude in the pole, middle-aged and premature stands. The share of tree fine root litter in the tree litter C input into the soil increased with stand age, being 22.0% in the pole stand, 31.6% in the middle-aged stand and 36.2% in the premature stand. An appreciable C input into the soil was formed of understorey belowground litter (Table 3). However, the herbaceous understorey was missing in the premature stand (Erastvere) (Uri et al., 2012) and the second tree layer was missing in the younger stands. At the same time, the second layer of spruce contributed one quarter of the annual C litter input into soil in the premature stand. The C input into the soil via tree leaf litter formed 42–51% of the total annual organic C input flux. Annual net primary production amounted to 7.4, 7.9 and 8.5 t C ha
1 year
1 in the pole, middle-aged and premature stands, respectively. 3.4. Soil microbial biomass and activity Soil microbial biomass as measured by SIR increased with stand age, being 0.390, 0.636 and 1.047 mg C per g of dry soil in the 13-, 32- and 45-year-old stands, respectively (t-test, P < 0.01). However, soil dehydrogenase activity was similar in all stands (t-test, P > 0.05) ranging from 50 to 67 mg INTF per g of dry soil h
1. 4. Discussion Annual C sequestration in the studied chronosequent silver birch stands occurred mainly in the stems, branches and coarse roots. As all studied Oxalis sites were of high fertility fine root turnover was relatively small (Lõhmus et al., 2006; Ostonen et al., 2011).

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Fig. 2. Seasonal dynamics of total soil respiration (Rs mmol CO2 m
2 s
1) and heterotrophic respiration (Rh mmol CO2 m
2 s
1) in (a) the 13-year-old, (b) the 32-year-old, and (c) the 45-year-old silver birch stands in 2010 and in 2011. Error bars represent the standard error of the means. * represents significant differences between total Rs and Rh (P < 0.05).

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291

Lukac and Godbold, 2001; Ostonen et al., 2005; Aosaar et al., 2013; Brunner et al., 2013), where the amount of fine roots which grow into root-free soil over a certain period of time is measured. Ingrowth cores are effective in investigating fast growing species and serve as the most suitable tool for comparing fine root production between sites or treatments (Neill, 1992; Messier and Puttonen, 1993; Vogt et al., 1998; Makkonen and Helmisaari, 1999; Oliveira et al., 2000; Godbold et al., 2003; Li et al., 2013). According to Ostonen et al. (2005), ingrowth cores require a stabilisation period: natural Norway spruce fine root structure started to re-establish in the third year after the installation of mesh bags at the fertile Oxalis site. The mean fine root biomasses estimated with the ingrowth method, 1.35, 1.95, and 2.57 t ha
1 in the 13-, 32- and 45-year-old stands, respectively, are in good accordance with earlier published data for a natural situation estimated by soil coring. Fine root biomass in chronosequent silver birch stands aged 14–60 years (Varik et al., 2013), measured by soil coring (0–40 cm), varied between 1.03 and 4.09 t ha
1, and increased also with stand age. Soil microbial biomass, too, increased with stand age. Fine root turnover rate is dependent on fine root biomass (explaining most of variation in fine root production), on the annual production of fine roots and on site conditions, as well as on various methods and calculations (e.g. Jourdan et al., 2008; Gaul et al., 2009; Finér et al., 2011; Yuan and Chen, 2010; Brunner et al., 2013). According to a meta-analysis by Finér et al. (2011), tree fine roots in boreal and temperate forests turned over on average 1.3 times a year; however, the turnover rate varied in a broad range: the coefficient of variation was 81% for temperate forests and 148% for boreal forests. The turnover rates found in this study, 0.51–0.74, remain in this range. The longevity of silver birch fine roots in 45-year-old stands was 714 days, which is close to the longevity of 922 days in a 50-year-old silver birch stand growing in southern Sweden and measured by minirhizotrons (Hansson et al., 2013a). 4.2. Soil CO2 effluxes

Fig. 3. Seasonal dynamics of soil moisture (%) in control and trenched conditions in (a) the 13-year-old, (b) the 32-year-old, and (c) the 45-year-old silver birch stands in 2010 and in 2011. Error bars represent the standard errors of the means. * represents significant differences between control and trenched conditions (P < 0.05).

4.1. Fine root turnover Fine root turnover is the process by which fine roots die and are replaced by new active roots (Block et al., 2006). Fine root production is still one of the least known processes of the C cycle of forests (Hertel and Leuschner, 2002). Estimation of fine root production is problematic, expensive, difficult and labour-intensive (Helmisaari et al., 2002; Xiao et al., 2008; Rytter, 2013); the practical and theoretical advantages and disadvantages of pertinent study methods are discussed in Majdi (1996), Vogt et al. (1998), Hertel and Leuschner (2002), Rytter (2013) and Li et al. (2013). The challenge to accurately measure fine root dynamics is actual. A widely used and relatively simple method to directly assess fine root (d < 2 mm) production is the ingrowth core method (Persson, 1980; Vogt and Persson, 1991; Bauhus and Messier, 1999;

Our estimates of the annual C respired from the soils of the stands fell in the range reported for forest ecosystems of the northern hemisphere (Bond-Lamberty et al., 2004b; Subke et al., 2006; Wei et al., 2010). Several studies have found a significant effect of stand age on Rs (Pregitzer and Euskirchen, 2004; BondLamberty et al., 2004a; Saiz et al., 2006; Luan et al., 2011), however, the results are contradictory. Among the three stands of the present study, modelled annual Rs rates were the lowest in the pole stand and the highest in the middle-aged stand, indicating a nonlinear relationship between Rs and stand age. This result is consistent with chronosequence studies by Tang et al. (2009) and Wang et al. (2002). The increase in soil respiration with stand age (1–25-year-old) was reported in a loblolly pine chronosequence study and attributed to increasing root biomass (Wiseman and Seiler, 2004). Both our estimated fine root biomass and fine root production increased with stand age, suggesting the significant effect of fine root dynamics on Rs; soil microbial biomass followed a similar pattern. This result is consistent with studies reporting a significant positive correlation between fine root biomass or fine root production and Rs (Lee et al., 2003; Knohl et al., 2008). In contrast, Saiz et al. (2006) studied a Sitka spruce chronosequence stands whose age range was similar to that of the stands in our study and found that the pole stands had significantly higher respiration rates than in older stands and explained it by a decrease in fine root biomass. For several reasons, it is highly important to examine the components of Rs separately. Firstly, forest productivity changes over the course of stand development and several reviews have

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Table 3 Carbon budget in silver birch stands (NPP: net primary production; NEP: net ecosystem production). Fluxes

Kambja 13-year-old

Alatskivi 2 32-year-old (t C ha
1 year
1)

Erastvere 45-year-old (t C ha
1 year
1)

(t C ha
1 year
1) Silver birch

2nd Norway spruce layer

Plant aboveground (1) Leafless tree biomass incrementa (2) Leaf littera Branch littera (3) (4) Understoreya

3.83 1.48 0.14 0.05

3.70 1.54 0.07 0.16

3.89 1.03 0.38

1.12 0.38

Plant belowground (5) Coarse root biomass incrementb (6) Birch fine root production (7) Understorey fine root and rhizome productiona

0.78 0.46 0.75

0.68 0.74 1.13

0.77 0.67

0.27 0.34

3.21 2.97 2.88
0.09

5.51 4.21 3.63
0.58

4.56 3.61 2.80
0.81

7.35 4.38

7.95 3.74

8.47 4.86

Soil (8) (9) (10) (11)

Autotrophic respiration Heterotrophic respiration (C output) C input = (2) + (3) + (4) + (6) + (7) Soil C exchange = (10)
(9)

Productivity NPP = (1) + (2) + (4) + (5) + (6) + (7) (12) (13) NEP = (12)
(9) a b

Uri et al. (2012). Varik et al. (2013).

found close correlation between forest primary production and Rs (Raich and Schlesinger, 1992; Janssens et al., 2001; Luo and Zhou, 2006). Moreover, recent photosynthate is the primary source of Ra (Högberg et al., 2001; Kuzyakov and Gavrichkova, 2010); while the litter input acts as the substrate for respiration of microbes (BondLamberty et al., 2004b; Cisneros-Dozal et al., 2006). Secondly, Ra and Rh vary differently with stand age (Bond-Lamberty et al., 2004a; Saiz et al., 2006; Luan et al., 2011; Ma et al., 2014). Thirdly, Rh values are needed for NEP calculation. Moreover, both soil respiration components, Ra and Rh, are thought to respond differently to climatic factors such as temperature and moisture (Boone et al., 1998; Högberg et al., 2001; Wei et al., 2010). The trenching method is widely used for separating heterotrophic and autotrophic components of soil respiration in forest ecosystems, however, this method has some disadvantages (Hanson et al., 2000; Kuzyakov, 2006). Problems with the trenching method are the higher CO2 efflux by cut-off decomposing roots, potentially higher soil water content in trenched soil volumes and the lack of fresh belowground litter input (Hanson et al., 2000; Ngao et al., 2007; Epron, 2009). Without any correction, Rh will be more or less overestimated (Subke et al., 2006; Ngao et al., 2007; Comstedt et al., 2011) also estimation of NEP and the Rh/Rs ratio will be biased. In this study trenching had no influence on soil temperature but it influenced significantly soil moisture due to eliminated tree (and understorey) transpiration; hence soil moisture was up to 30% higher in the trenched plots than in the control plots. After all corrections were taken into account, the Rh/Rs ratio decreased from 13% to 33% and ranged between 0.43 and 0.48. This result is consistent with studies where root decomposition and soil water content corrections have been used (Ngao et al., 2007; Comstedt et al., 2011). Still, corrections have remained unconsidered in many studies. Soil temperature was the dominant environmental factor influencing the seasonal dynamics of Rs. Rh was affected by both temperature and moisture which explained up to 93% of the temporal variation of Rh. In general, control of the temporal variability of Rs has been widely attributed to soil temperature and moisture (Raich and Schlesinger, 1992; Davidson et al., 1998; Luo and Zhou, 2006). Stand age affected soil temperature and

moisture; on average, the premature stand was drier and cooler than the younger stands. Changes in seasonal course of soil temperature in association with age may be explained by canopy shading, which affects soil exposure to solar radiation. In the premature stand the dense second layer of Norway spruce most probably prevents solar radiation and precipitation from reaching the ground. Our Q10 values of Rs (2.4–2.9) derived from the growing season fell within the range (2.0–6.3) reported for European and NorthAmerican forest ecosystems (Davidson et al., 1998; Janssens et al., 2003). Also our mean R10 values for Rs (2.0–2.6) were well within the range (0.7–4.9 mmol CO2 m
2 s
1) found in European forests (Janssens et al., 2003). As mentioned above, Rs is sum of an autotrophic and heterotrophic component, both may respond differently to the temperature (Boone et al., 1998; Korhonen et al., 2009; Wei et al., 2010; Ma et al., 2014). In this study, Q10 values were estimated only for heterotrophic component. We found lower Q10 values for Rh than for Rs, as found by Korhonen et al. (2009) in boreal Scots pine forest. The Q10 of Rs includes also the Q10 of autotrophic respiration which has found to be higher than Q10 of Rh (Boone et al., 1998; Korhonen et al., 2009; Ma et al., 2014). Climate change scenarios predict an increase in air temperature (by 2.3–4.5  C) in Baltic region (Kont et al., 2003) and soil warming experiments have showed significant enhancement of Rs and Rh (Bronson et al., 2008; Schindlbacher et al., 2009; Aguilos et al., 2013). Moreover, Aguilos et al. (2013) reported enhanced temperature sensitivity of Rh in soil warming experiment in cool-temperate forested peatland. However, some warming studies report either decrease or no significant change in Q10 values (Bronson et al., 2008; Niinistö et al., 2004). Studied silver birch stands acted as carbon sink and soil temperature explained a remarkable part of temporal variation of Rh. Increase of temperature might change the carbon balance and temperature sensitivity of Rh indicating the importance of component partitioning. Although, the mean Ts in trenched plots did not differ significantly between stands, our Q10 and R10 of Rh increased with stand age. One possible explanation could be attributed to changes in litter quantity and quality that can change with stand age (Saiz et al., 2006; Uri et al., 2011; Ma et al., 2014). Temperature sensitivity of Rs,

M. Varik et al. / Ecological Engineering 77 (2015) 284–296

especially Rh, has found to be dependent on substrate quality and availability (Conant et al., 2008; Gershenson et al., 2009; Erhagen et al., 2015). Conant et al. (2008) suggested that the decomposition of recalcitrant substrates is more temperature sensitive than labile substrates. Nevertheless, temperature, by influencing the seasonality of substrate supply, especially in deciduous forests in higher latitudes, affects soil CO2 effluxes indirectly as well. 4.3. Carbon budgets in chronosequent silver birch stands We proved the hypothesis that silver birch stands, growing in fertile sites, act as carbon sinks irrespective of stand age, moreover, NEP was similar in the pole, middle-aged and premature stands. According to literature data, the C balance of a forest stand can change to a great extent during stand’s ageing (Kolari et al., 2004). After clearcut a young stand first serves as a carbon source; during development, the stand gradually turns form the carbon source to a carbon sink. Mature or old stands can become weak carbon sinks or even sources of C (Goulden et al., 1996; Lindroth et al., 1998) since their annual biomass production decreases. Several studies suggest that the magnitude of a C sink or source varies with forest age (Law et al., 2003; Pregitzer and Euskirchen, 2004). The pole Kambja stand (13-year-old) is first-generation forest growing on abandoned agricultural land. In this stand an excessive input of organic matter into the soil (harvesting residues, stumps, dead roots) and a related intensive C efflux by decomposition was missing. We selected this kind of stand because during the last half of the 20th century extensively abandoned agricultural lands in Estonia were afforested naturally by silver birch (Uri et al., 2007). This leads to an increase in the area of silver birch stands and, as a rule, the Oxalis site type will be prevalent in such areas. Similar C accumulation in the studied chronosequent silver birch stands was also supported by similar litter production; total aboveground litter production (including the understorey) was of the same magnitude (1.7–1.8 t C ha
1 year
1), which is in good accordance with the results reported in Hansson et al. (2013b). Total belowground litter production was similar in the pole and premature stands (including the second layer of spruce) (1.2 and 1.0 t C ha
1 year
1), being the highest in the middle-age-stand (1.9 t C ha
1 year
1). Since the annual fine root production of the trees was modest, as is inherent for fertile sites, then also the C input into the soil through fine root litter was small. In the premature stand (Erastvere) the understorey biomass of herbaceous plants was negligible owing to poor light conditions which were caused by the dense canopy of the spruce layer. However, the second layer of spruce contributed significantly to the C input, approximately at 2 t C ha
1 year
1. Since spruce is a shade-tolerant species, such successional development took often place in older birch stands growing at fertile sites. In our earlier study (Uri et al., 2012), we found that the C pool in tree biomass increased with stand age, whereas the soil C pool remained stable and thus did not depend on stand age; according to Raich and Nadelhoffer (1989) and Simon et al. (2012), there must be equilibrium between the inputs and the outputs, unless significant changes are detected in the soil C storage. We proved the hypothesis that the annual C efflux from the soil through soil heterotrophic respiration is of the same magnitude as the annual C input into the soil through aboveground and belowground litter, which explains the stable C content in the soil of the studied chronosequent silver birch stands. Despite to more intensive use of eddy covariance measurement, which allows to determine net ecosystem exchange (NEE), only a few studies have addressed such C budgeting of birch forests (Wang et al., 1998). According to Baldocchi et al. (2001), NEP values between 0.7 and 7.4 t C ha
1 year
1 were observed at 10 temperate

293

deciduous broadleaf sites. In five deciduous forests in the USA, NEP estimated by eddy-covariance methods ranged from 1.7 to 5.8 t C ha
1 year
1 (Curtis et al., 2002). Our results about NEP fit into this range or exceed its upper value ranges. Approximately, three-fourths of total NPP was formed of the by aboveground components. The largest proportion of total NPP was made up by stemwood increment, which was 50–60%. Tree fine root NPP was relatively low and accounted for 6.2–12% of total ecosystem NPP, increasing with stand age. However, the role of fine roots in C cycling may be different in different forests; in some forest ecosystems fine roots are crucial contributors to resource capture and the C cycle (Berg, 1984; Joslin and Henderson, 1987; Hendrick and Pregitzer, 1993; Helmisaari et al., 2002; Finér et al., 2011; Malhi et al., 2011; Yuan and Chen, 2012). Fine root production and hence the C flux to belowground depends on site fertility; at poor sites fine root production may reach 0.86 t ha year
1 (Helmisaari et al., 2002) but may be modest at fertile sites (Ostonen et al., 2005; Uri et al., 2011; Aosaar et al., 2013; Finér et al., 2011). Consequently, in the studied silver birch stands the C input into the soil via leaf litter represented a considerably larger proportion in total NPP than that of the fine roots. Our results show the significant role of the herbaceous understorey in C budget in hemiboreal forest ecosystems. At the younger sites (Kambja and Alatskivi) the herbaceous understorey constituted about 30% of the total litter input into the soil. Regarding soil exchange, the budget compiled in the current study was approximately balanced for the pole stand. However, for the middle-aged and premature stands soil C loss by heterotrophic respiration exceeded the C input into the soil by litter; a possible reason for this is that the production and turnover of extramatrical mycorrhizal mycelia (Wallander et al., 2013) is commonly not taken into account in C budgets; moreover, Wallander et al. (2004) suggested that the C inputs from the fine roots and mycorrhizal hyphae were of the same order of magnitude. 5. Conclusions Our first hypothesis was confirmed. The annual C flux from the soil through soil heterotrophic respiration was of the same magnitude as the annual C input into the soil through aboveground and belowground litter. The soil organic carbon pool remained stable in silver birch chronosequence stands, which can be mainly explained by equilibrium between the soil organic C input and soil heterotrophic respiration. The second hypothesis was not proved: both fine root production and soil respiration were the highest in the middle-age stand. The third hypothesis was also confirmed. All investigated silver birch stands growing at fertile sites were acting as effective carbon sinks and the main C sink was the woody biomass of the trees. In the case of fertile silver birch stands NEP and annual C accumulation into woody biomass were similar. Thus, woody biomass increment of fertile silver birch stand reflects annual C sequestration in the ecosystem. Finally, our results highlight the importance of accounting stand age into carbon dynamics models. Acknowledgements This study was supported by the project by the Estonian Science Foundation grant No. 7069 and by the Institutional Research Funding IUT21-04 of the Estonian Ministry of Education and Research as well as by the KESTA BioAtmos project No. F12010PKTF and Environmental Investment Centre project No. 5725. We thank Mrs. Ester Jaigma for revising the English text of the manuscript. The authors are grateful to Sander Kutti for the help with microbiology analyses.

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