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Contents lists available at ScienceDirect
Agriculture, Ecosystems and Environment
journal homepage: www.elsevier.com/locate/agee
Research highlights
Comparing carbon fluxes between different stages of secondary
succession of a karst grassland
Agriculture, Ecosystems and Environment xx (2010) xxx–xxx
M. Ferlan∗ , G. Alberti, K. Eler, F. Batič, A. Peressotti, F. Miglietta, A. Zaldei, P. Simončič, D. Vodnik
Paired NEE measurements of two chronosequences on heterogeneous karstic terrain. Heterogeneity of studied ecosystems due to soil
conditions and vegetation structure. Woody-plant invaded ecosystem is substantial sink for CO2 compared with the pasture. Resource
acquisition strategy of woody plants is reflected in changed yearly NEE course. Yet unexplained high C losses after the rain events in the
cold period of the year.
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Agriculture, Ecosystems and Environment xxx (2010) xxx–xxx
1
Contents lists available at ScienceDirect
Agriculture, Ecosystems and Environment
journal homepage: www.elsevier.com/locate/agee
Comparing carbon fluxes between different stages of secondary succession of a
karst grassland
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M. Ferlan a,b,∗ , G. Alberti c , K. Eler a , F. Batič a , A. Peressotti c , F. Miglietta e , A. Zaldei d ,
P. Simončič b , D. Vodnik a
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b
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University of Ljubljana, Biotechnical Faculty, Ljubljana, Slovenia
Slovenian Forestry Institute, Ljubljana, Slovenia
Department of Agricultural and Environmental Sciences, University of Udine, Udine, Italy
d
CNR-IBIMET, Firenze, Italy
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E. Mach Foundation, IASMA, San Michele all’Adige (TN), Italy
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a r t i c l e
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i n f o
a b s t r a c t
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Article history:
Received 12 July 2010
Received in revised form
29 November 2010
Accepted 2 December 2010
Available online xxx
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Keywords:
Secondary succession
Carbon cycle
Eddy covariance
Net ecosystem CO2 exchange
Precipitation pulse
Burba correction
Karst ecosystem
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Abandonment of marginal agricultural areas with subsequent secondary succession is a widespread type
of land use change in Mediterranean and mountain areas of Europe, leading to important environmental
consequences such as change in the water balance, carbon cycling, and regional climate. Paired eddy
flux measurement design with grassland site and tree/shrub encroached site has been set-up in the
Slovenian Karst (submediterranean climate region) to investigate the effects of secondary succession on
ecosystem carbon cycling. The invasion of woody plant species was found to significantly change carbon
balance shifting annual NEE from source to an evident sink. According to one year of data succession site
stored −126 ± 14 g C m−2 y−1 while grassland site emitted 353 ± 72 g C m−2 y−1 . In addition, the seasonal
course of CO2 exchange differed between both succession stages, which can be related to differences in
phenology, i.e. activity of prevailing plant species, and modified environmental conditions within forest
fragments of the invaded site. Negligible effect of instrument heating was observed which proves the
Burba correction in our ecosystems unnecessary. Unexpectedly high CO2 emissions and large disagreement with soil respiration especially on the grassland site in late autumn indicate additional sources of
carbon which cannot be biologically processes, such as degassing of soil pores and caves after rain events.
© 2010 Published by Elsevier B.V.
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1. Introduction
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Grasslands contribute to the biosphere–atmosphere exchange
of greenhouse gases (GHGs) mainly with fluxes of carbon dioxide
(CO2 ) and methane (CH4 ) that are intimately linked to management (Soussana et al., 2007). Cutting regime, grazing, fertilization
and other disturbances can severely alter different components of
carbon cycle and can strongly influence rates of carbon gain or
loss. Contrary, effects on carbon cycling are also expected when
human disturbances seize and succession towards potential vegetation (e.g. shrubland or forest) starts. In relation to land use, the
spontaneous transition of grasslands to forests, which is especially
widespread in regions where the agriculture is limited due to unfavorable geomorphological, soil and climatic conditions, has been
one of the most evident environmental changes in recent decades
in Europe and beyond (McLauchlan et al., 2006; Mottet et al., 2006;
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∗ Corresponding author at: Slovenian Forestry Institute, Ljubljana, Slovenia.
E-mail address: [email protected] (M. Ferlan).
MacDonald et al., 2000). At global level it has been estimated that
this abandoned area amounts 385–472 × 106 ha (Campbell et al.,
2008). Hurtt et al. (2006), using HYDE (Historical Database of the
Global Environment, by Klein, 2001), estimated that 269 × 106 ha of
crop lands were permanently converted to other land uses between
the years 1700 and 2000. It has been estimated that about 13% of
agricultural areas were abandoned in Europe in four decades since
1961 (Rounsevell et al., 2003, 2006) with the Mediterranean (PintoCorreia, 1993) and mountain regions (MacDonald et al., 2000) being
subjected to the most intensive marginalizaton and abandonment.
For Italy, Falcucci et al. (2007) report on forest share increase from
18.7% of national territory in 1960 to 32.5% in 2000; the share of
agricultural (especially pasture) areas dipped simultaneously from
56.6% down to 38.5%. Similar pattern was also observed for SW part
of Slovenia (Kaligarič et al., 2006).
When grasslands are abandoned, becoming overgrown by
woody plants, their carbon balance drastically changes. This issue
has been addressed in several studies (Post and Kwon, 2000;
Jackson et al., 2002; McKinley and Blair, 2008) but, despite of
the rapid growth of regional and global networks for the mea-
0167-8809/$ – see front matter © 2010 Published by Elsevier B.V.
doi:10.1016/j.agee.2010.12.003
Please cite this article in press as: Ferlan, M., et al., Comparing carbon fluxes between different stages of secondary succession of a karst grassland.
Agric. Ecosyst. Environ. (2010), doi:10.1016/j.agee.2010.12.003
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surement of biosphere and atmosphere gas exchanges (Valentini
et al., 2000; Baldocchi, 2003; Papale et al., 2006), including the
Mediterranean region (Miglietta and Peressotti, 1999; Reichstein
et al., 2002; Rambal et al., 2003, 2004; Xu and Baldocchi, 2004;
Ciais et al., 2005; Ma et al., 2007; Pereira et al., 2007; SerranoOrtiz et al., 2007), the consequences of regional land use changes
on the carbon cycle remains poorly understood. Thus, it is urgent
to understand the change in carbon balance of the abandoned
and afforested agricultural lands of Europe and specifically of the
Mediterranean basin. Shifting dominance among herbaceous and
woody vegetation alters net primary production (NPP), plant allocation, rooting depth and soil processes affecting nutrient cycling
and carbon storage. The invasion of woody vegetation into grasslands is generally thought to lead to an increase in amount of carbon
in those ecosystems, changing two major carbon pools, woody
plant biomass and soil organic matter (e.g. Alberti et al., 2008).
While increasing aboveground biomass represents a dominant
sink of carbon, soil carbon pools show an inconsistent response
under woody plants encroachment. In fact, this response has been
found to be extremely dynamic and dependent on vegetation, litter recalcitrance properties and on environmental conditions that
influence decomposition. Jackson et al. (2002), studying carbon
budgets of woody plants invading grasslands with different precipitation regimes, found a clear negative relationship between
precipitation and changes in soil organic carbon and nitrogen, with
drier sites gaining and wetter sites losing carbon. In some cases the
rate of the loss overrode the sink strength gained by aboveground
biomass increment. Water relations also proved to be of significant
importance for carbon budget of invaded grasslands in other studies (Scott et al., 2006; Kurc and Small, 2007). Generally, much of
the variation in grassland net ecosystem exchange (NEE) is constrained by the amount of precipitation (Flanagan et al., 2002). In
this respect, arid and semi-arid grasslands are especially sensitive
to inter-annual variability in precipitation (Huxman et al., 2004).
For example, Nagy et al. (2007) studying NEE dynamics and carbon balance of a dry, extensively managed sandy grassland on the
Great Hungarian Plain in the years 2003 and 2004 found that it a
weak source of carbon in 2003 (80 g C m−2 ), owing to the exceptionally hot and dry conditions, while it was a moderate sink in
2004 (−188 g C m−2 ), when the amount of precipitation was considerably above the 10-year average. Carbon dioxide exchange of
dry annual C3 grassland and a proximate oak-grass savanna was
also studied by Ma et al. (2007). This 5–6-year study focused on
inter-annual variation in NEE, which was found to be significantly
related to length of growing season for the savanna, grassland,
and tree canopy: annual net carbon exchange (NEE) ranged from
−155 to −56 g C m−2 y−1 and from −88 to 141 g C m−2 y−1 at the
savanna and nearby grassland, respectively. Gross primary productivity (GPP) and ecosystem respiration (Reco ) depended primarily
on amount of seasonal precipitation. Inglima et al. (2009) reported
that Reco is stimulated after first autumn rains following summer
drought thus resulting in positive NEE in different Mediterranean
ecosystems.
A large portion of arid ecosystems in Mediterranean countries
is characterized by carbonate rocks, the bedrock material in Karst
systems. Carbonate rocks outcrop on ca. 12% of the water-free Earth
surface (Ford and Williams, 1989) and may play a direct role in the
global carbon cycle. Dissolution of limestone or dolomite, weathering and carbonate precipitation are the key reactions of geological
cycling of CO2 and are mostly governed by the physical–chemical
conditions of the soil environment. Several studies suggest that
cycling through the inorganic pool is an important contribution to
the ecosystem CO2 fluxes in Mediterranean ecosystems and should
not be neglected when partitioning the fluxes (Emmerich, 2003;
Kowalski et al., 2008; Inglima et al., 2009; Serrano-Ortiz et al., 2009,
2010).
Thus, the research of carbon cycling in karst grasslands that
are exposed to invasion of woody plants is challenging in many
respects. There are, however, difficulties that are inherent to experimentation in these karst ecosystems. To start with, relief with
depressions and sinkholes might affect, together with wind conditions, the quality of eddy flux measurements. This necessitates
a careful selection of the measuring site, for which, however, the
history of use has to be well-known, especially when C cycling is
studied in relation to natural succession. Secondly, the high degree
of heterogeneity of the ecosystems has to be taken into account.
This heterogeneity is to a large extent related to spatial heterogeneity of soil, which can be for example extremely shallow but can also
develop deeper organic patches. Stony soil with rocks limits the
application of some conventional methods (e.g. root exclusion for
partitioning of soil CO2 efflux) and makes other methods difficult
to be applied.
In the present study a paired eddy flux measurement design
was used in order to assess the NEE of two ecosystems: an extensively used semi-dry pasture and proximate abandoned grassland
with woody plants encroachment (succession site henceforth) at
Podgorski Kras plateau (SW Slovenia). The use of two eddy towers allowed detection of the influence of land use change, in our
case secondary succession, on C fluxes without confounding influences relating to meteorological variability, a serious shortcoming
of measurements with single eddy flux towers (Don et al., 2009).
Until now the altered pattern and magnitude of NEE has only rarely
been investigated by paired eddy-flux measurements (e.g. Scott
et al., 2006). The objectives of this paper are: (I) to analyze the yearly
NEE courses and seasonal changes in NEE for the grassland and the
succession site, (II) to compare the sites in their NEE response to
weather conditions, precipitation patterns and phenological development, and (III) to assess the role of the Burba correction for
accurate measurements of the carbon balance.
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2. Materials and methods
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2.1. Study area
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The study was conducted at the Podgorski Kras plateau
(45◦ 33 N, 13◦ 55 E, 400–430 m.a.s.l.) in the sub-mediterranean
region of Slovenia (SW Slovenia; Table 1). Due to its position at the
transition between the Mediterranean and central Europe, the karst
landscape of this area has been subjected to major human influences since at least 3000 years BC. Overgrazing effects during the
past centuries almost completely destroyed vegetation cover and
caused severe soil erosion which resulted in a stony, bare landscape.
Later, economic development leads to abandonment of agriculture which caused a slow but extensive spontaneous afforestation.
During the 18th century, some Austrian pine (Pinus nigra L.) plantations were also established. Historic human activities and natural
conditions resulted in today’s diverse landscape with co-occurring
successional stages ranging from grasslands to the secondary oak
forests.
Woody plant encroachment is characterized by shrubs of early
succession stages (Juniperus communis, Prunus mahaleb, Cornus mas,
Cotinus coggygria) and also tree species of mid- and late succession
(Quercus pubescens, Ostrya carpinifolia, Fraxinus ornus). Speciesrich semi-dry calcareous grasslands of the Scorzoneretalia order
still cover around 20% of the area, but more than 60% of former
grasslands were transformed to forest and shrub vegetation types
(Kaligarič et al., 2006). The most abundant grassland species are
Bromopsis erecta, Carex humilis, Stipa eriocaulis, Centaurea rupestris,
Potentilla tommasiniana, Anthyllis vulneraria, Galium corrudifolium
and Teucrium montanum.
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Please cite this article in press as: Ferlan, M., et al., Comparing carbon fluxes between different stages of secondary succession of a karst grassland.
Agric. Ecosyst. Environ. (2010), doi:10.1016/j.agee.2010.12.003
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Table 1
Main site characteristics.
Grassland
Succession
Meterorology
Mean annual temperature (1971–2000 data)
Mean annual precipitation (1971–2000 data)
10.5 ◦ C
1370 mm
10.5 ◦ C
1370 mm
Soil
Soil type
Soil rockiness (40 cm depth)
Average SOC (40 cm depth)
Soil carbon stock (40 cm depth)
Corg :N ratio
pH
Rendzic leptosol + eutric cambisols
53 ± 14%
9.1 ± 1.2%
167 ± 46 t ha−1
11.0 ± 0.6
7.2 ± 0.6
Rendzic leptosol + eutric cambisols
46 ± 30%
7.0 ± 2.4%
172 ± 52 t ha−1
12.2 ± 1.1
6.9 ± 0.8
Scorzoneretalia villosae (Carici
humilis-Centaureetum rupestris)
Succession stage towards Quercetalia
pubescentis (Ostryo-Quercetum
pubescentis)
40%
98 m3 ha−1
2.35 ± 0.80 t ha−1
29th April
22nd June
13th July
0.4/0.6 m
Vegetation
Vegetation type (alliance/association)
Tree cover
Aboveground tree biomass
Peak aboveground herbaceous biomass (2009 data)
Scorzonera austriaca peak flowering (2009 data)
Centaurea rupestris peak flowering (2009 data)
Euphorbia nicaeensis peak flowering (2009 data)
Mean/max vegetation height
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<5%
<5 m3 ha−1
2.45 ± 0.60 t ha−1
26th April
17th June
1st July
3.4/7.0 m
The prevailing soil type is rendzic leptosol on a paleogenic limestone bedrock. Soil depth is very uneven ranging from 0 cm (rocky
outcrops) to several decimeters in soil pockets between rocks.
Rocks occupy on average 50% soil volume in the upper 40 cm of
the soil profile. Shallow soil and frequent wind diminish the effect
of high precipitation level and promote drought. Soils have clay
texture and are low in plant nutrients, especially phosphorus. The
percentage of soil organic matter in the topsoil is 12–15%. Soil pH
ranges from slightly basic to slightly acidic. In small depressions
and sinkholes (small dolines) eutric cambisols of much larger soil
depth are developed.
The climate is transient between the Mediterranean and continental. It is generally considerably more humid than true
Mediterranean climate, has less pronounced dry period in summer
and colder winter. This type of climate is often designated as submediterranean. The mean annual temperature is 10.5 ◦ C, the mean
daily temperature in January is 1.8 ◦ C and in July 19.9 ◦ C. Average
annual precipitation reaches 1370 mm (data from 30 year average
[1971–2000] of four meteorological stations in submediterranean
region [Environmental Agency of the Republic of Slovenia]). There
are two precipitation heights; primary one occurs in autumn and
secondary in late spring. Winters are rather windy (Bora wind);
snow cover is only periodic. The growing season ranges from April
to October.
Within the study area two study sites were chosen on the basis
of current and historic land use. The spatial distance of the sites
is 1 km. The grassland site has been used more or less permanently as a low intensity pasture (donkey, horse or sheep grazing
at stocking rates below 0.25 livestock unit per hectare) in the
last few decades. Tree coverage on the grassland site is below
5%, concentrated around sinkholes, which is a traditional way of
wind erosion protection. On the succession site small trees and
shrubs cover 40% of the area. The average height of tree layer,
which is mostly represented by Q. pubescens, is 7 m and aboveground woody biomass is 96 m3 ha−1 . The coverage of woody
species is uneven. With the continuing succession woody species
spread from nests of shrubs, which are presumably located on
the deeper soil, leaving larger or smaller gaps covered by herbaceous species. The composition of herbaceous layer is similar as
for the grassland site, with B. erecta, C. humilis and S. eriocaulis
being the most abundant species. The slope of neither site exceeds
3◦ .
Since we are interested only in changes in type of aboveground
biomass cover, we take into account only two land uses: forest (or
forest patches) and other land use (mainly grasslands). For this
purpose we chose aero-photographs from years 1957, 1975 and
orto-photograph from year 2009 (Surveying and Mapping Authority of the Republic of Slovenia). Geo-referencing for years 1957
and 1975 was done in ESRI ArcMap with reference to the georeferencing orto-photograph from year 2009. The area of interest
was clipped within 1.7 km × 0.9 km rectangle (Fig. 1) and forest
and other land uses were separated. Polygons with area smaller
than 9 m2 were chosen and eliminate to the nearest land use. At
the end calculation of area for each polygon were performed and
summarized within land use. This analysis showed that forest has
overgrown 21% of the analyzed area (153 ha) in the last 52 years.
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2.2. Eddy covariance and meteorological measurement
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Eddy covariance systems and other meteorological measurements were installed on both research sites (locations are marked
with triangles in Fig. 1) in July 2008 and one year of measurements are presented in this paper (January 1st 2009–December
31th 2009).
A weather station was installed at each site to measure the
following environmental parameters: soil temperature at three
depths (2, 10 and 30 cm) using thermocouples (TCAV, Campbell
Scientific, Logan, UT USA), soil water content (0–20 cm) using three
time domain reflectometers (CS616, Campbell Scientific, Logan, UT,
USA) inserted vertically, incident radiation (LP02, Campbell Scientific, Logan, UT, USA), incident (PPFDi) and reflected (PPFDr)
photosintetic flux density (LI-190, Li-Cor, Lincoln, NE USA), net
radiation (NR-LITE, Campbell Scientific, Logan, UT, USA), air temperature and humidity (HMP45AC, Vaisala, Helsinki, Finland), soil
heat flux (10 cm) using three soil heat flux plates (HFP01SC, Campbell Scientific, Logan, UT, USA) and precipitation (Rain gauge, Davis,
Hayward, CA, USA). All variables were measured at 0.1 Hz and then
averaged half-hourly.
For the location of the eddy tower on the grassland site special attention was paid to avoid the sinkholes in the vicinity, since
these might substantially affect horizontal and vertical wind direction. The eddy tower was located at least 140 m from the deeper
sinkholes with a height of 2 m. On the succession site sinkholes are
densely covered or surrounded by woody species and presumably
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Please cite this article in press as: Ferlan, M., et al., Comparing carbon fluxes between different stages of secondary succession of a karst grassland.
Agric. Ecosyst. Environ. (2010), doi:10.1016/j.agee.2010.12.003
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Fig. 1. Study area with the position of two eddy towers (upper triangle: site grassland 13◦ 55 27 ; 45◦ 33 2 ; lower triangle: site succession: 13◦ 55 16 ; 45◦ 32 37 )
and area of interest used for land use change analysis (rectangle 850 by 1700 m).
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have no major influence on wind direction and speed. At both sites,
an open-path eddy covariance system consisting of an open path
infrared gas (CO2 and H2 O) analyzer (LI-7500, Li-Cor, Lincoln, NE
USA) and sonic anemometer (Succession: CSAT3, Campbell Scientific, Logan, UT, USA. Grassland: USA-1, Metek GmbH, Elmshorn,
Germany) was installed at 15 m height and 2 m for succession and
grassland, respectively. The LI-7500 was pointed towards the north
by an angle of 20◦ to minimise solar radiation influence and to facilitate the shedding of water droplets from the sensor lenses after rain
events. Data from the sonic anemometer and the open path infrared
gas analyzer (IRGA) were recorded at a frequency of 20 Hz using
Q2 a CR3000 (Campbell Scientific) and Compact Eddy (Matese et al.,
2008) for the succession and grassland site, respectively. Ecosystem fluxes of CO2 , momentum, sensible (H) and latent heat (LE)
were averaged on a half-hourly base.
The applied methodology was based on the Euroflux protocol (Aubinet et al., 2000) with the Webb Pearman Leuning
correction (Webb et al., 1980) and method 4 of Burba correction (Burba et al., 2008). All post processing elaborations and
frequency response corrections have been performed using EdiRe
Data software (University of Edinburgh, 1999) and quality assessment and quality check analysis (QA/QC) were conducted according
to Foken and Wichura (1996). As it is well known, open path IRGA
provides inadequate and erroneous data during rainy or foggy
conditions, or when condensation occurs on the instrument optical lens, especially in autumn. Typically, the malfunctioning of
IRGA, in such conditions, causes the occurrence of spikes, and
in this case a spike analysis algorithm was applied to accept
or discard data, before the QA/QC analysis. A gap-filling procedure was applied to obtain daily fluxes (Reichstein et al., 2005;
http://gaia.agraria.unitus.it/database/eddyproc/index.html) when
the QA/QC criteria were not satisfied. Also fluxes when friction
velocity (u* ) was below of calculated u* threshold according to
Reichstein et al. (2005) was gap-filled. Thresholds were 0.27 m s−1
and 0.1 m s−1 for succession and grassland site, respectively. The
partitioning of NEE between gross primary productivity (GPP) and
total ecosystem respiration (TER) was performed according to
Lasslop et al. (2010).
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2.3. Uncertainty analysis
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To estimate the uncertainty of carbon balance for each site two
different sources of random errors were investigated. First, we
followed the Richardson and Hollinger (2007) methodology to calculate the uncertainty introduced in NEE by the random errors in
measurements ( MEAS ). Pairs of half-hourly fluxes in similar climatic conditions on two successive days (criteria after Richardson
et al. (2006)), were used to determine random errors (ı) which were
defined as differences between corresponding half hourly NEEs of a
pair of successive days. To consider higher errors at higher NEE values the relation between (ı) and NEE was established as described
in Beziat et al. (2009). Random noise was then added 100 times to
the filtered half hourly NEE values following a Laplace distribution
with 0 mean and (ı) standard deviation dependent on half hourly
NEE value. For each repetition dataset was gap-filled according to
Reichstein et al. (2005) and half-hourly cumulative NEE was calculated. Daily, monthly or annual sums, different due to random
noise, were used to obtain ( MEAS ).
Second, uncertainty and errors introduced by the gap-filling
procedure ( GAP ) were calculated following Beziat et al. (2009).
Gaps (same number, same size and with similar distribution
between night and day) were randomly created in continuous
annual dataset. Then gap-fill procedure according to Reichstein
et al. (2005) was performed. Gap generation and gap-fill were
repeated 100 times. Daily, monthly or annual sums, different due
to errors introduced by the gap-filling, were used to obtain ( GAP ).
Finally, daily, monthly or annual cumulative NEE uncertainty
( NEE ) was estimated by taking the square root of the sum of vari2
2 .
ances MEAS
and GAP
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3. Results
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For the observed period (January 1th 2009–December 31th
2009) no major differences were measured between grassland
and succession site concerning air temperature and precipitation
(Fig. 2). Mean daily air temperature at succession site was 12.7 ◦ C
and was 0.5 ◦ C higher than mean daily air temperature at the
grassland but soil temperature at the grassland was higher in
summer and lower in winter than at the succession. Total precipitation was 1018 mm. Soil water content was higher at succession
(0.21 m3 m−3 ) than at the grassland (0.18 m3 m−3 ) on average.
Observed period was compared to the normal of region (long term
averages 1971–2000). Mean annual temperature at our sites was
1.8 ◦ C higher and differences in precipitation were also detected in
comparison with climatic normal of the region. In 2009 there was
less precipitation in spring, summer and autumn but more in winter, compared to the average precipitation pattern. No distinctive
drought period was observed in 2009 during summer months.
Concerning the eddy covariance data, 67% and 33% percent of
expected data have not been discarded for succession and grassland, respectively. Most data discards occurred during night and
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Fig. 2. Environmental conditions in 2009. (A) Mean air temperature, (B) mean soil temperature, and (C) soil water content (SWC) and rain at the two study site (succession:
dotted line; grassland: continuous line).
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winter-time even though, because of a problem with the anemometer, two weeks of data were missing at the grassland site in
September. A good agreement between energy fluxes measured
at the eddy station and energy balance, calculated at the weather
stations using net radiation and soil heat fluxes, was found for both
sites (grassland: slope = 1.15, intercept = 33.03 W m−2 , R2 = 0.81;
succession: slope = 1.09, intercept = 22.87 W m−2 , R2 = 0.92). Overestimation of energy fluxes measured with eddy covariance (slopes
were greater than 1 at both sites), which is otherwise rarely
reported (Twine et al., 2000; Wilson et al., 2002), could be explained
by the high spatial heterogeneity of our ecosystems (i.e. tree
patches and white, highly reflective stones) which could have
caused an underestimation of net radiation at the eddy tower
resulting in the unrepresentativeness of the entire footprint.
On a yearly basis, succession site was a net sink of carbon
(NEE = −126 ± 14 g C m−2 y−1 ) while grassland site was a source
of carbon (NEE = 353 ± 72 g C m−2 y−1 ). For both land uses Fig. 4A
clearly shows the differences in growing season length and net
production rates. The grassland site had a maximum rate of net C
uptake of −74.6 ± 11.5 g C m−2 month−1 , while the succession site
had a maximum net uptake of −86.4 ± 3.9 g C m−2 month−1 (Fig. 4).
Both the land uses had their maximum uptake in May.
After Burba correction was applied on our datasets cumulative NEE fluxes changed (Fig. 3). Succession site shifted from
sink (−126 g C m−2 y−1 ) to weak source (33 g C m−2 y−1 ) of carbon (Fig. 3B), while the grassland remained a source (309 and
353 g C m−2 y−1 without and with Burba correction, respectively)
(Fig. 3A).
Both ecosystems peaked as sources of carbon in autumn (Fig. 4):
even though gross primary production (GPP) was still positive
(Fig. 4B), total ecosystem respiration (Reco ) measured at the grassland was particularly high in November and December when most
of the precipitation occurred thus causing a positive NEE (Fig. 4C).
In fact, soon after intensive autumn rain events, daily mean NEE
became largely positive in response to enhanced ecosystem respiration, but rapidly decreased in the following days (Fig. 5).
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4. Discussion
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Eddy covariance measurements in 2009 revealed weak sink
activity of pubescent oaks invading grassland and relatively high
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annual release of CO2 from the pasture. The later observation does
not correspond with the generalized view that European grassland ecosystems predominantly act as sink for atmospheric CO2
reported in previous works (Soussana et al., 2007; Gilmanov et al.,
2007). On the other hand, the shifts from sink to source are frequently reported for conditions of limited productivity (e.g. Nagy
et al., 2007). In ecosystems which are often faced by drought periods (due to low precipitation rates or shallow soils) the annual
productivity and consequently the NEE are primarily controlled
by precipitation levels and distribution. During the study period,
there was a short drought period with strongest effects in late
May which differently affected the two investigated ecosystem. In
the grassland, late May is generally the period of the most intensive growth of the herbaceous layer and peak flowering time of
Fig. 3. Cumulative fluxes of net ecosystem exchange (NEE) with and without Burba
correction (A: grassland; B: succession). Uncertainty (width of ± NEE —see text)
band is shown for NEE cumulative without Burba correction.
Please cite this article in press as: Ferlan, M., et al., Comparing carbon fluxes between different stages of secondary succession of a karst grassland.
Agric. Ecosyst. Environ. (2010), doi:10.1016/j.agee.2010.12.003
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Fig. 4. (A) Monthly net ecosystem exchange (NEE) with uncertainty (error bars of NEE ), (B) monthly gross primary production (GPP) and (C) monthly ecosystem respiration
(Reco ) at the two experimental sites.
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many herbaceous species. Consequently, the shortage of water
resulted in a growth retardation and in a reduced or absent flowering of many herbaceous species. Due to the phenology of the
most abundant species in the area (negligible summer and autumn
re-growth), this effect on productivity could not be mitigated
later in the season. A tight coupling of productivity (and NEE) to
timing of precipitation has been previously reported by Xu and
Baldocchi (2004) for Mediterranean annual grassland in California and by Frank and Karn (2005) for the mixed-grass prairie of
the Northern Great Plains. The succession site appears, in contrast to pasture, less susceptible to drought episodes which might
be the consequence of larger rooting depth (Jackson et al., 1996;
Potts et al., 2006): deeper is soil where the shrubs and trees are
invading, higher is soil water content due to lower levels of evaporation caused by tree/shrub shading which effects soil temperature
(Fig. 2). Additionally, another possible explanation is related to different strategies of grasses and woody plants to cope with water
stress (intensive vs. extensive water users according to RodriguezIturbe et al. (2001)). The conservative use of water by woody plants
(stomata closure during highest daily temperatures and radiation
in summer) was shown in different water limited ecosystems (Laio
et al., 2001; Wan and Sosebee, 1991). The lower water use efficiency of grassland in comparison with the succession site might
be detected in our evapotranspiration (ET) data (not shown here)
Fig. 5. Daily net ecosystem exchange (NEE) and soil respiration (SR) with uncertainty (error bars of ± NEE ), from 1st November to 31th December 2009 (A: grassland; B:
succession). Environmental condition of the period: (C) daily mean soil water content (SWC) with precipitation and (D) daily mean soil temperature (Ts ).
Please cite this article in press as: Ferlan, M., et al., Comparing carbon fluxes between different stages of secondary succession of a karst grassland.
Agric. Ecosyst. Environ. (2010), doi:10.1016/j.agee.2010.12.003
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with higher values during drought period for grassland (in period
from 16th to 25th May 2009 sums of ET: 44 mm in grassland vs.
31 mm on succession site) which was similarly reported by Frank
and Karn (2005) when comparing summer ET between short-grass
prairie and shrub invaded prairie. However lower ET values for succession site might also be the sheer effect of lower soil temperatures
due to tree shading.
Despite the Burba correction was found to be more appropriate
for cold ecosystems (Burba et al., 2008), significant effect of Burba
correction was also observed in our case especially for the succession site where the ecosystem turned from sink to weak source.
Similar results were also shown by Reverter et al. (2010). However, the difference between the cumulative carbon fluxes with
and without Burba correction is well within the uncertainty for
cumulative flux in grassland site but not for cumulative flux at
the succession site (Fig. 3). For this reason, we further investigated
the instrument heating and the influence of Burba correction on
cumulative fluxes of the two ecosystems. Following Burba et al.
(2008), air temperature and temperature at the bottom of IRGA
were measured in December 2009. Only night time measurements
were considered in order to avoid any influence of solar radiation on
temperature probes (air temperature range: −10 to 15 ◦ C). A strong
linear relationship between air temperature (Ta ) and temperature
at the bottom of the IRGA (Ts ) was found at both the ecosystems. Difference between Ts and Ta was within the probe precision (±0.5 ◦ C)
and could not be considered significant. Furthermore, Burba et al.
(2008) reported much higher difference between Ts and Ta during
nights (slope = 0.88, intercept = 2.17 ◦ C). Thus, instrument surface
heating can be assumed negligible and the application of method 4
proposed by Burba et al. (2008) was avoided at our site.
Our measurements clearly revealed differences in the annual
course of NEE for the two studied sites. The succession showed one
month time lag before becoming a net C sink in spring and continued to fix carbon for further two months in autumn in comparison
to the grassland. Thus, grassland and succession showed growing
seasons of five and seven months, respectively. Since both sites are
similar in terms of the herbaceous layer (82% of common species),
phenological development of its main species and peak biomass
(244 ± 60 g of dry mass m−2 on grassland vs. 227 ± 80 g m−2 on the
succession site), it is possible to conclude that the shifts of C balance are mainly governed by the activity of the forest patches. In the
period when the herbaceous layer of the succession site sequesters
carbon to a similar intensity as the grassland site (based on peak
biomass per hectare) it is to be expected that the respiration of
forest patches compensates this sink making the succession ecosystem close to carbon neutral. These conclusions can be supported
by phenological observations (data not reported) which show that
the negative NEE values match with bud bursting and early leaf
development. Interestingly, Frank and Karn (2005) reported the
contrary: in their study the shrub prairie acted as sink earlier in
growing season compared with the grass prairie which is probably
governed by different ecology of the invading shrubs.
Concerning with the unexpectedly high CO2 emissions after
rain events, recent works highlighted the role of geochemical rock weathering (dissolution and precipitation) processes in
the total surface-atmosphere CO2 exchange (Emmerich, 2003;
Kowalski et al., 2008; Serrano-Ortiz et al., 2009, 2010). Furthermore, CO2 degassing from subterraneous systems can significantly
contribute to NEE of karst ecosystems as shown by Were et al.
(2010). Comparison of daily NEE course and daily precipitations
for November–December period revealed clear response of CO2
effluxes to precipitations. These responses were most prominent
after the first rain pulses that followed a relatively dry period (e.g.
beginning of December). To verify the consistency of eddy measurements, soil respiration (SR) was periodically measured and
then modeled using SWC and Ts on both sites. A good agreement
7
between NEE and modeled SR has been found at the succession
site (Fig. 5), while at the grassland site SR showed an increase
after rains even though at a lower rate. This behavior seems to
indicate that SWC and Ts can explain only part of the variability
in fluxes for the grassland. One hypothesis for higher CO2 release
at the grassland site could be the degassing of caves after rain
events (Serrano-Ortiz et al., 2010). In fact, preliminary radar surveys
showed the presence of caves at the pasture but, unfortunately, we
were not able to perform such a survey at the succession site. It can
be concluded that high concentrations of CO2 , built up from inorganic C sources and soil microbial activity during the previous dry
and warm period (interpulse), are physically displaced as percolating water fills soil pore spaces and caves (Huxman et al., 2004).
However, more detailed studies are needed to elucidate how these
sources differently contribute to NEE at the pasture and succession site, respectively. In fact, as suggested by Serrano-Ortiz et al.
(2009) biogeochemical modeling that would couple existing models for biological and geochemical processes, is needed to separate
net CO2 fluxes into geochemical and biological components.
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5. Conclusions
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CO2 exchange over carbonaceous substrate is highly complex.
In the case of our study, this complexity is further increased by
the issue of natural succession. In the first period of research at
Podgorski Kras we were able, by applying a paired eddy flux measurement design, to show that invasion of woody plant species
drastically change fluxes of CO2 shifting annual NEE from source to
sink. In addition, seasonal course of CO2 exchange differed between
both succession stages, which can be related to the differences
in phenology, i.e. activity of prevailing plant species and changed
micrometeorological conditions within forest fragments of invaded
site. However, future studies in climatically different years that will
address biological processes (photosynthesis and respiration), geochemical processes (carbonaceous rock dissolution and carbonate
precipitation) and macro pore ventilation are needed, for a more
thorough analysis of carbon cycling in invaded karst pastures.
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Acknowledgements
536
The research was supported with funds of Slovenian Research
Agency and Slovenian Ministry of Agriculture, Forestry and Food
(project J4-1009, project V4-0536 and young researcher program)
and programs CARBO-EXTREME EU and GHG-Europe. We thank
Franci Veturazzi and Zlatko Rojc for their permissions to perform
the study on their lands and for their interest in our activities. We
also thank Marjanca Jamnik, Diego Chiabà, Gabrijel Leskovec, Milan
Kobal and Iztok Sinjur for their help during fieldwork. The authors
would like to thank to two anonymous referees whose comments
greatly improved the text.
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