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SC IE N CE OF T H E TOT AL E N V I RO N ME N T 4 0 7 ( 2 00 8 ) 6 9 2–6 97
a v a i l a b l e a t w w w. s c i e n c e d i r e c t . c o m
w w w. e l s e v i e r. c o m / l o c a t e / s c i t o t e n v
Carbon and nitrogen cycles in European ecosystems respond
differently to global warming☆
C. Beier a,⁎, B.A. Emmett b,1 , J. Peñuelasc,2 , I.K. Schmidt d,3 , A. Tietemae,4 , M. Estiartec,2 ,
P. Gundersend,3 , L. Llorensc,2,5 , T. Riis-Nielsend,3 , A. Sowerbyb,1 , A. Gorissen f,6
a
RISØ National Laboratory for Sustainable Energy, Risø DTU, P. O. Box 49, DK-4000 Roskilde, Denmark
Centre for Ecology and Hydrology-Bangor, Environment Centre Wales, Deiniol Road, Bangor, Gwynedd LL572UP, UK
c
Ecophysiology and Global Change Unit CSIC-CEAB-CREAF, CREAF (Center for Ecological Research and Forestry Applications), Edifici C,
Universitat Autònoma de Barcelona, 08193 Bellaterra, Barcelona, Spain
d
Forest and Landscape, Denmark, Royal Agricultural and Veterinary University, Hørsholm Kongevej 11, DK-2970 Hørsholm, Denmark
e
Center for Geo-ecological Research (ICG), Institute for Biodiversity and Ecosystem Dynamics (IBED) – Physical Geography,
University of Amsterdam, Nieuwe Achtergracht 166, 1018 WV Amsterdam, The Netherlands
f
Plant Research International, P. O. Box 16, Bornsesteeg 65, NL-6700 AA Wageningen, The Netherlands
b
AR TIC LE D ATA
ABSTR ACT
Available online 19 October 2008
The global climate is predicted to become significantly warmer over the next century. This
will affect ecosystem processes and the functioning of semi natural and natural ecosystems
Keywords:
Climate change
Global warming
Ecosystem effects
C & N interactions
in many parts of the world. However, as various ecosystem processes may be affected to a
different extent, balances between different ecosystem processes as well as between
different ecosystems may shift and lead to major unpredicted changes. In this study four
European shrubland ecosystems along a north–south temperature gradient were
experimentally warmed by a novel nighttime warming technique. Biogeochemical cycling
of both carbon and nitrogen was affected at the colder sites with increased carbon uptake for
plant growth as well as increased carbon loss through soil respiration. Carbon uptake by
plant growth was more sensitive to warming than expected from the temperature response
across the sites while carbon loss through soil respiration reacted to warming in agreement
with the overall Q10 and response functions to temperature across the sites. Opposite to
carbon, the nitrogen mineralization was relatively insensitive to the temperature increase
and was mainly affected by changes in soil moisture. The results suggest that C and N cycles
respond asymmetrically to warming, which may lead to progressive nitrogen limitation and
thereby acclimation in plant production. This further suggests that in many temperate
☆
This paper was presented at the 5th International Symposium on Ecosystem Behaviour, held at the University of California, Santa Cruz,
on June 25–30, 2006.
⁎ Corresponding author. Tel.: +45 4677 4161; fax: +45 4677 4160.
E-mail addresses: [email protected] (C. Beier), [email protected] (B.A. Emmett), [email protected] (J. Peñuelas), [email protected]
(I.K. Schmidt), [email protected] (A. Tietema), [email protected] (M. Estiarte), [email protected] (P. Gundersen),
[email protected] (L. Llorens), [email protected] (A. Sowerby), [email protected] (A. Gorissen).
1
Tel.: +44 1248 376500; fax: +44 1248 362133.
2
Tel.: +34 9358 12199; fax: +34 9358 11312.
3
Tel.: +45 4576 3200; fax: +45 4576 3233.
4
Tel.: +31 20 525 7458; fax: +31 20 525 7431.
5
Present address: Department of Environmental Sciences, Faculty of Sciences, University of Girona, Campus Montilivi, E-17071, Girona,
Spain.
6
Tel.: +31 3174 75046; fax: +31 3174 23110.
0048-9697/$ – see front matter © 2008 Elsevier B.V. All rights reserved.
doi:10.1016/j.scitotenv.2008.10.001
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S CIE N CE OF T H E TOT AL E N V I RO N ME N T 4 0 7 ( 2 00 8 ) 6 9 2–6 97
693
zones nitrogen deposition has to be accounted for, not only with respect to the impact on
water quality through increased nitrogen leaching where N deposition is high, but also in
predictions of carbon sequestration in terrestrial ecosystems under future climatic
conditions. Finally the results indicate that on the short term the above-ground processes
are more sensitive to temperature changes than the below ground processes.
© 2008 Elsevier B.V. All rights reserved.
1.
Introduction
Elevated atmospheric CO2 generated through human activities is predicted to affect the global climate by increasing the
global mean surface temperature by 1.4–5.8 °C (IPCC, 2001).
Different ecosystem processes and biological species may
respond asymmetrically to climatic changes (Walther et al.,
2002) and the overall effect on ecosystem functioning is
therefore often highly complex and determined by the relative
sensitivity of the different processes to climate change.
Recently, significant changes in ecosystem functioning and
structure for a wide range of biomes and ecosystems have
already been demonstrated (Walther et al., 2002) as well as
evidence for climate change related extended growth season,
advancement of spring phenology and upward and northward
movement of the plant species distributions (Myneni et al.
1997; Peñuelas and Filella, 2001; Root et al. 2003; Parmesan and
Yohe, 2003).
Predictions from different types of models have indicated
that global warming may accelerate due to C-cycle feedbacks
(Agren and Bosatta, 1996; Cox et al., 2000; Cramer et al., 2001), i.e.
decrease terrestrial carbon sequestration, but very few realistic
measurements have been available to test these predictions.
Understanding the effects of warming on the balance between
changes in C vegetation uptake and the loss of carbon through
respiration is essential if we are to reliably predict climate
change effects on net ecosystem carbon sequestration. The
confounding effects of nitrogen have also been discussed (Luo
et al., 2004) although very few data are available or it has
generally been limited to the impacts of nitrogen deposition
(Nadelhoffer et al., 1999) rather than differential responses of
the internal carbon and nitrogen cycles that we describe here.
The majority of previous studies of climate change effects
on terrestrial ecosystems in the field face two limitations.
First, studies are geographically unbalanced as the main focus
has been on biomes from arctic, boreal or temperate regions
(Van Breemen et al., 1998; Chapin et al., 1995) because
ecosystem effects and feedback mechanisms have been
expected to be largest in these regions and because global
climate models predict greater temperature increases at
higher latitudes (IPCC, 2001). Second, the methods used to
experimentally warm ecosystems, which include soil electric
heating cables (Van Breemen et al., 1998; Melillo et al., 2002), IR
radiators (Harte and Shaw, 1995) and growth chambers
(Chapin et al., 1995), are subjected to various artifacts and
thus, concerns have been raised that they do not realistically
simulate global warming (Schulze et al., 1999). Within two EU
projects CLIMOOR and VULCAN (Beier et al., 2004) we studied
effects of warming in so far underrepresented shrubland
ecosystems at lower latitudes across Europe. We did this by
combining a field scale experimental approach with a gradient
(space for time substitution) approach. The combination of
field-scale manipulations conducted along climatic gradients
provides a tool to evaluate short-term (treatment) and longterm (gradient) effects and the relative sensitivity of different
biomes to climatic perturbations. The aim of the study was to
assess the short and long term effects of warming on key
ecosystem processes and ecosystem functioning. The objectives of the present paper are:
• To synthesise the effects of warming on carbon and nitrogen
sequestration and on the main release processes in shrubland ecosystems.
• To relate the short term response after 3 years of warming
treatment to the long term changes represented by the
temperature gradient across the sites.
• To compare the above- and below-ground responses.
2.
Methods
2.1.
Study sites and experimental design
The studies were carried out at 4 shrubland sites in Mols,
Denmark (DK, 56°23′N 10°57′E, MAT 8.7 °C, MAP 750 mm year− 1,
elevation 58 m); Oldebroek, the Netherlands (NL, 52°24′N 5°55′E,
MAT 9.3 °C, MAP 1033 mm year− 1, elevation 25 m); Clocaenog,
United Kingdom (UK, 53°03′N 3°28′W, MAT 7.0 °C, MAP 1607 mm
year− 1, elevation 490 m) and Garraf, Spain (SP, 41°18′N 1°49′E,
MAT 15.6 °C, MAP 456 mm year− 1, elevation 210 m). The soils
cover an organic rich podzol in UK, nutrient poor podzols in DK
and NL and an old weathered soil in SP. Vegetation is dominated
by Calluna vulgaris and Deschampsia flexuosa (DK, UK and NL) or
Erica multiflora and Globularia alypum (SP).
In these four sites experimental night time warming was
applied to three 20 m2 study plots at each site. The night time
warming approach was chosen because greenhouse gas accumulation in the atmosphere reduces loss of long wave IRradiation from the earth back into the atmosphere mainly at
night. Consequently, it is the increased minimum temperatures
that have been shown to be mainly responsible for the global
temperature increase observed so far (IPCC, 2001) and have been
shown of significant importance for the effects (Alward et al.,
1999). The experimental warming method employed in this
study was designed to simulate this night time warming
pattern. A light scaffold at the height of the vegetation (0.6–
1 m) carried a reflective aluminium foil (ILS ALU, AB Ludvig
Svensson, Sweden) over each plot. The foils reflected 97% of the
direct and 96% of the diffuse radiation. The curtains were
automatically pulled over the vegetation at sunset (light
intensity b200 lux) and automatically removed at sunrise to
leave the plots open during daytime. During nocturnal rain
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Fig. 1 – Relationships between a) above-ground plant
productivity (gC m− 2 year− 1) and b) below ground soil
respiration (gC m− 2 year− 1) and mean annual temperature in
the control (open squares and solid line) and warming
treatments (black diamonds and dashed lines) over the first
3 years of manipulation. Lines are simple best fitted lines.
events and high wind speeds the curtains were removed to keep
hydrological conditions unaffected and to avoid damage to the
system respectively (Beier et al., 2004). The curtains reduced the
heat loss during night by 64% from 33 W m− 2 to 12 W m− 2
increasing the temperature in the soil by 0.5–1.5 °C (DK), 0–2 °C
(UK), 0–1 °C (NL), and 1–2 °C (SP). These moderate temperature
elevations increased the average annual growth potential
(Growing Degree Days — GDD (threshold 5 °C)) by 9–16% at the
non-Mediterranean sites (UK, NL, DK, no change in SP) and
reduced the number of days with frost by 19–44% (Beier et al.,
2004). Three 20 m2 untreated reference plots at each site served
as control for comparison of responses.
The method has the advantage that unintended edge
effects and artefacts were small as documented by measurements of curtain movement, temperatures, precipitation and
water input to the plots, radiation balance during campaigns,
relative humidity and wind speed (Beier et al., 2004). Light
conditions were not affected since the plots were kept open
during daytime (Beier et al., 2004). Disadvantages of the
methodology include lack of control on the degree of warming,
and little or no warming of plants during daytime and
therefore no influence on daytime maximum temperatures.
2.2.
Measurements
Total plant productivity was estimated as the sum of the
change in total above-ground biomass and litterfall. Total
above-ground biomass was estimated through non destructive point frequency measurements conducted during summer each year in 5 fixed study areas (UK, DK and NL) or
transects (SP) in each plot (n = 100 per quadrat/transect). At
each site, conversion of the point frequency measurements to
above-ground biomass was calibrated in harvested subplots
outside the experimental plots (n = 5/site; p b 0.01) (Peñuelas
et al., 2004). Litterfall from shrub plants was collected monthly
or bimonthly by litterfall collectors placed randomly under the
vegetation (n = 5–10/plot). Litterfall from grasses (Mols) was
estimated by assuming that annual litterfall equals the aboveground biomass production. Plant material (current year
shoots, branches and stems) was collected and chemically
analysed for nitrogen and carbon in the lab according to
standard procedures (Peñuelas et al., 2004).
Below-ground soil respiration was measured seasonally or
monthly in the 3rd treatment year by Infra Red Gas Analysers
(IRGA — PP-systems EGM2 or EGM4) applied to 2 vegetation
free permanent bases in each plot or by syringe sampling from
static chambers and subsequent analyses by gas chromatography (Emmett et al., 2004). Single exponential response
curves of soil CO2 emissions to temperature were fitted to all
data as well as the site specific data. Annual soil CO2 fluxes for
each site and treatment were estimated from these functions
and monthly average temperatures.
Below-ground net N mineralisation was measured seasonally in the second treatment year by the buried bag technique
with parallel soil core incubation in the field for 0 and 1 month
and N-mineralisation estimated from difference in inorganic
N (Emmett et al., 2004).
Soil water below the root zone was continuously extracted
by porous cup soil water samplers (PRENART super quartz,
Frederiksberg, DK) and nitrogen content was analysed
monthly at UK, DK and NL sites. N leaching was estimated
from soil water N content and model estimated water fluxes
(Schmidt et al., 2004). Soil water surplus at the SP site was too
low to allow soil water collection.
Treatment and site effects were analysed by using a two-way
ANOVA with treatment and site as factors (n=3/treatment/site)
(plant and soil responses) and by a repeated measure ANOVA
with temperature as the main factor (soil solution chemistry). ttests were conducted to compare control and warming in each
particular site, and linear and/or non-linear multiple regression
analyses were conducted to analyse the relationships between
the studied response variables and soil moisture and temperature
for the control and warming treatments at each site In all cases, pvaluesb 0.05 were considered as statistically significant. Analyses
on plant responses were performed with software packages from
Statview (Abacus Concepts Inc., Cary, North Carolina, USA) and
Statistica (StatSoft, Inc. Tulsa, Oklahoma), on soil responses by
Minitab (Minitab Inc., Coventry, UK) and on soil water by the GLM
procedure in SAS (SAS Institute, Cary, North Carolina, USA).
3.
Results
3.1.
Plants
Plant productivity in the control plots showed no temperature sensitivity among the sites since no significant
differences were observed across the temperature gradient
(ANOVA, Fig. 1a). On the other hand, warming increased
total above-ground biomass production at the colder NL (68%,
but not significant, t-test) and UK (156%, p b 0.05, t-test) sites
(Fig. 1a). Warming had no effect on total above-ground biomass
production at the warm Mediterranean ecosystem.
3.2.
Soil carbon and nitrogen
Below-ground carbon loss measured as soil respiration was 2–
6 times bigger than carbon assimilation with the biggest
differences being at the cold and carbon rich site in Wales and
at the warm site in Spain (Fig. 1a and b). Carbon loss from
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Fig. 2 – Relationship between soil respiration (gC m− 2 h− 1) and soil temperature in the control (open squares, solid line) and
warming (black diamonds, dotted line) treatments at all four sites together with best fitted exponential response functions, r2
and Q10 values. C: control; W: warming.
below-ground biological activity was largely controlled by
temperature both across the natural temperature gradient
across the sites with a Q10= 1.8 (r2 = 0.22, p b 0.01) as well as
within each site (Fig. 2). The Q10 values had a strong relationship
to the mean annual temperature with the biggest temperature
sensitivity (Q10 = 7.8) at the colder site in UK and the lowest
sensitivity (Q10= 1.4) in the warm dry site in Spain (Fig. 3). The
response functions for soil respiration to temperature and the
Q10 values were not affected by warming at any of the sites
(Fig. 2) and thus soil respiration was stimulated at 7–26% by the
imposed experimental warming at the 3 colder Northern sites
(UK, DK and NL) (Fig. 1b) with a sensitivity to the experimental
warming similar to the sensitivity across the natural temperature gradient represented by the sites (Figs. 1b, 4a). In contrast to
the colder northern sites warming slightly reduced soil respiration in the warm and water limited Spanish site (Figs. 1b, 4a).
In contrast to carbon mineralisation inorganic-N production by soil microbes (net N-mineralisation) was sensitive to
soil moisture extremes when compared over the climatic
gradient across the sites (r2 = 0.49; p b 0.001). Temperature
explained only 24% (p = 0.06) of the variation in net Nmineralisation with a Q10 of 1.5 and only when soil moisture
was neither limiting (b20%) or in excess (N60%) (Emmett et al.,
2004). In agreement with the N mineralisation observed from
the climatic gradient across sites, the results from the
experimental warming showed that temperature was not
the primary control of N mineralisation (Fig. 4b).
N leaching was not directly related to climatic factors but
rather reflected site-specific differences in N deposition rates
and N-status across the sites. Only the NL site, which received
high inputs of atmospheric N-deposition and already leached
significant levels of nitrate, responded significantly to warming by doubling N-leaching from 18 to 35 kgN ha− 1 year− 1
(Schmidt et al., 2004, Fig. 4c).
4.
Discussion
4.1.
Plants
The stronger response of plant growth to warming at the
colder sites may seem surprising given the lag of response in
Fig. 3 – Relationship between Q10 calculated for soil
respiration and mean annual temperature in the control plots
at the four sites.
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Fig. 4 – Relationships between below-ground ecosystem processes — a) annual average soil respiration (gC kg soilC− 1 year− 1),
b) seasonal average nitrogen mineralisation rate (mgN kg soilC− 1 year− 1) and c) annual average NO3-leaching (gN m− 2 year− 1) in
the control (open squares and solid line) and warming treatment (black diamonds and dashed lines) and environmental
gradients (mean annual temperature, seasonal soil moisture and NO3-deposition respectively) across the sites over the first
3 years of manipulation. The indicated lines are simple best fitted lines.
N-mineralisation as well as the relatively small difference in
plant growth across the sites despite big differences in
ambient climatic conditions. On the other hand the lag of a
warming effect on total above-ground biomass production at
the warm Mediterranean ecosystem agrees with the expectation of these ecosystems being water limited with temperatures already close to the optimum for photosynthesis
(Larcher, 2000) and reinforce the expectation of greater
responses of plant production to warming in the colder
environments, which are often limited by temperature and
short growing season (van Cleve et al., 1991). The increased
plant growth by warming may be a direct effect of the small
constant temperature increase on top of the annual mean, a
reduction in the number of days with frost or an indirect
effect of the warming such as an extension of the growing
season.
4.2.
Soil carbon and nitrogen
The results from the first 3 years of the experiment showed
that warming caused an increase in soil respiration in
accordance with the general Q10 function for each site as
neither the response functions nor the Q10 for soil respiration
was affected by warming at any site and thereby no acclimation was observed. This is opposite to findings by other groups
who have demonstrated acclimation of soil respiration due to
limitation of the labile soil carbon pool (Melillo et al., 2002; Luo
et al., 2001) or stimulation of physico-chemical reactions
which transfer organic-C to more stable and, thus, unavailable
carbon pools (Thornley and Cannell, 2001). At the northern
sites the increased soil carbon loss may partly be a consequence of increased availability of labile carbon from
increased litter production since plant productivity was also
increased by warming, or it may be related to depletion of
existing soil carbon pools or both. However, over time both,
plant production and depletion of “old” soil carbon pools, should
stabilise at a new steady state and soil carbon loss should
acclimate, but this may clearly not happen instantaneously.
The limitation of key soil processes at extreme water
conditions across the sites is in agreement with findings
elsewhere (e.g. Savage and Davidson, 2001; Borken et al., 2006)
but could in this study potentially be a result of differences in
vegetation characteristics. However, it was previously
reported from the same sites how experimental drought
reduced N mineralization in accordance with the response
function across the sites indicating the importance of extreme
water conditions on N-mineralisation (Emmett et al., 2004).
The high variability in net N-mineralisation in response to
warming across the sites agrees with previous observations
across a range of ecosystems evaluated by metanalysis
(Rustad et al., 2001). The lag of direct connection between
temperature and nitrogen mineralization suggests that
changes in the nitrogen cycle appear to occur more slowly
and to have little direct influence on the carbon cycle. Further,
it suggests that the effect on the overall carbon balance on the
short term may be controlled by the direct influence of
temperature on soil respiration rather than the water controlled N mineralization. At sites being limited by excess or lag
of water, which often coincide with relatively cold and warm
sites respectively, the lack of response in N mineralization
may lead to progressive N limitation for plant and microbial
growth and therefore limit carbon sequestration. It may be
noted that in this study with temperature elevation of c. 1 °C
the treatment had no measurable effect on soil moisture but if
climate change leads to larger temperature elevations this
may also affect soil moisture and thereby lead to interaction
between temperature and moisture conditions which may
cause changes in water controlled processes like N mineralization. Clearly, elevated N deposition in many areas of
Europe may interact with climate change by reducing N
limitation to enhance N leaching and C sequestration. Therefore it may have to be considered when dealing with effects of
near future global warming on carbon sequestration in
terrestrial ecosystems.
In accordance with the expectations given by the natural
gradients, warming induced a temporary change in the
balance between the above-ground and below-ground carbon
processes, with plant production being more sensitive to
warming than soil C fluxes. This is in contrast to evidence
from other studies where soils have been found to have
greater sensitivity to warming than plant production (Agren
and Bosatta, 1996) and to model predictions with GCMs (Cox
et al., 2000) and DGVMs (Cramer et al., 2001) predicting a
reduction in the carbon sink strength of terrestrial ecosystems
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S CIE N CE OF T H E TOT AL E N V I RO N ME N T 4 0 7 ( 2 00 8 ) 6 9 2–6 97
as a consequence of elevated temperatures. On the other
hand, the small difference in plant production along the
climatic gradient suggests that the enhanced C fixation by
plants induced by warming during the 3 years experiment
may not be maintained in the long term. This may occur as a
consequence of progressive nutrient limitation (Luo et al.,
2004; Hungate et al., 2004), since our results do not indicate
any consistent increase in net N mineralisation to provide the
additional inorganic-N required for continued enhanced plant
growth.
The strong sensitivity and response of both plant production and soil respiration to warming within the first 3 years
suggests that changes in N deposition and N availability may
have to be accounted for in predictions of carbon sequestration by terrestrial ecosystems under future climatic conditions. Limitations in other nutrients such as phosphorus may
also become progressively important mechanisms controlling
acclimation in these areas (Peñuelas et al., 2004).
Acknowledgements
We thank all the people involved in the extensive activities of
running and maintaining the treatments and the measurements in the CLIMOOR and VULCAN projects. The work was
financially supported by EU (Contracts ENV4-CT97-0694 and
EVK2-CT-2000-00094) and the participating research institutes.
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