GLOBAL BIOGEOCHEMICAL CYCLES, VOL. 19, GB2003, doi:10.

1029/2004GB002264, 2005

Temperature independence of carbon dioxide supersaturation

in global lakes
Sebastian Sobek and Lars J. Tranvik
Limnology/Department of Ecology and Evolution, Uppsala University, Uppsala, Sweden

Jonathan J. Cole
Institute of Ecosystem Studies, Milbrook, New York, USA
Received 22 March 2004; revised 29 January 2005; accepted 18 February 2005; published 5 April 2005.

[1] A growing body of evidence suggests that most of the world’s lakes are
supersaturated with CO2 and export significant amounts of CO2 to the atmosphere. Still,
the temperature dependence of the partial pressure of CO2 (pCO2) in lakes, which is the
main driver of carbon flux across the air-water interface, has not yet been assessed.
Analyzing a global-scale database of 4902 lakes, we show that temperature is not an
important regulator of pCO2 in lakes. Instead, the concentration of dissolved organic
carbon (DOC), a substrate for microbial respiration, explains significant variation in lake
pCO2. Contrary to what may be expected from the physiological constraints of
temperature, effects of climate change on the carbon balance of lakes may not be due to
rising temperature per se, but rather to climatically induced changes in the export of DOC
from terrestrial soils to aquatic habitats.
Citation: Sobek, S., L. J. Tranvik, and J. J. Cole (2005), Temperature independence of carbon dioxide supersaturation in global lakes,
Global Biogeochem. Cycles, 19, GB2003, doi:10.1029/2004GB002264.

1. Introduction external inputs is less clear. Studies on the significance of

[2] The majority of the world’s lakes are supersaturated
in CO2 with respect to the atmosphere, resulting in an
export flux of CO2 from lakes to the atmosphere [Cole et
al., 1994]. The loss of CO2 from freshwater systems
constitutes a significant carbon flux in both tropical and
boreal forest areas, probably affecting the overall carbon
balance of these large biomes [Richey et al., 2002;
Algesten et al., 2004]. Even though lake sediments have
been recognized as globally significant carbon sinks [Dean
and Gorham, 1998], recent studies in temperate and boreal
lakes have shown that CO2 emission to the atmosphere
may often be an even greater carbon loss factor than
carbon burial in the sediments [Algesten et al., 2004;
Hanson et al., 2004; Kortelainen et al., 2004]. Accord-
ingly, the partial pressure of CO2 (pCO2) in lakes, which
is the main driver of carbon flux across the air-water
interface, has received considerable attention during recent
years.
[3] CO2 in freshwaters can be both produced within the
system and imported to the water body from its terrestrial
surroundings. CO2 derived from soil respiration or weath-
ering can be transported to lakes and rivers via groundwater
or surface water flows. For rivers and streams, these
external inputs of CO2 have been shown to be highly
important [Jones and Mulholland, 1998; Hope et al.,
2001; Jones et al., 2003], but for lakes, the importance of
Copyright 2005 by the American Geophysical Union.
0886-6236/05/2004GB002264
external CO2 inputs to the inorganic carbon budget of
lakes have arrived at different conclusions, both when
investigating surface water inflow [Jones et al., 2001;
Jonsson et al., 2001] and groundwater-mediated inflow of
CO2 [Kratz et al., 1997; Striegl and Michmerhuizen,
1998]. Thus, while external inputs of inorganic carbon
are probably the dominating source of CO2 in running
water, the partial pressure of CO2 (pCO2) in a lake is the
result of both external and internal processes [Kling et al.,
1991]. In fact, a large body of literature suggests that net
heterotrophy, i.e., the dominance of in-lake respiration
over in-lake primary production, is the main factor causing
the frequently observed supersaturation of CO2 in lakes [del
Giorgio et al., 1999; Cole et al., 2000; Jansson et al., 2000;
Jonsson et al., 2001; Prairie et al., 2002; Hanson et al.,
2003; Jonsson et al., 2003; Sobek et al., 2003; Hanson et
al., 2004]. The high extent of respiration in many lakes is
fueled by inputs of allochthonous dissolved organic carbon
(DOC), a heterogeneous mixture of heavily stained organic
molecules exported from terrestrial soils to lake waters.
Allochthonous DOC has been recognized as a major
modifier of lake ecosystem structure and function, both
serving as a substrate for microbial respiration [Tranvik,
1988], and impeding photosynthesis due to its effective
light absorption [Jones, 1998]. Thus, even though direct
inputs of CO2 from the terrestrial surroundings to lakes
may influence the pCO2 of lake water to a certain extent,
the balance of evidence suggests that lake CO2 is mainly a
result of internal metabolic processes. Hence the pCO2 of
lake water can be used as a proxy for the balance between

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GB2003 SOBEK ET AL.: CARBON DIOXIDE SUPERSATURATION IN GLOBAL LAKES
primary production (P) and respiration (R), and thus of net
ecosystem metabolism (P/R).
[4] The issue of temperature dependence of ecosystem
processes is crucial for predictions of the effects of climate
change. If temperature in itself were a major regulator of
ecosystem processes at a global scale, one could predict the
biosphere’s feedback to climate warming in a straightfor-
ward way. As the metabolism of organisms strongly
responds to changes in temperature, global-scale ecosystem
processes can be expected to be sensitive to temperature as
well. However, recent studies [Giardina and Ryan, 2000;
Valentini et al., 2000; Enquist et al., 2003] emphasize that
important biospheric processes such as soil or forest respi-
ration may not be regulated by temperature across large
latitudinal gradients. In fact, also the abundance and quality
of substrate might play a regulative role for ecosystem-scale
processes [e.g., Liski et al., 1999].
[5] Hence ‘‘while temperature is always a factor [. . .], it is
not always the only factor or even a dominant one.’’ This
quotation from Pomeroy and Wiebe [2001] refers to the
growth of marine bacterioplankton, but may be applicable
to other processes and ecosystems as well.
[6] The temperature dependence of the CO2 balance of
lakes has as yet only been investigated at a limited geo-
graphic scale. In a study on boreal lakes situated along a
5
C gradient of annual mean temperature, lake pCO2 was
independent of temperature [Sobek et al., 2003]. These
lakes represented a substantial north-south gradient within
the northern boreal zone, but it remained unclear to what
extent temperature controls the net ecosystem metabolism
of lakes at the global scale. Hence we collected for this
analysis pCO2 data from globally distributed lakes.
2. Methods
2.1. Data Collection
[7] We collected 12,898 pCO2 data points from 4902
globally distributed natural lakes from the literature, unpub-
lished data, and internet resources (Table 1). Reservoirs
were not included in the study, as carbon cycling in
reservoirs may be affected by the type of flooded soils
and the age of the reservoir [Bergström et al., 2004]. For
literature searches, we used the ASFA and ISI Science
citation index databases. Unpublished data cover mainly
high-arctic and tropical areas and were acquired via per-
sonal communication. Data from the year 2000 Swedish
national lake monitoring were acquired from a freely
available database (Swedish National Lake Monitoring,
2000, data available on-line (http://info1.ma.slu.se/ri/
www_ri.acgi$Project?ID=2000KS) from the Department
of Environmental Assessment, Swedish University of
Agricultural Sciences, Ultuna, Sweden). All data are
derived from surface water samples; that is, water was
sampled within the 0 – 1 m depth interval. As direct
measurements of pCO2 are comparatively rare, we also
collected measurements of alkalinity and/or dissolved
inorganic carbon (DIC), pH, and water temperature, which
were used to calculate pCO2 according to Stumm and
Morgan [1996] and Weiss [1974]. We also recorded
altitude, month of sampling, and dissolved organic carbon
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(DOC) concentration, as all these factors may influence
lake pCO2 [e.g., Sobek et al., 2003]. In cases where total
organic carbon (TOC) was measured, it was converted to
DOC by multiplying with 0.9 [Wetzel, 2001]. Saline lakes
(conductivity > 600 mS cm 1) were excluded because the
calculation of pCO2 in these lakes requires more back-
ground data. If a lake was temporarily ice covered, only
data from the ice-free period were included, as the ice
cover leads to the accumulation of CO2 in the lake water.
Permanently ice-covered lakes were excluded for the same
reason. Two-hundred-twenty-seven lakes were sampled
several or many times. For each of these lakes, pCO2
was calculated for each sampling occasion separately, and
mean values of pCO2, DOC, pH, and conductivity were
entered into the database.
[8] In order to investigate the influence of climate and
soil character on lake pCO2, the lake data set was
expanded with data from global-scale databases, which
all are available on the internet. Mean annual air temper-
ature and mean annual precipitation were acquired from a
global climate database [New et al., 2000]. Mean annual
runoff was taken from B. M. Fekete et al. (UNH/GRDC
composite runoff fields V 1.0, Global Runoff Data Centre
(GRDC) (available at http://www.grdc.sr.unh.edu/)), and
soil carbon concentration was taken from the Global Soil
Data Task Group [2000] database.
2.2. Statistical Analyses
[9] Correlation analysis between variables of the data set
was conducted by means of linear regression. Variables with
skewed distributions were log-transformed in order to
approach normality. In order to account for different sam-
pling frequencies of individual lakes, we assigned the
number of measurements at each lake as weights in linear
regression analyses. The outcome of both weighted and
unweighted linear regressions is described in section 3.
[10] Along with the univariate linear regressions, we also
performed multivariate data analysis. We used partial least
squares regression (PLS) [e.g. Höskuldsson, 1988; Eriksson
et al., 2001] in order to find out how different variables
perform as predictors of lake pCO2. The most important
advantages of PLS compared to ordinary multiple regres-
sion are that PLS is insensitive against dependence of
X variables on each other (co-correlation), and that the data
need not be normally distributed. Also, the PLS algorithm
is very tolerant to missing values. A PLS regression
extracts for each of the X variables the degree of explana-
tion of the Y variable (i.e., pCO2), and shows the results in
a two-dimensional scatterplot. In this way, a complex
multidimensional data matrix can be dissected and shown
in one simple graph. More precisely, PLS regressions place
uncorrelated latent components (axes) into the X data space
in order to maximally explain the variance in the Y data.
Thereby, PLS uses the variance in the X data to explain the
variance in the Y data. The results of a PLS analysis are
explored in a series of plots, one of which is the ‘‘loadings
plot,’’ depicting the importance of the different X-variables
in explaining the Y-variable. The first component of a PLS
(horizontal axis in a loadings plot) always explains more
of the variance than the second component (vertical axis),
GB2003 SOBEK ET AL.: CARBON DIOXIDE SUPERSATURATION IN GLOBAL LAKES GB2003

Table 1. Sources of Data for the Present Study

Number Number of
Data Source Geographical Region Lake of Lakes Measurements
I. Ahlgren, unpublished data, 1990, 1997, 1998 Nicaragua Cocibolca 1 7
Anderson et al. [1999] Minnesota, United States Williams 1 27
Ball and Glucksmann [1980] Papua New-Guinea Dakataua 1 2
Berman-Frank et al. [1994] Israel Kinneret 1 27
S. Bertilsson, unpublished data, 1999 Canadian tundra 53 53
Carignan [1998] Canada Croche 1 42
Cole and Caraco [1998] New Hampshire, United States Mirror 1 208
Cole et al. [1994] global 1676 3454
Coyne and Kelley [1974] Alaska, United States 2 2563
del Giorgio et al. [1999] Quebec, Canada 9 45
Gelbrecht et al. [1998] Germany 8 8
Hesslein et al. [1991] ELA, Canada Lake 239 1 23
Alaska, Canada 5 105
Hope et al. [1996] Wisconsin, United States 20 20
Jones et al. [2001] Great Britain Loch Ness 1 12
Karlsson [2001] Sweden 51 51
Kelly et al. [2001] ELA, Canada 3 924
NOLSS, Canada 6 294
Ontario, Canada Nipigon 1 13
Kling et al. [1992] Alaska 25 136
Kortelainen et al. [2000] Finland 12 12
Kratz et al. [1997] Wisconsin, United States 8 104
Weiler [1975]; Leggett et al. [1999] Canada Ontario 1 27
P. Lehmusluoto, unpublished data, 1992 – 1993 Indonesia 18 27
E. Lindström, unpublished data, 1997 Svalbard 4 4
Löffler [1968] Kenya 34 34
Löffler [1978] Ethiopia 3 3
Maberly [1996] Great Britain Esthwaite 1 1275
Maehl [1982] Greenland Lake 95 1 6
Milbrink [1977] Kenya Naivasha 1 5
Miyajima et al. [1997] Japan Biwa 1 2
Mizandrontseva and Mizandrontseva [1994] Russia Baikal 1 96
Murugavel and Pandian [2000] India Azhakia 1 72
Pedrosa and Rezende [2000] Brazil Cima 1 3
Prairie et al. [2002] Quebec, Canada 32 128
Qadri and Yousuf [1978] India Manasbal 1 35
Quay et al. [1986] Washington, United States Washington 1 13
Rai and Hill [1981] Brazil Tupé 1 12
Ramlal et al. [1994] Alaska, United States Lake 18 1 6
Swedish National Lake Monitoring (2000, data available online) Sweden 2851 2851
Sharma and Pant [1987] India Bhimtal 1 10
Sobek et al. [2003] Sweden 33 88
Striegl and Michmerhuizen [1998] Minnesota, United States Shingobee 1 13
Talling and Talling [1965] East Africa 14 28
Weiler [1975] United States Erie 1 10
Vyverman [1994] Papua New-Guinea 10 10
Zinabu [2002] Ethiopia Zwai 1 10
Total 4902 12,898

and is therefore of higher importance when interpreting the
loadings plot. The correlation structure of the data set is
shown in the spatial distribution of variables in the plot
area. Variables are positively correlated when situated
close to each other, while they are negatively correlated
if they are placed at opposite ends of the plot. Variables in
the center of the plot are at most poorly related to the
variables at the outer ends of the plot area.
[11] The performance of a PLS model is expressed in the
terms R2Y and Q2. R2Y is comparable to R2 in linear
regression and expresses how much of the variance in Y
is explained by the X variables. Q2 is a measure of the
predictive power of the PLS model. The closer Q2 to R2Y,
the better and more robust is the model. Calculated models
were validated using a permutation test, which results in a
measure of the intrinsic ‘‘background correlation’’ of the
data, i.e., a baseline in the coefficients R2Y and Q2 that is
not indicative for any correlations between parameters but
only due to chance. The lower this background correlation,
the better and more stable the model. Highly skewed
variables (skewness > 2.0 and min/max-ratio < 0.1) were
log-transformed prior to modeling in order to increase
model performance. All PLS modeling was done on the
SIMCA-P 9.0 software (Umetrics AB, Umeå, Sweden).
3. Results and Discussion
3.1. Global Lake pCO2
[12] The data set presented in this study is the so far
largest collection of pCO2 in lakes, covering essentially all
major climatic zones (Figure 1 and Table 1). Most of the
lakes are situated in the northern temperate zone, in part

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GB2003 SOBEK ET AL.: CARBON DIOXIDE SUPERSATURATION IN GLOBAL LAKES
Figure 1. Histogram of the global distribution of lakes
included in the data set (total n = 4902). The number of
lakes in each latitude class is plotted. Note scale break. See
color version of this figure in the HTML
reflecting the global distribution of lakes. Mean pCO2 for all
4902 lakes was 1287 ± 41 microatmospheres (matm; ±95%
confidence interval), ranging between 17 and 65,250 matm.
Figure 2 shows the distribution of pCO2 in lakes of different
climatic regions. For all climatic regions, the distribution of
pCO2 is tailed toward higher values. An ANOVA of log
pCO2 between different climatic regions, combined with a
post-hoc test (Tukey HSD for unequal N), reveals that pCO2
is significantly lower in Arctic lakes compared with lakes
from all other climatic regions (p < 0.0001). There are
significant differences (p < 0.05) in pCO2 between lakes
from some of the other climatic regions; however, as
evident from Figure 2, these differences do not follow any
latitudinal pattern. Ninety-three percent of the lakes were
supersaturated in CO2 with respect to the atmosphere. This
corroborates the earlier finding by Cole et al. [1994] that
most of the world’s lakes are sources of CO2 to the
atmosphere.
3.2. Role of Lake pCO2 in Gas Flux Across the
Air-Water Interface
[13] The flux of CO2 across the air-water interface is
driven by the gradient in gas concentration between the air
and the surface water, and regulated by the gas exchange
velocity k. Hence the pCO2 of the lake surface water is not a
measure of carbon flux per se. However, lake pCO2 is the
most important term in the flux equation. On one hand, lake
pCO2 varies over several orders of magnitude, and is often
well above atmospheric pCO2 (Figure 2). Atmospheric
pCO2 is also subject to seasonal and diurnal variation, but
to a much lesser extent. Lake pCO2 is therefore the main
factor in determining the magnitude and direction of the gas
gradient. The other term in gas flux across the air-water
interface, the gas exchange velocity k, is rather well con-
strained in lakes. It is very rarely lower than 0.3 m d 1,
rarely higher than 1 m d 1 except in the largest lakes, and is
often about 0.5 m d 1 [Cole and Caraco, 1998]. Thus, even
though lake pCO2 is not to a metric of CO2 flux, it is the
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main driver of CO2 exchange between lakes and the
atmosphere. It is therefore likely that the general patterns
of regulation of pCO2 in lakes presented in this paper to a
large extent are applicable to CO2 flux between lakes and
the atmosphere.
3.3. Regulation of pCO2 in Lakes
[14] We found that the concentration of dissolved organic
carbon (DOC) is a much better predictor of pCO2 in lakes
than is temperature. This is evident from both linear
regression analysis (Figures 3 – 5, as well as from PLS
regression analysis (Figure 6). Linear regression shows that
annual mean air temperature (Figure 3) and in situ water
temperature at the time of sampling (Figure 4) explain only
a trivial proportion of the total variance in pCO2 (R2 = 0.06
and 0.003, respectively), even though the regression slopes
are highly significant (p < 0.001). On the other hand, linear
regression of log pCO2 against log DOC is highly signif-
icant and explains 26% of the variation in log pCO2 (p <
0.0001; n = 4556; Figure 5). As evident from Figure 5, the
relationship between log pCO2 and DOC is different for the
lakes with several measurements (log pCO2 = 1.98 + 1.04 
log DOC; R2 = 0.37; n = 93), as compared to the lakes that
were measured only once. However, the lakes with several
measurements of both pCO2 and DOC are not distributed
globally, but restricted to the temperate and boreal zone.
The carbon metabolism of such lakes was investigated in
detail elsewhere [Hope et al., 1996; Hanson et al., 2003;
Sobek et al., 2003] and will therefore not be discussed in
this paper.
[15] In order to account for different sampling frequencies
of individual lakes, we assigned the number of measure-
ments at each lake as weights in linear regression analyses.
This procedure renders significantly different slopes (test on
Figure 2. Distribution of pCO2 in different climatic
regions, as defined by latitude (Arctic: >56
; cold
temperate: 48
– 56
; temperate: 40
– 48
; warm temperate:
34
– 40
; subtropical: 20
– 34
; tropical: 0
– 20
). The
points depict the median, the boxes show the quartiles, and
the whiskers mark the 10% and 90% percentiles. The
number of lakes in each climatic region is shown. See color
version of this figure in the HTML.
GB2003 SOBEK ET AL.: CARBON DIOXIDE SUPERSATURATION IN GLOBAL LAKES GB2003

Figure 3. Plot of log pCO2 against annual mean air temperature. Each point in the plot represents one
individual lake. Circles: lakes with a single measurement. Triangles, mean values for lakes with multiple
measurements. Solid line, linear regression for all data points in plot (y = 2.95 + 0.012  x; R2 = 0.06;
p < 0.0001; n = 4902). See color version of this figure in the HTML.

homogeneity of slopes in an ANCOVA model, p < 0.001)
compared to the unweighted regressions between log pCO2
and annual mean air temperature (weighted linear fit: y =
2.87 + 0.009  x; p < 0.0001). Weighting also increased
degrees of explanation to R2 = 0.08. Contrarily, the slope
between log pCO2 and log DOC was not significantly
changed by weighting (p = 0.64), and the regression R2
decreased from 0.26 to 0.21 (weighted linear fit: y = 2.61 +
0.421  x; R2 = 0.21; p < 0.0001). Weighting rendered
minor changes, even though using the number of measure-
ments as weights overestimates the importance of repeated
sampling. Therefore, text and figures present only the
unweighted regressions.
[16] The PLS regression analysis confirms that the con-
centration of DOC is a much better predictor of pCO2 than
any other parameter in the data set. This is illustrated in the
PLS loadings plot (Figure 6) by DOC being situated at the
far end of the same directional axis as pCO2. Table 2 gives
an overview of all variables that were included in the PLS.
The PLS model extracted three components from the data

Figure 4. Plot of log pCO2 against in situ water temperature at time of sampling for lakes with a single
measurement. Each point in the plot represents one individual lake. Solid line, linear regression for all
data points in plot (y = 2.96 + 0.004  x; R2 = 0.003; p < 0.001; n = 4605). See color version of this
figure in the HTML.

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Figure 5. Plot of log pCO2 against log DOC for 4555 globally distributed lakes with DOC data
available. Each point in the plot represents one individual lake. Circles, lakes with a single measurement.
Triangles, mean values for lakes with multiple measurements. Solid line, linear regression for all data
points in plot (y = 2.67 + 0.414  x; R2 = 0.26; p < 0.0001). See color version of this figure in the
HTML.

set, collectively explaining 26% of the variation in pCO2
(R2Y = 0.26). The first component (horizontal axis in
Figure 6) explained 17.6% of the variation in pCO2, while
the second component (vertical axis in Figure 6) explained
5.8%. The third component contributed with only 2.9% to
the total explanatory power of the PLS model, and is not
shown in the graph for reasons of clarity. Model predict-
ability was high (Q2 = 0.23), and background correlation
was low (0.87% of R2Y). The variables that are situated on
a moderate distance from the center of the PLS loadings plot
(Figure 6) are moderately important in explaining the
variability in pCO2. These variables are conductivity, annual
mean air temperature, autumn and longitude, which are
positively related to pCO2, and summer and pH, which are
negatively related to pCO2. Annual precipitation and the
method of determining pCO2 are moderately important on

Figure 6. Loadings plot of the PLS regression analysis. The graph depicts the correlation structures
between the X variables and pCO2; variables situated along the same directional axis correlate positively
with each other; variables situated at opposite ends of the plot correlate negatively with each other. For
explanation of variables, see Table 2. See color version of this figure in the HTML.

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Table 2. Variables Used in the PLS Analysis
Variable in PLS
pCO2
Spring, Summer, Autumn,
Open, Year, Several years
Method
Temp_W
pH
Latitude and Longitude
Altitude
Conductivity
DOC
N number of measurements of pCO2
Temp
Prec
Runoff
Soil_C
Runoff X Soil_C
the second (vertical) component, which is attributed less
explanatory power. Hence these variables explain very little
of the variability in lake pCO2. Runoff, soil carbon concen-
tration, runoff X soil carbon concentration, latitude, altitude,
number of measurements, and water temperature are situat-
ed close to the center of the plot, and therefore do not make
any substantial contribution to the model.
[17] Both autochthonous and allochthonous DOC are
important substrates for aquatic heterotrophic bacteria
[Azam et al., 1983; Tranvik, 1988]. Numerous studies have
shown that allochthonous DOC fuels net heterotrophy in
lakes, leading to CO2 supersaturation and CO2 emission
[del Giorgio et al., 1999; Cole et al., 2000; Jansson et al.,
2000; Jonsson et al., 2001; Prairie et al., 2002; Hanson et
al., 2003; Jonsson et al., 2003; Sobek et al., 2003; Hanson
et al., 2004]. The positive relationship between DOC and
pCO2 (Figure 5) and the high frequency of supersaturation
in CO2 in lakes (93%) reported in this study substantiate
the concept that lakes are primarily net heterotrophic
ecosystems.
[18] Among the variables that are moderately important in
explaining pCO2, conductivity and pH are connected to the
DOC concentration, as a large proportion of the allochtho-
nous DOC in lakes usually consists of organic acids. The
importance of longitude is probably an artifact, because
many high-pCO2 boreal and tropical lakes in our data set are
situated east of Greenwich (positive longitude), while most
low-pCO2 arctic lakes in our data set are found west of
Greenwich (negative longitude). The moderate negative
influence of summer, as well as the moderate positive
influence of autumn, illustrate the seasonal variation of
pCO2 observed in many lakes [Kelly et al., 2001]. Abundant
light during summer triggers photosynthesis by phytoplank-
ton and benthic algae, leading to a drawdown of pCO2 in
lakes. In autumn, on the contrary, less light limits photo-
synthesis; thus pCO2 is often higher than in summer.
[19] Interestingly, neither soil carbon concentration nor
annual runoff explained a significant proportion of the
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Description
partial pressure of CO2 in surface water (matm); Y variable in PLS
season of sampling for nontropical lakes; ‘‘Open’’ describes lakes
that were sampled several times during the open-water period;
‘‘Year’’ means lakes that were sampled during one annual cycle,
‘‘Several years’’ means lakes that were sampled during several
annual cycles
method for determining pCO2; either measurement after headspace
equilibration, or calculation from pH and inorganic carbon
concentration
water temperature in the surface water (
C)
pH in the surface water
geographical position of the lake
altitude (m above sea level)
electrical conductivity in surface water (mS cm 1)
concentration of dissolved organic carbon in surface water (mg L 1)
annual mean air temperature (
C) from New et al. [2000]
annual precipitation (mm) from New et al. [2000]
annual runoff (mm) from Fekete et al. (2000)
soil carbon concentration (kg m 2) from Global Soil Data Task
Group [2000]
interaction term of Annual runoff and Soil carbon concentration
variation in lake pCO2. The soil carbon concentration was
previously shown to be coupled to the pCO2 of streams
[Hope et al., 2001], owing to the import of CO2 derived
from soil respiration to streams. Our results indicate that the
direct coupling between soil carbon concentration, soil
respiration, and pCO2 in lakes may be weak. In lakes,
contrarily to running waters, water retention time is long,
and internal metabolic processes may therefore be more
important than direct imports of CO2 from the surrounding
soils. On the other hand, Sobek et al. [2003] demonstrated
an indirect link between soil carbon and pCO2 in boreal
lakes, via the export of DOC from carbon-rich wetlands and
the subsequent in-lake mineralization of DOC to CO2.
Possibly, when analyzing a data set stretching over several
climatic zones, it may not be the amount of carbon in the
soil that affects lake pCO2, but rather the transport of
bioavailable carbon from soils to surface waters. Therefore
factors describing the generation and transformation of soil
organic carbon, as well as the export of different fractions of
DOC to surface waters, may be better predictors of lake
pCO2. The fact that runoff was not found to be an important
predictor of lake pCO2 may be attributable to similar
reasons. While the amount of water transported downstream
was no significant predictor of lake pCO2, downstream
transport of different carbon fractions might explain some
additional variation in lake pCO2. However, there were no
data with global resolution available to address these
questions.
3.4. Additional Sources of Variability in Lake pCO2
[20] None of the parameters included in our analysis
explained more than a moderate proportion of the variation
in pCO2, neither as single factors, nor as a combination of
factors. Both univariate (linear regression) and multivariate
(PLS regression) data analysis did not render a degree of
explanation higher than 26%. Differences in methods for
measuring and/or calculating pCO2 are unlikely to represent
a major source of variation. First, the largest proportion of
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the data (4377 lakes) originates from national lake surveys,
which use standardized methods and accredited laboratories
for physicochemical water analyses. Second, it has previ-
ously been shown that calculated pCO2 values agree well
with directly measured pCO2 data [Cole et al., 1994; Hope
et al., 1996]. Third, the variable ‘‘method’’ (i.e., calculated
or directly measured pCO2) included in the PLS analysis did
not contribute any substantial explanatory power (Figure 6).
On the other hand, previous studies have shown that both
diurnal and seasonal variations in pCO2 can be substantial
[Carignan, 1998; Kelly et al., 2001]. The importance of
seasonal variation is shown, and to a certain degree
accounted for, in the PLS analysis (Figure 6), whereas
diurnal variation is not included in the data analysis owing
to lack of data. This implies that a considerable share of the
unexplained variability in pCO2 can probably be attributed
to temporal variation in lake pCO2.
[21] The largest source of variability is probably the very
high diversity of lake ecosystems in terms of geographical,
geological, and hydrological setting, basin shape, chemical
composition of the lake water, and biological communities,
which is largely unaccounted for by the variables in our data
set. Several variables would have been desirable to include
in the data set, but often such data were only available for a
limited number of lakes in a restricted climatic zone owing
to incomplete reporting in the literature. Such variables are
the hydrological type of the lake (seepage or drainage),
which influences the importance of groundwater-mediated
import of CO2, the depth and volume of the lake, which are
connected to the effects of water retention time and sedi-
ment metabolism on lake carbon cycling [Curtis, 1998; den
Heyer and Kalff, 1998], and the size and character of the
catchment, which strongly affect carbon cycling in lakes
[Sobek et al., 2003]. The influence of lake surface area on
lake pCO2 could be tested for a subset of globally distrib-
uted lakes (n = 3459); however, the degree of explanation
was very low (log pCO2 = 3.02 + 3  10 6  log lake area;
R2 = 0.0003).
[22] Despite this great variability inherent in the world’s
lakes, DOC as a single factor explained 26% of the variation
in pCO2 (Figure 4). The DOC pool in lakes consists of both
autochthonous and allochthonous carbon, but frequently a
large proportion of the DOC in lakes originates from
terrestrial vegetation in the lake catchment [Rasmussen et
al., 1989; Hessen and Tranvik, 1998]. Studies in geograph-
ically limited areas have previously indicated that in-lake
mineralization of allochthonous DOC by aquatic heterotro-
phic microbes may lead to net heterotrophic ecosystem
metabolism and consequently to CO2 supersaturation in
lakes [Hope et al., 1996; Sobek et al., 2003]. This study
provides evidence that in spite of the great diversity of the
world’s lakes, DOC imported from the catchment area is a
globally important modifier of lake ecosystem metabolism.
3.5. Temperature and Substrate as Interacting
Regulators
[23] Temperature is a key regulator of the physiology of
cells and organisms. This control is often manifested at
higher levels of organization as well. In aquatic systems,
several aggregate features of the planktonic community
8 of 10
GB2003
such as respiration, primary production, bacterial produc-
tion, and growth have been reported to be temperature-
dependent [White et al., 1991; Rivkin and Legendre, 2001;
Hoppe et al., 2002]. Studies on soil respiration point toward
a strong temperature regulation [Raich and Schlesinger,
1992; Updegraff et al., 2001; Risk et al., 2002], and the
carbon balance within a boreal forest is reported to be
strongly controlled by temperature [Lindroth et al., 1998].
Hence there is an unambiguous temperature dependence of
many ecosystem-level processes in a wide range of ecosys-
tems. The lack of a global-scale temperature effect on lake
pCO2 in spite of many well-known temperature dependen-
cies of aquatic organisms and processes is surprising. A
similar paradox was recently shown for terrestrial ecosys-
tems by Enquist et al. [2003]. Similar cases of a lacking
temperature effect along a large spatial gradient were
demonstrated by Giardina and Ryan [2000] and Valentini
et al. [2000] for soils and forest ecosystems. The concept of
substrate and temperature as interacting regulators [Pomeroy
and Wiebe, 2001] might be helpful to understand the
paradox of local (i.e., temporal) but not global (i.e., large-
scale spatial) temperature regulation. The temperature sen-
sitivity of a process depends on substrate supply [Pomeroy
and Wiebe, 2001]. The temporal variation of substrate
supply at a certain location is likely to be much smaller
than the variation of substrate supply across a large spatial
gradient. Hence, at a local scale, we might expect a
comparatively higher potential for a detectable temperature
effect on ecosystem processes. We suggest that even though
temperature is likely to be a more important regulator at a
local scale than across a large spatial gradient, the interplay
between temperature and substrate is the main regulatory
mechanism of net ecosystem metabolism. This concept may
resolve conflicting results of apparently comparable studies
(e.g., the regulation of global soil respiration by Raich and
Schlesinger [1992] and Giardina and Ryan [2000]), since
contrasting results may be explained by differences in
temperature gradient and/or substrate supply. As both
temperature and substrate supply vary in both time and
space, the result of their interplay will be difficult to
predict. Also, the term ‘‘substrate supply’’ comprises both
quantitative and qualitative aspects, and is therefore
connected to both a multitude of ecosystem processes
and anthropogenic modifications (e.g., changes in hydrol-
ogy or land use). Hence, global-scale regulation of eco-
system processes should not be predicted from spatially
limited studies, but needs to be empirically assessed at a
global scale. In other words, global extrapolation of either
single factor effects (e.g., temperature), or of results from
local studies, is an intrinsically questionable approach for
the analysis of climate change effects.
4. Conclusions
[24] We found that temperature explains only a trivial
proportion of the variation in lake pCO2, while the concen-
tration of DOC is a significant regulator of lake pCO2 at a
global scale. The absence of a direct relationship between
temperature and lake pCO2 indicates that the metabolic
balance of lakes is not under strong, direct control by
GB2003 SOBEK ET AL.: CARBON DIOXIDE SUPERSATURATION IN GLOBAL LAKES
temperature. This is an intriguing result since both primary
production and, more strongly, respiration, do show rela-
tionships to temperature in the laboratory [Wetzel, 2001] and
over seasonal cycles [Takahashi et al., 1995; Sommaruga
and Conde, 1997]. Environmental change affects whole
ecosystems, where rate processes have multiple and indirect
controls. The relationship between DOC and pCO2 in global
lakes indicates that it is likely that the indirect effects of
climate warming, such as changes in terrestrial vegetation
and catchment hydrology, will be the dominant factors
regulating the net ecosystem metabolism of lakes.
[25] Acknowledgments. We thank Pasi Lehmusluoto for data on
Indonesian lakes acquired by Expedition Indodanau, Eva Lindström for
data on Svalbard lakes, and Stefan Bertilsson for data from lakes in the
Canadian Arctic acquired during the Swedish Tundra Northwest Expedi-
tion. Zinabu Gebre-Mariam and Ingemar Ahlgren provided both data and
help to find data from tropical lakes. The Swedish Research Council for
Environment, Agricultural Sciences and Spatial Planning, the Swedish
Research Council, and the National Center for Ecological Assessment
and Synthesis provided financial support.
References
Algesten, G., S. Sobek, A.-K. Bergström, A. Ågren, L. J. Tranvik, and
M. Jansson (2004), Role of lakes for organic carbon cycling in the boreal
zone, Global Change Biol., 10, 141 – 147.
Anderson, D. E., R. G. Striegl, D. I. Stannard, C. M. Michmerhuizen, T. A.
McConnaughey, and J. W. LaBaugh (1999), Estimating lake-atmosphere
CO2 exchange, Limnol. Oceanogr., 44(4), 988 – 1001.
Azam, F., T. Fenchel, J. G. Field, J. S. Gray, L. A. Meyer-Reil, and
F. Thingstad (1983), The ecological role of water-column microbes in
the sea, Mar. Ecol. Prog. Ser., 10, 257 – 263.
Ball, E., and J. Glucksmann (1980), A limnological survey of Lake
Dakataua, a large caldera lake on West New Britain, Papua New
Guinea, with comparisons to Lake Wisdom, a younger nearby caldera
lake, Freshwater Biol., 10, 73 – 84.
Bergström, A.-K., G. Algesten, S. Sobek, L. J. Tranvik, and M. Jansson
(2004), Emission of CO2 from hydroelectric reservoirs in northern
Sweden, Arch. Hydrobiol., 159(1), 25 – 42.
Berman-Frank, I., T. Zohary, J. Erez, and Z. Dubinsky (1994), CO2 avail-
ability, carbonic anhydrase, and the annual dinoflagellate bloom in Lake
Kinneret, Limnol. Oceanogr., 39(8), 1822 – 1834.
Carignan, R. (1998), Automated determination of carbon dioxide, oxygen
and nitrogen partial pressures in surface waters, Limnol. Oceanogr.,
43(5), 969 – 975.
Cole, J. J., and N. F. Caraco (1998), Atmospheric exchange of carbon
dioxide in a low-wind oligotrophic lake measured by the addition of
SF6, Limnol. Oceanogr., 43(3), 647 – 656.
Cole, J. J., N. F. Caraco, G. W. Kling, and T. K. Kratz (1994), Carbon
dioxide supersaturation in the surface waters of lakes, Science, 265,
1568 – 1570.
Cole, J. J., M. L. Pace, S. R. Carpenter, and J. F. Kitchell (2000), Persis-
tence of net heterotrophy in lakes during nutrient addition and food web
manipulations, Limnol. Oceanogr., 45(8), 1718 – 1730.
Coyne, P. I., and J. J. Kelley (1974), Carbon dioxide partial pressures in
arctic surface waters, Limnol. Oceanogr., 19(6), 928 – 938.
Curtis, P. J. (1998), Climatic and hydrologic control of DOM concentration
and quality in lakes, in Aquatic Humic Substances, edited by D. O.
Hessen and L. J. Tranvik, pp. 93 – 104, Springer, New York.
Dean, W. E., and E. Gorham (1998), Magnitude and significance of carbon
burial in lakes, reservoirs, and peatlands, Geology, 26(6), 535 – 538.
del Giorgio, P. A., J. J. Cole, N. F. Caraco, and R. H. Peters (1999), Linking
planktonic biomass and metabolism to net gas fluxes in northern temper-
ate lakes, Ecology, 80(4), 1422 – 1431.
den Heyer, C., and J. Kalff (1998), Organic matter mineralization rates in
sediments: A within- and among-lake study, Limnol. Oceanogr., 43(4),
695 – 705.
Enquist, B. J., E. P. Economo, T. E. Huxman, A. P. Allen, D. Ignace, and
J. F. Gillooly (2003), Scaling metabolism from organisms to ecosys-
tems, Nature, 423, 639 – 642.
Eriksson, L., E. Johansson, N. Kettaneh-Wold, and S. Wold (2001), Multi-
and Megavariate Data Analysis: Principles and Applications, Umetrics
AB, Umeå, Sweden.
9 of 10
GB2003
Gelbrecht, J., M. Fait, M. Dittrich, and C. Steinberg (1998), Use of GC and
equilibrium calculations of CO2 saturation index to indicate whether
freshwater bodies in north-east Germany are net sources or sinks for
atmospheric CO2, Fresenius J. Anal. Chem., 361, 47 – 53.
Giardina, C. P., and M. G. Ryan (2000), Evidence that decomposition rates
of organic carbon in mineral soil do not vary with temperature, Nature,
404, 858 – 861.
Global Soil Data Task Group (2000), Global gridded surfaces of selected
soil characteristics (IGBP-DIS), data set, Oak Ridge Natl. Lab. Distrib.
Active Arch. Cent., Oak Ridge, Tenn. (Available at http://www.
daac.ornl.gov)
Hanson, P. C., D. L. Bade, S. R. Carpenter, and T. K. Kratz (2003), Lake
metabolism: Relationships with dissolved organic carbon and phos-
phorus, Limnol. Oceanogr., 48(3), 1112 – 1119.
Hanson, P. C., A. I. Pollard, D. L. Bade, K. Predick, S. R. Carpenter, and
J. A. Foley (2004), A model of carbon evasion and sedimentation in
temperate lakes, Global Change Biol., 10, 1285 – 1298.
Hessen, D. O., and L. J. Tranvik (1998), Aquatic Humic Substances:
Ecology and Biogeochemistry, Ecol. Stud., vol. 133, Springer, New
York.
Hesslein, R. H., J. W. M. Rudd, C. A. Kelly, P. Ramlal, and K. A. Hallard
(1991), Carbon dioxide pressure in surface waters of Canadian lakes, in
Air-Water Mass Transfer, edited by S. C. Wilhelms and J. S. Gulliver,
pp. 413 – 431, Am. Soc. of Civ. Eng., New York.
Hope, D., T. K. Kratz, and J. L. Riera (1996), Relationship between PCO2
and dissolved organic carbon in northern Wisconsin lakes, J. Environ.
Qual., 25, 1442 – 1445.
Hope, D., S. M. Palmer, M. F. Billett, and J. J. C. Dawson (2001), Carbon
dioxide and methane evasion from a temperate peatland stream, Limnol.
Oceanogr., 46(4), 847 – 857.
Hoppe, H.-G., K. Gocke, R. Koppe, and C. Begler (2002), Bacterial growth
and primary production along a north-south transect of the Atlantic
Ocean, Nature, 416, 168 – 171.
Höskuldsson, A. (1988), PLS regression methods, J. Chemometr., 2, 211 –
228.
Jansson, M., A.-K. Bergström, P. Blomqvist, and S. Drakare (2000),
Allochthonous organic carbon and phytoplankton/bacterioplankton
production relationships in lakes, Ecology, 81(11), 3250 – 3255.
Jones, J. B. J., and P. J. Mulholland (1998), Influence of drainage basin
topography and elevation on carbon dioxide and methane supersaturation
of stream water, Biogeochemistry, 40, 57 – 72.
Jones, J. B., E. H. Stanley, and P. J. Mulholland (2003), Long-term
decline in carbon dioxide supersaturation in rivers across the contiguous
United States, Geophys. Res. Lett., 30(10), 1495, doi:10.1029/
2003GL017056.
Jones, R. I. (1998), Phytoplankton, primary production and nutrient cycling,
in Aquatic Humic Substances: Ecology and Biogeochemistry, edited by
D. O. Hessen and L. J. Tranvik, pp. 145 – 195, Springer, New York.
Jones, R. I., J. Grey, C. Quarmby, and D. Sleep (2001), Sources and fluxes
of inorganic carbon in a deep, oligotrophic lake (Loch Ness, Scotland),
Global Biogeochem. Cycles, 15(4), 863 – 870.
Jonsson, A., M. Meili, A.-K. Bergström, and M. Jansson (2001), Whole-
lake mineralization of allochthonous and autochthonous organic carbon
in a large humic lake (Örträsket, N. Sweden), Limnol. Oceanogr., 46(7),
1691 – 1700.
Jonsson, A., J. Karlsson, and M. Jansson (2003), Sources of carbon dioxide
in clearwater and humic lakes in Northern Sweden, Ecosystems, 6, 224 –
235.
Karlsson, J. (2001), Pelagic energy mobilization and carbon dioxide
balance in subarctic lakes in northern Sweden, Ph.D. thesis, Umeå
Univ., Umeå, Sweden.
Kelly, C. A., E. Fee, P. S. Ramlal, J. W. M. Rudd, R. H. Hesslein,
C. Anema, and E. U. Schindler (2001), Natural variability of carbon
dioxide and net epilimnetic production in the surface waters of boreal
lakes of different sizes, Limnol. Oceanogr., 46(5), 1054 – 1064.
Kling, G. W., G. W. Kipphut, and M. C. Miller (1991), Arctic lakes and
streams as gas conduits to the atmosphere: Implications for tundra carbon
budgets, Science, 251, 298 – 301.
Kling, G. W., G. W. Kipphut, and M. C. Miller (1992), The flux of
CO2 and CH4 from lakes and rivers in arctic Alaska, Hydrobiologia,
240, 23 – 36.
Kortelainen, P., J. T. Huttunen, T. Väisäinen, T. Mattsson, P. Karjalainen,
and P. J. Martikainen (2000), CH4, CO2 and N2O supersaturation in 12
Finnish lakes before and after ice-melt, Verh. Int. Ver. Limnol., 27, 1410 –
1414.
Kortelainen, P., H. Pajunen, M. Rantakari, and M. Saarnisto (2004), A large
carbon pool and small sink in boreal Holocene lake sediments, Global
Change Biol., 10, 1648 – 1653.
GB2003 SOBEK ET AL.: CARBON DIOXIDE SUPERSATURATION IN GLOBAL LAKES
Kratz, T. K., J. Schindler, D. Hope, J. L. Riera, and C. J. Browser (1997),
Average annual carbon dioxide concentrations in eight neighboring lakes
in northern Wisconsin, USA, Verh. Int. Ver. Limnol., 26, 335 – 338.
Leggett, M. F., M. R. Servos, R. H. Hesslein, O. Johansson, E. S. Millard,
and D. G. Dixon (1999), Biogeochemical influences on the carbon iso-
tope signatures of Lake Ontario biota, Can. J. Fish. Aquat. Sci., 56,
2211 – 2218.
Lindroth, A., A. Grelle, and A.-S. Morén (1998), Long-term measurements
of boreal forest carbon balance reveal large temperature sensitivity,
Global Change Biol., 4, 443 – 450.
Liski, J., H. Ilvesniemi, A. Mäkelä, and C. J. Westman (1999), CO2 emis-
sions from soils in response to climatic warming are overestimated —
The decomposition of old soil organic matter is tolerant to temperature,
Ambio, 28(2), 171 – 174.
Löffler, H. (1968), Die Hochgebirgsseen Ostafrikas, Hochgebirgs-
forschung, 1, 1 – 68.
Löffler, H. (1978), Limnological and paleolimnological data on the Bale
Mountain lakes (Ethiopia), Verh. Int. Ver. Limnol., 20, 1131 – 1138.
Maberly, S. C. (1996), Diel episodic and seasonal changes in pH and
concentrations of inorganic carbon in a productive lake, Freshwater Biol.,
35, 579 – 598.
Maehl, P. (1982), Phytoplankton production in relation to physico-chemical
conditions in a small, oligotrophic subarctic lake in South Greenland,
Holarctic Ecol., 5, 420 – 427.
Milbrink, G. (1977), On the limnology of two alkaline lakes (Nakuru and
Naivasha) in the East Rift Valley system in Kenya, Int. Rev. Ges. Hydro-
biol., 62(1), 1 – 17.
Miyajima, T., Y. Yamada, E. Wada, T. Nakajima, T. Koitabashi, Y. T.
Hanba, and K. Yoshii (1997), Distribution of greenhouse gases, nitrite,
and d13C of dissolved inorganic carbon in Lake Biwa: Implications for
hypolimnetic metabolism, Biogeochemistry, 36, 205 – 221.
Mizandrontseva, I. B., and K. N. Mizandrontseva (1994), Partial pressure
and free CO2 exchange in the Baikal L. water-atmosphere system (in
Russian), Vodnye Resur., 21(1), 72 – 79.
Murugavel, P., and T. J. Pandian (2000), Effect of altitude on hydrology,
productivity and species richness in Kodayar—A tropical peninsular
Indian aquatic system, Hydrobiologia, 430, 33 – 57.
New, M., M. Humle, and P. D. James (2000), Global 30-year mean monthly
climatology, 1961 – 1990, data set, Oak Ridge Natl. Lab. Distrib. Active
Arch. Cent., Oak Ridge, Tenn. (Available at http://www.daac.ornl.gov)
Pedrosa, P., and C. E. Rezende (2000), Dissolved inorganic carbon and
metabolism of an eutrophic lacustrine system: Variations from a 36-hour
study, Rev. Bras. Biol., 60(4), 607 – 614.
Pomeroy, L. R., and W. J. Wiebe (2001), Temperature and substrates as
interactive limiting factors for marine heterotrophic bacteria, Aquat.
Microbiol. Ecol., 23, 187 – 204.
Prairie, Y. T., D. F. Bird, and J. J. Cole (2002), The summer metabolic
balance in the epilimnion of southeastern Quebec lakes, Limnol. Ocean-
ogr., 47(1), 316 – 321.
Qadri, M. Y., and A. R. Yousuf (1978), Seasonal variations in the physico-
chemical factors of a subtropical lake in Kashmir, J. Inland Fish. Soc.
India, 10, 89 – 96.
Quay, P. D., S. R. Emerson, B. M. Quay, and A. H. Devol (1986), The
carbon cycle for Lake Washington—A stable isotope study, Limnol.
Oceanogr., 31(3), 596 – 611.
Rai, H., and G. Hill (1981), Physical and chemical studies of Lago Tupé, a
central Amazonian black water ‘‘Ria Lake’’, Int. Rev. Ges. Hydrobiol.,
66(1), 37 – 82.
Raich, J. W., and W. H. Schlesinger (1992), The global carbon dioxide flux
in soil respiration and its relationship to vegetation and climate, Tellus,
Ser. B, 44(2), 81 – 99.
Ramlal, P. S., R. H. Hesslein, R. E. Hecky, E. J. Fee, J. W. M. Rudd, and
S. J. Guildford (1994), The organic carbon budget of a shallow Arctic
tundra lake on the Tuktoyaktuk Peninsula, N.W.T. Canada, Biogeo-
chemistry, 24(2), 145 – 172.
10 of 10
GB2003
Rasmussen, J. B., L. Godbout, and M. Schallenberg (1989), The humic
content of lake water and its relationship to watershed and lake morpho-
metry, Limnol. Oceanogr., 34(7), 1336 – 1343.
Richey, J. E., J. M. Melack, A. K. Aufdenkampe, V. M. Ballester, and L. L.
Hess (2002), Outgassing from Amazonian rivers and wetlands as a large
tropical source of atmospheric CO2, Nature, 416, 617 – 620.
Risk, D., L. Kellman, and H. Beltrami (2002), Carbon dioxide in soil
profiles: Production and temperature dependence, Geophys. Res. Lett.,
29(6), 1087, doi:10.1029/2001GL014002.
Rivkin, R. B., and L. Legendre (2001), Biogenic carbon cycling in the
upper ocean: Effects of microbial respiration, Science, 291, 2398 –
2400.
Sharma, P. C., and M. C. Pant (1987), Limnology of a subtropical lake,
Bhimtal (U.P.), India, Limnologica, 18(1), 15 – 27.
Sobek, S., G. Algesten, A.-K. Bergström, M. Jansson, and L. J. Tranvik
(2003), The catchment and climate regulation of pCO2 in boreal lakes,
Global Change Biol., 9, 630 – 641.
Sommaruga, R., and D. Conde (1997), Seasonal variability of metabolically
active bacterioplankton in the euphotic zone of a hypertrophic lake,
Aquat. Microbiol. Ecol., 13, 241 – 248.
Striegl, R. G., and C. M. Michmerhuizen (1998), Hydrologic influence on
methane and carbon dioxide dynamics at two north-central Minnesota
lakes, Limnol. Oceanogr., 43(7), 1519 – 1529.
Stumm, W., and J. J. Morgan (1996), Aquatic Chemistry: Chemical
Equilibria and Rates in Natural Waters, Wiley-Interscience, Hoboken,
N. J.
Takahashi, M., T. Hama, K. Matsunaga, and N. Handa (1995), Photosyn-
thetic organic carbon production and respiratory organic carbon
consumption in the trophogenic layer of Lake Biwa, J. Plankton Res.,
17(5), 1017 – 1025.
Talling, J. F., and I. B. Talling (1965), The chemical composition of African
lake waters, Int. Rev. Ges. Hydrobiol., 50(3), 421 – 463.
Tranvik, L. J. (1988), Availability of dissolved organic carbon for plank-
tonic bacteria in oligotrophic lakes of differing humic content, Microbial
Ecol., 16, 311 – 322.
Updegraff, K., S. D. Bridgham, J. Pastor, P. Weishampel, and C. Harth
(2001), Response of CO2 and CH4 emissions from peatlands to warming
and water table manipulation, Ecol. Appl., 11(2), 311 – 326.
Valentini, R., et al. (2000), Respiration as the main determinant of carbon
balance in European forests, Nature, 404, 861 – 865.
Vyverman, W. (1994), Limnological features of lakes on the Sepik-Ramu
floodplain, Papua New Guinea, Aust. J. Freshwater Res., 45, 1209 –
1224.
Weiler, R. R. (1975), Carbon dioxide exchange and productivity in Lake
Erie and Lake Ontario, Verh. Int. Ver. Limnol., 19, 694 – 704.
Weiss, R. F. (1974), Carbon dioxide in water and seawater: The solubility of
a non-ideal gas, Mar. Chem., 2, 203 – 215.
Wetzel, R. G. (2001), Limnology: Lake and River Ecosystems, Elsevier,
New York.
White, P. A., J. Kalff, J. B. Rasmussen, and J. M. Gasol (1991), The effect
of temperature and algal biomass on bacterial production and specific
growth rate in freshwater and marine habitats, Microbial Ecol., 21, 99 –
118.
Zinabu, G.-M. (2002), The effects of wet and dry seasons on concentrations
of solutes and phytoplankton biomass in seven Ethiopian rift-valley lakes,
Limnologica, 32, 169 – 179.
J. J. Cole, Institute of Ecosystem Studies, 65 Sharon Turnpike, Milbrook,
NY 12545, USA. (colej@ecostudies.org)
S. Sobek and L. J. Tranvik, Limnology/Department of Ecology and
Evolution, Evolutionary Biology Centre, Uppsala University, Norbyvägen
20, SE-75236 Uppsala, Sweden. (sebastian.sobek@ebc.uu.se; lars.tranvik@
ebc.uu.se)