BGBiogeosciencesBGBiogeosciences1726-4189Copernicus PublicationsGöttingen, Germany10.5194/bg-13-865-2016Temperature dependence of the relationship between pCO2 and dissolved organic carbon in lakesPinhoL.luana.pinho@uerj.brDuarteC. M.MarottaH.Enrich-PrastA.Postgraduate Program in Ecology, Department of Ecology, Institute of
Biology, Federal University of Rio de Janeiro, Av. Carlos Chagas Filho, 373, Cidade Universitária (Ilha do Fundão), P. O. Box
68020, Rio de Janeiro – RJ, 21941-901, BrazilGlobal Change Department, IMEDEA (CSIC-UIB), Mediterranean Institute for
Advanced Studies, C. Miquel Marquès, 21, 07190 Esporles, Balearic Islands, SpainDepartment of Chemical Oceanography, Rio de Janeiro State University, Pavilhão João Lyra Filho, sala 4008 Bloco E, Rua
São Francisco Xavier, 524, Maracanã – RJ, 20550-900, BrazilKing Abdullah University of Science and Technology (KAUST), Red Sea
Research Center (RSRC), Thuwal 23955-6900, Saudi ArabiaResearch Center on Biomass and Water Management (NAB/UFF), Sedimentary
Environmental Processes Laboratory (LAPSA/UFF), International Laboratory of
Global Change (LINC Global), Federal Fluminense University, Av. Litorânea
s/n, Campus Praia Vermelha, Niterói – RJ, 24210-340, BrazilPostgraduate Program in Geography, Postgraduate Program in
Geosciences (Geochemistry), Federal Fluminense
University, Niterói – RJ, 24220-900, BrazilDepartment of Environmental Changes, Linköping University, 581 83 Linköping, SwedenL. Pinho (luana.pinho@uerj.br)15February201613386587125November20146February201511January201624January2016This work is licensed under a Creative Commons Attribution 3.0 Unported License. To view a copy of this license, visit http://creativecommons.org/licenses/by/3.0/This article is available from https://bg.copernicus.org/articles/13/865/2016/bg-13-865-2016.htmlThe full text article is available as a PDF file from https://bg.copernicus.org/articles/13/865/2016/bg-13-865-2016.pdf
The relationship between the partial pressure of carbon dioxide
(pCO2) and dissolved organic carbon (DOC) concentration in Brazilian lakes, encompassing 225
samples across a wide latitudinal range in the tropics, was tested. Unlike
the positive relationship reported for lake waters, which was largely based
on temperate lakes, we found no significant relationship for low-latitude
lakes (< 33∘), despite very broad
ranges in both pCO2 and
DOC levels. These results suggest substantial differences in the carbon
cycling of low-latitude lakes, which must be considered when upscaling
limnetic carbon cycling to global scales.
Introduction
Lakes cover less than 2 % of the continent's surface (Downing et al.,
2006; McDonald et al., 2012) but play a significant role in the global carbon (C)
cycle (Cole et al., 1994, 2007; Tranvik et al., 2009), contributing
significantly to C burial and emissions to the atmosphere (Cole et al.,
2007; Downing et al., 2008; Tranvik et al., 2009). Dissolved organic
carbon (DOC) represents a major C pool in lakes, with both autochthonous and
allochthonous contributions (Duarte and Prairie, 2005; Cole et al., 2007;
Prairie, 2008; Tranvik et al., 2009), supporting heterotrophy (Sobek et al.,
2007) and affecting key biological and physicochemical processes involved
in C cycling (Steinberg et al., 2006). Large inputs of terrestrial organic C
and its subsequent mineralization have been suggested to be a major driver
of CO2 supersaturation commonly encountered in lakes (Duarte and
Prairie, 2005; Cole et al., 2007; Prairie, 2008; Marotta et al., 2009).
The mechanistic connection between DOC and heterotrophic CO2 production
is believed to underpin the significant positive relationship between
pCO2 and DOC reported in comparative analyses (Houle et al., 1995; Sobek et
al., 2005; Larsen et al., 2012). However, recent analyses have revealed that
the relationship between pCO2 and DOC in lake waters is regionally
variable and not universal (Lapiere and del Giorgio, 2012). Hence, the
relationship between pCO2 and DOC reported in comparative analyses,
based on data sets dominated by temperate and high-latitude lakes
(> 33∘), may not be extrapolated for all types of lakes,
mainly because the tropical low-latitude lakes (< 33∘) are
generally underrepresented in global data sets (Raymond et al., 2013).
One priority of comparative studies is the latitudinal variance, where lake
temperature, ice cover and mixing regime will differ and these climatically
driven processes, in turn, should strongly influence organic carbon cycling (Hanson et
al., 2015). At low latitudes, warm conditions over the whole year may
increase the metabolic rates involved in the C cycling in terrestrial
(Ometto et al., 2005) and aquatic (Marotta et al., 2009, 2010) ecosystems on
an annual basis compared to the high-latitude lakes. High temperatures
affect heterotrophic activity and the associated mineralization rates of
organic matter in soils (Davidson and Janssens, 2006), waters (López-Urrutia
and Morán, 2007; Wohlers et al., 2008; Regaudie-de-Gioux and Duarte, 2012) and
aquatic sediments (Wadham et al., 2012; Gudasz et al., 2010; Marotta et al.,
2014). Enhanced heterotrophic activity in warm ecosystems would support high
aquatic CO2 production and subsidize high CO2 evasion from global
lake water to the atmosphere.
Geographic location of Brazilian lakes sampled in different biomes
(IBGE 2004, available at ftp://geoftp.ibge.gov.br/mapas_tematicos/mapas_murais/biomas.pdf): Amazonia forest (vertical
lines), Pantanal floodplain (dark gray) and Atlantic Forest (gray; tropical
and subtropical coastal lakes).
The largest previous comparative analysis already published in the
literature for global lake waters (Sobek et al., 2005) reported a
significant positive relationship between DOC and pCO2 and a
non-significant variation of pCO2 among lakes with changing temperature.
However, both analyses were characterized by a paucity of low-latitude data.
A strong positive relationship between temperature and pCO2 was observed
when subtropical and tropical ecosystems were included in the data set
(Marotta et al., 2009), likely caused by the potential increase in metabolic
rates under warmer conditions (Brown et al., 2004; López-Urrutia et al.,
2006). Hence, the relationship between lake pCO2 and DOC could also be
temperature-dependent and, therefore, may differ between temperate and
tropical lakes. The extensive low-latitude territory of Brazil, which has a
high density of lakes and ponds (Downing et al., 2006), is appropriate to
examine general patterns in the tropics (e.g., Marotta et al., 2009; Kosten
et al., 2010). Here, we test the applicability of the relationship between
pCO2 and DOC using inputs derived from a high-latitude data set (Sobek et
al., 2005) with added tropical and subtropical data of low-latitude lakes
from Brazil.
MethodsStudy area and lakes
Brazil extends from 5∘16′20′′ N to 33∘44′42′′ S, covering an area of approximately 8 547 000 km2, constituting
half of South America, and it encompasses a high diversity of low-latitude
landscapes (Ab'Saber, 2003) that are predominantly located within tropical
latitudes. We conducted a survey of pH, alkalinity and DOC between 2003 and
2011 in surface waters of 166 permanent lakes from 0 to 33∘ of
south latitude across Brazil (Fig. 1), yielding a total of 225 water
samples. The lakes were sampled in representative biomes of Brazil: (1) the
Amazonia forest (Amazonia biome, n= 65), (2) the Pantanal floodplain
(Pantanal biome, n= 29) and (3) the tropical (< 24∘ of
latitude) and (4) subtropical (> 24∘ and < 33∘
of south latitude) coasts, both in the Atlantic Forest biome (n= 35 and n= 37 lakes, respectively; Fig. 1). These biomes follow the
classification of the Brazilian Institute of Geography and Statistics for
biomes (IBGE 2004, ftp://geoftp.ibge.gov.br/mapas_tematicos/mapas_murais/biomas.pdf). Our data set encompasses a
broad inter-lake heterogeneity (n= 166) for pH, alkalinity and DOC,
simultaneously sampled among Brazilian biomes and along the latitudinal
gradient, independent of the year's season.
The Amazonian Forest biome is formed by the most extensive hydrographic
network on the globe – the Amazon River basin – which occupies a total area of
approximately 6.11 million km2 from its headwaters in the
Peruvian Andes to its mouth in the Atlantic Ocean (ANA – www.ana.gov.br).
The Amazon Forest is the Brazilian biome with the highest mean annual
precipitation (approximately 2200 mm) and has warm mean air temperatures,
approximately 25 ∘C, high cloud coverage and high humidity with
low fluctuations over the whole year (Chambers, 1999). We sampled a wide
variety of lakes, characteristic of different areas of the Amazonian Forest,
encompassing “clear” (low DOC and suspended solids), “white” (low DOC
and high suspended solids) and “dark” (high DOC and low suspended solids)
lakes.
The Pantanal floodplain is the world's largest tropical freshwater wetland,
extending across an area of approximately 150 000 km2 between
16 and 20∘ S and 58 and 55∘ W
(Por, 1995). The annual average temperature and precipitation are
approximately 22 ∘C and 1000 mm, respectively (Mariot et al.,
2007), with a strong seasonality and subsequent variation in the flooded
area (Junk and Nunes da Cunha, 2005). The high-water period occurs during
the rainy summer (usually from September to December), and low waters
typically occur during the dry winter (from March to July; Hamilton et al., 2002).
The Atlantic Forest biome extends along a broad latitudinal belt, between
5 and 30∘ S from the subtropics to tropics and a narrow
longitudinal section between 55 and 56∘ W, and occupies
an area of 1.11 million km2 along the Brazilian coast
(IBGE; www.ibge.gov.br). This biome is characterized by numerous shallow
coastal lakes, receiving high inputs of refractory organic matter (Farjalla
et al., 2009) derived from the typical open xerophytic vegetation on sandy
soils, where water retention is low (Scarano, 2002). The mean air
temperatures vary from 27 ∘C in winter to 30 ∘C in
summer at the tropical coast (< 24∘ of latitude; Chellappa et
al., 2009) and from 17 and 20 ∘C at the subtropical coast
(> 24∘ of latitude; Waechter, 1998). The mean annual
precipitation reaches 1164 mm (Henriques et al., 1986) and 1700 mm
(Waechter, 1998) in the tropical and subtropical Brazilian coast,
respectively. This biome is also characterized by strong seasonality, with
rainy summers and dry winters (Chellappa et al., 2009).
Sampling design and analytical methods
Our sampling design encompassed the most representative Brazilian biomes
from tropical and subtropical coastal areas to tropical and subtropical
forests (Amazon and Atlantic Forest) and inland wetlands (Pantanal), with
the intra-lake heterogeneity and seasonal fluctuations randomly assessed and
further integrated by means of each ecosystem. To analyze the relationship
between pCO2 and DOC in tropical lake waters, we joined data on 194
lakes (< 33∘ of latitude) with both variables sampled
at the same time, including 166 data samples from our own survey and 28 from
the literature compilation (Table S1 in the Supplement). The values reported here,
gathered in an opportunistic manner, represent daily averages (N= 4 or 5
samples) for a given year's season or/and one sampling time over different
seasons, which were also both integrated by means of each lake. To test the
global importance of the relationship between pCO2 and DOC, we added our
low-latitude data (225) to the Sobek et al. (2005) data set (4902 lakes) as
this data set had a paucity of tropical ecosystem data (148 tropical lakes,
but only one with pCO2 and DOC sampled at the same time).
Values of (a) temperature (∘C), (b) DOC
concentrations (mg C L-1) and (c)pCO2 concentration (µatm)
of Brazilian lakes sampled from different biomes, as defined by
subtropical coastal lakes (n= 37), tropical coastal lake (n= 63),
Pantanal floodplain (n= 58) and Amazonia forest (n= 67). The line depicts the median. The boxes show the quartiles, and the
whiskers mark the 10th and 90th percentiles. Different lowercase
letters near the box plot indicate significant statistic differences between
the groups (Kruskall–Wallis followed by Dunn's multiple comparison post hoc
test, p < 0.05).
pH, salinity and temperature were measured in situ. pH was determined using a pH
meter (Digimed – DM2) with reference standards certified by Mettler Toledo
(4.00 ± 0.01 and 7.00 ± 0.01 units) before each sampling hour.
Temperature and salinity were measured using a thermosalinometer (Mettler
Toledo – SevenGo™ SG3) coupled to a probe in Lab 737 previously calibrated
with 0.01 M KCl. Surface lake water was collected for total alkalinity and
DOC analyses, taking care to avoid bubbles at approximately 0.5 m of depth
using a 1 L Van Dorn bottle. Total alkalinity (TA) was determined in the
field by the Gran's titration method with 0.0125 M HCl
immediately after sampling (Stumm and Morgan, 1996). Water samples for DOC
were pre-filtered (0.7 µm, Whatman GF/F) and preserved by
acidification with 85 % H3PO4 to reach a pH < 2.0 in
sealed glass vials (Spyres et al., 2000). In the lab, DOC was determined by
high-temperature catalytic oxidation using a TOC-5000 Shimadzu Analyzer;
quality control was checked with a calibration curve made with potassium
hydrogen phthalate before each sample battery analysis. pCO2
concentrations in surface waters were calculated from pH and alkalinity
following Weiss (1974), after corrections for temperature, altitude and
ionic strength according to Cole et al. (1994).
In order to address the potential contribution of DOC to TA, which is
especially important in DOC-enriched acid freshwaters, we used the data set
from Abril et al. (2015) to correct pCO2 values calculated from pH
and TA after the corrections for temperature, altitude and ionic strength
(Cole et al., 1994). Full details on fitted regression equations to correct
pCO2 in function of the DOC and pH are described in the Supplement
(Fig. S3).
Comparisons of pCO2 against DOC concentrations for lakes from
this study (black circles) and from Sobek et al. (2005; gray circles). Each
point in the plot represents one measurement. The dashed line represents the
linear regression for all Brazilian data points (not significant; p > 0.05), and the solid line represents the linear regression from
Sobek et al. (2005; p < 0.05, R2= 0.26, log pCO2 (µatm) = 2.67 + 0.414 log DOC; mg C L-1).
Statistical analyses
The variables pCO2 and DOC did not meet the assumptions of parametric
tests even after logarithmic transformations (Zar, 1996) as the data were
not normally distributed (Kolmogorov–Smirnov, p < 0.05) and the
variances were heterogeneous (Bartlett, p > 0.05). Therefore, we
used medians and nonparametric tests to compare these variables among
biomes (Kruskall–Wallis followed by Dunn's multiple comparison post hoc
test, p < 0.05). The linear regression equations were fitted to
compare our results with those of previous studies from Sobek et al. (2005). Statistical analyses were performed using the software Graphpad
Prism version 4.0 for Macintosh (GraphPad Software, San Diego, CA).
Results
The lake waters surveyed were warm across all biomes (median 25–75 %, interquartile range = 27.5 ∘C, 25.2–30.1) but colder in
subtropical coastal lakes (23.4 ∘C, 20.0–26.2) than in Pantanal
and Amazonian lakes (29.5 ∘C, 27.7–31.4 and 29.4 ∘C,
27.6–31.0, respectively; Dunn's test, p < 0.05, Fig. 2a). DOC
concentrations were consistently high (6.3 mg C L-1, 4.3–11.9) for all Brazilian biomes but significant lower in the Amazonian Forest
(3.8 mg C L-1, 2.7–5.8) than in the tropical coast (13.4 mg C L-1, 6.1–32.8; Fig. 2b; Dunn's test, p < 0.05). Most lakes
(approximately 83 % of raw data) showed surface waters supersaturated in
CO2 relative to the atmospheric equilibrium (pCO2 in atmospheric
equilibrium is 400.83 µatm, 2015 annual mean; data available in
www.esrl.noaa.gov/gmd/ccgg/trends), with much higher pCO2 values in
Amazonian lakes (7956 µatm, 3033–11 346) than in subtropical
coastal lakes (900 µatm, 391.3–3212; Fig. 2c; Dunn's test, p < 0.05).
The pCO2 in the surface waters of Brazilian lakes was independent of DOC
concentrations (linear regression for raw data, p > 0.05, Fig. 3). The
same absence of positive significance pattern was found in comparison with
corrected data. A negative (linear regression, p < 0.05, R2= 0.03,
n= 194, pCO2=-98.76 (±39.92) × DOC + 6529
(±641.1)) or non-significant (linear regression, p > 0.05)
DOC–pCO2 relationship for tropical lakes (N= 194, DOC- and pH-corrected
data, respectively (Fig. S3a and c)) contrasted with a significant
positive relationship for those at other latitudes (N= 4433; linear
regression, p < 0.05, R2= 0.20, pCO2= 64.43
(±2.04) × DOC + 625.1 (±20.87) and R2= 0.12,
pCO2= 45.70 (±1.84) × DOC + 623.7 (±18.83)) for DOC-corrected data
and pH-corrected data, respectively (Fig. S3b and d, full details on
corrections in the Supplement). The range of pCO2 for a
similar DOC range in Brazilian lakes was larger than that reported by Sobek
et al. (2005) for the data set dominated by high-latitude cold lakes,
despite the number of lakes in their data set being much larger (more details
in the Supplement, Fig. S3).
Discussion
The Brazilian lakes sampled here were characterized by a prevalence of
CO2 supersaturation, consistent with general trends previously reported
for global lakes (e.g., Raymond et al., 2013; Cole et al., 1994, 2007),
including those at tropical latitudes (Marotta et al., 2009). The very high
pCO2 levels observed here, with a median of 900 and 8300 µatm for
subtropical and Amazon lake waters, respectively, are consistent with those
reported previously for the Amazon River and tributaries (2000–12 000 µatm; Richey et al., 2002), Amazon floodplain lakes
(3000–4898 µatm; Rudorff et al., 2012), Pantanal lakes and wetlands
(2732–10 620 µatm; Hamilton et al., 1995), and coastal lakes (768–9866 µatm; Kosten et al., 2010; 361–20 037 µatm; Marotta
et al., 2010) and for global values for tropical lakes (1255–35 278 µatm; Marotta et al., 2009), reservoirs (1840 µatm;
Aufdenkampe et al., 2011) and wetlands (3080–6170 µatm;
Aufdenkampe et al., 2011).
The non-significant or weakly negative relationship (Fig. S3) between DOC
and pCO2 reported here for warm low-latitude lakes contrasted with
significant positive relationships derived from previous data sets dominated
by high-latitude lakes (Houle, 1995; Prairie, 2002; Jonsson et al.,
2003; Sobek et al., 2005; Roehm et al., 2009; Lapiere and del Giorgio, 2012;
Larsen et al., 2012). The results presented show that warm low-latitude
lakes range widely in pCO2, reaching very high and low values, but tend
to have comparatively more uniform DOC concentrations (Fig. 3). More
intense metabolic processes that uptake and release CO2 in lake
waters, autotrophy and heterotrophy, respectively, could determine an
enhanced variability in lake pCO2 with decreasing latitude (Marotta et
al., 2009).
In this way, the inclusion of warm tropical data in our study revealed novel
increases in the variability of the DOC–pCO2 relationship in lakes over
the latitudinal gradient. One explanation for this pattern is that even
similar DOC concentrations, representing the total pool of DOC, may show
different mixtures between origins from aquatic primary producers and
terrestrial sources (Kritzberg et al., 2006). The autochthonous DOC (i.e., produced in the lake) is related to the net CO2 uptake (Staehr and Sand
Jansen, 2007), while the allochthonous DOC (i.e., produced in the catchment)
is a resource to the net CO2 release in lake waters (Sobek et al., 2007).
The increased DOC release from aquatic primary producers into waters under
tropical conditions, especially warmer annual conditions and higher solar
incidence, can offset any positive relationship between pCO2 and the
terrestrial DOC that causes the net aquatic heterotrophy to subsidize (Marotta et al.,
2010, 2012). This contributes to the explanation of non-significant relationships
reported here (Fig. 3), suggesting a temperature dependence of the
DOC–pCO2 relationship in global lakes.
In conclusion, the finding that pCO2 does not increase with DOC
concentration in Brazilian tropical lakes rejects the hypothesis that DOC
serves as a universal predictor for pCO2 in lake waters (Larsen et al.,
2012). Even discounting a possible artifact of the method that could be
causing an overestimation in the values of pCO2 or considering the
contribution of organic acids to the alkalinity, the pattern of no
relationship between DOC and pCO2 in the tropical lakes was strongly
confirmed (Fig. S3). Therefore, our results, contributing to the filling of a gap
in the literature of tropical studies, suggest potentially important latitudinal differences for
depositional aquatic environments, whose causes still need to be better
addressed to improve accuracy of global C cycle models.
The Supplement related to this article is available online at doi:10.5194/bg-13-865-2016-supplement.
All authors contributed to the study design, data interpretation and
preparation or refinement of the manuscript. L. Pinho and H. Marotta performed the
sampling and sample analyses.
Acknowledgements
This research is a contribution to projects from Brazilian research agencies
(FAPERJ, CAPES and CNPq). L. Pinho was supported by PhD scholarships from CAPES
(period in Brazil) and FAPERJ (period in Spain). A. Enrich-Prast received
postdoctoral and other CAPES and CNPq fellowships during studies at
Linkoping University. H. Marotta was supported by a research fellowship from
FAPERJ (Programa Jovem Cientista do Nosso Estado), and a research grant from
CNPq.
Edited by: M. Dai
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