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Atmospheric Environment 81 (2013) 373e379

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Atmospheric Environment

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Methane emissions in two small shallow neotropical lakes: The role oftemperature and trophic level

Cleber Palma-Silva a,*, Cláudio Cardoso Marinho b, Edélti Faria Albertoni a,Iara Bueno Giacomini a, Marcos Paulo Figueiredo Barros b, Leonardo Marques Furlanetto a,Claudio Rossano Trindade Trindade a, Francisco de Assis Esteves b

a Laboratório de Limnologia, Instituto de Ciências Biológicas, Universidade Federal do Rio Grande e FURG, Rio Grande, RS, Brazilb Laboratório de Limnologia, Departamento de Biologia, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brazil

h i g h l i g h t s

� Emissions of methane are estimated to subtropical shallow lakes.� Shallow lakes have a great potential to produce higher methane emissions.� Emissions of methane are higher at eutrophic lake mainly at summer.

a r t i c l e i n f o

Article history:Received 31 March 2013Received in revised form12 September 2013Accepted 14 September 2013

Keywords:Methane concentrationEutrophicationGreenhouse gasesGlobal warming

* Corresponding author.E-mail addresses: dmbcps@furg.br, cleber.limno@g

1352-2310/$ e see front matter � 2013 Published byhttp://dx.doi.org/10.1016/j.atmosenv.2013.09.029

a b s t r a c t

It is estimated that lakes are responsible for up to 16% of global methane (CH4) emissions. Studying theCH4 concentrations and emissions in these environments is important to estimate the total regionalproduction of CH4 and to understand the main factors related to these emissions. The aim of this studywas to measure the CH4 emissions from two shallow polymictic lakes in southern Brazil and to evaluatethe roles of temperature and trophic level in increasing these emissions. Temperature was positivelycorrelated with CH4 concentration in the water column, bubble emissions and diffusion. Both lakesexhibited significant seasonal differences in water-column and sediment methane concentrations anddiffusion. The eutrophic lake produced more bubble emissions [6868.95 (�7645.97) mmol m�2 d�1 inwinter and 11,251.10 (�10,160.92) mmol m�2 d�1 in summer]. Water-column and sediment concentra-tions [19.92 (�11.74) mmol L�1 and 1727.85 (�1581.19) mmol g�1, respectively)] and diffusion [27,549.94(�18,258.15) mmol m�2 d�1] were also higher in summer than in winter in both lakes. All measuredparameters were higher in the eutrophic lake, highlighting the maintenance of aquatic ecosystems in alow trophic state. Based on bubble emissions, the oligo-mesotrophic lake released an estimated3142.8 g ha�1 yr�1 of CH4, while the eutrophic lake contributed 287,868.6 g ha�1 yr�1. Estimates ofdiffusive flux were higher: 41,832 g ha�1 yr�1 in summer for the oligo-mesotrophic lake and1388.52 kg ha�1 yr�1 for the eutrophic lake. Our results show that shallow aquatic subtropical ecosys-tems are potential sources of atmospheric methane, and their contribution to global warming must betaken into account.

� 2013 Published by Elsevier Ltd.

1. Introduction

Methane (CH4) is among the greenhouse gases of greatestconcern due to its increasing concentrations and its high capacity toabsorb infrared radiation, approximately 23 times higher than thatof CO2 (Houghton et al., 2001). The metabolism of carbon

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compounds in aquatic ecosystems is an important source of at-mospheric carbon. Among all natural sources of this gas, lakes areestimated to be responsible for up to 16% (8e48 Tg yr�1) of globalCH4 emissions (Bastviken et al., 2004). In a recent review of datafrom freshwater ecosystems, Bastviken et al. (2011) increased thisestimate to approximately 72 Tg yr�1. Greenhouse gases are pro-duced under different conditions in the aquatic environment, andthe effect of global warming on water temperature may haveimportant consequences for the biological processes responsiblefor CH4 emissions (Moss et al., 2003). Emissions of CH4 to the

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atmosphere from water bodies can occur by diffusion in theaqueous medium or by the formation of bubbles. The latter processis of significant importance when high CH4 concentrations arepresent in the sediment (Marinho et al., 2004).

Today, anthropogenic pressures on the environment havemodified CH4 production and, consequently, the carbon cycle andmay significantly influence global climatic changes (Verville et al.,1998). Thus, controlling CH4 emissions is an important strategyfor controlling global warming. Although there are many estimatesof CH4 emissions from North American wetlands (Bridgham et al.,2006) and northern lakes (e.g., Juutinen et al., 2001; Huttunenet al., 2003; Walter et al., 2007), similar data are rare for southernBrazil. For the entire subtropical region, only a few studies haveexamined the contribution of shallow aquatic ecosystems to theglobal CH4 budget (Marinho et al., 2009; Furlanetto et al., 2012).Huttunen et al. (2003) have affirmed that to better understand thelacustrine carbon cycle, it is necessary to integrate data from lakesin different geographical regions. Global CH4 emissions from wet-lands, lakes and anthropogenic ecosystems remain largely uncer-tain, and ongoing in situ data acquisition is needed to moreaccurately quantify global methane emissions (Zhuang et al., 2009).Some studies, mainly in the northern hemisphere, have attemptedto quantify important methane sources, such as northern lakes(e.g., Walter et al., 2007) and a tropical (West African) coastal riverand lagoons (Kone et al., 2010). However, subtropical lakes aregenerally shallow and tend to be eutrophic, and the quantificationof methane emissions from these lakes is necessary and valuable(Xing et al., 2005).

Global characterizations of wetlands and lakes are too coarse torepresent significant differences in methane-emission rates(Zhuang et al., 2009). It is therefore imperative to understand thesources and sinks of atmospheric CH4 and to obtain better esti-mates of their carbon fluxes so that we can better predict, preparefor, and perhaps even mitigate future changes (Walter et al., 2007).Floodplains and lakes are important environmental sources of at-mospheric CH4 where the decomposition by methanogenic bacte-ria may cause significant emissions of CH4 to the atmosphere(Marani and Alvalá, 2007). It was emphasized that small waterbodies have the potential to produce higher methane-emissionrates than larger water bodies (Michmerhuizen et al., 1996;Bastviken et al., 2004). Indeed, carbon-cycling rates may be manyorders of magnitude higher in small lakes than in other globalecosystems (Dean and Gorham, 1998; Downing, 2010), possiblybecause small lakes and ponds are substantially more biologicallyactive than large lakes. An accurate view of the global carbonbudget will be elusive unless small lakes and ponds are analyzed,understood and considered (Downing, 2010). Besides, lacustrineshallow ecosystems are often highly eutrophic, resulting in sub-stantial CH4 and N2O releases (Michmerhuizen et al., 1996;Bastviken et al., 2004) and thus exacerbating atmosphericgreenhouse-gas levels.

Pollution may increase CH4 emissions through, for example, theincrease in biomass production due to the eutrophication of waterbodies (Juutinen et al., 2003). Excess availability of nutrientsstimulates primary production but can also have significant effectson microbial processes (Liikanen and Martikainen, 2003) The largeamounts of labile organic matter in eutrophic systems consumedissolved oxygen and release a large amount of substrate formethanogenesis (Segers, 1998). It was emphasized by many au-thors that increasing eutrophication, and consequently the netprimary production of freshwaters, could increase the CH4 emis-sions from lakes (e.g., Huttunen et al., 2003; Xing et al., 2005). Thetrophic status of shallow lakes also could influence methane con-centration at water column and sediment. In one study of methaneconcentrations in three shallow subtropical lakes, a high

concentration was observed in the sediment of the eutrophic lake(Furlanetto et al., 2012). Furthermore, the highest levels of organicmatter, total carbon, total nitrogen, and total phosphorus werefound in the superficial sediments of the eutrophic lake, contrib-uting to the higher CH4 concentration in the sediment.

Researchers have formed a consensus that climatic changes willaffect CH4 emissions from shallow aquatic ecosystems (Ehhalt et al.,2001). The global warming observed since the 1990s is expected toincrease CH4 emissions from these environments (Fletcher et al.,2004). Therefore, it is extremely important that the CH4 dynamicsand potential CH4 production of each region be studied and known.Previous studies have demonstrated the contributions of temper-ature and eutrophication to increased methane emissions (e.g.,Verma et al., 2002; Xing et al., 2005; Bastviken et al., 2008). Thus,the aim of this study is to measure and compare, during the winterand summer, the CH4 concentrations and emissions in two shallowsubtropical lakes of different trophic states. The hypothesis of thisstudy is that higher temperatures favor increased methane emis-sions in eutrophic shallow subtropical lakes compared to oligo-mesotrophic ones.

2. Materials and methods

The aquatic ecosystems of the sandy coastal plain of Rio Grandedo Sul (southern Brazil) are mainly wetlands and shallow lakes. Theclimate of this region is characterized as Cfa (humid subtropical) bythe Köppen classification. The average annual temperature variesbetween 13 �C (winter) and 24 �C (summer), and the total annualrainfall is between 1200 and 1500 mm.

The study was conducted in two small, shallow lakes, one oligo-mesotrophic (Polegar Lake) (32� 010 4000 S, 52� 050 4000 W) and oneeutrophic (Biguás Lake) (32� 040 4300 S, 52� 100 0300 W), in thesouthern coastal plain of Brazil, municipality of Rio Grande. Theoligo-mesotrophic lake has an area of approximately 0.01 km2 andan average depth of 1.5 m. This lake is characterized by low primaryproduction and nutrient concentrations (Albertoni et al., 2007;Marinho et al., 2009). The sediment is sandy and contains lownutrient and organic-matter concentrations (Furlanetto et al.,2012). The eutrophic lake has an area of 0.015 km2 and amaximum depth of 2.40 m. It is characterized by high concentra-tions of nitrogen, phosphorus and organic matter in the watercolumn and sediment (Furlanetto et al., 2012).

Sampling took place during the winter of 2006 and the summerof 2007 at two sites in each lake. Each sampling lasted two to fourconsecutive days and utilized a system designed to collect the CH4bubbles released from the sediment. It was sampled the water andsediment to measure CH4 concentrations, and a water sample todetermine nutrient concentration (nitrogen and phosphorus) andthe abiotic variables at each sampling point. To measure sedimentCH4 concentrations, samples were collected with a corer (8-cminternal diameter and 50-cm length) attached to a Kajak sedi-ment sampler. Five cores were collected at each sampling point,and the upper 10 cm of each core was considered. The bubble-collection system consisted of an inverted funnel (24-cm mouthdiameter) with a glass flask attached to the posterior part of theopening. This systemwas kept in situ for 24 h (Casper et al., 2000).After 24 h, the tubes were collected and replaced, taking care tomaintain the tube in an inverted position in the water whileinserting a rubber stopper. All samples were transported to thelaboratory in an insulated box for gas-composition analysis. Thisprocedure was performed on four consecutive days at each sam-pling point. To determine the CH4 concentration in the water col-umn, 8-ml water samples were collected in situ with a syringe andinjected into sealed 12-ml glass flasks with negative pressure intheir interiors and containing 1.6 g of NaCl. Diffusive flux (F) was

Table 1Abiotic variables of the water column in the oligo-mesotrophic and eutrophic lakes in winter (June 2006) and summer (February 2007). DO ¼ dissolved oxygen (mg L�1);Temp ¼ temperature (�C); TN ¼ total nitrogen (mg L�1); TP ¼ total phosphorus (mg L�1). Values are presented as the mean � standard deviation.

DO Temp Depth (m) pH TN TP

Oligo-mesotrophic Winter 10.71 � 0.84 16.5 � 0.67 0.85 7.39 � 0.15 0.72 � 0,09 0.04 � 0.01Summer 9.03 � 0.07 26.1 � 3.21 0.35 7.56 � 0.15 0.36 � 0.13 0.03 � 0.01

Eutrophic Winter 12.77 � 2.53 13.1 � 1.33 0.80 8.81 � 0.25 4.14 � 1.01 0.49 � 0.06Summer 8.26 � 0.85 30.3 � 2.81 0.40 9.09 � 0.27 3.85 � 0.63 0.78 � 0.19

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estimated using the expression F ¼ KCH4 (Cw e Ceq) (Liss andSlater, 1974). This expression describes the use of a two-layermodel to estimate the fluxes of various gases across the airewa-ter interface, where KCH4 is the piston velocity of methane at eachwater temperature, Cw is the dissolved-methane concentration atthe lake surface, and Ceq is the equilibrium watereair methaneconcentration.

The CH4 analysis was performed in a VARIAN Star 3400 gaschromatograph (Varian Co., USA) equipped with a Poropak-Q col-umn (60/100mesh). The FID detector wasmaintained at 200 �C, theinjector at 120 �C and the column at 85 �C. Nitrogenwas used as thecarrier gas.

The environmental parameters measured in the water columnwere temperature and dissolved oxygen (Oakton DO 300 oxygenmeter), pH (Hanna HI 8314 pHmeter) and depth (ruler). In addition,total nitrogen (TN) was determined by the Kjeldahl method ac-cording to Allen et al. (1974), and total phosphorus (TP) wasmeasured using the method of Fassbender (1973).

The mean values were calculated for the two sampling points ineach lake and for winter and summer. The water-column andsediment CH4 concentrations and the bubble-emissions anddiffusive-flux values (log x þ 1 transformed) were compared be-tween the two lakes, between the two seasons, and between thetwo seasons in each lake using t-tests (applying the Welchcorrection for unequal variances). The correlation between diffu-sion and temperature was evaluated using exponential fitting. Non-parametric Spearman correlation coefficients were calculated toevaluate the relationships between water-column methane con-centration and temperature, sediment methane concentration andbubble emissions, water-column methane concentration anddiffusive flux, and sediment methane concentration and diffusiveflux.

3. Results

3.1. Abiotic variables

The eutrophic lake exhibited a shallower average depth, mainlyin summer, and higher nutrient concentrations than the oligo-

Table 2Sediment methane concentration ([] sediment, mmol g�1), water-column methane con(mmol m�2 d�1) in the oligo-mesotrophic and eutrophic lakes in winter (June 2006) a(�SD) ¼ mean � standard deviation; n ¼ number of samples.

[] sediment [] water

WinterOligo-mesotrophic Min-max 0.58e36.96 0.055e0.66

M(�SD) 3.06 (�5.64) (n ¼ 60) 0.27 (�0.14) (n ¼Eutrophic Min-max 148.33e3404.86 0.21e1.93

M(�SD) 1425.15 (�860.31) (n ¼ 60) 0.95 (�0.43) (n ¼SummerOligo-mesotrophic Min-max 3.02e6273.92 1.15e4.64

M (�SD) 523.9 (�1395.55) (n ¼ 60) 2.49 (�1.36) (n ¼Eutrophic Min-max 16.45e6206.71 1.13e43.74

M (�SD) 1727.85 (�1581.19) (n ¼ 60) 19.92 (�11.74) (

mesotrophic lake (Table 1). The data showed clear seasonal varia-tion in water temperature, which is typical in subtropical regions.

We compared the abiotic variables between lakes and betweenseasons. The values of pH, dissolved oxygen and temperature didnot differ significantly between lakes in the same season. Nutrientconcentrations differed significantly between the two lakes in bothwinter (phosphorus: t ¼ 12.55, P ¼ 0.006, 4 df; nitrogen: t ¼ 5.86,P ¼ 0.027, 4 df) and summer (phosphorus: t ¼ 6.65, P ¼ 0.021, 4 df;nitrogen: t ¼ 9.39, P ¼ 0.011, 4 df). Within each lake, the nutrientconcentrations did not differ between seasons. The pH values alsodiffered between the two lakes in both seasons (t ¼ 8.30, P ¼ 0.001,4 df inwinter; t¼ 8.53, P¼ 0.001, 4 df in summer) but did not differbetween seasons within each lake.

3.2. Methane concentrations in the sediment

The sediment methane concentrations differed between thetwo lakes, with higher values in the eutrophic lake during bothwinter and summer (winter: t ¼ 48.36, P < 0.0001, 117 df; summer:t ¼ 10.63, P < 0.0001, 94 df). Considering seasonal differenceswithin each lake, the oligo-mesotrophic lake showed higher valuesin summer (t ¼ 8.31, P < 0.0001, 69 df), while the eutrophic lakeshowed no seasonal difference (t¼ 8.31, P¼ 0.4143, 69 df) (Table 2).

3.3. Methane concentrations in the water column

The water-column methane concentrations differed betweenthe two lakes and between seasons in each lake. Both lakesexhibited the same pattern, with significantly higher CH4 concen-trations in summer than in winter (Table 2, Figs. 1 and 2). Theconcentrations in the eutrophic lakewere approximately four timeshigher in winter and eight times higher in summer than those inthe oligo-mesotrophic lake (0.95 � 0.43 mmol L�1 in winter and19.91 �11.74 mmol L�1 in summer; t ¼ 6.52, P < 0.0001, 80 df). Theconcentrations also differed between seasons in each lake (oligo-mesotrophic lake: t ¼ 10.33, P < 0.0001, 58 df; eutrophic lake:t ¼ 10.21, P < 0.0001, 77 df).

The Spearman correlation between the water-column CH4

concentration and water temperature was positive and significant

centration ([] water, mmol L�1), bubble emissions (mmol m�2 d�1) and diffusionnd summer (February 2007). Min ¼ minimum value; max ¼ maximum value; M

Bubbles Diffusion

0.12e540 17.78e331.6940) 73.30 (�127.14) (n ¼ 28) 135.34 (�68.99) (n ¼ 40)

172.32e24,591.49 93.46e1248.4540) 6868.95 (�7645.97) (n ¼ 30) 584.52 (�269.32) (n ¼ 40)

0.05e1033.4 830.02e4366.7420) 117.34 (�266.51) (n ¼ 30) 2190.89 (�1048.69) (n ¼ 20)

127.7e38,863.73 1026.90e60,233.71n ¼ 39) 11,251.10 (�10,160.92) (n ¼ 59) 27,549.94 (�18,258.15) (n ¼ 19)

Fig. 3. Variation in water temperature (Temp., �C) and methane-bubble emissions(Bubbles, mmol m�2.d�1) across sampling periods in the oligo-mesotrophic lake. Totaln ¼ 57; Winter ¼ June 2006, n ¼ 31; Summer ¼ February 2007, n ¼ 26.

Fig. 1. Variation in water temperature (Temp., �C) and water-column methane con-centration ([] water, mmol L�1) across sampling periods in the oligo-mesotrophic lake.Total n ¼ 57; Winter ¼ June 2006, n ¼ 40; Summer ¼ February 2007, n ¼ 17.

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for both the oligo-mesotrophic lake (r ¼ 0.88, P < 0.0001) and theeutrophic lake (r ¼ 0.96, P < 0.0001).

3.4. Methane-bubble emissions

The CH4-bubble emissions followed the same pattern as thewater-column concentrations. Although this measurement washighly variable, the eutrophic lake exhibited values that wereapproximately 94 times higher than the oligo-mesotrophic lake(Table 2, Figs. 3 and 4). The two lakes yielded significantly differentvalues over all seasons (t ¼ 12.56, P < 0.0001, 37 df) and whenconsidering each season separately (winter: t¼ 3.44, P¼ 0.0029, 18df; summer: t ¼ 5.20, P < 0.0001, 30 df). Within each lake, nosignificant difference was found between seasons (oligo-mesotro-phic lake: t ¼ 0.60, P ¼ 0.5508, 23 df; eutrophic lake: t ¼ 0.25,P ¼ 0.2490, 25 df).

The Spearman correlation between CH4-bubble emissions andtemperature was not significant for either the oligo-mesotrophiclake (r ¼ �0.015, P ¼ 0.9409) or the eutrophic lake (r ¼ �0.119,P ¼ 0.5699) (Table 3).

3.5. Diffusive emissions

The CH4-diffusion values differed between lakes andbetween seasons within each lake (Table 2). The valuesobtained in the eutrophic lake were four times higher thanthose obtained in the oligo-mesotrophic lake during winter

Fig. 2. Variation in water temperature (Temp., �C) and water-column methane con-centration ([] water, mmol L�1) across sampling periods in the eutrophic lake. Totaln ¼ 79; Winter ¼ June 2006, n ¼ 40; Summer ¼ February 2007, n ¼ 39.

(584.52 � 269.32 mmol.m�2 d�1 vs. 135.34 � 68.99 mmol m�2

d�1; t ¼ 30.43, P < 0.0001, 18 df) and twelve times higher duringsummer (27,549.94 � 18,258.15 mmol m�2 d�1 vs. 2190.89 �1048.69 mmol m�2 d�1; t ¼ 5.57, P < 0.0001, 18 df) (Fig. 5).Similarly, CH4 diffusion differed significantly between seasons inboth lakes (P < 0.0001). The relationship between CH4 diffusionand water temperature was positive and significant for both theeutrophic (r2 ¼ 0.81) and the oligo-mesotrophic lake (r2 ¼ 0.67).

The Spearman correlation between the water-column CH4concentration and diffusive flux was significant for both lakes andboth periods (Table 3). The correlation between the sedimentconcentration and bubble emissions was also significant in somecases. Both correlations were higher for the eutrophic lake.

As bubble emissions did not show significant differences atsame lake, we estimate that oligo-mesotrophic lake release3142.8 g ha�1 yr�1, and eutrophic lake contributes with287,868.6 g ha�1 yr�1. The diffusive flux was significant differentbetween the two periods studied, than we estimate the release ofmethane by diffusion to atmosphere from oligo-mesotrophic lakeat a rate of 680 g ha�1 yr�1 in winter times, and 41,832 g ha�1 yr�1

in summer times. To eutrophic lake in winter, we estimate27,640.8 g ha�1 yr�1, and reaches 1388.52 kg ha�1 yr�1 in summertimes.

4. Discussion

The CH4-concentration, on water and sediment, and emissionpatterns of the two lakes are consistent with the hypothesis thathigher temperatures favor more CH4 emissions.

Fig. 4. Variation in water temperature (Temp., �C) and methane-bubble emissions(Bubbles, mmol m�2.d�1) across sampling periods in the eutrophic lake. Total n ¼ 88;Winter ¼ June 2006, n ¼ 33; Summer ¼ February 2007, n ¼ 54.

Table 3Spearman correlation coefficients between sediment methane concentrations andbubble emissions (sed � bubble) and between water-column methane concentra-tions and diffusive fluxes (wat � diffusion) in the oligo-mesotrophic and eutrophiclakes in winter (June 2006) and summer (February 2007).

Winter Summer

Sed �bubble

Wat �diffusion

Sed �bubble

Wat �diffusion

Oligo-mesotrophic r ¼ �0.33,P ¼ 0.07

r ¼ 0.85,P < 0.0001

r ¼ 0.29,P ¼ 0.123

r ¼ �0.51,P < 0.0001

Eutrophic r ¼ �0.25,P ¼ 0.18

r ¼ 0.97,P < 0.0001

r ¼ �0.53,P < 0.0001

r ¼ 0.78,P < 0.0001

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In the present study, water-column CH4 concentrations weresignificantly higher in summer, suggesting the influence of tem-perature on methanogenesis and indicating that the CH4 flux fromsediment to water is more intense during warmer periods of theyear, as showing at Table 2. Similar to other biological processes,methanogenesis is affected by temperature, with consequences forCH4 production and emissions in aquatic environments (Singhet al., 2000). This temperature effect may explain the strong posi-tive correlation betweenwater temperature and water-column CH4concentration. Studies in one oligo-mesotrophic lake, located alongthe northern coast of Rio de Janeiro, Brazil, have demonstrated theeffect of temperature on the water-column CH4 concentration(Fonseca et al., 2004; Marinho et al., 2004). Marinho et al. (2009)observed seasonal variations in the water-column CH4 concentra-tion of this oligo-mesotrophic lake, with differences of up to 10 �Cbetween sampling periods (November 2001 and June 2002).

The methane sediment concentration also showed positivecorrelation with temperature, mainly at oligo-mesotrophic lake. Inthis system at summer we detected methane concentration atsediment close to two hundred times higher than winter (Table 2).In two German lakes, Furtado and Casper (2000) found that tem-perature was the most important factor in regulating CH4 con-centration. It was demonstrated by Bastviken et al. (2008), in astudy of three temperate lakes in summer, that not only ebullitionbut also diffusive fluxes depend primarily on shallow sedimentprocesses further illustrates the importance of sediments for lakeCH4 dynamics and emissions.

Temperature is an important factor to consider also in bubbleemissions, especially in shallow environments with lower hydro-static pressure (Bastviken et al., 2004). These authors highlighted

Fig. 5. Average values of methane-diffusive flux (mmol m�2 d�1) in the oligo-mesotrophic2007). Bars represent standard deviation.

the need for more studies in lakes at different latitudes to consol-idate the evidence for a relationship between temperature andwater depth for methane emissions. In lakes and flooded areas ofthe Brazilian Pantanal, Marani and Alvalá (2007) found high vari-ability in CH4 emissions but noted that this variability was ex-pected. The authors attributed this variability, especially in shallownatural lakes, to the fact that the bubble mechanism involves manyvariables, like the water turbulence and changes in the hydrostaticpressure near-bottom. Water depth can influence methane flux bychanging the solubility of methane through pressure and temper-ature variations, providing a greater opportunity for oxidation ofmethane in the sediments and water column (Joyce and Jewell,2003). According the authors, for these reasons, ebullition typi-cally is not important in deep water but is generally the primarymode of gas transport in shallow lakes. Our measurements ofbubble emissions exhibited even higher variability, differing be-tween the two lakes (Table 2). It was observed, despite this vari-ability, the summer time with values around two times higher thanwinter, for both lakes. In a study of a shallow, hyper-eutrophicsubtropical lake in China, Xing et al. (2005) reported wide sea-sonal variations in CH4 emissions, with low emissions in autumn,winter and spring and high emissions in summer. These authorsalso reported that CH4 emissions were much higher when thetemperature at the sediment surface exceeded the threshold valueof 25 �C, a temperature equivalent to those observed during sum-mer in the lakes studied here.

Also important when reported temperature effects is thediffusive flux. Our results showed always higher values in summer,for both lakes studied. We found significant correlation with waterconcentration, for both lakes (Table 3). Similar results are reportedby Yvon-Durocher et al. (2011) in mesocosms experiments, withthe rate of CH4 efflux showed strong seasonal trends with peaks inearly summer and lowest rates in winter, and strong correlationwith the concentration of CH4 in the water column. These obser-vations demonstrate the importance of seasonality in the envi-ronments studied, highlighted the tendency of warming of aquaticecosystems and consequently increase in metabolic pathways.

The emission of CH4 by bubbles and/or diffusive flux is reportedfor many aquatic ecosystems, mainly in temperate and boreal re-gions (e.g., Huttunen et al., 2003;Walter et al., 2007; Juutinen et al.,2001). In a series of studies on methane dynamics in Lake Biwa,Japan, Murase et al. (2005) observed that resuspension of thesediment surface causes methane to be released from the sediment

(OMT) and eutrophic (EUT) lakes in winter (W, June 2006) and summer (S, February

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since profundal zone (80 m isoclines). In shallow environments,wind promotes intense water-column circulation, frequently per-turbs the sediment surface, and can facilitate the release of bubblestrapped in the sediment (Walter et al., 2007). This process may be asource of methane in the lake water as pointed by Juutinen et al.(2001) that wind forced mixing as an important factor to increaseCH4-concentration at water column at shallow lakes. Point-sourceebullition from shallow lakes is a dominant source of methaneemission to the atmosphere (Ostrovsky et al., 2008). To shallow andpolymictic Lake Apopka (Florida, USA), frequently wind mixingmay affected the CH4 and CO2 released during methanogenesis bywind-induced resuspension of sediments that occurs on temporalscales of days or weeks (Gu et al., 2004). Aquatic ecosystems of thesouthern coastal plain in Brazil are typically shallow, and the con-stant winds make them polymictic (Trindade et al., 2009), withrapid interaction between the water column and the atmosphere.These conditions may facilitate the release of methane from sedi-ments in these systems.

The eutrophic lake presented higher values of methane con-centration and emission during both seasons, as can be seen inFigs. 1e5, confirmed our study hypothesis. Considering thedifferent trophic states of the two lakes, we attribute the highermethane concentrations and emissions of the eutrophic lake tohigher organic-matter concentrations resulting from higherprimary-production rates, as reported by Furlanetto et al. (2012).Bastviken et al. (2004) have previously reported a positive corre-lation between methane emissions and primary production andphosphorus concentration in Swedish lakes, where annual ebulli-tion per m2 was best predicted from total phosphorous. In water-enrichment experiments in Hallwill Lake, a temperate lake inSwitzerland, Flury et al. (2010) reported emission values rangingfrom200 to 30,000 mmol CH4.m�2 d�1 and related the higher valueswith more enriched waters. Compared to the values reported byMarani and Alvalá (2007) for tropical lakes and floodplains(1825.00 mmol m�2 d�1), the bubble-emissions values of theeutrophic lake were 3.5 times higher inwinter and 5.4 times higherin summer. The trophic status of shallow lakes influenced CH4emission fluxes was recently emphasized for Yang et al. (2011) inChinese lakes, when the authors pointed out that their highernutrient enrichment, higher organic matter input, and shallow lakewater depth are factors that allow to much higher estimatives ofcontribution from these ecosystems to global greenhouse-gasbalance.

Recently, Bastviken et al. (2011) estimated the total CH4 emis-sions from freshwater ecosystems to be 103 Tg yr�1 (72 Tg yr�1

from lakes). These authors emphasized that freshwater ecosystemscan be substantial sources of methane and must be taken into ac-count in global estimates. In shallow sediments, a larger proportionof the CH4 produced may escape oxidation, resulting in aturbulence-induced ‘‘shortcut’’ for dissolved CH4 to move fromshallow sediments to the atmosphere (Bastviken et al., 2004). Thisprocess may be responsible for the observed CH4 concentrationsand emissions in the eutrophic and oligo-mesotrophic lakes stud-ied here. Although our data are conservative, we estimated the totalannual CH4 emissions from these ecosystems. The eutrophic lakealways emitted larger amounts of methane at both low and hightemperatures. As discussed above, the trophic state has an impor-tant effect on methane production and emission, especially inshallow aquatic ecosystems. The observed values in the two lakescorroborate this hypothesis. In the Brazilian southern coastal plain,shallowwater bodies cover a total area of 14,260 km2 (Schwarzboldand Schäfer, 1984). Based on our data from the eutrophic lake, weestimate that the shallow water bodies in this geographical regioncontribute 0.4 Tg ha�1 yr�1 of CH4 via bubble emissions and1.9 Tg ha�1 yr�1 via diffusive flux. At Bastviken et al. (2011) global

estimative from freshwaters, for South America (SA) only tropicallakes were included, mainly at Amazonian and Pantanal region. Asdescribed above, the subtropical region of SA shelter many shallowlakes, and our results could contribute to more data of methanesources to the atmosphere from these aquatic systems to improveregional and global methane budgets.

5. Conclusions

Our data confirm our initial hypothesis and highlight thecontribution of the studied ecosystems to atmospheric methaneconcentrations. The methane emissions are higher in summer,especially in the eutrophic lake. Greater attention should be paid tothe eutrophication of aquatic ecosystems because the eutrophiclake presented values many times higher than the oligo-mesotrophic lake. These results show that shallow subtropicalaquatic ecosystems have a high potential to release CH4 to the at-mosphere, especially during summer, and that their methaneproduction increases with the increases in temperature. Therefore,we predict that global warming may significantly increase thecontribution of shallow subtropical aquatic systems to atmosphericmethane concentrations.

Acknowledgments

This work was supported by CNPq and CAPES.

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