Science of the Total Environment 542 (2016) 685–693

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Edaphic factors controlling summer (rainy season) greenhouse gasemissions (CO2 and CH4) from semiarid mangrove soils (NE-Brazil)

Gabriel N. Nóbrega a, Tiago O. Ferreira a,⁎, M. Siqueira Neto b, Hermano M. Queiroz c, Adriana G. Artur c,Eduardo De S. Mendonça d, Ebenezer De O. Silva e, Xosé L. Otero f

a Departamento de Ciência do Solo, Escola Superior de Agricultura Luiz de Queiroz, ESALQ/USP, Av.Pádua Dias 11, Piracicaba, São Paulo 13.418-260, Brazilb Laboratório de Biogeoquímica Ambiental, Centro de Energia Nuclear na Agricultura, CENA/USP, Av. Centenário 303, Piracicaba, São Paulo 13.400-970, Brazilc Departamento de Ciências do Solo, Universidade Federal do Ceará, UFC, Av. Mister Hull 2977, Campus do Pici, Fortaleza, Ceará 60.440-554, Brazild Departamento de Produção Vegetal, Universidade Federal do Espírito Santo, UFES, Alto Universitário s/n, Alegre, Espírito Santo 29.500-000, Brazile Empresa Brasileira de Pesquisa Agropecuária, Centro Nacional de Pesquisa de Agroindústria Tropical, Pós Colheita, Dra. Sara Mesquita Street, 2270, Planalto Pici, Fortaleza, Ceará 60.511-110, Brazilf Departamento Edafoloxía e Química Agrícola, Facultade de Bioloxía, Universidade de Santiago de Compostela, Rúa Lope Gómez deMarzoa, s/n. Campus sur, Santiago de Compostela 15.782, Spain

H I G H L I G H T S G R A P H I C A L A B S T R A C T

• GHG emission was associated withdifferent soil characteristics.

• Highest CO2 emissions were found inmangroves with larger dissolved C andlower DOP.

• Less CH4 flux was due to low DOP insemiarid mangrove soils.

⁎ Corresponding author.E-mail address: toferreira@usp.br (T.O. Ferreira).

http://dx.doi.org/10.1016/j.scitotenv.2015.10.1080048-9697/© 2015 Published by Elsevier B.V.

a b s t r a c t

a r t i c l e i n f o

Article history:Received 19 May 2015Received in revised form 3 October 2015Accepted 21 October 2015Available online xxxx

Editor: D. Barcelo

Keywords:Blue CarbonCoastal wetland soilsMethaneCarbon dioxideSoil organic matter

The soil attributes controlling the CO2, and CH4 emissions were assessed in semiarid mangrove soils (NE-Brazil)under different anthropogenic activities. Soil samples were collected from different mangroves under differentanthropogenic impacts, e.g., shrimp farming (Jaguaribe River); urban wastes (Cocó River) and a control site(Timonha River). The sites were characterized according to the sand content; physicochemical parameters (Ehand pH); total organic C; soil C stock (SCS) and equivalent SCS (SCSEQV); total P and N; dissolved organic C(DOC); and the degree of pyritization (DOP). The CO2 and CH4 fluxes from the soils were assessed using staticclosed chambers. Higher DOC and SCS and the lowest DOP promote greater CO2 emission. The CH4 flux wasonly observed at Jaguaribe which presented higher DOP, compared to that found in mangroves from humidtropical climates. Semiarid mangrove soils cannot be characterized as important greenhouse gas sources,compared to humid tropical mangroves.

© 2015 Published by Elsevier B.V.

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1. Introduction

Mangroves are tropical and subtropical coastal ecosystems charac-terized by their high productivity (Komiyama et al., 2008) and their ca-pacity to store large amounts of organic C in its soils (Donato et al., 2011;Nellemann et al., 2009). The C accumulation in its soils is a function be-tween the inputs of organic C compounds, formed basically by photo-synthetic processes sequestering atmospheric CO2, and the lossescaused by decomposition, erosion and leaching (Neue et al., 1997;Stockmann et al., 2013). The organic compounds enter the edaphic sys-tem as litter, decaying roots, root exudates, and microbial biomass,which are decomposed by the activity of micro- and mesofauna(Oades, 1998).

In mangroves, due to the frequent flooding event by seawater,organic matter decomposition occurs by reducing other electronacceptors substituting the O2 (i.e., O2 → NO3

− → Mnoxyhydroxides → Fe oxyhydroxides → SO4

2− → CO2), decreasing thedecomposition rate as a result of the lower energetic yield (Alongiet al., 2001; Howarth, 1984; Neue et al., 1997; Reddy et al., 1986). Be-cause of the combination of high biomass production and low de-composition rates, mangroves, and other coastal wetlands havebeen denominated as “Blue Carbon sinks” emphasizing the impor-tant role that these ecosystems perform in sequestering atmosphericCO2 (Duarte et al., 2005; Mcleod et al., 2011; Nellemann et al., 2009;Howard et al., 2014).

Despite its ecological importance, including its role in sequesteringatmospheric CO2, the mangrove forests are declining to extinction dueto anthropogenic impacts that directly remove the vegetation,e.g., aquaculture, urbanization and coastal landfill (Duke et al., 2007).Globally, the mangroves occupy 0.7% of the tropical forest area, buttheir destruction currently adds 10% to global CO2 release from tropicaldeforestations (Alongi and Mukhopadhyay, 2015).

Other activities (i.e., shrimp farming and eutrophication) are re-lated to nutrient-rich effluent release, which promotes changes inthe soil characteristics and stimulates organic matter decomposition,increasing CO2 fluxes (Aschenbroich et al., 2015; Chen et al., 2010;Suarez-Abelenda et al., 2014). In addition, mangroves can be an im-portant source of CH4 and N2O to the atmosphere (Barnes et al.,2006; Kristensen et al., 2008b; Purvaja and Ramesh, 2001) contribut-ing to global climatic changes due to its warming potential (Lashofand Ahuja, 1990; Chauhan et al., 2015).

CO2 production in mangrove soils refers to microbial activity dur-ing organic matter degradation, mainly, and root respiration (Chenet al., 2012; Lovelock et al., 2011). The CO2 flux to the atmosphere oc-curs when microorganisms oxidize the organic C using O2, NO3−,Mn4+, Fe3+, and SO4

2− as electron acceptors. On the other hand,CH4 production occurs in flooded areas using CO2 or other methylcompounds under extreme anoxic conditions (Eh b −150 mV;Chen et al., 2010; Kristensen et al., 2008a, 2008b; Yu et al., 2006). Be-sides, N2O is produced by nitrification processes, converting ammo-nium to nitrate under aerobic conditions or by a denitrificationprocess that involves anaerobic reduction of nitrate to N2 (Conrad,1995; Chauhan et al., 2015). Since the GHG emission is performedthrough microbial processes, the edaphic and climatic factors(e.g., redox potential; organic C content; salinity and temperature)may affect these emissions (Chen et al., 2010, 2011, 2012; Livesleyand Andrusiak, 2012).

This study aimed to evaluate edaphic factors influencing greenhousegas (CO2 and CH4) emissions from semiarid mangrove soils (NE-Brazil)under different anthropogenic activities, in order to better comprehendthe role of these endangered ecosystems for GHG emissions and C se-questration, based on the hypothesis that: 1) lower redox potentialand higher degree of iron pyritization can enhance methane emissionwhereas higher redox potential and lower degree of pyritization pro-mote higher CO2; and 2) the mangrove soils with greater soil carbonstock present lower CO2 emission.

2. Material and methods

2.1. Study site

The study site is located at the Brazilian semiarid coast (Ceará state,NE-Brazil; Fig. 1), which is characterized by two distinct seasons: an ex-tended dry period (rainfall b200mm; from June to January) and a rainyseason (from February to May; approximately 1000 mm rainfall), butwith a small variation in the daily mean temperature (from 25 to 29°C; Fig. 1; IPECE, 2010; Sales, 2008; Silva and Souza, 2006). The coastalzone of the Ceará is characterized by a small river discharge into the es-tuaries, which results in higher salinity and a decrease in the develop-ment of mangrove forests (Maia et al., 2006; Schaeffer-Novelli et al.,1990).

The samples were collected from 3 mangroves under different an-thropogenic impacts: the Cocó River is mostly affected by urban wastesand deforestation; the Jaguaribe River receives effluent discharge fromshrimp farming ponds; whereas the Timonha River is far west of thestate, where anthropic influences are minimal, and considered an un-disturbed mangrove (Fig. 1; Silva and Souza, 2006; Nóbrega et al.,2015).

2.2. Soil sampling procedure and physicochemical (Eh and pH)characterization

The soil sampleswere collected during the rainy period (April 2012)in mangrove forests predominantly vegetated by Rhizophora spp. Wecollected nine undisturbed soil samples using PVC tubes attached to asoil sampler for flooded soils in each mangrove. The samples were her-metically sealed and transported in a vertical position at approximately4 °C. In the laboratory, six of the soil samples (collected with the PVCtubes) were cut at intervals of 10 cm until a depth of 40 cm (0–10;10–20; 20–30 and 30–40 cm), accounting for 24 samples from each es-tuary. Sub-samples were dried (105 °C) and sieved (2 mm mesh),whereas other sub-samples were frozen for posterior analysis. Theother three undisturbed samples were used to obtain the soil bulk den-sity (ρ = mass of the soil solids / total soil volume) for the soil carbonstock (SCS) calculation.

The redox potential (Eh) and pH were measured in the field afterequilibrating the electrodes with the samples collected using a semi-opened cylinder soil sampler. The Eh was measured using a platinumelectrode and the final readings were corrected adding the potential ofthe calomel reference electrode (+244 mV). The pH values were ob-tained used a glass electrode previously calibrated with pH 4.0 and 7.0standard solutions.

2.3. Soil characterization

The soils from each sampling site were characterized regarding thecontent of sand, total contents of organic carbon (TOC), nitrogen (TN),sulfur (TS) and phosphorous (TP), dissolved organic carbon (DOC), re-active iron (FeREACTIVE) and pyritic iron (FePYRITE). Also, the degree ofFe pyritization (DOP), the soil C stock (SCS) and the equivalent soil Cstock (SCSEQV) was calculated.

The sand content was quantified by sieving the sample in a 50 μmmesh after the oxidation of the soil organic matter (using H2O2, 30%)and chemical dispersion (0.015 M (NaPO3)6 + 1.0 M NaOH; Gee andBauder, 1986). The TOC and TN contents were obtained by an elementalanalyzer (LECO 144 SE-DR). For TOC quantification, subsamples werepretreated usingHCl to remove the inorganic Cwhile the TN quantifica-tion was performed using untreated samples (Byers et al., 1978;Schulte, 1995). The TPwas extractedwith nitric acid boiling the samplesfor 3 h (130 °C, approximately) and calorimetrically quantified using themolybdenum blue method (Pansu and Gautheyrou, 2006). The dis-solved organic carbon (DOC) was calorimetrically quantified (Bartlett

Fig. 1. Sampling site location and climatic classification for the three studiedmangroves (1— Timonha River, control site; 2— Cocó River, affected by urbanwastes and 3— Jaguaribe River,affected by shrimp farming).

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and Ross, 1988) in interstitial water samples, obtained by centrifugation(6000 rpm for 30 min).

The quantification of FeREACTIVE and FePYRITE was performed usingfrozen samples according to the sequential extractionmethod proposedbyHuerta-Diaz andMorse (1990, 1992). Initially, FeREACTIVEwas extract-ed with a 1 M HCl solution (16 h agitation), followed by pre-treatmentto remove Fe associated with silicates (HF 10 M) and organic matter(H2SO4). Afterward, the FePYRITE was extracted using concentrated nitricacid (2 h agitation). Thus, the degree of pyritization (DOP)was calculat-ed according to Berner (1970) (DOP (%) = FePYRITE /(FeREACTIVE + FePYRITE).

The soil carbon stock (SCS) was quantified to a 40 cm depth using ρand the TOC content (SCS=TOC × ρ× 40 cm;Mckenzie et al., 2000) forthe 3 estuaries. To compare the soil carbon stock for the same soilmasses, equivalent soil depths were calculated for the disturbed estuar-ies using ρTIMONHA as a reference soil bulk density (Ellert and Bettany,1995). The equivalent depth was calculated as ZEQV = (ρTIMONHA /ρDISTURBEDESTUARY) and, thus, the corrected SCS was calculated asSCSEQV = TOC × ρDISTURBEDESTUARY × ZEQV). The use of an equivalentdepth for soil carbon stock calculations can be useful when comparingecosystems with different values of soil bulk density, when higherstock values are related tomore dense soils (e.g., due to grain size com-position, compaction, subsidence) instead to higher organic carbon con-tent (Ellert and Bettany, 1995).

2.4. GHG sampling and analysis

In each sampling site, three static chamberswere used for carbon gas(CO2 and CH4) collection. The rigid chambers (17.5 cm diameter and17.5 cm height, inserted 5 cm into the soil) presented a low volume/basal area ratio for rapid gas concentration, but large enough to mini-mize surface effects. The samples were collected using nylon syringes(BD type) attached to the top of the chamber after a short stabilization

time. Gas samples were taken using pre-established intervals (0, 10,20, 30 min), at the same time, measuring the air and soil temperatureand air humidity. The samples were sent to the laboratory where thegas concentrations were measured by gas chromatography (VarianInc., Palo Alto, CA). The GHG flux (g m−2 h−1) was calculated usingthe gas concentration, air temperature, chamber volume, basal area(area of soil inside the chamber), and atmospheric pressure (Howardet al., 2014). The changes in the concentration over the time in theclosed chamber, with a measured volume, reflect the gas emissionfrom the basal area (also known). Thus, the mass of GHG in each timeinterval is calculated using the universal gas equation (PV = nRT),obtaining an equation for mass flux (g h−1) for each chamber. Andthen the mass flux isdivided by basal to express the emission on a perarea basis (g m−2 h−1; for further details, please see Howard et al.,2014).

2.5. Statistical analysis

To compare the results obtained in each mangrove, the averagevalues were evaluated by one-way ANOVA and compared by theposthoc Tukey test with a 5% minimum significance value.

3. Results

3.1. Characterization of the sampling sites

The results indicate a marked difference between the areas studied.The lower Eh values were found in the mangrove from JaguaribeRiver (average of all the depths: −87 ± 76 mV), followed by Timonha(average: +93 ± 107 mV) and Cocó (average: +168 ± 94 mV). In allthree sites, the Eh values were lower at deeper layers (Fig. 2A). On theother hand, higher pH values were found in samples from Jaguaribe

Fig. 2. Physico-chemical characterization: Eh (A) and pH (B) for the three studied mangroves (Timonha River, control site; Cocó River, affected by urban wastes; and Jaguaribe River,affected by shrimp farming).

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River (average: 8.3 ± 0.3), while the samples from Timonha and CocóRiver presented the same pH average (average: 7.9 ± 0.2; Fig. 2B).

Regarding the sand contents, the studied sites presented a wide var-iation in the grain size composition with sand content ranging between2.7% and 75.8%. The lower sand contents were found in the samplesfrom Jaguaribe River (average: 3.4 ± 1.0%), whereas higher werefound in the Cocó River mangrove (average: 62.4 ± 11.9%). In theTimonha River, the sand content ranged between 39.4 and 56.3%, withan average of 48.2 ± 7.4% (Fig. 3).

Comparing the TOC contents, the measured values presented signif-icant differences (P b 0.005) among the three studied mangroves, withhigher values found at Jaguaribe River (average value for all depths:46.8 ± 10.8 g kg−1) followed by Timonha (average: 37.0 ±2.8 g kg−1) and Cocó (average: 25.7 ± 9.4 g kg−1; Fig. 4A). Similarly,higher TP content (P b 0.005) was measured in the Jaguaribe River(average: 0.33 ± 0.05 g kg−1; Fig. 4B), followed by Timonha (average:0.17 ± 0.01 g kg−1). The TN content ranged from 3.0 ± 0.2 g kg−1

(Jaguaribe River, 0–10 cm) to 0.6 ± 0.1 g kg−1 (Timonha, 0–10 and30–40 cm). The significantly higher (P b 0.005) TN values were foundin Jaguaribe (average for all depths: 2.4 ± 0.5 g kg−1; Fig. 4C), followedby Cocó (average for all depths: 1.1 ± 0.5 g kg−1) and Timonha (0.7 ±0.1 g kg−1).

The dissolved organic carbon (DOC) concentrations were signifi-cantly higher (P b 0.005) at the Timonha mangrove (average of alldepths 9.0 ± 0.6 mmol l−1), when compared to Jaguaribe (average of

Fig. 3. Sand and silt+clay contents for the three mangroves (Timonha River, control site; C

all depths 7.9 ± 1.3 mmol l−1) and Cocó (average of all depths 7.9 ±0.3 mmol l−1; Fig. 4D), which did not presented significant difference.

The FeREACTIVE contents varied between 21.0 ± 2.9 mmol kg−1 and72.5 ± 6.3 mmol kg−1 (Fig. 4E). Significative (P b 0.005) highestFeREACTIVE values were found in the Jaguaribe mangrove (average forall depths equal to 70.7 ± 14.8 mmol kg−1), compared to the valuesfrom the Cocó and Timonha (average for all depths: 26.4 ± 11.9 and23.0± 3.4mmol kg−1, respectively; Fig. 4E). Similarly, the FePYRITE con-tents varied widely within the samples (from 24.5 ± 5.4 to 286.0 ±48.7 mmol kg−1), with significantly higher values (P b 0.005) in thesamples from Jaguaribe River (average for all depths: 76.4 kg ±202.5 mmol kg−1; Fig. 4F), followed by Cocó River (average for alldepths: 55.9 ± 23.7 mmol kg−1) and Timonha (average for all depths:34.8 ± 11.8 mmol kg−1). Despite the wide variation in the FePYRITE, theDOP values showed a smaller variation, with values ranging from56.0 ± 4.8 to 78.5 ± 3.9%. The higher DOP values were found inJaguaribe (72.2 ± 9.5%), followed by Cocó (67.7 ± 8.7%) and TimonhaRivers (58.1 ± 13.4%; Fig. 4G).

A significantly higher (P b 0.005) ρ value was found in the TimonhaRiver mangrove (ρTIMONHA; mean value: 1.01 ± 0.06 g cm−3), whereasthe lowest value was measured for the Jaguaribe mangrove soil(ρJAGUARIBE; mean of 0.45 ± 0.02 g cm−3) and the for the Cocó River(ρCOCÓ) it was equal to 0.81 ± 0.04 g cm−3. The higher soil carbonstock (P b 0.005) was calculated for the Timonha River (14.8 ±1.1 kg m−2), while the C stocks for the Cocó and Jaguaribe Rivers

ocó River, affected by urban wastes; and Jaguaribe River, affected by shrimp farming).

Fig. 4.Contents of total organic carbon (TOC; A), total phosphorus (TP; B), total nitrogen (TN; C), dissolved organic carbon (DOC; D), reactive and pyritic Fe (FeREACTIVE and FePYRITE; E and F,respectively) and degreeof pyritization (DOP) for the threemangroves (TimonhaRiver, control site; CocóRiver, affectedbyurbanwastes; and Jaguaribe River, affectedby shrimp farming).The average values followed by different capital letters present significative different values (P b 0.005).

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were 8.3 ± 3.0 kg m−2 and 8.3 ± 1.9 kg m−2, respectively (Fig. 5A).When the SCS was calculated for the same soil mass (SCSEQV), thevalue accounted for the Jaguaribe soils was 17.8 ± 4.3 kg m−2 and10.3 ± 3.8 kg m−2 for the Cocó soils (Fig. 5A).

3.2. CO2 and CH4 fluxes

The significantly higher (P b 0.005) CO2 flux was observed in theTimonha River mangrove (44.4 ± 2.2 mg m−2 h−1; Fig. 5B), followedby Jaguaribe (20.5 ± 1.1 mg m−2 h−1) and Cocó (16.4 ±3.8 mg m−2 h−1). The highest (P b 0.005) methane flux was recorded

Fig. 5. Soil carbon stock (A) CO2 (B) and CH4 (C) fluxes from the different mangroves (Timonhshrimp farming). For the SCS, CO2 and CH4 fluxes, the averages values followed by different cavalues followed by different lowercase letters present significative different values (P b 0.005)

for the Jaguaribe River (8.8 ± 13.8 μg m−2 h−1), followed by Timonha(1.3 ± 3.3 μg m−2 h−1) and Cocó (Cocó: 0.7 ± 0.5 μg m−2 h−1).

4. Discussion

TheTOC, TNand TP contents of this study emphasize the great abilityof mangrove soils to accumulate carbon and nutrients (Bosire et al.,2008; Bouillon et al., 2003; Donato et al., 2011; Duarte et al., 2005;Gonneea et al., 2004; Khan et al., 2006; Kristensen et al., 2008a;Nellemann et al., 2009). Due to the frequent flooding to which thesesoils are subject, the microbial respiration occurs by anaerobic path-ways, mainly by reducing Fe3+ compounds and sulfate (Alongi et al.,

a River, control site; Cocó River, affected by urban wastes; and Jaguaribe River, affected bypital letters present significative different values (P b 0.005). For the SCSEQV, the averages.

Fig. 7. Correlation between sand content and FeREACTIVE; and between sand and FePYRITE.

Fig. 6. Correlation between TOC and TN (A); and TOC and TP (B).

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2001). These metabolic pathways (Fe3+ and SO42− reduction) have a

lower energetic performance compared to aerobic metabolism, around14.7 and 13.3%, respectively (Reddy et al., 1986). In fact, the organic Ccontents obtained for mangrove soils are, on average, up to 4.5 timesthe TOC values quantified for other semiarid tropical ecosystems soils,such as the Caatinga (Sousa et al., 2012), 2.5 times the content of theCerrado soils, the most extensive Brazilian biome (Bayer et al., 2006)or 1.4 times the content of the soils of the Amazon rainforest(Kauffman et al., 1995).

The highest TN and TP contents were found in the mangrove fromJaguaribe River. This mangrove is characterized as an area with an in-tense anthropogenic impact, especially shrimp farming (Silva andSouza, 2006). This activity is known by its necessity of huge inputs ofN and P, but only a small portion (35.5 and 6.1% of the total N and Pinput, respectively) is retained in shrimp tissues (Páez-Osuna et al.,1997), resulting in high emission factors (1.9 and 0.23 t km−2 yr −1 ofN and P, respectively; Lacerda et al., 2006). Thus, the disposal of waste-water rich in N and P from shrimp farming ponds resulted in an accu-mulation of these nutrients (Lacerda et al., 2006). The significantcorrelations between TOC and TN (r = 0.747; P b 0.0001 n = 60; Fig.6A) and TP (r= 0.781; P b 0.0001, n= 60) indicate that these nutrientsare foundmainly in organic compounds, emphasizing the importance ofstudies on C dynamics for understanding the nutrient geochemical pro-cesses in the mangroves soils.

The FeREACTIVE and FePYRITE contents showed a negative correlationwith the sand content of the samples (Fig. 7). This fact highlights therole of soil texture on the Fe availability for the metabolic process ofreducing Fe oxyhydroxides. In mangrove soils, the reduction of Feoxyhydroxides, followed by sulfate reduction, leads to the formationof iron sulfides, e.g., pyrite (FeS2), mackinawite (FeS) and greigite(Fe3S4) (Nóbrega et al., 2013; Otero et al., 2009). These sulfide speciespresent a significant environmental importance, especially in control-ling trace metal bioavailability (Bayen, 2012; Berner, 1970, 1983;Huerta-Diaz andMorse, 1992). Since the soil texture directly influencesthe availability of FeREACTIVE, an electron acceptor more energetic thanSO4

2− and CO2 (electron acceptor used in the methanogenesis), it canbe assumed that in soils with a finer texture the microbial metabolismextends reducing Fe oxyhydroxides and inhibiting the production ofCH4 (Canfield, 1994; Koretsky et al., 2006).

The dissolved organic carbon (DOC) consists of a range of moleculesfrom simple sugars and acids to complex humic substances produced bythe decomposition of the litter but also directly secreted as root exu-dates. Thus, the concentration of DOC depends on factors such as theproductivity of vegetation and carbon consumption bymicroorganisms(Van Den Berg et al., 2012; Weston and Joye, 2005). The DOC is a frac-tion of the labile organic matter of high importance for the microbialmetabolism regulating microbiological metabolic processes. (Weston

and Joye, 2005). The highest DOC values were found in Timonha(mean value: 9.0 ± 0.6 mmol l−1), followed by Jaguaribe (average:7.9 ± 1.3 mmol l−1) and Cocó Rivers (average: 7.9 ± 0.3 mmol l−1).Similarly, the highest SCS was quantified for the Timonha mangrove(average: 14.4± 1.1 kgm−2) followed by Cocó and Jaguaribe (average:8.3±3.0 and 8.3±1.9 kgm−2, respectively). The greater C bioavailabil-ity and, especially, higher concentrations of DOC in Timonha Riverman-grovewould promote greatermicrobial activity increasing CO2 flux. Thelower DOC concentrations at Cocó and Jaguaribe would limit this meta-bolic process (Figs. 4D and 5B).

In addition to the higher DOC concentration, the differences found inthe DOP values of the three areas point to significant differences in themetabolism of the three areas. Since the Timonha mangrove presentedthe lowest DOP (mean: 58.1± 13.4%), it can be assumed that sulfate re-duction occurs less intensively in this environment and that the micro-bial metabolism occurs by more energetic pathways (Araújo et al.,2012; Nóbrega et al., 2013) resulting in higher CO2 emissions (Fig. 5B).

Conversely, the higher CO2 flux from the Timonha did not result inlower SCS or SCSEQV. This fact suggests that, at this site, there is a higherorganic matter input from the vegetation, which is better preservedfrom anthropogenic impacts (Silva and Souza, 2006). On the otherhand, it can be assumed that the anthropogenic impacts resulted inthe reduction of the organic C input and/or to an intensification of theCO2 flux during a short period (prior to this study measurements),which would reduce the SCS (and SCSEQV). In fact, anthropogenic im-pacts (e.g., tree removal) results in quick and significant increase inCO2 and CH4 emissions, with a declining trend during the time(Lovelock et al., 2011; Lang'at et al., 2014). As labile organic carbonwas consumed during this initial peak of GHG emission, it would be

Table 1CO2 and CH4 emission from mangroves around the world under different climatic conditions.

Location Climate Precipitation(mm yr−1)

Average temperature(°C)

CO2 flux(mg m−2 h−1)

CH4 flux(μg m−2 h−1)

Reference

Mornington Peninsula, Victoria, Australia Temperate 719 19 45.6 25.1 Livesley and Andrusiak (2012)Moreton Bay, Queensland, Austrália Subtropical 1155 15–24 n.d. 20–350 Kreuzwieser et al. (2003)Dar es Salaam, Tanzania Humid tropical 1100 28–31 70–160 7–233 Kristensen et al. (2008b)Shenzhen, China Subtropical monsoonal 1927 22 24.6–904.6 190.6–4390.9 Chen et al. (2010)Chelmer, South East Queensland, Australia Subtropical 1146 20.4 n.d 3.0–17370.0 Allen et al. (2007)Hong Kong, China Subtropical monsoonal 2383 23.1 20.2–74.4 96.5–269.8 Chen et al. (2011)North Sulawesi, Indonesia Equatorial 2661 20–28 0–170.7 0–210.24 Chen et al. (2014)Sawi Bay, Thailand Tropical monsoonal 908 23.6 30.36–96.8 n.d. Alongi et al. (2001)

n.d.: not determined.

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expected a decline on CO2 since recalcitrant organic C proportionally ac-cumulates in soil (Lovelock et al., 2011).

Based on the average CO2 emission of the three areas, it is possible toestimate that mangroves of Ceará emit about 43.9 ± 21.1 Gg CO2 yr−1,corresponding to a minimum portion of the Brazilian CO2 emissions(380 Tg CO2; Olivier and Peters, 2010). Although the mangroves areconsidered marine environments that mostly emit CO2 to the atmo-sphere (Allen et al., 2007; Chen et al., 2012), the results obtained inthis study (averageof three areas equal to27.1±13.3mgCO2m−2 h−1)1) indicates that the mangrove soils emit lower amounts of CO2 com-pared to agricultural areas (average 1310 mg CO2 m−2 h−1; La Scalaet al., 2006).

Regarding the methane emission, the CH4 fluxes recorded are in ac-cordance with the physicochemical conditions of the studied man-groves. The higher CH4 flux was recorded for the Jaguaribe River(average: 8.8 ± 13.8 μg m−2 h−1), the site with lower Eh, higher DOPand TOC, whereas the other mangroves presented lower CH4 flux,higher Eh, and a lower DOP. Two reasons may be influencing the lowCH4 flux within these environments. For methanogenesis to occur, thedepletion of the more energetic electron acceptors is necessary(O2 → NO3

− → Mn oxyhydroxides → Fe oxyhydroxides and SO42−), and

then, methanogen metabolism uses CO2 or other methyl compounds(Kristensen et al., 2008a). In mangrove soils, the sulfate is directly sup-plied via the seawater and, because of its high concentration(2650 mg l−1; Driscoll, 1989) it is an almost inexhaustible supply. Fur-thermore, in semiarid mangrove soils with a lower DOP compared tohumid tropical mangroves (Nóbrega et al., 2013),microbialmetabolismis maintained at Fe reduction pathways, avoiding the CO2 consumptionformethanogenesis. Moreover, the oxidation of CH4 bymethanotrophicmicroorganisms in such environmentswould be able to reduce the pos-sible emission of CH4 (Kristensen et al., 2008a, 2008b). In fact, themeth-ane emission fromour results is considerably lower than those recordedfor other tropical humid mangrove soils, as occurred for temperatemangrove, at same vegetation stand (Table 1).

Despite the low emissions of CO2 and CH4 derived from studiedmangrove soils, anthropogenic and natural changesmay alter the abilityof these ecosystems to absorb carbon, making them important sourcesof GHG (Lovelock et al., 2010; Yu et al., 2006). The vegetation removaland drainage of mangrove areas restrict hydromorphism, acceleratingthe process of oxidation of soil organic matter (Lovelock et al., 2011).Similarly, the fertilization of mangroves by effluents rich in N,e.g., effluent from shrimp farming, can accelerate the decomposition oforganic matter reducing the C content and increasing GHG emissions(Chmura, 2011; Nóbrega et al., 2013). On the other hand, the dischargeof effluents rich in the labile organic matter can increase microbial me-tabolism (Purvaja and Ramesh, 2001) or extend waterflooding periods(Marchand et al., 2011), restricting the availability of sulfate as an elec-tron acceptor and resulting in the methanogenesis.

Since the study area is in the Brazilian semi-arid coast, with twowell-defined seasons (IPECE, 2010; Sales, 2008; Silva and Souza,2006), the results obtained in this study, during the rainy season, maypresent a considerable variation when compared to other studies

during the dry season. As mentioned in the literature, seasonal varia-tions lead to substantial changes in the metabolism of the Braziliansemi-arid mangrove soils (for more information, see Nóbrega et al.,2013). Thus, further studies are needed to verify the effect of seasonalityon the emission of greenhouse gases during the dry season, since therainfall distribution along the year may affect the temperature, charac-teristics, and decomposition rate of the organic matter, and also the O2

diffusion through the soil, affecting soil biogeochemical processes andmicrobial metabolic pathways (Kristensen et al. 2008a, 2008b).

5. Conclusions

The CO2 emissions are highly influenced by soil conditions. Thehighest CO2 fluxes were recorded for the undisturbed mangrove,which had a larger amount of dissolved carbon (labile), greater Cstock, and lower pyritization degree. Although they are considered ma-rine areas that contribute most to global warming, CO2 emission rate ofmangroves is about 2% of the issue caused by agriculture. The anthropo-genic impacts seem to have decreased the organic C input to soils andintensified the CO2 emission prior to the measurements.

The little methane flux is due to the constant supply of high energyelectron acceptors (e.g., iron and sulfate) than CO2, the substrate usedby microorganisms for methanogenesis. However, the predominanceof anoxic conditions and a higher degree of pyritization may drive themicrobial metabolism to methanogenesis.

Further studies are needed to see how seasonal climate variationswork in the emission of CO2 and CH4 in semiarid mangroves in Brazil.

Acknowledgments

The authors are thankful to National Counsel of Technological andScientific Development (CNPq), grant # 308288/2014-9, and São PauloResearch Foundation (FAPESP), grant # 2014/11778-5, for financialsupport. The present study was partially funded by the Conselleriade Innovación e Industrial Xunta de Galicia (Spain)(PGIDIT08MDS036000PR) and PROMETEO program from the Ecuadorgovernment. The authors also thank both anonymous reviewers fortheir insightful comments.

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