Science of the Total Environment 502 (2015) 617–626

Contents lists available at ScienceDirect

Science of the Total Environment

j ourna l homepage: www.e lsev ie r .com/ locate /sc i totenv

Temporal variability of CO2 fluxes at the sediment-air interface inmangroves (New Caledonia)

Audrey Leopold a,b, Cyril Marchand a,⁎, Jonathan Deborde a, Michel Allenbach b,1

a Institut de Recherche pour le Développement (IRD), UMR 7590, UR 206, BP A5, 98848 Nouméa, New Caledoniab Université de la Nouvelle-Calédonie, PPME, EA 3325, BP R4, 98851 Noumea, New Caledonia

H I G H L I G H T S

• Seasonal variations in sediment CO2 flux were studied in three mangrove stands.• Seasonal variations in fluxes were studied taking biofilm development into account.• Seasonal variations are linked to the quantity and quality of biofilm.• Sediment water content is a major driving factor of biofilm growth and activity.• Biofilm development should be considered in the mangrove carbon cycling budget.

⁎ Corresponding author.E-mail address: cyril.marchand@ird.fr (C. Marchand).

1 Labex Corail.

http://dx.doi.org/10.1016/j.scitotenv.2014.09.0660048-9697/© 2014 Elsevier B.V. All rights reserved.

a b s t r a c t

a r t i c l e i n f o

Article history:Received 30 April 2014Received in revised form 9 September 2014Accepted 22 September 2014Available online xxxx

Editor: P. Kassomenos

Keywords:In situ sediment CO2 fluxesSeasonal variationBiofilmMangroveNew Caledonia

Carbon budgets in mangrove forests are uncertain mainly due to the lack of data concerning carbon export indissolved and gaseous forms. Temporal variability of in situ CO2 fluxes was investigated at the sediment–airinterface in different seasons in different mangrove stands in a semi-arid climate. Fluxes were measured usingdynamic closed incubation chambers (transparent and opaque) connected to an infra-red gas analyzer. Microcli-matic conditions and chl-a contents of surface sediments were determined. Over all mangrove stands, CO2 fluxeson intact sediments were relatively low, ranging from−3.93 to 8.85 mmolCO2·m−2·h−1 in the light and in thedark, respectively. Changes in the fluxes over time appeared to depend to a great extent on the development ofthe biofilm at the sediment surface. We suggest that in intact sediments and in the dark, CO2 fluxes measured atthe sediment–air interface rather reflect themetabolism of benthic organisms than sediment respiration (hetero-trophic and autotrophic). However, without the biofilm, sediment water content and air temperatureweremaindrivers of seasonal differences in CO2 fluxes, and their influence differed depending on the intertidal location ofthe stand. After removal of the biofilm, Q10 values in the Avicennia and the Rhizophora stands were 1.84 and 2.1,respectively, revealing the sensitivity of mangrove sediments to an increase in temperature. This study providesevidence that, if the influence of the biofilm is not taken into account, the in situ CO2 emission data currently usedto calculate the budget will lead to underestimation of CO2 production linked to heterotrophic respiration fueledby organic matter detritus from the mangrove.

© 2014 Elsevier B.V. All rights reserved.

1. Introduction

As a consequence of the increase in atmospheric CO2 and its role inglobal warming, it has become important to quantify and understandthe ability of ecosystems to act as carbon sinks and/or sources (IPCC,2007). Forest ecosystems are particularly important in the global carboncycling, representing a pool of 1146 PgC in their biomass (31%) and theirsoils (69%) as belowground biomass and soil organic carbon (Dixonet al., 1994). Among forest ecosystems, mangrove forest ecosystems

develop in tropical and sub-tropical intertidal areas, they cover approx-imately 136,760 km2 and extend from 30°N to 38°S (Duke et al.,1998; Giri et al., 2011). Mangroves are among the most productiveecosystems, their net primary production (NPP) is estimated at218 ± 72 TgC·y−1 (Bouillon et al., 2008). In addition, they are charac-terized both by high deposition rates of autochthonous and allochtho-nous organic matter, and by low rates of organic matter oxidation,since anaerobic decay processes dominate (Kristensen et al., 2008).Sixty percent of total organic carbon input may be preserved in man-grove sediments (Alongi et al., 2001) making mangrove ecosystems avery important terrestrial carbon sink (Chmura et al., 2003; Bouillonet al., 2008; Kristensen et al., 2008; Kauffman et al., 2011; Lee et al.,2014). Donato et al. (2011) suggested that mangroves can store up to

618 A. Leopold et al. / Science of the Total Environment 502 (2015) 617–626

1023MgC·ha−1 in their biomass and their substrate. Mangrove carbonstorage in aboveground biomass, and to a lesser extent in belowgroundbiomass, is relatively well known. But many uncertainties remainconcerning the fate of the organic carbon produced. Indeed, more thanhalf mangrove NPP (112 ± 85 TgC·y−1) is not accounted for in currentcarbon budgets (Bouillon et al., 2008). Recent studies revealed a majorrole for pore water seepage in carbon export (Maher et al., 2013;Stieglitz et al., 2013), underlining that part of mangrove NPP may bemineralized and/or emitted into the atmosphere as CO2 in adjacentecosystems, and thus that the CO2 diffusion from mangrove sedimentsmay be lower than the mineralization rate (Alongi et al., 2012). How-ever, data and knowledge are still lacking on the direct export of carboninto the atmosphere when sediments are exposed to the air, and notsubmerged in tidal water.

In a previous study (Leopold et al., 2013), we focused on the spatialvariability of CO2 fluxes from mangrove sediments, particularly onthe influence of different mangrove stands. We reached two mainconclusions: i) spatial inter-stand variability of fluxes resulted from dif-ferent sediment organic contents and redox conditions, both controlledby the position and the elevation of stand in the intertidal zone on theone hand, and by the physiological activities of the root systems onthe other, ii) the intertidal position also partly controlled the develop-ment of the biofilm, which affects the magnitude of the CO2 flux fromthe sediments in the different mangrove stands.

Seasonal variations in temperature and rainfall are known to strong-ly influence CO2 fluxes in different ecosystems because of the change insoil temperature and humidity, which, in turn, affect the metabolic ac-tivity of both the autotrophic and heterotrophic components (Raichand Schlesinger, 1992). In the sameway, it seems reasonable to assumethat over the course of the year, these parameters also affect the growthof biofilm organisms whose seasonal development may control themagnitude and direction of diffusive CO2 fluxes, depending on the fea-tures of each mangrove stand as shown in a previous study (Leopoldet al., 2013). The main objective of the present study was thus to inves-tigate changes in in situ diffusive CO2 fluxes at the sediment–air inter-face over time in a mangrove located in a semi-arid climate, taking thedevelopment of microphytobenthic biomass into account. To this end,wemeasured CO2fluxes during eightfieldtrips conducted in period rep-resentative of the changes in temperature and precipitation that occurthroughout the year. Fluxes were measured: i) in the dark in an opaqueincubation chamber, before and after removing the biofilm, since thebiofilm could influence fluxes, and ii) in the light in intact sedimentsin a transparent incubation chamber. We also evaluated the effectsof biotic and abiotic parameters (temperature, sediment water content,photosynthetically active radiation, chlorophyll-a) on CO2 emissionsfrom different mangrove sediments, as well as the effects of abioticparameters on the chlorophyll-a content used as a proxy to assess themicrophytobenthic biomass in each mangrove studied.

2. Material and methods

2.1. Study area

New Caledonia (NC) is an archipelago located in the southwesternpart of the Pacific Ocean. The main island is characterized by the world'slargest lagoon. Its climate is strongly influenced by the inter-tropical con-vergence zone (ITCZ), mean annual rainfall is 1100 mm and averagemonthly air temperatures range between 20 °C and 27 °C (MeteoFrance data). Thewest coast of themain islandhas a semi-arid tropical cli-mate. The lowest thermal amplitude and the highest temperatures occurfromDecember to February (i.e. in summer), and the highest thermal am-plitude and the lowest temperatures occur from July to September (i.e. inwinter). Tropical depressions can occur during summer, which is conse-quently the wet season. In New Caledonia, 24 mangrove species occupymore than 35,000 ha divided between around 9,000 ha of saltflats andSarcocornia salt marshes, and around 26,000 ha of tree and shrub stands.

Due to the coastal morphology, the great majority (88%) of mangroves islocated on the west coast, but biodiversity is higher on the east coastbecause it is less dry. Rhizophora spp. and Avicennia marina stands rep-resent respectively, 55% and 14% of the total mangrove area on the ar-chipelago (Virly, 2006). The mangrove stand we studied is located onthe west coast, in the estuary of the La Foa River (21°42′41″S; 165°49′06″E), with the typical zonation of New Caledonian mangroves, i.e.trees of the genus Rhizophora in the low intertidal zone, trees of thegenus Avicennia higher in the intertidal zone, and the saltflats in themost landward position (Fig. 1). The elevation of the sediment mainlydrives this distribution, as it defines both the length and the frequencyof tidal immersion and, as a consequence, pore water salinity(Marchand et al., 2011, 2012). The saltflats very rarely flooded, onlyduring spring tides, and their sediments can become very dry and cov-ered by a crystallized salt layer. The Avicennia stands are floodedwhen the tidal range is very high, whereas Rhizophora stands areflooded to a greater or lesser extent at each high tide. The tidal regimein NC is irregular semi-diurnal, and the maximum tidal range is1.70 m. The vegetation and sediment characteristics of each stand arelisted in Table 1. The La Foa river catchment covers 406 km2. The man-grove growing in the estuary covers more than 1000 ha (Fig. 1). Themean annual temperature in La Foa is 23.1 °C and mean annual rainfallis 928.5 mm (May 2009 to May 2012, Meteo France data).

2.2. CO2 flux measurements

CO2 fluxes were measured in the field at the sediment–air interfaceof the saltflat in the Avicennia and the Rhizophora stands during eightfieldtrips conducted between September 2010 and November 2011.Data from all the field trips are unfortunately not available for thethree mangrove stands due to instrument failure. During each fieldcampaign, fluxes were measured at four randomly selected sites ineach mangrove stand to account for intra-site spatial variability. Mea-surements were made from low tide and during the theoretical firststages of flooding between 11 am and 1 pm, to limit differencesbetween campaigns and stands due to putative daily variability. Sincethe level of the tide may influence CO2 diffusive fluxes from the sedi-ment, all our measurements were made at the same stage of the tidalcycle and at approximately the same stage of the diurnal cycle.

To measure CO2 fluxes at the sediment–air interface, a custom-builtsystem comprising a closed dynamic chamber (5,050 cm3; 455 cm2)coupled with a non-dispersive infrared gas analyzer (Li-820) wasused. Variations in CO2 partial pressure under the chambers were mea-sured during short incubation periods (from2min to 3 min). The cham-bers were placed in locations where there were no animals, animalburrows, litter fall or mangrove seedlings. However in the Avicenniastand, the locations of the chambers included a random number ofpneumatophores.

Sediment CO2 fluxes (F) were calculated as:

F ¼ δpCO2=δtð Þ � V=R:T :S

where F is the CO2 flux from the sediments (μmolCO2·m−2·s−1);δpCO2/δt is the variation in pCO2 as a function of the measurementtime (ppm·s−1), V is the total volume of the system (m3); R is theideal gas constant of 8,20528·10−05 (atm·m3·K−1·mol−1), T is theabsolute air temperature (K), and S is the surface area of the bottomof the incubation chamber (m2).

Two chambers were used: one was transparent and was equippedwith a photosynthetically active radiation (PAR) sensor, and one cham-ber was opaque. Three types of measurements were made: (i) on intactsediments in the dark in the opaque chamber (hereafter referred to as“dark flux”), (ii) in the light in the transparent chamber (hereafter re-ferred to as “light flux”), and (iii) in the dark in the opaque chamberafter having carefully removed the uppermost millimeters of surfacesediments (less than 2 mm) that may contain the microbial mat

Fig. 1.Map of the study area, (A) extent of each stand studied (saltflat, Avicennia sp., Rhizophora spp.) in the La Foa Mangrove; (B) satellite view (Google Earth©) of the study site.

619A. Leopold et al. / Science of the Total Environment 502 (2015) 617–626

(hereafter referred to as “without mat flux”). At each sampling site,each measurement was replicated three times to test measurementreproducibility. Benthic photosynthesis can take place in the transpar-ent chamber if autotrophic benthic organisms are developing there, assunlight reaches the sediment surface. Light measurements thus corre-spond to the net exchange between the soil and the atmosphere. In thedark, the measurement strategy enabled us to compare the magnitudeof the CO2 flux with and without biofilm but theoretically excludingmetabolism of photoautotrophic benthic species and to assess the roleof biofilm micro-organisms on diffusive CO2 fluxes.

2.3. Environmental parameters and sediment properties

Before each measurement of the CO2 flux, the air temperaturewas measured at a distance of 1.50 m from the sediment with a hand-held thermometer. Sediment temperatures are available only for thefinal surveys due to instrument failure. However, at low tide, there is adirect relationship between the temperature of the surface sediment,measured at a depth of 3 cm, and air temperature. Our data set showedstrong linear relationships between air and sediment temperatures. Therelationships we obtained were tair = 1.261·tsediment (R2adjusted (R

2a) =

99.5%, p b 0.001) for the saltflat, tair = 0.96·tsediment (R2a = 99.7%,

p b 0.001) for the Avicennia stand, and tair = 0.940·tsediment (R2a =

99.6%, p b 0.001) for the Rhizophora stand. Consequently, we trans-formed air temperature values into sediment temperature values to an-alyze the relationships between sediment CO2 fluxes and sedimenttemperatures (Lloyd and Taylor, 1994).

Sediment water contents (SWCs) and chlorophyll a (chl-a) contentsof surface sedimentswere determined in triplicate at each point the CO2

fluxwasmeasured. Percentage SWCwas estimated using the gravimet-ric method: sediment samples were weighed before and after lyophili-zation, sediment water contents correspond to the water weight loss.Chl-a content was used as an index for microphytobenthic biomass(MacIntyre et al., 1996), and was determined using the fluorescencemethod (Yentsch and Menzel, 1963).

2.4. Data analysis

A parametric two-way ANOVA (repeated measures effect) was usedto test the effect of the sampling site and month on CO2 fluxes for eachtype of flux separately, and their effect on abiotic and biotic parameters(Tair, chl-a, SWC). A one-way ANOVA (repeated measures) was used toidentify any differences in the different types of measurements eachmonth in each stand. If the ANOVA results were significant (p b 0.05),

Table 1Vegetation characteristics of the mangrove stands studied: biomass per area (Mg·ha−1),tree density (stem·ha−1), tree height (cm), and 13C isotopic value (‰) of leaves andwoodfrom Avicennia and Rhizophora trees. Sediment characteristics of mangrove standsstudied: bulk density (g.·cm−3), total carbon content (%), porewater salinity and redoxpotential (mV). The sediment characteristics are the mean of different samples analyzedin a core drilled to a depth of 50 cm. The δ13C values are the isotopic signatures of surfacesediments (‰). Values in brackets are the standard deviation (SD). n is the number ofsamples.

Saltflat Avicennia sp. Rhizophora spp.

Biomass (Mg·ha−1) – 54 (13) 92 (5)Basal stem density (N·ha−1) – 7168 (814) 3733 (37)Tree height (cm) –

Mean (SD) – 79 (55) 263 (42)Range (min–max) – 15 to 150 165 to 420

n sampled trees 215 112Root density (g.cm−3) –

Mean (SD) 15.7 (5.6) 42.2 (10.5)n sampled cores 26 39δ13C (‰)

Leaves (n = 12/stand) – −27.2 (0.43) −29.8 (0.14)Wood (n = 12/stand) – −26.6 (0.42) −30.3 (0.25)Surface sediments

(n = 16/stand)−23.9 (0.83) −25.9 (0.29) −27.2 (0.19)

Bulk density (g.cm−3)Mean (SD) 1.17 (0.11) 0.56 (0.1) 0.53 (0.06)

Total carbon (%)Mean (SD) 1.71 (0.77) 8.48 (3.88) 8.32 (2.6)Range (min–max) 0.49 to 2.95 2.54 to 17.53 4.02 to 15.06

n samples 30 30 30Porewater salinity(n = 60/stand)

Mean (SD) 55.37 (12.6) 53.4 (7.8) 39.35 (81)Range (min–max) 7 to 100 21 to 67 13 to 51

Redox potential (mV)Mean (SD) 75.6 (150.4) 1.4 (126.6) −86.9 (65.6)Range (min–max) −163 to +357 −136 to +343 −163 to +112

n samples 60 60 60

Table 2F values of two-way ANOVA tests showing the effect of sampling site and month on thedifferent types of CO2 fluxes and environmental parameters. *,**, and*** indicate statisti-cally significant effects for p-Values b0.05, b0.01 and b0.001, respectively. ns means nostatistically significant difference (p N 0.05).

Source of variation

Parameters Site Month Interaction

Dark CO2 fluxes 14.69*** 12.41*** 16.55***Light CO2 fluxes 18.68*** 25.59*** 15.59***Without mat CO2 fluxes 78.23*** 23.88*** 13.57***Tair 2.276ns 140.804*** 26.747***Tsediment 966.97*** 126*** 31.18***Chl-a 600.48*** 113.7*** 78.27***SWC 9332.5*** 156.8*** 154.4***

620 A. Leopold et al. / Science of the Total Environment 502 (2015) 617–626

a pairwise test was performed to see where the differences occurred.We first aimed to identify the individual factors responsible for theCO2 fluxes we measured by evaluating them against appropriatemeasured abiotic and/or biotic variables.We inspected all theunivariaterelationships graphically and determined that linear regressions wereappropriate for our range of data. We used the same protocol to studythe relationships between chl-a and abiotic parameters. The relation-ship between the dark CO2 fluxes (with and without biofilm) and airtemperature, from 25 °C to 35 °C, allowed us to estimate the Q10 ratiovalue. The Q10 ratio represents the sensitivity of a reaction to tempera-ture (for an increase of 10 °C) and is commonly used in global soil CO2

flux studies (Fang and Moncrieff, 2001; Xu and Qi, 2001; Janssens andPilegaard, 2003). Second, we analyzed the contribution of independentvariables to CO2 fluxes with stepwise multiple regressions based on theAkaike Information Criterion (AIC). Application conditions werechecked, especially the homoscedasticity of variances, and the residualnormality of the model was tested. All statistical tests were conductedwith R software (Version 2.15.1).

3. Results

3.1. Seasonal variations in biotic and abiotic parameters

Instantaneous air temperatures varied from 24 °C in August to 37 °Cin January, and followed the same trend as the air temperature curves inthis region, with the highest temperatures measured in January and thelowest in August, reflecting the New Caledonia climate (see ‘study area’section). Sediment temperature followed the same pattern of seasonalvariability in all the mangrove stands, with the lowest values measuredin winter, and the highest in summer. However, their magnitude varieddepending on the mangrove stand and showed a decreasing gradientfrom the saltflat to the Rhizophora stand over the year ranging from

30.5 °C to 43.5 °C in the saltflat, from 23 °C to 35.5° in the Avicenniastand, and from 23.8 °C to 35.1 °C in the Rhizophora stand. Thus, boththe sampling month and the interaction between the sampling monthand the site had a significant effect on both air and sediment tempera-tures (Table 2). These results and the relationships established betweenair and sediment temperatures (see the ‘Material andmethods’ section)indicated that at low tide, i.e., when the sediments were not floodedwith seawater, sediment temperature mainly depended on the degreeof canopy closure, which affected the amount of solar radiation receivedby the sediment: the more closed the canopy, the less direct sunlightreached the sediment, and hence the lower the temperature of thesediments.

Sedimentwater content (SWC) varied significantlywith the site andthe season, and their interaction (Table 2). Mean SWC values rangedfrom 2.5 ± 0.6% to 47.1 ± 2.8% in the saltflat, from 58.2 ± 5.2% to75.3 ± 3.0% in the Avicennia stand, and from 70.3 ± 1.5% to 77.2 ±0.3% in the Rhizophora stand (Table 4). Over all seasons, the SWCshowed an increasing gradient, and its range of variation showed adecreasing gradient from the saltflat to the Rhizophora stand. In April,SWC was lowest in the saltflat and in the Avicennia stand, and highestin the Rhizophora stand (Table 4).

Chlorophyll a contents of surface sediments varied significantly bothwith the site and the samplingmonth, and the interaction between thesetwoparameterswas also significant (Table 2).Minimumchl-a content inthe saltflat was 2.1 ± 1.1 μg·g−1 in April 2011 and maximum was20.8± 3.0 μg·g−1 in September 2010. The chl-a content in the Avicenniastand ranged from 28.5 ± 5.0 in April to 199.4 ± 13.5 μg·g−1 in January2011. Chl-a content in the Rhizophora stand ranged from 45 ± 3.5 inApril to 117.9 ± 32.2 μg·g−1 in August 2011 (Table 4). Like chl-a con-tents, the lowest % of active chl-a was measured in all the mangrovestands in April 2011 (Table 4). The chl-a content in the Avicenniastand sediments varied significantly and positively with SWC, Tairand PAR (R2a = 84.8%, p b 0.001), even though SWC alone accountedfor over 44% of the explained variance in this model. SWC was theonly significant variable in the saltflat and in the Rhizophora stand,where it explained 65% (p b 0.001) and 21.8% (p b 0.001) of chl-avariance, respectively. However, the relationship between these twoparameters was negative in the Rhizophora stand.

3.2. Seasonal variations in in situ diffusive CO2 fluxes

Both sampling sites and months had a significant effect on CO2

fluxes, for all types of measurement considered, and the interaction be-tween these two parameters was also significant (Table 2). CO2 fluxesshowed significant seasonal variations (p b 0.001, for all) in each man-grove stand. Moreover, the differences between the types of measure-ments varied with the sampling month with a particular patternobserved in each stand (Fig. 2).

Considering thewhole set of measurements, CO2 fluxes ranged from−3.93 mmolCO2·m−2·h−1 to 17.97 mmolCO2·m−2·h−1 (Table 3).Focusing on the measurements made on intact sediments both in the

Table 3Range of sediment CO2fluxvalues (minimumandmaximumvalues) in each stand studiedand for each type of measurement made (mmolCO2·m−2·h−1).

Sediment CO2 fluxes (mmolCO2·m−2·h−1)

“Dark” “Light” “Without mat”

Min Max Min Max Min Max

Saltflat −2.59 7.66 −3.93 5.69 0.11 10.36Avicennia sp. −0.72 8.85 −3.31 6.42 1.40 17.58Rhizophora spp. 0.10 7.17 −1.06 4.86 2.87 17.97

621A. Leopold et al. / Science of the Total Environment 502 (2015) 617–626

light and in the dark, CO2 fluxes in the Avicennia stand and the saltflatfollowed the same seasonal pattern: the lowest fluxes were measuredin January 2011 (in summer) (Fig. 2A, B). CO2 fluxes in the Rhizophorastand displayed the opposite trend (Fig.2C), i.e. the lowest fluxes weremeasured in August 2011 (in winter). However, without the biofilm,the highest CO2 fluxes were measured during the warmer period in allthe mangrove stands (Fig. 2).

3.3. Relationships between CO2 fluxes and biotic/abiotic parameters

Principal component analysis (PCA) enabled us to view the magni-tude and the direction of correlations between both dependent(“Dark”, “Light” and “Without mat” CO2 fluxes) and independent(SWC, Ts, Chl-a and PAR) variables (Fig. 3). Strong correlations werefound between variables and the two first axes, and between thevariables themselves in the saltflat (Fig. 3A), but particularly in theAvicennia stand (Fig. 3B) and the Rhizophora stand (Fig. 3C).Multiple re-gression analyses identified the independent variables that significantlyinfluenced the CO2 fluxes. In the dark, on intact sediments, theseanalyses showed that SWC, sediment temperature, and the number ofpneumatophores affected CO2 fluxes from Avicennia stand sediments(R2a = 57.6%, p b 0.001). SWC and sediment temperature explainedmore than 44% of the dark CO2 fluxes from the Rhizophora stand

Table 4Water (%) and chlorophyll a contents (quantity, μg·g−1 and proportion of active Chl a, %)of surface sediments in each stand and each samplingmonth. sd is the standard deviation.

SedimentaryChl-a

ActivesedimentaryChl-a

Sediment watercontent

μg.g−1 % %

Saltflat

Mean sd Mean sd Mean sd

Sept-10 20.8 3.0 72.6 0.6 47.1 2.8Oct-10 8.0 2.0 77.5 3.3 25.1 1.3Jan-11 14.8 4.6 90.1 2.6 29.7 2.0Mar-11 13.6 4.8 90.6 1.2 30.2 5.8Apr-11 2.1 1.1 68.3 7.1 2.5 0.6Aug-11 12.9 3.8 88.4 1.6 18.9 6.9Nov-11 na na na na 18.4 1.7

Avicennia sp.Oct-10 62.9 11.4 88.4 2.4 61.3 1.6Jan-11 199.3 13.5 89.3 1.7 75.3 3.0Mar-11 39.2 7.0 74.5 5.3 58.9 2.0Apr-11 28.5 5.0 58.3 5.2 58.2 5.2Aug-11 94.8 23.2 81.6 3.4 59.1 1.8Sept-11 126.5 3.4 77.4 5.8 60.9 0.7Nov-11 68.6 14.3 79.2 4.3 68.8 0.4

Rhizophoras pp.Oct-10 56.8 15.5 91.4 3.1 72.2 0.8Jan-11 65.3 24.3 88.2 3.7 76.7 0.6Apr-11 45.0 3.47 74.8 4.8 77.2 0.3Aug-11 117.9 32.2 80.2 5.6 70.9 1.5Sept-11 109.9 31.3 75.6 4.5 71.0 0.4Nov-11 85.2 12.8 76.3 2.4 74.3 0.8

Fig. 2. CO2 fluxes measured at the sediment–air interface (mean ± SD,mmolCO2·m−2·h−1) in the saltflat (A), the Avicennia stand (B) and the Rhizophorastand (C) for the different months. The color of the bars indicates the type ofmeasurement: in the dark (black bar), in the light (white bar), in the dark without thebiofilm (gray). Mean values were obtained from the measurements made at four pointsin each stand eachmonth. The vertical black bars represent the standard deviation. Lettersabove the error bars indicate statistically significant differences between the types ofmeasurements in the same month (for a p-Value b 0.05, one-way repeated measuresANOVA). ns means no significant difference (p-Value N 0.05).

sediments (p b 0.001). SWC, sediment temperature, and chl-a ex-plained more than 45% of the flux variance (p b 0.01) in the saltflat.However, it should be noted that even if other variables were selectedstepwise, SWC was the variable that explained the most variance in allcases. In the light, SWC, chl-a, sediment temperature, the number ofpneumatophores, and PAR explained more than 78% of variance in theCO2 flux from the Avicennia stand. The same variables (chl-a, SWC, sed-iment temperature, and PAR) explained more than 54% of variance inthe CO2 flux from sediments in the Rhizophora stand, whereas chl-a,SWC and sediment temperature explained 58.4% of CO2 flux variancefrom the saltflat (p b 0.001, for all). Finally, in the dark without the bio-film, sediment temperature explained more than 47% of variance in theCO2 flux from the Rhizophora stand. SWC, sediment temperature, andthe number of pneumatophores explained more than 65% of variance

622 A. Leopold et al. / Science of the Total Environment 502 (2015) 617–626

in the CO2 flux from the sediment in the Avicennia stand. In the saltflat,SWC was the only significant variable, and explained more than 37% ofvariance in the “without mat” CO2 flux (p b 0.001, for all).

Fig. 4. Sediment CO2 fluxes (mmolCO2·m−2·h−1) per month measured in the light vs. inthe dark, both on intact sediments, in the saltflat (A), the Avicennia stand (B) and theRhizophora stand (C). The linear models in the graphs were plotted from the followinglinear relationships: Y = 0.8511. X (R2 = 93.5%, p b 0.001) for the saltflat, Y = 0.7897.X (R2 = 85.3%, p b 0.001) for the Avicennia stand, and Y = 0.6258. X (R2 = 90%,p b 0.001) for the Rhizophora stand (R2a = 0.8975, p b 0.001). Y is the CO2 flux fromthe sediment in the light, and X is the CO2 flux from the sediment in the dark (bothwith biofilm). The standard deviation error bars were removed to make the differentmeasurement points per month easier to see.

3.4. Comparison of different types of CO2 fluxes

In addition to following the same seasonal pattern, the dark and lightCO2 fluxesmeasured on intact sedimentswere linearly correlated in thesaltflat (Eq. (2.1)), the Avicennia (Eq. (2.2)) and the Rhizophora stands(Eq. (2.3)). The slopes of these relationships showed a decreasinggradient from the saltflat to the Rhizophora stand (Fig. 4):

Light CO2flux ¼ 0:8511: Dark CO2flux R2 ¼ 93:5%;pb0:001� �

ð2:1Þ

Fig. 3. Centered and normalized results of principal component analysis showing themagnitude and the direction of correlations between the different dependent variables(“Dark”, “Light” and “Withoutmat” CO2 fluxes) and independent variables (sediment wa-ter content: SWC, sediment temperature: Ts, chlorophyll a content: Chl a, photosyntheti-cally active radiation: PAR, and number of pneumatophores: Npneuma), in the saltflat (A),the Avicennia stand (B) and the Rhizophora stand (C) according to the two first axes. Thecorrelation circle was drawn to make it easier to see the correlations.

Fig. 5. Ratios between CO2 fluxes measured on intact sediments (both in the dark (graybars) and in the light (white bars)), and CO2 measured after the removal of biofilm, inthe saltflat (A), the Avicennia stand (B) and the Rhizophora stand (C). A ratio value of 1(horizontal gray line) means there were no statistically significant differences betweenthe two types of measurements. The vertical gray bars represent the standard deviation.

623A. Leopold et al. / Science of the Total Environment 502 (2015) 617–626

Light CO2flux ¼ 0:7897: Dark CO2flux R2 ¼ 85:3%;pb0:001� �

ð2:2Þ

Light CO2flux ¼ 0:6258: Dark CO2flux R2 ¼ 90:0%;pb0:001� �

: ð2:3Þ

CO2 fluxesmeasuredwithout themat did not follow the same trend.For that reason, we analyzed the ratio between CO2 fluxes with andwithout the biofilm in the dark and in the light to assess the differencein the magnitude of the fluxes (Fig. 5). The “dark” ratio (the ratio ofdark fluxes from intact sediments to fluxes from sediments withoutthe biofilm) ranged from −3.9 to 1.0 in the saltflat, from 0.16 to 0.89in the Avicennia stand and from 0.21 to 0.73 in the Rhizophora stand.The “light” ratio (the ratio of light fluxes on intact sediments to fluxesfrom sediments without the biofilm) ranged from −5.8 to 1 in thesaltflat, from −0.03 to −0.85 in the Avicennia stand, and from 0.14 to

0.39 in the Rhizophora stand. These ratios showed a decreasing gradientof variation from the saltflat to the Rhizophora stand. In the saltflat, theratioswere often close to 1 except in September and January, when theywere negative both in the dark and in the light (Fig. 5). In the Avicenniastand, the ratios were close to 1 only in April and August, while in theRhizophora stand, the ratios were never close to 1 at any point in theyear.

4. Discussion

4.1. Mangrove sediments as a low direct source of CO2 for the atmosphere

CO2 fluxes measured at the sediment–air interface in the dark onintact sediments in all the mangrove stands throughout the yearranged between −0.71 and 2.41 mmolC·m−2·h−1 (Table 5). Thesevalues are lower than those measured in other forest ecosystems inboth tropical and temperate regions (Table 5), but are of the sameorder of magnitude as those measured in wetland forests and othermangrove systems (Table 5). All these results confirm that even ifmangroves are characterized by high NPP and by high sedimentary or-ganic carbon contents (Kristensen, 2007; Bouillon et al., 2008), theirsediments are a low direct source of CO2 for the atmosphere comparedto other forest soils. However, these measurements do not account forthe fact that part of the mangrove NPP can be mineralized and/oremitted toward the atmosphere as CO2 after export to adjacentecosystems.

4.2. Temporal variability of CO2 fluxes in the absence of biofilm: the respectiveinfluence of temperature and SWC differed with the stand

In mangrove ecosystems, the temperature is considered to be themost important factor driving seasonal variations in CO2 fluxes undersubtropical climates (Chen et al., 2012; Livesley and Andrusiak, 2012;Chanda et al., 2013), whereas at tropical latitudes, soil moisture maybe the most important determining factor as a result of the limited var-iation in temperature between seasons (Kirui et al., 2009; Poungparnet al., 2009). New Caledonia has a sub-tropical climate with a pro-nounced semi-arid character on thewest coast. Consequently, both sed-iment temperature and humidity vary considerably throughout the year(Table 4), andmay have influenced the seasonal variations in CO2 fluxeswe observed (Fig. 2, Table 2). Without the biofilm, temperature was themain driving factor of the seasonal variations in CO2 fluxes in theRhizophora and Avicennia stands. Thus Q10 values for the Avicennia andtheRhizophora standswere 1.84 and 2.52, respectively. TheseQ10 valuesare close to those computed by Lovelock (2008) (2.6) in a set of man-groves growing between latitude 27°N and 37°S, as well as the medianvalue (2.4) estimated for different terrestrial ecosystems (Raich andSchlesinger, 1992), and confirmed that, in the absence of biofilm,mangrove sediments are potentially as sensitive to temperature asother ecosystems.

Because of the intertidal location of ourmangrove ecosystem, SWC iscontrolled by rainfall and by the tidal cycle, i.e. by flood length and fre-quency. It is consequently difficult tomeasure the exact influence of theseasonal rainfall pattern on seasonal variations in the CO2 flux at thesediment–air interface inmangroves. However, SWC showed a decreas-ing gradient and an increasing range of variation from the seaward tothe landward side of the mangrove, suggesting increasing influence ofrainfall on SWC from the Rhizophora stand to the saltflat (Table 4).Although temperature had no effect on the sediment CO2 fluxesfrom the saltflat, their seasonal variations were linked to SWC, andthis parameter also influenced seasonal variations in the CO2 flux inthe Avicennia stand. The different influence of temperature and SWCon the temporal dynamics of CO2 fluxes in each stand depended onthe location of the stand along the topographic gradient: the lower thelevel of hydration over the course of the year, i.e. the lower the intertidallocation, the greater the sensitivity of the mangrove sediment to

Table 5Range of CO2 fluxes (mmolC·m−2·h−1) measured at the sediment–air interface in mangroves growing at different latitudes and at the soil–air interface in forests. Results of the presentstudy are in boldface.

Ecosystems Study sites CO2 fluxes(mmolC·m−2·h−1)

References

Mangroves Semi-arid mangroves (New Caledonia)“Dark fluxes” −0.71 2.41 This study“Light fluxes” −1.07 1.75 This study

Data compilation from mangroves 0.25 10.04 Bouillon et al., 2008“Dark fluxes” 2.54 ± 1.92“Light fluxes” −0.63 ± 2.25

Tropical mangrove (India) 0.15 2.32 Chanda et al., 2013Subtropical mangrove (China) 0.69 20.56 Chen et al., 2010Subtropical mangrove (China) 0.24 31.23 Chen et al., 2012Tropical mangrove (Indonesia) −1.34 3.88 Chen et al., 2014Subtropical mangrove (China) 0.35 6.05 Jin et al., 2013Tropical mangrove (Tanzania) 1.17 4.67 Kristensen et al., 2011Varied mangroves (Caribbean, Australia, New-Zealand) −0.97 10.69 Lovelock, 2008; Lovelock et al., 2014Tropical mangrove (Thailand) 1.67 3.21 Poungparn et al., 2009

Wetland forests Subtropical wetland forest (Georgia, USA) 1.26 4.94 Krauss and Withbeck, 2012Temperate wetland forest (New York, USA) −1.54 5.75 Miller et al., 1999

Tropical and temperate forests Temperate beech forest (France) 1.80 14.4 Epron et al., 1999Tropical rainforest (Malaysia) 20.5 21.6 Katayama et al., 2009Tropical wet forest (Hawaï) 12.30 21.4 Litton et al., 2011Tropical rainforest (Amazon) 12.40 16.2 Metcalfe et al., 2007Temperate spruce forest (Germany) 1.55 18.54 Subke et al., 2003Temperate deciduous forest (France) 3.60 36.0 Vincent et al., 2006

624 A. Leopold et al. / Science of the Total Environment 502 (2015) 617–626

temperature. Thus, authors shown that temperature sensitivity in-creases as inundation is prolonged, and obtained Q10 values (between23 °C and 27 °C) in Avicennia germinans stand greater for soils with20-hr hydroperiods (Q10 value = 3.40) than for soils with 4-hrhydroperiods (Q10 = 1.50) (Lewis et al., 2014). Moreover, it shouldalso be noted that the autotrophic respiration component of foreststands, i.e. the Avicennia and Rhizophora stands, may be also involvedin seasonal variations in CO2 fluxes, because of the higher sensitivityof roots to temperature than that of bulk soil (Boone et al., 1998).

4.3. Temporal variability of CO2 fluxes on intact sediments: influence ofbiofilm development

For intact sediments, the Q10 values computed were 0.7, 0.6 and 2.3in the saltflat, the Avicennia and the Rhizophora stands, respectively. Forthe saltflat and the Avicennia stand, these values, lower than 1, revealeda decrease in CO2 fluxes with an increase in temperature. Indeed, thesevalues were therefore the opposite of those computed without biofilmand what is usually described in the literature, i.e. an increase in CO2

fluxes with increasing temperature (e.g. Chen et al., 2012; Livesleyand Andrusiak, 2012). Lovelock (2008) showed that soil respirationdeclined when the soil temperature was above 26 °C. In sparse dwarfcanopies, direct sunlight warms the sediment surface and stimulatesgrowth of the biofilm (Lovelock, 2008; Molnar et al., 2014), and as aconsequence enhances the activity of photosynthetic benthic microbialcommunities. However, for intact sediments, the effect of SWC on thetemporal dynamics of CO2 fluxes appeared to be greater than that oftemperature. On the one hand, CO2 fluxes depend on soil humidity, be-cause this influences the activity of both autotrophic and heterotrophicorganisms, as well as gas diffusivity (Bridgham and Richardson, 1992;Davidson et al., 2000; Chimner and Cooper, 2003; Vincent et al.,2006). On the other hand, SWC influences the growth, biomass, andmetabolic activity of the biofilm (Coelho et al., 2009; Rajeev et al.,2013; Strong et al., 2013). In the present study, biofilm, measured aschl-a content, varied with the season and a different pattern was ob-served in each mangrove stand, but in all the stands, SWC was clearlya major driving factor of the seasonal development of the biofilm. Sea-sonal variations in CO2fluxes, both in the dark and in the light, appearedto be closely linked to the seasonal development of the biofilm (Figs. 2,3, Table 4). In the dark, the temporal dynamics of the CO2 fluxes was

correlated with the variables that explained chl-a content, mainlySWC; whereas in the light, the temporal dynamics of CO2 fluxes waslinked to, on the one hand, the variables that explained the quantity ofchl-a, and on the other hand, chl-a itself (Fig. 3, result section). Whenthe quantity of primary producers (chl-a biomass) increased, the auto-trophicmetabolism rate increased, and CO2 fluxes decreased.Moreover,throughout the year, light CO2 fluxes were equivalent to 85%, 79% and63% of dark CO2 fluxes in the saltflat, the Avicennia stand and theRhizophora stand, respectively. This increasing gradient of differencesbetween light and dark CO2 fluxes from the landside to the seasidecorresponds to an increasing gradient in the level of hydration and adecreasing in the length of time sediments are desiccated. Other authorshave also shown that hydration is important for the activity ofcyanobacteria soil crusts (Thomas et al., 2011; Rajeev et al., 2013;Strong et al., 2013). Indeed, the net photosynthesis in response totemperature and photon flux density has been shown to depend onthe degree of hydration of a soil biological crust (Lange et al., 1998).Our results are in agreement with the results of these studies. Previous-ly, we showed that the Avicennia stand had the highest chl-a content,notably because of the absence of light stress compared to theRhizophora stand, and to the relative absence of desiccation comparedto the saltflat (Leopold et al., 2013). However, differences betweenlight and dark measurements were greatest in the Rhizophora stand,suggesting a very strong effect of the level of hydration (in terms ofamplitude and duration), supported by the hypothesis that the shorterthe dry phase, the faster the activation of photosynthetic capability inthe wet phase (see Strong et al., 2013).

The influence of both the quantity and quality of the biofilm on thetemporal dynamics of CO2 fluxes was also confirmed by the ratios offluxesmeasured with andwithout biofilm. The “dark” ratio was highestin April when chl-a contents and the proportion of active chl-a werelowest in all themangrove stands (Table 4; Fig. 5). Conversely, these ra-tios were lowest when chl-a contents and/or the proportion of activechl-a were highest (Table 4; Fig. 5). These results indicate that themore developed the biofilm, the greater its photosynthetic capability,and the bigger the difference between fluxes with and without biofilm.We can thus conclude that (1) the biofilm represents a significant activebiological interface between the sediment surface and the atmosphereand (2) the temporal dynamics of the CO2 flux from intact sedimentsis linked to the growth and metabolism of biofilm organisms.

625A. Leopold et al. / Science of the Total Environment 502 (2015) 617–626

4.4. Intermittent uptake of CO2 by mangrove sediments

Ratios of CO2 fluxes measured with and without the biofilm weresometimes negative both in the dark and in the light, indicating CO2 up-take by sediments (Fig. 5). Negative light ratios indicate that net photo-synthesis is higher than total respiration. Moreover, CO2 uptake bysediments even occurred in the dark, as negative dark ratios were alsomeasured. Similar observations have beenmade both in freshwater for-ests and mangroves (Miller et al., 1999; Lovelock, 2008; Krauss andWhitbeck, 2012). Some authors suggested a putative role for ebb withhigh tidal range (Krauss and Withbeck, 2012), while others showedthat part of this uptakewas related to diffusion and dissolution process-es driven by soil pH and moisture (Ma et al., 2013). In our study, sinceCO2 fluxes were positive after biofilm removal, we suggest that this up-take is linked to biofilm organismmetabolisms. Wolhfhart et al. (2008)described uptake of CO2 into the soil via the metabolism of the photo-synthetic crust organisms in a desert ecosystem. In the dark, this uptakemay also be linked to chemoautotrophic organisms, which has alreadybeen suspected or observed in mangrove sediments (Kristensen et al.,1991; Lee, 2006). However, it is also possible that this CO2 uptake result-ed from a methodological problem linked to the duration of incubationand the fact that photosynthesis could continue until coenzymes(NADPH, ATP) were lacking. In the latter case, some authors recom-mend extending the incubation time to reach the physiological steadystate of benthic organisms (Migné et al., 2002). However, given thehigh relative humidity of the air and of the sediment, and the high tem-perature and irradiance in our mangrove systems, especially in thesaltflat and the Avicennia stand, it is likely that extended incubationtimes would alter the ambient conditions in the enclosure too much,and as a consequence would also modify the CO2 diffusion gradient aswell as the rates of metabolism. Whatever, Castillo-Monroy et al.(2011) showed net CO2 uptakes during specific short intervals butindicated that conditions under which the soil biological crusts formare net carbon sinks or largely unknown sources, and with our dataset, we cannot draw any firm conclusions concerning the physiologicaland/or abiotic/biotic conditions required for such uptake.

5. Conclusions

CO2 fluxes at the sediment–air interface were relatively lowthroughout the year but seasonal variations were nevertheless ob-served. We suggest that the seasonal variations in CO2 fluxes weremainly linked to the seasonal development of biofilm, notably photoau-totrophic organisms at the sediment surface. Temperature and especial-ly sediment water content appeared to be key factors in both thequantity and the quality of the biofilm, and likely influence sedimentaryrespiration through their influence on mangrove roots and on the me-tabolism of the heterotrophic organisms in the sediment. Favorable en-vironmental conditions for the production of CO2 through heterotrophicand autotrophic respirationmay favor growth of the biofilm. The devel-opment of a biofilm that results in a reduction in CO2 fluxes toward theatmosphere, or in the uptake of CO2 into the sediment, increases theability of mangrove ecosystems to be a sink for atmospheric CO2. Wesuggest that more attention should be paid to its composition and tothe metabolism of the organisms that compose it, in order to improveour knowledge of its role in mangrove carbon cycling. From a method-ological point of view, it would be necessary to assess biofilm metabo-lism in situ to accurately estimate CO2 fluxes from backgroundmangrove sediments, since, even in the dark, CO2 fluxes may be linkedto the metabolism of biofilm organisms. Without taking the biofilminto account, and irrespective of the length of incubation or the typeof measurement (dark vs. light), it is likely that in situ CO2 fluxes reflectthe metabolism of the biofilm organisms rather than the autotrophicand heterotrophic components of the sedimentary column. Not takingthis component into account could lead to significant underestimation

of CO2 production linked to heterotrophic respiration fueled by man-grove organic matter, and thus to imprecise mangrove carbon budgets.

6. Acknowledgments

This work was supported by the “Air Liquide Foundation” and“Fonds Pacifiques”. We thank Gladwys Toulemonde, Magali Teurlai,ChristopheMenkes, and MorganMangeas for help and advice with sta-tistics. We thank Corinne Voisin, the Mayor of La Foa, and Jean-PierreLafay for their logistic support, and “Météo France Nouvelle-Calédonie” for the weather data. The help of anonymous reviewers inimproving the ms. is gratefully acknowledged.

References

Alongi DM, Wattayakorn G, Pfitzner J, Tirendi F, Zagorkis I, Brunskill GJ, et al. Organiccarbon accumulation and metabolic pathways in sediments of mangrove forests insouthern Thailand. Mar Geol 2001;179:85–103.

Alongi DM, de Cavarlho NA, Amaral AL, da Costa A, Trott L, Tirendi F. Uncoupled surfaceand below-ground soil respiration in mangroves: implications for estimates ofdissolved inorganic export. Biogeochemistry 2012;109:151–62.

Boone RD, Nadelhoffer KJ, Canary JD, Kaye JP. Roots exert a strong influence on thetemperature sensitivity of soil respiration. Nature 1998;396:570–2.

Bouillon S, Borges AV, Castaneda-Moya E, Diele K, Dittmar T, Duke NC, et al. Mangroveproduction and carbon sinks: a revision of global budget estimates. GlobalBiogeochem Cycles 2008;22. [GB2013].

Bridgham SD, Richardson CJ. Mechanisms controlling soil respiration (CO2 and CH4) inSouthern peatlands. Soil Biol Biochem 1992;24:1089–99.

Castillo-Monroy AP, Maestre FT, Rey A, Soliveres S, García-Palacios P. Biological soil crustmicrosites are the main contributor to soil respiration in a semiarid ecosystem.Ecosystems 2011;14:835–47.

Chanda A, Akhand A, Manna S, Dutta S, Das I, Hazra S, et al. Measuring daytime CO2 fluxesfrom the inter-tidal mangrove soils of Indian Sundarbans. Environ Earth Sci 2013.http://dx.doi.org/10.1007/s12665-013-2962-2.

Chen GC, Tam NFY, Ye Y. Summer fluxes of atmospheric greenhouse gases N2O, CH4 andCO2 from mangrove soil in South China. Sci Total Environ 2010;408:2761-2737.

Chen GC, Tam NFY, Ye Y. Spatial and seasonal variations of atmospheric N2O and CO2

fluxes from a subtropical mangrove swamp and their relationships with soil charac-teristics. Soil Biol Biochem 2012;48:175–81.

Chen GC, Ulumuddin YI, Pramudji S, Chen SY, Chen B, Ye Y, et al. Rich soil carbon andnitrogen but low atmospheric greenhouse gas fluxes from North Sulawesi mangroveswamps in Indonesia. Sci Total Environ 2014;487:91–6.

Chimner RA, Cooper DJ. Influence of water table levels on CO2 emissions in a Coloradosubalpine fen: an in situ microcosm study. Soil Biol Biochem 2003;35:345–51.

Chmura GL, Anisfeld SC, Cahoon DR, Lynch JC. Global carbon sequestration in tidal, salinewetland soils. Global Biogeochem Cycles 2003;17:1111.

Coelho H, Vieira S, Serôdio J. Effects on dessication on the photosynthetic activity of inter-tidal microphytobenthos biofilm as studied by optical method. J Exp Mar Biol Ecol2009;381:98–104.

Davidson EA, Verchot LV, Henrique Cattânio J, Ackerman IL, Carvalho JEM. Effects on soilwater content on soil respiration in forests and cattle pastures of eastern Amazonia.Biogeochemistry 2000;48:53–69.

Dixon RK, Brown S, Houghton RA, Solornon AM, Trexler MC, Wisniewski J. Carbon poolsand flux of global forest ecosystems. Science 1994;263:185–90.

Donato DC, Kauffman JB, Murdiyarso D, Kurnianto S, Stidham M, Kanninen M. Mangroveamong the most carbon-rich forests in the tropics. Nat Geosci 2011;4:293–7.

Duke NC, Ball MC, Ellison JC. Factors influencing biodiversity and distributional gradientsin mangroves. Glob Ecol Biogeogr 1998;7:27–47.

Epron D, Farque L, Lucot É, Badot PM. Soil CO2 efflux in a beech forest: dependence on soiltemperature and soil water content. Ann For Sci 1999;56:221–6.

Fang C, Moncrieff JB. The dependence of soil CO2 efflux on temperature. Soil Biol Biochem2001;33:155–65.

Giri C, Ochieng E, Tieszen LL, Zhu Z, Singh A, Loveland T, et al. Status and distribution ofmangrove forests of the world using earth observation satellite data. Glob EcolBiogeogr 2011;20:154–9.

IPCC, Intergovernmental Panel on Climate Change. Fourth assessment report: synthesisreport; 2007. p. 104 [Geneva, Switzerland].

Janssens IA, Pilegaard K. Large seasonal changes in Q10 of soil respiration in a beechforest. Glob Chang Biol 2003;9:911–8.

Jin L, Lu CY, Ye Y, Ye GF. Soil respiration in a subtropical mangrove wetland in the JiulongRiver Estuary, China. Pedosphere 2013;23(5):678–85.

Katayama A, Kume T, Komatsu H, Ohashi M, Nakagawa M, Yamashita M, et al. Effect offorest structure on the spatial variation in soil respiration in a Bornean tropicalrainforest. Agr Forest Meteorol 2009;149:1666–73.

Kauffman JB, Heider C, Cole TG, Dwire KA, Donato DC. Ecosystem carbon stocks ofMicronesian mangrove forests. Wetlands 2011;31:343–52.

Kirui B, Huxham M, Kairo GJ, Mencuccini M, Skov MW. Seasonal dynamics of soil carbondioxide flux in a restored young mangrove plantation at Gazi Bay. In: Hoorweg J,Muthiga N, editors. Advances in Coastal Ecology: People, Processes and Ecosystemsin Kenya. Leiden, Netherlands: African Studies Centre; 2009.

Krauss KW, Whitbeck JL. Soil greenhouse gas fluxes during wetland forest retreat alongthe lower Savannah River, Gerogia (USA). Wetlands 2012;32:73–81.

626 A. Leopold et al. / Science of the Total Environment 502 (2015) 617–626

Kristensen E. Carbon balance in mangrove sediments: the driving processes and theircontrols. In: Tateda Y, et al, editors. Greenhouse gas and carbon balances inmangrovecoastal ecosystems. Japan: Gendai Tosho Kanagawa Japan; 2007. p. 61–78.

Kristensen E, Holmer M, Busarawit N. Benthic metabolism and sulfate reduction in asoutheast Asian mangrove swamp. Mar Ecol Prog Ser 1991;73:93–103.

Kristensen E, Bouillon S, Dittmar T, Marchand C. Organic carbon dynamics in mangroveecosystems: a review. Aquat Bot 2008;89:201–19.

Kristensen E, Mangion P, Tang M, Flindt MR, Holmer M, Ulomi S. Microbial carbonoxidation rates and pathways in sediments of two Tanzanian mangrove forests.Biogeochemistry 2011;103:143–58.

Lange OL, Belnap J, Reichenberger H. Photosynthesis of the cyanobacterial soil-crustlichen Collema tenax from arid lands in southern Utah, USA: role of water contenton light and temperature responses of CO2 exchange. Funct Ecol 1998;12:195–202.

Lee RY. Primary production, nitrogen cycling and the ecosystem role of mangrove micro-bial mats on Twin Cays, Belize. Dissertation University of Georgia; 2006 [150 pp.].

Lee SY, Primavera JH, Dahdouh-Guebas F, McKee K, Bosire JO, Cannicci S, et al. Ecologicalrole and services of tropical mangrove ecosystems: a reassessment. Glob EcolBiogeogr 2014. http://dx.doi.org/10.1111/geb.12155.

Leopold A, Marchand C, Deborde J, Chaduteau C, Allenbach M. Influence of mangrovezonation on CO2 fluxes at the sediment–air interface (New Caledonia). Geoderma2013;202–203:62–70.

Lewis DB, Brown JA, Jimenez KL. Effects of flooding and warming on soil organic mattermineralization in Avicennia germinans mangrove forests and Juncus roemerianus saltmarshes. Estuar Coast Shelf Sci 2014;139:11–9.

Litton CM, Giardina CP, Albano JK, Long MS, Asner GP. The magnitude and variability ofsoil-surface CO2 efflux increase with mean annual temperature in Hawaiian tropicalmontane wet forests. Soil Biol Biochem 2011;43:2315–23.

Livesley SJ, Andrusiak SM. Temperate mangrove and salt marsh sediments are a smallmethane and nitrous oxide source but important carbon store. Estuar Coast ShelfSci 2012;97:19–27.

Lloyd J, Taylor JA. On the temperature dependence of soil respiration. Funct Ecol 1994;8:315–23.

Lovelock CE. Soil respiration and belowground carbon allocation in mangrove forests.Ecosystems 2008;11:342–54.

Lovelock CE, Feller IC, Reef R, Ruess RW. Variable effects of nutrient enrichment on soilrespiration in mangrove forests. Plant and Soil 2014;379:135–48.

Ma J, Wang ZY, Stevenson BA, Zheng XJ, Li Y. An inorganic CO2 diffusion and dissolutionprocess explains negative CO2 fluxes in saline/alkaline soils. Sci Rep 2013;3:2025.

MacIntyre HL, Geider RJ, Miller DC. Microphytobenthos: the ecological role of the “secretgarden” of unvegetated, shallow-water marine habitats. I. Distribution, abundanceand primary production. Estuaries 1996;19:186–201.

Maher DT, Santos IR, Golsby-Smith L, Gleeson J, Eyre BD. Groundwater-derived dissolvedinorganic and organic carbon exports from a mangrove tidal creek: the missingmangrove organic sink? Limnol Oceanogr 2013;58:457–88.

Marchand C, Allenbach M, Lallier-Vergès E. Relationship between heavy metals distribu-tion and organic matter cycling in mangrove sediments (Conception Bay, NewCaledonia). Geoderma 2011;160:444–56.

Marchand C, Fernandez J, Moreton B, Landi L, Lallier-vergès E, Baltzer F. The partitioningof transitional metals (Fe, Mn, Ni, Cr) in mangrove sediments downstream of aferralitized ultramafic watershed (New Caledonia). ChemGeol 2012;300–301:70–80.

Metcalfe DB, Meir P, Aragão LEOC, Malhi Y, da Costa ACL, Braga A, et al. Factors controllingspatio-temporal variation in carbon dioxide efflux from surface litter, roots, and soilorganic matter at four rain forest sites in the eastern Amazon. J Geophys Res 2007;112:G04001.

Migne A, Davoult D, Spilmont N, Menu D, Boucher G, Gattuso JP, et al. A closed-chamberCO2 flux method for estimating intertidal primary production and respiration underemersed conditions. Mar Biol 2002;140:865–9.

Miller DN, Ghiorse WC, Yavitt JB. Seasonal patterns and controls on methane and carbonfluxes in forested swamp pools. Geomicrobiol J 1999;16:352-331.

Molnar N, Marchand C, Deborde J, Patrona LD, Meziane T. Seasonal Pattern of the Biogeo-chemical Properties of Mangrove Sediments Receiving Shrimp Farm Effluents (NewCaledonia). J Aquac Res Dev 2014;5:262. http://dx.doi.org/10.4172/2155-9546.1000262(2014).

Poungparn S, Komiyama A, Tanaka A, Sangtiean T,Maknual C, Kato S, et al. Carbon dioxideemission through soil respiration in a secondarymangrove forest of eastern Thailand.J Trop Ecol 2009;25:393–400.

Raich JW, Schlesinger WH. The global carbon dioxide fluxes in soil respiration and itsrelationship to vegetation climate. Tellus 1992;44B:81–99.

Rajeev L, da Rocha UN, Klitgord N, Luning EG, Fortney J, Axen SD, et al. Dynamiccyanobacterial response to hydration and dehydration in a desert biological soilcrust. ISME J 2013;7:2178–91.

Stieglitz TC, Clark JF, Hancock GJ. The mangrove pump: the tidal flushing of animalburrows in a tropical mangrove forest determined from radionuclide budgets.Geochim Cosmochim Acta 2013;102:12–22.

Strong CL, Bullard JE, Burford MA, McTainsh GH. Response of cyanobacterial soil crusts tomoisture and nutrient availability. Catena 2013;109:195–202.

Subke JA, Reichstein M, Tenhunen JD. Explaining temporal variation in soil CO2 efflux in amature spruce forest in Southern Germany. Soil Biol Biochem 2003;35:1467–83.

Thomas AD, Hoon SR, Dougill AJ. Soil respiration at five sites along the Kalahari transect:effects of temperature, precipitation pulses and biological soil crust cover. Geoderma2011;167–168:284–94.

Vincent G, Shahriari AR, Lucot E, Badot PM, Epron D. Spatial and seasonal variations in soilrespiration in a temperate deciduous forest with fluctuating water table. Soil BiolBiochem 2006;38:2527–35.

Virly S. Atlas des mangroves de Nouvelle-Calédonie. Typologies et Biodiversité des man-groves de Nouvelle-Calédonie: ZoNéCo program report. New-Caledonia: Nouméa;2006. p. 213.

Wohlfahrt G, Fenstermaker LF, Arnone III JA. Large annual net ecosystem CO2 uptake of aMojave desert ecosystem. Glob Chang Biol 2008;14:1475–87.

XuM, Qi Y. Spatial and seasonal variations of Q10 determined by soil respiration measure-ments at a Sierra Nevadan forest. Global Biogeochem Cycles 2001;15:687–96.

Yentsch CS, Menzel DW. A method for the determination of phytoplankton chlorophylland phaeophytin by fluorescence. Deep Sea Res 1963;10:221–31.