Soil greenhouse gases emissions reduce the benefit of mangrove plant to mitigating atmospheric warming effect

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1 Soil greenhouse gses emissions reduce the enefit of mngrove plnt to mitigting tmospheric wrming effect Gungcheng Chen 1, Bin Chen 1, Dn Yu 2, Yong Ye 2, Nor F.Y. Tm 3, Shunyng Chen 1 1 Third Institute of Ocenogrphy, Stte Ocenic Administrtion, Ximen, Fujin, 360, Chin 2 Key Lortory of the Ministry of Eduction for Costl nd Wetlnd Ecosystems, Ximen University, Ximen, Fujin, 3612, Chin 3 Deprtment of Biology nd Chemistry, City University of Hong Kong, Hong Kong SAR, Chin Correspondence to: G. Chen (gc.chen@tio.org.cn) 1 Astrct Mngrove soils hve een recognized s sources of tmospheric greenhouse gses ut the tmospheric fluxes re poorly chrcterized, nd their dverse wrming effect hs scrcely een considered with respect to the role of mngrove wetlnds in mitigting glol wrming. The present study lnced the wrming effect of soil greenhouse gs emissions with plnt cron dioxide (CO 2 ) sequestrtion rte in highly productive mngrove wetlnd in South Chin to ssess the role of mngrove wetlnd in mitigting tmospheric wrming. The results showed tht mngrove soils were significnt sources of greenhouse gses, nd the fluxes were significntly higher in summer nd lso different mong mngrove sites. Gses fluxes were positively correlted with the soil orgnic cron, totl nitrogen, nd NH + 4 -N contents. The mngrove plnt ws le to sequester considerle mount of tmospheric CO 2 t 9 g CO 2 m 2 yr 1 in the present study, nd the ecosystem ws source of methne (CH 4 ) nd nitrous oxide (N 2 O) gses ut more intense CO 2 sink. However, the wrming effect of soil gs emissions, equivlent to 1222 g CO 2 m -2 yr -1, ws le to offset lrge proportion (~22%) of plnt CO 2 sequestrtion, nd the two trce gses comprised ~24 % of the totl wrming effect. We therefore propose the ssessment of the direct mitigtion of tmospheric wrming y mngrove ecosystem tht should tke into ccount oth soil greenhouse gses emissions nd plnt CO 2 sequestrtion. 1 Introduction 2 The glol tmospheric concentrtions of greenhouse gses, cron dioxide (CO 2 ), nd other two trce gses, methne (CH 4 ) nd nitrous oxide (N 2 O) hve ll shown lrge increses since the pre-industril times nd cuse the glol wrming prolems. The tmospheric concentrtions of CO 2, CH 4 nd N 2 O hve incresed from 278 ppm in 170 to 391 ppm in 11, y fctor of 2. from 722 pp to 1803 pp, nd from 270 pp to 342 pp, respectively (IPCC, 14). CO 2 concentrtion is incresing t the fstest oserved decdl rte of chnge in the pst ten yers nd unfortuntely the tmospheric greenhouse gs concentrtions continue to rise. In order to mintin glol temperture wrming elow 2 C over the 21 st century reltive to 1

2 1 2 pre-industril levels, reduction y 40% to 70% of glol nthropogenic greenhouse gses emissions y 0 compred to, nd incresing the existing iologicl cron pools for cron sequestrtion hve een proposed (IPCC, 14). Mngroves grow long the costlines of most of the world s tropicl nd sutropicl regions. Despite the limited re occupied y mngrove wetlnds compred to terrestril forests, these highly productive ecosystems re ecologiclly importnt on glol scle, nd hve een suggested to e responsile for % of glol terrestril cron export to the ocen nd ~% of the glol ocenic uril of cron (Durte et l., 0; Dittmr et l., 06). Recent studies hve lso highlighted the vlule role plyed y mngrove wetlnds in cron sequestrtion, nd estimted the cron uril rte in mngrove soil s 226 g C m -2 yr -1 from 34 sites (Mcleod et l., 11). Plnts sequester CO 2 from the tmosphere through photosynthesis nd store it in their iomss. The cpility of mngrove plnts to sequester tmospheric CO 2 is therefore relted to their net primry production (NPP). The overll glol mngrove NPP, recently estimted y Bouillon et l. (08), is g C m -2 yr-1, i.e g CO 2 m -2 is directly cptured y mngrove plnts ech yer. Being inter-tidl, mngrove wetlnds re regulrly flooded y incoming tides, nd their soils ltering etween oxic nd noxic conditions, fvor microil processes like nitrifction, denitrifiction nd methnogenesis tht produce greenhouse gses. Numerous studies hve recognized mngrove soil s sources of tmospheric greenhouse gses (Allen et l., 07; Chuhn et l., 08; Chen et l., ). The iogenic emission of greenhouse gses from mngrove soil to the tmosphere could e further enhnced y nthropogenic nitrogen input (Purvj nd Rmesh, 01; Muñoz-Hincpiéet l., 02; Kreuzwieser et l., 03; Chen et l., 11). These gs emissions contriute to tmospheric wrming nd reduce the overll mitigtion of glol wrming y mngroves. Therefore, the role tht mngrove wetlnds ply in directly mitigting tmospheric wrming is reflected y the exchnge of greenhouse gses etween the mngrove ecosystem nd the tmosphere. Assessments of the direct effect of mngrove wetlnds, on the ecosystem scle, in mitigting tmospheric wrming, re importnt ut still lcking. Although some studies hve focused on the net ecosystem production (NEP) tht comined the net primry production nd gseous cron emissions from soil respirtion (Golley et l., 1962; Komiym, 08) in mngrove wetlnds, for ssessing the contriution of mngrove wetlnds to tmospheric cron gs exchnge on the ecosystem scle, these studies re indequte for ssessing the contriution of mngroves to mitigting tmospheric wrming, s the contriutions of N 2 O emission nd the wrming effect of gses emissions were not tken into ccount. On the glol scle, the men soil CO 2 -C flux represents ~% of the mngrove NPP in cron udget quntified y Bouillon et l. (08); this indictes tht the soil CO 2 emission from mngrove wetlnd reduces % of the CO 2 sequestrtion rte y mngrove plnt. In ddition, lthough the tmospheric fluxes of CH 4 nd N 2 O re generlly 2 or 3 orders of mgnitude lower thn CO 2 flux in mngrove wetlnds (Chen et l., ), their contriutions to glol wrming could lso e relevnt nd re worthy ttention, ecuse these two gses re more stle nd hve considerly higher rdioctive forcing thn CO 2, with direct glol wrming potentil (GWP) 298 nd 34 times, respectively, s tht of CO 2 (Myhre et l., 13). However, the greenhouse gses emissions from mngrove soils remin poorly chrcterized, nd few studies hve considered the wrming effect of the simultneous emissions of the three forementioned gses from mngrove soils when evluting the role of mngrove ecosystems in mitigting glol wrming. 2

3 In this study, sptil nd sesonl vritions in soil greenhouse gses emissions were investigted in highly productive mngrove wetlnd in South Chin; the wrming effect of the gses emissions ws quntified nd then lnced with the plnt CO 2 sequestrtion rte to estimte the mitigting effect of mngrove wetlnd on tmospheric wrming. We lso evluted the effects of soil chrcteristics on greenhouse gses emissions. We hypothesized tht mngroves my e ecologiclly importnt in sequestrtion of tmospheric CO 2 nd mitigtion of glol wrming ut tht the greenhouse gs emissions from mngrove soil might lso e significnt nd would lrgely offset ny enefits. In ddition, the contriutions of the two trce gses, N 2 O nd CH 4, to wrming might e relevnt nd were considered. 2 Mterils nd Methods 2.1 Study re 1 Soil greenhouse gses emissions nd plnt CO 2 sequestrtion rtes were studied in sutropicl mngrove re in the Jiulong River Estury in southern Chin. The region is sutropicl (men nnul temperture:.9 C), with most of the nnul rinfll (1284 mm) derived from summer typhoons. Tides re semi-diurnl, with n verge rnge of 4 m. Most forests (~32 h) in this re re locted on the southwestern shore, with Kndeli oovt s the dominnt cnopy species. The mngrove soils re minly composed of silt nd cly (Alongi et l., 0). Smplings were crried out in three mngrove sites (Fig. 1) locted t Coputou Villge (24 23'40.89"N, 117 4'42.90"E) nd Xiguo Villge (24 23'36.24"N, 117 '19.48"E) nd on Himen Islnd (24 24'24.0"N, 117 6'28.1"E). The width of ech smpling re ws ~40 m, ~90 m nd ~90 m from the lndwrd to sewrd fringes in the three mngrove sites, respectively. Coputou (CPT) mngrove ws rehilitted K. oovt forest locted in the high intertidl zone on the south nk of the estury, nd this mngrove hd the highest cnopy height (7.8 m). Xiguo (XG) mngrove ws locted in the mid intertidl zone; this mngrove ws composed of dense K. oovt tress (1.7 stem m -2 ). The lowest vegettion density (0.9 stem m -2 ) nd cnopy height (. m) occurred in the nturl mngrove on Himen Islnd (HMI). Slinity of the soil porewter, mesured using pocket refrctometer (0 0 prts per thousnds, Atgo PAL-06 S, Jpn) ws 11, 11 nd 14 in the three mngrove forest, respectively Soil to tmosphere greenhouse gses fluxes Soil to tmosphere fluxes of greenhouse gses were quntified in Jnury, April, August nd Octoer 12, representing the sesons winter, spring, summer nd utumn, respectively. All smpling ws conducted two hours efore the lowest e tide during the dytime s the study res re suject to semi-diurnl tides, nd the exposure times of mngrove wetlnds re reltive short. Nine replicte plots were chosen t ech of the three mngrove sites during ech smpling cmpign to chieve more ccurte estimtion of gs emissions ecuse gret sptil vrition is chrcteristic of gs flux, even on smll scle (Allen et l., 07; Chen et l., ). 3

4 1 2 To mesure the soil to tmosphere fluxes of greenhosue gses, some studies in slt mrshes rest the gs chmer on the collr tht hs een permnently inserted into the surfce sediment to collect the gses (e.g. Mgenheimer et l. 1996, Mosemn-Vltierr et l. 11). In these studies, the chmers re generlly lrge nd the intct live mrsh plnts or plnt community re covered within the chmers, so the pre-instlled collr could e helpful to chieve enclosed irtight spce nd void the disturnce from inserting the lrge chmer. However, most studies on gs flux mesurements in mngroves employed smller chmer (e.g. with n internl volume of ~1L) thn tht pplied in sltmrshes, nd the chmer ws directly inserted into the sediment tht ws lso softer (e.g. Corredor et l., 1999; Buz et l., 02; Allen et l., 07; Chen et l., 12). Moreover, unlike sltmrsh, the studies in mngrove forest quntify the fluxes etween sediment nd tmosphere; therefore, the chmer covers only sediment nd is smller. The single-chmer method similr to tht used in mngroves hs lso een employed in sltmrshes (Morries nd Whiting, 1986; Adms et l. 12). Gs flux in this study ws quntified using the sttic (closed) chmer technique followed y gs chromtogrphy s descried y Chen et l. (). The chmers hd n re of 0.02 m 2 nd n internl volume of 1.2 l, which is similr to those used y previous reserchers (e.g. Corredor et l., 1999; Buz et l., 02). They stted tht the volume/sl re rtio of the chmer ws esy for deployment nd sufficiently smll for the rpid increse in gs concentrtions, ut lrge enough to minimize disturnce of the enclosed sediment surfce. Therefore, no dditionl device like electric fn ws instlled to stir the ir inside the chmer in their studies nd the present study. Chen et l. () further reveled tht gses continuously relesed nd their concentrtions linerly relted with the deployment time, indicting tht this sttic chmer is suitle for the smpling. The open end of the chmer ws inserted 3 cm into the soil. Chmers were plced in loctions without mngrove seedlings, oveground roots or litter fll to void the influences of these fctors on gs fluxes, nd the deployment time ws set to minutes, with smpling t -minute intervls. At ech smpling time, -ml gs smple ws collected with hypodermic needle ttched to -ml glss syringe from the chmer nd then injected into -ml gs smpling g. Gs concentrtions were nlyzed in prllel with gs chromtogrphy system (7890A, Agilent Technologies, Snt Clr, Cliforni, USA) configured with single chnnel nd two detectors, y compring the pek res of smples ginst n Agilent Greenhouse Gs Checkout Smple (1 ppm N 2 O, ppm CH 4 nd 600 ppm CO 2 in N 2 ). The N 2 O nd CH 4 concentrtions were determined with 63Ni electron cpture detector nd flme ioniztion detector (FID), respectively. The CO 2 concentrtion ws nlyzed y FID fter methniztion. During mesurement, the stndrd smple ws nlyzed in every 1- smples to ensure the dt qulity. The reltive stndrd devitions of replicte stndrd mesurements were 3.6%, 2.% nd 3.4% for N 2 O, CH 4 nd CO 2, respectively. The soil to tmosphere fluxes of greenhouse gses were clculted from the following formul: F m = VΔM/Aρ where F m is the interfcil gs flux (mol m -2 h -1 ), V is the internl ir volume (m 3 ) in the chmer fter eing plced, ΔM (h -1 ) is the chnge in gs concentrtion in the continer, A is the surfce re of the soil (m 2 ) nd ρ is the volume of per mol gs (m 3 mol -1 ). During ech smpling, the open ir temperture ws simultneously mesured with mercury thermometer to clculte the ρ vlue. 4

5 Although CO 2 emissions from sediment include the CO 2 efflux from plnt roots nd heterotrophic respirtion, the chmers used for flux mesurement were plced in loctions without oveground roots, nd the CO 2 flux mesured in this study cn e ttriuted to soil heterotrophic respirtion ecuse most metolic respirtion from underground roots is relesed through lenticels nd the flux otined using sttic chmers would e close to the levels of CO 2 relesed due to soil respirtion (Tomlinson, 1986). The gs fluxes were converted to CO 2 -equivlent fluxes to indicte their respective contriutions to glol wrming using the GWP vlue of ech gs (1, 34 nd 298 for CO 2, CH 4 nd N 2 O, respectively, over 0-yer timefrme) ccording to Myhre et l. (13). 2.3 Smpling nd nlysis of soil 1 Soil prmeters were lso mesured t these smpling sites in summer to check their reltionship with gses fluxes. Soil redox potentil (Eh) under the chmer ws mesured using ph/eh meter (WP-81, TPS, Austrli) fter gs smpling, y inserting the pltinum proe directly into the soil t depth of cm from the surfce. Independent soil cores to depth of 1 cm (6 cores for ech mngrove site) were then collected using hnd-held PVC corers. Soil orgnic cron (OC) concentrtion ws nlyzed using rpid dichromte oxidtion procedure. Totl Kjeldhl nitrogen (TKN) content fter Kjeldhl digestion nd NH4+-N nd NO3 -N contents in the KCl (2M) extrcts were mesured y the Continuous Flow Anlyzer (CFA, Futur II, Allince Instruments). All soil nlyses were sed on the stndrd methods for soil nlyses descried y Pge et l. (1982), nd dt were expressed in terms of o C oven-dried weight. 2.4 Plnt CO 2 sequestrtion rte 2 Plnt CO 2 sequestrtion rte ws clculted from the NPP, the cron content nd the formul weights of CO 2 nd C. Mngrove NPP ws estimted using the litter fll technique proposed y Tes (1979), which postultes tht 1/3 of the NPP is returned s litter fll. A glol extrpoltion lso showed cler reltionship etween litter fll nd wood production nd further suggested tht litter production mounts to ~32% of the totl mngrove NPP including root production (Bouillon et l., 08). This rpid nd direct method ws lso pplied in other studies (e.g. Lee, 1990; Alongi, 09), ut its ccurcy depends on the vilility of good conversion fctor (Odum et l., 1982). In this study, conversion fctor 2.7 ws pplied for the estimtion of NPP, which ws clculted from the previous reported NPP (including root production) nd the concurrent litter fll production for K. oovt mngrove in the Jiulong River Estury (Lin et l., 198). The men cron content in vrious plnt frctions ws 47% for K. oovt in the Jiulong River Estury (Zheng et l., 199). Litter fll smples were collected using metl-frmed litter trps (Φ=70 cm for surfce re, cm depth) with 2-mm mesh. Nine trps were plced rndomly t similr height ove the mximum tide level (1.m ove the sediment) in ech mngrove site, under cnopies. Trp contents were collected monthly nd sorted into the ctegories of leves, wood, flowers nd propgules nd were then dried t 60 C to constnt weight nd weighed.

6 2. Sttisticl nlysis The normlity of vriles ws checked using the Kolmogorov-Smirnov test, nd those tht did not follow norml distriution were trnsformed to improve normlity nd homoscedsticity prior to nlysis. Two-wy ANOVA ws used to test differences in greenhouse gs flux mong the four sesons nd the three sites. If the difference ws significnt (p<0.0), post hoc Tukey test ws used to determine the differences. Differences in litter fll production nd soil chrcteristics mong different mngroves were compred y one-wy ANOVA. Person correltion coefficients were clculted to determine the reltionships etween soil properties nd greenhouse gs fluxes in summer. All sttisticl nlyses were performed using SPSS 18.0 for Windows (SPSS Inc., USA). 3 Results Soil to tmosphere greenhouse gs fluxes The soil to tmosphere greenhouse gs fluxes rnged from -1.6 to 0.0 μg m -2 h -1, -1.4 to μg m -2 h -1 nd -31 to 12 mg m -2 h -1, for N 2 O, CH 4 nd CO 2, respectively, in the three mngrove wetlnds in Jiulong River Estury (Fig. 2). The nnul emissions of N 2 O, CH 4 nd CO 2 from soil were then estimted to e 0.18 gn 2 O m -2 yr -1, 7.0 g CH 4 m -2 yr -1 nd gco 2 m -2 yr -1, respectively. The N 2 O fluxes were found to vry significntly mong the three mngrove sites (F=.63, p=0.000) nd mong the four sesons (F=17.21, p=0.000) ccording to two-wy ANOVA test; however, no significnt interction ws found etween these two fctors (F=1.28, p>0.0). XG mngrove hd higher N 2 O flux thn the other two sites, which hd similr fluxes. The highest N 2 O flux ws mesured in summer, while the lowest ws in the winter nd utumn. Both mngrove site (F=1.36, p=0.000) nd seson (F=26.03, p=0.000) hd significnt effects on CH 4 flux, nd significnt effect of the interction etween the two fctors ws lso found on the gs fluxes (F=3.83, p=0.000). No significnt difference ws mesured in spring, ut the gs fluxes were vrile in other sesons. Higher CH 4 flux ws found t CPT mngrove in winter, ut ws t XG in utumn. In summer, XG nd CPT hd comprle CH 4 fluxes, higher thn tht mesured t HMI. The gs fluxes were found to e lowest in winter nd spring in CPT nd XG sties nd highest in the summer. For HMI, significntly higher CH 4 flux ws lso mesured in summer, with lowest flux found in winter. For CO 2, the flux lso vried significntly mong the mngrove sites (F=.24, p=0.000) nd sesons (F=73.2, p=0.000), nd the interction etween these two fctors ws lso significnt (F=4.42, p=0.001). CO 2 fluxes were comprle mong the three mngrove sites in winter, while HMI site hd the lowest gs fluxes in the three sesons. Higher fluxes were recorded in CPT (in spring nd summer) or XG (in summer nd utumn) mngroves. Among the four sesons, the highest CO 2 fluxes were found in summer, irrespectively the mngrove sites, with utumn fluxes following (except CPT). 6

7 3.2 Soil chrcteristic nd their reltionship with gses fluxes Soil chrcteristics except NO - 3 -N concentrtion nd E h significntly vried mong the three mngrove sites in Jiulong River Estury (Fig. 3). Lower soil wter content ws mesured in CPT thn in other two sites (p<0.01). Soil NH + 4 -N content ws lower in CPT nd HMI (p<0.0). XG mngrove site hd the highest soil OC nd TKN concentrtions while the lowest concentrtions were mesured t HMI. Among the mesured soil prmeters, NH + 4 -N, OC nd TKN concentrtions were positively correlted with fluxes of the three gses (Tle 1), ut no significnt effect ws detected for other soil prmeters on the gses fluxes. 3.3 Litter fll nd net primry productions 1 This study mesured high litter fll productions of the sutropicl mngroves ( gdw m -2 yr -1 ), nd the men totl production ws 121 gdw m -2 yr -1 in Jiulong River Estury (Tle 2). Lef fll nd reproduction components were 0 nd 14 gdw m -2 yr -1, comprising 44% nd 41%, respectively, of the totl litterl production. The present study lso mesured lower litter fll production in the HMI mngrove site compred to the other two mngrove sites due to its lower lef nd twig production. Using the conversion fctor 2.7, the net primry production of mngrove clculted from litter fll production ws 3441 gdw m -2 in the Jiulong River Estury, equivlent to 1617 g C m -2 yr -1. Gretly sptil vrition ws found mong the three mngrove sites, nd the CPT mngrove hd twice production s high s tht of HMI mngrove. 3.4 Mitigting effect of the mngrove ecosystem on tmospheric wrming 2 In cse of high primry productions nd low soil cron gs emissions, the mngrove wetlnds in this study hd high NEP rtes rnging from 912 to 1746 g C m -2 yr -1 (Tle 3), with men s 138 g C m -2 yr -1. The cron gs emission ccounted for 16 % of the totl mngrove NPP, nd the CH 4 mde negligile contriution (0.2 %-3.4 %) to the totl cron gs emission. With oth plnt CO 2 sequestrtion (Tle 3) nd soil gs emissions comined, the net ecosystem exchnges of greenhouse gses were 0.1 g N 2 O m -2 yr -1, 1.91 g CH 4 m -2 yr -1 nd -640 g CO 2 m -2 yr -1 for CPT site, nd 0. N 2 O m -2 yr -1, g CH 4 m -2 yr -1 nd -249 g CO 2 m -2 yr -1 for XG site, nd 0.08 g N 2 O m -2 yr -1, 0.2 g CH 4 m -2 yr -1 nd -334 g CO 2 m -2 yr -1 for HMI site. The men net exchnges of greenhouse gses etween the mngrove ecosystem nd tmosphere ws 0.18 gn 2 O m - 2 yr -1, 7.00 g CH 4 m -2 yr -1 nd g CO 2 m -2 yr -1 in Jiulong River Estury. Bsed on the nnul emission rtes from mngrove soils, the CO 2 -equivlent fluxes of CO 2, CH 4 nd N 2 O were clculted to e 931, 238 nd 3 g CO 2 m 2 yr 1, respectively, in the mngrove wetlnds (Tle 3), nd the wrming effect of these greenhouse gses is equivlent to 1222 g CO 2 m 2 yr 1. The two trce gses, CH 4 nd N 2 O comprised 19. % nd 4.3 %, respectively, of the totl wrming effect. When lncing the wrming effect of the gses nd the concurrent CO 2 - sequestrtion rte of the mngrove plnts, the net effect of the mngrove ecosystem on tmospheric wrming is estimted to 7

8 e g CO 2 m -2 yr -1 (Tle 4), further indicting the mngrove wetlnd s n ffirmtive role in mitigting glol wrming. 4 Discussion 1 2 Although numerous studies hve chrcterized the C sequestrtion/ury in mngrove wetlnds nd their greenhouse gs emissions, few hve focused on the role of mngrove wetlnds in mitigting tmospheric wrming y considering oth the plnt CO 2 sequestrtion nd soil greenhouse gs emissions. The present study demonstrtes tht mngrove plnts ply n importnt role in mitigting tmospheric wrming through their CO 2 sequestrtion; however, mngrove soils on the other hnd could e significnt sources of greenhouse gses, nd the wrming effect of the gses emissions would reduce lrge proportion of the vegettion enefit. The soil to tmosphere gses fluxes in the Jiulong River Estury fell within the rnges previously reported for other mngrove wetlnds (Chuhn et l., 08; Chen et l., ), nd the results further demonstrte tht mngrove soils cn e sources of greenhouse gses. The greenhouse gses fluxes re relted to mngrove soil properties, including concentrtions of orgnic cron, totl nd inorgnic nitrogen, ulk density, slinity nd redox potentil (Purvj nd Rmesh, 01; Allen et l., 07; Chen et l.,, 12), s microil processes involved in the gses productions re regulted y the soil chrcteristics. In ddition to our previous studies in other sutropicl K. ovot-dominted wetlnds in South Chin (Chen et l., ), the greenhouse gses fluxes in Jiulong River Estury lso significntly incresed with soil orgnic cron, nitrogen nd NH + 4 -N concentrtions. Allen et l. (07) suggested tht the site-level control of N 2 O production in mngrove soils ws ttriuted to nitrifiction when sediment hd high mmonium levels nd positive E h ut to denitrifiction when sediment hd high nitrte levels nd negtive E h. The positive soil E h in the mngrove soil nd significnt correltion etween N 2 O flux nd soil NH + 4 -N concentrtion therefore indicted the importnce of nitrifiction process in mngrove soil responsile for the N 2 O production. Nevertheless, the results didn t exclude the potentil of denitrifiction for N 2 O production s the soil E h in this study ws elow mv, elow which denitrifiction usully strts (Pitty, 1979). This is different from the previous study in Mipo mngrove, where denitrifiction ws suggested to e the dominnt mechnism for N 2 O production (Chen et l., 12). The mngrove soil in this study hd comprle or higher NO - 3 -N concentrtion compred with the Mipo mngrove ut the N 2 O flux ws much lower in Jiulong River Estury. This could e ttriuted to the lower soil E h mesured in Mipo (-18 to 6 mv), which ws more fvorle to denitrifiction, nd further demonstrtes the significnce of denitrifiction in Mipo mngrove. Methne emission from the costl soils hve een known to e limited y high slinity s the presence of high sulfte in costl soils llows sulfte-reducing cteri to outcompete methnogens for energy sources (Bisws et l., 07; Poffenrger et l., 11). The contrrily sptil vrition in soil CH 4 emissions to slinity in Jiulong River Estury ws lso consistent to such inhiition effect, nd lower CH 4 flux ws recorded in the HMI site with higher porewter slinity. The high soil NH + 4 -N concentrtion lso enhnced the CH 4 emission into the tmosphere in this study, similrly to some other 8

9 studies (e.g. Allen et l., 07; Chen et l., ), proly due to the inhiition effect of soil NH 4 + -N on CH 4 oxidtion under high concentrtion (Bosse et l., 1993). Mngrove soils with more positive E h nd longer exposure would led to 1 2 higher eroic respirtion nd chemicl oxidtion of orgnic mtter in soil, nd re on the other hnd unfvourle to CH 4 emission. However, no significnt correltions were found etween soil E h nd the gses fluxes in the present study, nd the C/nutrient vililities were the most influencing fctors. As the microil mechnisms tht driving the greenhouse gses productions re lcking in this study, more detiled studies on microil processes involved in the gses emissions in the soil, e.g. methnogenesis, methne oxidtion, nitrifiction nd denitrifiction, nd their interctions with soil iotic fctors re therefore needed nd worthy further studies. Similr to previous studies (e.g. Allen et l., 11; Chen et l.,, 12), gs fluxes in this region vried with mngrove site nd seson. For instnce, the CO 2 flux rnged etween s low s 7 g m -2 yr -1 nd up to 1470 g m -2 yr -1. Even greter sptil vrition ws fould in CH 4 flux. The sptil vritions of gses fluxes could e prtly ttriuted to the differences in soil orgnic cron nd nitrogen contents s the sustrtes for soil respirtion mong the study sites. Such sptil vrition nd the sesonl vrition in gs fluxes, suggested to e minly due to temperture in sutropicl mngroves nd moisture in tropicl mngroves (Chen et l., 12), therefore should e tken into ccount for inventory of greenhouse gs emissions. Difference in the ecosystem mitigting effect were lso found mong the three mngrove sites, with lower vlue occurring t HMI due to much lower plnt CO 2 sequestrtion rte. The XG site hd the highest CO 2 -equivlent flux of greenhouse gs emissions, which offset 33 % of the plnt CO 2 cpture rte, while this rtio ws < % in the HMI mngrove site. We lso mesured lower primry production ccompnied y low gs emission rtes in this study. Similrly, the soil respirtion rte ws found to e correlted with litter fll production on lrge rnge of ltitude extending from 27 N to 37 S (Lovelock, 08). This pttern suggested tht the more CO 2 is sequestrted y mngroves, the more sustntil the effect of the soil greenhouse gs emissions might e, nd their wrming effect should not e ignored. The sutropicl K. oovt mngrove forest hd high net primry productivity, close to mounts reported in tropicl regions, nd higher thn the glol men production (Bouillon et l., 08). This high NPP ut low cron gses emissions from soil indicted tht the mngrove wetlnd in this re hs strong sequestrtion cpility of tmospheric cron on the ecosytem scle. The NEP in this mngrove ws lso higher thn the glol men vlue 10 g C m -2 yr -1 reported y Bouillon et l. (08), nd those estimted in Rhizophor mngle forest (61 gc m -2 yr -1 ) in Puerto Rico (Golley et l., 1962) nd in the mngrove in western Florid Evergldes (1170 gc m -2 yr -1 ) (Brr et l., ). Although CH 4 emission ws lso significnt (7.0 g CH 4 m -2 yr -1, nd up to 321 μg m -2 h -1 ) in the esturine mngrove wetlnds in this study, it ccounted for unelectle proportion (1.4%) of the soil gseous cron emission in this study. The present study ssessed the role of mngrove wetlnd in mitigting tmospheric wrming effect, through direct quntifiction of the gseous exchnge etween mngrove ecosystem nd tmosphere. The nnul gses emission rtes were estimted from the fluxes from the exposed soil, nd this estimtion ws sujected to the ssumption tht the wtertmosphere fluxes during inundtion were similr to the soil-tmosphere fluxes during exposure. The ssumption ws sed on the following findings from previous studies. Bouillon et l. (08) reported tht there ws no significnt difference in the 9

10 1 2 CO 2 emission etween exposed nd inundted periods lthough the processes of gses diffused from soil to wter then to ir ws likely ffected during the inundtion period. A diurnl mesurement of CH 4 nd N 2 O fluxes in n esturine mrsh in Fujin Province lso showed no cler difference etween the inundtion nd exposure periods (Tong et l., 13). Moreover, the mngrove sites in this study locte in the mid to high intertidl zones, nd the forest floor ws not flooded y tides in most of the times (Chen et l., 08). Therefore, the clcultions of nnul emissions from fluxes during exposure time should not ffect the findings of the present study. On the ecosystem scle, the mngrove wetlnd ws smll sources of CH 4 nd N 2 O, compred to the significnt CO 2 sink. However, the wrming effect of soil greenhouse gses emissions offset 22% of the plnt CO 2 sequestrtion rte in this study, nd the net effect of the mngrove ecosystem on tmospheric wrming effect ws estimted to e g CO 2 m -2 yr -1. This vlue ws higher thn the glol vlue (~ g CO 2 m -2 yr -1, without considertion of soil non-co 2 gses emissions) clculted from the glol NPP nd soil respirtion rtes (Bouillon et l., 08). Some other studies in sltmrshes lso quntified the potentil glol wrming feedcks sed on the soil cron sequestrtion rte nd non-co 2 gses emission rtes (e.g. Chmur et l., 11; Yun et l., 14). In cse of the rpid soil ccumultion rte in the mngrove wetlnd in Jiulong River Estury (33.7 mol C m -2 yr -1, equivlent to g CO 2 m -2 yr -1, Alongi et l., 0), the glol wrming potentil of this mngrove re is clculted s ~1190 g CO 2 m -2 yr -1 (the CO 2 -equivelent flux of CH 4 nd N 2 O fluxes hd sum of 290 g CO 2 m -2 yr -1, Tle 3). This vlue ws much higher thn those reported in northern nd northwestern Atlntic sltmrshes estimted in the growing seson (74-00 g CO 2 m -2 yr -1, Chmur et l., 11) nd the mrshes in estern Chin ( g CO 2 m -2 yr -1, Yun et l., 14). Unlike the slt mrsh, which hs een supposed tht its cron ccumultion through plnt growth is roughly lnced y losses through grzing, decomposition nd fire, nd no gin is chieved (IPCC, 06, 14), mjority of C cptured y mngrove plnt is stored in their iomss. Tke these into ccount, it cn e suggested tht the mngrove wetlnd plys more ecologiclly relevnt role in mitigting glol wrming. Despite their low fluxes compred to CO 2, the contriutions of the trce CH 4 nd N 2 O gses, when considering their wrming effect, re lso relevnt to glol wrming in the mngrove wetlnd. When sujected to nthropogenic nutrient inputs, the emissions of these two gses nd CO 2, could e more considerle (Muñoz-Hincpiéet l., 02; Chen et l., 11, 14), which would lrgely enhnce their contriutions to the wrming effect. For instnce, the nnul men fluxes of CH 4 nd N 2 O could e up to 3899 µg CH 4 m -2 h -1 nd 7.1 µg N 2 O m -2 h -1, respectively, in the Brisne mngrove, which receives dischrge from sewge tretment plnt in Queenslnd, Austrli (Allen et l., 07). Even higher gs fluxes hve een reported from mngrove soil, nd N 2 O nd CH 4 contriuted twice the glol wrming potentil s CO 2 in the Futin mngrove in South Chin which receives dischrges nd nthropogenic nutrient inputs from Perl River Delt nd nery polluted rivers (Chen et l., ). The emissions of CH 4 nd N 2 O from mngrove soils therefore should lso e documented in ddition to tht of CO 2 to quntify the contriution of greenhouse gses emissions from mngrove soil to glol wrming, especilly for those receiving exogenous nutrients. Liu nd Grever (09) hve lso suggested tht lthough the ddition of N incresed the glol terrestril C sink, CO 2 sequestrtion could e lrgely offset y N stimultion of glol CH 4 nd N 2 O

11 emissions; nd N 2 O ws found to dominte the totl wrming effect of gses emissions in some gro-ecosystems (Mosier et l., 0). Mngrove ecosystem is open nd dynmic in the cron iogeochemicl processes. In ddition to the cron gses exchnges, cron exchnges etween mngrove nd the djcent ecosystems include the uril of exogenous cron, the loss from mngrove ecosystem through production of dissolved orgnic nd dissolved inorgnic cron when the soils re covered y wter, nd y loss of prticulte orgnic cron to costl zone (Ye et l., 11; Bouillon et l., 08). These cron lnce nd dynmics relte to the potentil of mngrove wetlnd in reducing cron gses emissions, therefore their involvements in the mitigtion effect of wetlnds on glol wrming deserve further studies. Conclusions 1 The present study showed tht mngrove soils re significnt sources of greenhouse gses, nd the wrming effect of gses emissions could lrgely offset the enefit of plnt CO 2 sequestrtion to mitigting tmospheric wrming. We therefore propose tht ny ssessment of the direct mitigtion of tmospheric wrming should tke into ccount soil greenhouse gs emissions s well s plnt CO 2 sequestrtion. The contriutions of trce mounts of CH 4 nd N 2 O gses to the wrming effect should not e ignored, especilly in nutrient-enriched mngrove wetlnds. Moreover, the temporl nd sptil vritions in gs fluxes nd plnt CO 2 sequestrtion should e tken into ccount to improve the ccurcy of estimtes of the mitigting effect of mngroves on tmospheric wrming. Author contriution G. Chen designed the experiments, nd S. Chen nd D. Yu crried out the field smpling nd lortory nlysis. B. Chen performed the dt nlysis. G. Chen wrote the first drft of the mnuscript, nd ll uthors contriuted sustntilly to revisions. Acknowledgements 2 The work descried in this pper ws supported y the Ntionl Nturl Science Foundtion of Chin (4168) nd the Fujin Province Science nd Technology Pln Project (14Y0067). The 973 Progrm (1CB4290) nd Science Reserch Foundtion of the Third Institute of Ocenogrphy, SOA (14011), lso provided support. The uthors hve no conflict of interest. The uthors re grteful to Ms. Y.P. Chen, Dr. X.Q. Zheng nd Mrs. Q.Y. Lin for their ssistnce with field smpling nd lortory nlysis, s well s Mr. Z.Y. Xue for ssistnce with mngrove site selection. 11

12 References 1 2 Adms, C.A., Andrews, J.E., nd Jickells, T.: Nitrous oxide nd methne fluxes vs. cron, nitrogen nd phosphorous uril in new intertidl nd sltmrsh sediments, Sci. Totl Environ., 434, , 12. Allen, D.E., Dll, R.C., Rennenerg, H., Meyer, R.L., Reeves, S., nd Schmidt, S.: Sptil nd temporl vrition of nitrous oxide nd methne flux etween sutropicl mngrove sediments nd the tmosphere, Soil Biol. Biochem., 39, , 07. Allen, D., Dll, R.C., Rennenerg, H., nd Schmidt, S.: Sesonl vrition in nitrous oxide nd methne emissions from sutropicl estury nd costl mngrove sediments, Austrli, Plnt Biol., 13, , 11. Alongi, D.M., Pfitzner, J., Trott, L.A., Tirendi, F., nd Klumpp, D.W.: Rpid sedimenttion nd microil minerliztion in mngrove forests of the Jiulongjing estury, Chin, Estur. Cost. Shelf Sci., 63, , 0. Alongi, D.M.: The Energetics of Mngrove Forests, Springer Verlg Press, London, 09. Brr, J.G., Engel,V., Fuentes, J.D., Ziemn, J.C., O Hllorn, T.L., Smith III, T.J., nd Anderson, G.H.: Controls on mngrove forest-tmosphere cron dioxide exchnges in western Evergldes Ntionl Prk, J. Geophys. Res., 11, G0,. Buz, J., Morell, J.M., nd Corredor, J.E: Biogeochemistry of nitrous oxide production in the red mngrove (Rhizophor mngle) forest soils. Estur. Cost. Shelf Sci.,, , 02. Bisws, H., Mukhopdhyy, S.K., Sen, S., nd Jn, T.K.: Sptil nd temporl ptterns of methne dynmics in the tropicl mngrove dominted estury, NE cost of By of Bengl, Indi, J. Mr. Syst., 68, 64, 07. Bosse, U., Frenzer, P., nd Conrd, R.: Inhiition of methne oxidtion y mmonium in the surfce lyer of littorl sediment, FEMS Microiol. Ecol., 13, , Bouillon, S., Borges, A.V., Cstñed-Moy, E., Diele, K., Dittmr, T., Duke, N.C., Kristensen, E., Lee, S.Y., Mrchnd, C., Middelurg, J.J., River-Monroy,V.H., Thoms J. Smith III, T.J., nd Twilley, R.R.: Mngrove production nd cron sinks: revision of glol udget estimtes, Glol Biogeochem. Cycles, 22, GB13, 08. Chen, G.C., Tm, N.F.Y., nd Ye, Y.: Summer fluxes of tmospheric greenhouse gses N 2 O, CH 4 nd CO 2 from mngrove soil in South Chin, Sci. Totl Environ., 408, ,. Chen, G.C., Tm, N.F.Y., Wong, Y.S., nd Ye, Y.: Effect of wstewter dischrge on greenhouse gs fluxes from mngrove soils, Atmos. Environ., 4, , 11. Chen, G.C., Tm, N.F.Y., nd Ye, Y.: Sptil nd sesonl vritions of tmospheric N 2 O nd CO 2 fluxes from sutropicl mngrove swmp nd their reltionships with soil chrcteristics, Soil Biol. Biochem., 48, , 12. Chen, G.C., Tm, N.F.Y., nd Ye, Y.: Does zinc in livestock wstewter reduce nitrous oxide (N 2 O) emissions from mngrove soils? Wter Res., 6, , 14. Chen, G.C., Ye, Y., nd Lu, C.Y., Sesonl vriility of lef litter removl y crs in Kndeli cndel mngrove forest in Jiulongjing Estury, Chin, Estur. Cost. Shelf Sci., 79, ,

13 1 2 Chuhn, R., Rmnthn, A.L., nd Adhy, T.K.: Assessment of methne nd nitrous oxide flux from mngroves long Estern cost of Indi, Geofluids, 8, , 08. Chmur, G.L., Kellmn, L., nd Guntenspergen, G.R.: The greenhouse gs flux nd potentil glol wrming feedcks of northern mcrotidl nd microtidl slt mrsh, Environ. Res. Lett., 6, , 11. Corredor, J.E., Morell, J.M., nd Buz, J.: Atmospheric nitrous oxide fluxes from mngrove soils. Mr. Pollut. Bull., 3, , Dittmr, T., Hertkorn, N., Kttner, G., nd Lr, R.J.: Mngroves, mjor source of dissolved orgnic cron to the ocens, Glol Biogeochem. Cycles,, GB12, 06. Durte, C.M., Middelurg, J.J., nd Crco, N.: Mjor role of mrine vegettion on the ocenic cron cycle, Biogeosciences, 2, 1 8, 0. Golley, F., Odum, H.T., nd Wilson, R.F.: The structure nd metolism of Puerto Ricn red mngrove forest in My. Ecology, 43, 9-19, IPCC: 06 IPCC guideline for ntionl greenhouse gs inventory, Prepred y the Ntionl Greenhouse Gs Inventories Progrmme, Eggleston HS, Buendi L, Miw K, Ngr T nd Tne K (eds). IGES, Jpn, 06. IPCC: Climte Chnge 14: Synthesis Report. Contriution of Working Groups I, II nd III to the Fifth Assessment Report of the Intergovernmentl Pnel on Climte Chnge [Core Writing Tem, R.K. Pchuri nd L.A. Meyer (eds.)]. IPCC, Genev, Switzerlnd, 14. IPCC: 13 Supplement to the 06 IPCC guideline fir ntionl greenhouse gs inventories: wetlnd, Hirishi, T., Krug, T., Tne, K., Srivstv, N., Bsnsuren, J., Fukud, M., nd Troxler, T.G. (eds). IPCC, Switzerlnd, 14. Kreuzwieser, J., Buchholz, J., nd Rennenerg, H: Emission of methne nd nitrous oxide y Austrlin mngrove ecosystems, Plnt Biol.,, , 03. Komiym, A., Ong, J.E., nd Poungprn, S.: Allometry, iomss, nd productivity of mngrove forests: review, Aqut. Bot., 89, , 08. Lee, S.Y.: Primry productivity nd prticulte orgnic mtter flow in n esturine mngrove-wetlnd in Hong Kong, Mr. Biol., 6, , Lin, P., Lu, C.Y., Lin, G.H., Chen, R.H., nd Su, L.: Studies on mngrove ecosystem of Jiulongjing River Estury in Chin I. The iomss nd productivity of Kndeli cndel community, J. Ximen Univ. Nt. Sci. 24, 08-14, 198. (In Chinese) Liu, L. nd Grever, T.L.: A review of nitrogen enrichment effects on three iogenic GHGs: the CO 2 sink my e lrgely offset y stimulted N 2 O nd CH 4 emission, Ecol. Lett., 12, , 09. Lovelock, C.E.: Soil respirtion nd elowground cron lloction in mngrove forests, Ecosystems, 11, , 08. Mgenheimer, J.F., Moore, T.R., Chmur, G.L., nd Doust, R.J.: Methne nd cron dioxide flux from mcrotidl slt mrsh, By of Fundy, NewBrunswick, Esturies, 19, ,

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15 Yun, J., Ding, W., Liu, D., Kng, H., Freemn, C., Xing, J., nd Lin, Y.: Exotic Sprtin lterniflor invsion lters ecosystem tmosphere exchnge of CH 4 nd N 2 O nd cron sequestrtion in costl slt mrsh in Chin, Glol Chnge Biol., doi:.1111/gc.12797, 14. Zheng, W.J., Xue, X., nd Lin, P.: Studies on dynmics of cron, hydrogen nd nitrogen elements for Kndeli cndel mngrove community in Fujin, Chin, Act Ecol. Sin., 1, ,

16 Tle 1. Litter fll production nd net primry production (gdw m -2 yr -1 ) in the three mngrove sites in Jiulong River Estury. Mngrove Lef Twig Re-production Totl NPP CPT 683±1 241± 641±234 16±246 46±676 XG 692±86 267±164 48± ± ±19 HMI 27±121 2±72 444± ± ±393 Men CPT: Coputou; XG: Xiguo; HMI: Himen Islnd; NPP: Net primry production. Different letters in one column indicte significnt difference mong the three mngrove sites. 16

17 Tle 2. Person correltion coefficient vlues (r) etween soil properties nd summer fluxes of greenhouse gses in Jiulong River Estury. Soil prmeter Fluxes of gses N 2 O CH 4 CO 2 Redox potentil Wter content NH + 4 -N 0.7* 0.7** 0.618* NO - 3 -N OC 0.76*** 0.838*** 0.713** TKN 0.812*** 0.41* 0.724** *, ** nd *** indicte significnt r vlue t p<0.0, 001 nd 0001, respectively (n=18). 17

18 4 Tle 3. Net ecosystem production nd the mitigting effects of wetlnds on glol wrming in the Jiulong River Estury Study site Soil C-gs emission (g C m -2 yr -1 ) Net primry production (gc m -2 yr -1 ) Net ecosystem production (gc m -2 yr -1 ) CO2 equivlent flux (g CO2 m -2 yr -1 ) N2O CH4 CO2 Totl Plnt CO2 sequestrtion rte (g CO2 m -2 yr -1 ) Ecosystem mitigtion effect (g CO2 m -2 yr -1 ) CPT XG HMI Men CPT: Coputou; XG: Xiguo; HMI: Himen Islnd. 18

19 6 7 8 Figure cptions Fig. 1 Mp of the Jiulong River Estury, Chin. Numers 1-3 indicte the positions of the three smpling sites in this study. 1: Coputou; 2: Xiguo; 3: Himen Islnd Fig. 2 Soil to tmosphere greenhouse gs flux t the mngrove sites in Jiulong River Estury. Sme revition s Fig. 1. In ech seson, different letters (in lower cse) indicted significnt difference mong the three mngrove sites ccording to ANOVA test. For ech mngrove site, different letters (in cpitl) indicted significnt difference mong the four sesons Fig. 3 Soil chrcteristics t the mngrove sites in Jiulong River Estury. Sme revition s Fig. 1. Different letters indicted significnt difference mong the three mngrove sites ccording to ANOVA test. 19

20 Fig. 1

21 18 19 Flux ( g m -2 h -1 ) Flux ( g m -2 h -1 ) 170 N2O CPT XG HMI Winter Spring Summer Autumn Annul Seson A A A A A AB ns CH4 B B AB Winter Spring Summer Autumn Annul B Seson AB B 10 CO2 Flux (mg m -2 h -1 ) A A ns A A c B AB B D C A C B Winter Spring Summer Autumn Annul Seson Fig. 2 21

22 00 Redox potentil 60 Wter content Eh (mv) NS Percentge (%) CPT XG HMI 40 CPT XG HMI 24 Concentrtion (µg g -1 ) NO 3 - -N NS CPT XG HMI Concentrtion (µg g -1 ) NH + 4 -N CPT XG HMI 2 Concentrtion (mg g -1 ) OC CPT XG HMI Concentrtion (mg g -1 ) TKN CPT XG HMI 26 Fig