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

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1 Soil greenhouse gses emissions reduce the benefit of mngrove plnts to mitigting tmospheric wrming effect Gungcheng Chen 1 Bin Chen 1, Dn Yu, Nor F.Y. Tm, Yong Ye, Shunyng Chen 1 1 Third Institute of Ocenogrphy, Stte Ocenic Administrtion, Ximen, Fujin, 0, Chin Key Lbortory of the Ministry of Eduction for Costl nd Wetlnd Ecosystems, Ximen University, Ximen, Fujin, 1, Chin Deprtment of Biology nd Chemistry, City University of Hong Kong, Hong Kong SAR, Chin Correspondence to: G. Chen (gc.chen@tio.org.cn); Y. Ye (yeyong@xmu.edu.cn) Abstrct Mngrove soils hve been recognized s sources of tmospheric greenhouse gses, but the tmospheric fluxes re poorly chrcterized, nd their dverse wrming effect hs scrcely been considered with respect to the role of mngrove wetlnds in mitigting globl wrming. The present study blnced the wrming effect of soil greenhouse gs emissions with plnt crbon dioxide (CO ) sequestrtion rte derived from net primry production of plnts in productive mngrove wetlnd in South Chin to ssess the role of mngrove wetlnd in mitigting tmospheric wrming. Sesonl flues of the three greenhouse gses, nitrous oxide (N O), methne (CH ) nd CO, were mesured t three mngrove sites in Jiulong River Estury, nd net primry productions of mngrove plnts were estimted from the litter fll production ( replictes for these smplings in ech site). Soil chrcteristics were lso studied in the summer to exmine their reltionships with gs fluxes. Soil to tmosphere gs fluxes rnged from -1. to 0.0 μg N O m - h -1, from -1. to 1. μg CH m - h -1 nd from -1 to 1 mg CO m - h -1 in the present study, indicting tht soils relese significnt greenhouse gses into tmosphere. The results lso showed tht gs fluxes were significntly higher in the summer nd lso different mong mngrove sites. Gs fluxes in summer were positively correlted with the soil orgnic crbon, totl nitrogen, nd NH + -N contents. The mngrove plnts were ble to sequester considerble mount of tmospheric CO t rtes between - g CO m yr 1 nd -0 g CO m yr 1. The ecosystem ws source of methne (CH ) nd nitrous oxide (N O) gses but menwhile 1

2 more intense CO sink. However, the totl CO -equivelent flux of the three gses indicting their wrming effect ccounted for.-. % of the plnt CO sequestrtion rte, indicting tht the wrming effect of soil greenhouse gs emissions could prtilly offset the benefit of mngrove plnts to in mitigting tmospheric wrming. We therefore propose the ssessment of the direct mitigtion of tmospheric wrming by mngrove ecosystem tht tke into ccount both soil greenhouse gses emissions nd plnt CO sequestrtion. Moreover, the contribution of two trce gses, N O nd CH, ws lso relevnt, comprising.-. % of the totl wrming effect. 1 Introduction The globl tmospheric concentrtions of greenhouse gses, crbon dioxide (CO ), nd other two trce gses, methne (CH ) nd nitrous oxide (N O) hve ll shown lrge increses since the pre-industril times nd contribute the globl wrming. The tmospheric concentrtions of CO, CH nd N O hve incresed from ppm in 0 to 1 ppm in 0, by fctor of. from ppb to 0 ppb, nd from 0 ppb to ppb, respectively (IPCC, 01). The CO concentrtion is incresing t the fstest observed decdl rte of chnge in the pst ten yers, nd unfortuntely the tmospheric greenhouse gs concentrtions continue to rise. In order to mintin globl temperture wrming below C over the 1 st century reltive to pre-industril levels, reduction by 0% to 0% of globl nthropogenic greenhouse gses emissions by 00 compred to 0, nd incresing the existing biologicl crbon pools for crbon sequestrtion hve been proposed (IPCC, 01). Mngroves grow long the costlines of most of the world s tropicl nd subtropicl regions. Despite the limited re occupied by mngrove wetlnds compred to terrestril forests (0.%, Mcleod et l. 0), these highly productive ecosystems re ecologiclly importnt on the globl scle, nd hve been suggested to be responsible for -% of globl terrestril crbon export to the ocen (Dittmr et l., 00; Alongi, 01) nd -1% of crbon sequestrtion in the world s ocens (Durte et l., 00; Alongi, 01b). Recent studies hve lso highlighted the vluble role tht mngrove wetlnds ply in crbon sequestrtion, nd estimted the crbon buril rte in mngrove soil s g C m - yr -1 from sites (Mcleod et l., 0; Alongi, 01b). Plnts sequester CO from the tmosphere through photosynthesis nd store it in their biomss nd s detritus in soil. The cpbility of mngrove plnts to sequester CO from tmosphere is therefore relted to their net primry production (NPP). The overll

3 globl mngrove NPP recently estimted by Bouillon et l. (00) is 1. g C m - yr -1, indicting tht the CO sequestrtion cpbility of globl mngrove is equl to g CO m - yr -1. Being inter-tidl, mngrove wetlnds re regulrly flooded by incoming tides nd their soils lternte between oxic nd noxic conditions, which fvors microbil 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., 00; Chuhn et l., 00; Chen et l., 0). The biogenic emission of greenhouse gses from mngrove soil to the tmosphere could be further enhnced by nthropogenic nitrogen input (Purvj nd Rmesh, 001; Muñoz-Hincpié et l., 00; Kreuzwieser et l., 00; Chen et l., 0). These gs emissions contribute to tmospheric wrming nd reduce the overll mitigtion of globl wrming by mngroves. Therefore, the role tht mngrove wetlnds ply in directly mitigting tmospheric wrming is reflected by the exchnge of greenhouse gses between mngrove ecosystem nd the tmosphere s it reltes to the ecosystem reducing or contributing to the tmospheric rditive forcing (Chmur et l., 0). Assessments of the direct effect of mngrove wetlnds in mitigting tmospheric wrming on the ecosystem scle re importnt but still lcking. Although some studies hve focused on the net ecosystem production (NEP) tht combined the net primry production nd gseous crbon emissions from soil respirtion in mngrove wetlnds, for ssessing the contribution of mngrove wetlnds to tmospheric crbon gs exchnge on the ecosystem scle (Golley et l., ; Komiym, 00), these studies re indequte for ssessing the contribution of mngroves to mitigting tmospheric wrming s the contributions of N O emission nd the wrming effect of gs emissions were not tken into ccount. According to globl crbon budget quntified by Bouillon et l. (00), the men soil CO -C flux represents ~0% of the mngrove NPP, indicting tht the soil CO emission from mngrove wetlnd offsets 0% of the CO sequestrtion rte by mngrove plnt. Although the tmospheric fluxes of CH nd N O re generlly or orders of mgnitude lower thn CO flux in mngrove wetlnds (Chen et l., 0), their contributions to globl wrming could lso be substntil nd re worthy ttention becuse they re more stble nd hve considerbly higher rdioctive forcing thn CO, with direct globl wrming potentil (GWP) nd times s tht of CO, respectively (Myhre et l., 01). For instnce, the nnul men fluxes of CH could be up to µg CH m - h -1 (Allen et l., 00), with wrming effect of 1 g CO m - yr -1. Our previous studies hve demonstrted tht some mngrove wetlnds in South Chin subjected to exogenous nutrient inputs were significnt sources of

4 1 1 greenhouse gses (Chen et l., 0, 0). The wrming effect of N O nd CO emissions in Mi Po mngrove in Hong Kong equted to 0 nd g CO m - yr -1, respectively (Chen et l., 0). Given tht the NPP of the Mi Po mngrove ws gdw m - yr -1 (Lee, ) nd crbon content of % in plnts is ssumed (Bouillon et l., 00), the wrming effect of gs emissions, totlled 0 % of the plnt CO sequestrtion. However, the greenhouse gs emissions from mngrove soils remin poorly chrcterized, nd to wht extend the gs emissions would offset the benefit of plnt crbon sequestrtion is still uncler. In this study, we compred the wrming effect of the gs emissions ginst the plnt CO sequestrtion rte to estimte the mitigting effect of mngrove wetlnd on tmospheric wrming, nd this blncing is bsed on the exchnge of greenhouse gses between the mngrove ecosystem nd the tmosphere. The Jiulong River Estury in South Chin is considered s the distribution centre of Kndeli obovte (Wng nd Wng, 00), which is wide-spred nd well suited for use in restortion of res of north Asi s costline (Field, ). Previous studies hve exmined the production in this re nd 1 reported the litter fll production rnging from - g m - yr -1, similr to those in tropicl mngroves (Lin et l., ; Lu et l., ; Ye et l., 01); this finding indictes tht the mngrove forests in this region re productively nd ecologiclly importnt in the sequestrtion of tmospheric CO. However, mngroves in this re re ffected by wide vriety of humn ctivities, including the mriculture tht intermittently dischrges pond effluents into the costl wter nd potentilly impct mngrove forest. Alongi et l. (00) hs reported rpid minerliztion rtes of soil crbon nd nitrogen in this re; for instnce, soil denitrifiction rte rnged from 1 to 0 mmol N m - d -1, nd equted to -0% of totl soil nitrogen inputs. These rpid minerliztion processes suggest significnt greenhouse gs emissions from the mngrove soils. In this study, sptil nd sesonl vritions in soil greenhouse gs emissions were investigted, nd the wrming effect of the gs emissions ws quntified nd then blnced with the plnt CO sequestrtion rte to estimte the mitigting effect of mngrove wetlnd on tmospheric wrming. We lso evluted the effects of soil chrcteristics on greenhouse gs emissions. We hypothesized tht (1) the mngrove soils in this region could be sources of greenhouse gses, nd the gs emissions would to certin offset the benefits of mngrove plnts to mitigting tmospheric wrming; () the contribution of the two trce gses, N O nd CH, to tmospheric wrming might be relevnt nd were considered; nd () the mitigting effects might vry sptilly mong different mngrove sites.

5 Mterils nd Methods.1 Study re Soil greenhouse gs emissions nd plnt CO sequestrtion rtes were studied in the subtropicl mngroves in the Jiulong River Estury. The region is subtropicl hs men nnul temperture of 0. C, nd most of the nnul rinfll ( mm) is derived from summer typhoons. Tides re semidiurnl, with n verge rnge of m (Alongi et l., 00). The mjority of the primry mngrove forests in this region were destroyed for quculture ctivity nd se wll construction. Plnttion of K. obovt.ws crried out ner Coputou Villge to protect the shoreline in 0s nd 0s (Chen et l., 00). Most mngrove forests (~ h) in this region now re locted on the southwestern shore (Alongi et l., 00), nd re nrrow fringing forests due to the destruction. The mngrove soils re minly composed of silt nd cly (Alongi et l., 00). As some mngrove dominted shores were subjected to erosion, Sprtin lterniflor invsion or grbge from upstrem, the present study chose sites in good conditions for comprison study so s to eliminte such exogenous impcts. Smplings were crried out in three mngrove sites (Fig. 1) locted ner Coputou Villge (CPT, '0."N, '.0"E), Xiguo Villge (XG, '."N, '."E) nd on Himen Islnd (HMI, '.0"N, '.1"E). CPT mngrove ws rehbilitted nd now mture K. obovt forest plnted in t the high intertidl zone on the south bnk with density of 1.0 stem m - (Chen et l., 00) nd hd the highest cnopy height (.m). XG mngrove ws t the mid intertidl zone, bsed on its intertidl elevtions nd the intertidl zontion scheme in Jiulong River Estury, s described by Chen et l. (00); this mngrove ws composed of nturl nd dense K. obovt tress (.m-high, 1. stem m - ). The lowest vegettion density (0. stem m - ) nd cnopy height (.m) occurred in the mid-low nturl mngrove site on Himen Islnd. The width of ech smpling re ws ~0 m, ~0 m nd ~0 m from the lndwrd to sewrd fringes in the three mngrove sites, respectively, nd the smpling length ws round 0 m for ech site.. Soil to tmosphere greenhouse gs fluxes Soil to tmosphere fluxes of greenhouse gses were quntified in Jnury, April, August nd October 01, representing the sesons winter, spring, summer nd utumn, respectively. All smplings were conducted two hours before the lowest ebb tide during the dytime s the study res re subject to semi-diurnl tides nd the exposure times of mngrove wetlnds re reltive short. The tidl rnge,

6 tidl flooding nd exposure durtion were comprble mong the smpling dys nd the three mngrove sites. Nine replicte plots were chosen t ech mngrove site during ech smpling cmpign to chieve more ccurte estimtion of gs emissions becuse of high levels of sptil vrition, even on smll scle (Allen et l., 00; Chen et l., 0). Gs flux in this study ws quntified using the sttic (closed) chmber technique followed by gs chromtogrphy s described by Chen et l. (0). The circulr nd trnsprent chmbers were plced between the trees, in loctions without mngrove seedlings, boveground roots or litter fll to void the influences of these fctors on gs fluxes, nd the open end of the chmber ws inserted cm into the soil. The chmbers hd bsl re of 0.0 m, n internl volume (hedspce volume over the soil) of 1. l, nd did not include fn (Corredor et l., ; Buz et l., 00). The volume/bsl re rtio ws similr to those (1l vs. 0.0 m ) used by previous reserchers (Corredor et l., ; Buz et l., 00) which is sufficiently smll for the rpid increse in gs concentrtions. A comprison study by Moore nd Roulet (1) showed tht the fluxes mesured using sttic chmbers (0.0 m bsl re nd 0cm height) hs no difference from those using dynmic chmber (the insider ir ws circulted) with similr height, indicting tht the gs mixing in the sttic chmber ws s efficient s the dynmic chmber even with height of 0 cm. The chmbers used in this study hve hole t their top. When pushing the chmbers into soils, these holes were left open to eliminte the pressure disturbnce, nd were closed using rubber stoppers for first gs collection. The deployment time ws set to 0 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 chmber nd then injected into 0-ml gs smpling bg. Previous study by Chen et l. (01) reveled tht gses were continuously relesed nd their concentrtions were significntly nd linerly relted to the deployment time (with regulr smpling t 1-0 minutes intervls), even in event tht the gs concentrtions in the chmber were very high. In this study, the gs flux ws much lower thn those reported by Chen et l. (0), nd the dimension of smpling chmber ws the sme s tht used by them. Therefore, the smplings t -minute intervls were pproprite nd the rpid gs ccumultions in the chmber (especilly for CO ) would not result in significnt underestimtion of gs flux. Gs concentrtions were nlysed in prllel with gs chromtogrphy system (0A, Agilent Technologies, Snt Clr, Cliforni, USA) configured with single chnnel nd two detectors, by compring the pek res of smples ginst n Agilent Greenhouse Gs Checkout Smple (1 ppm

7 N O, ppm CH nd 00 ppm CO in N ). The N O nd CH concentrtions were determined with Ni electron cpture detector nd flme ioniztion detector (FID), respectively. The CO concentrtion ws nlyzed by FID fter methniztion. During the mesurement, the stndrd smple ws nlyzed in every 1-0 smples to ensure dt qulity. The reltive stndrd devitions of replicte stndrd mesurements were.%,.% nd.% for N O, CH nd CO, respectively. The soil to tmosphere fluxes of greenhouse gses were clculted using the following formul: F m = VΔM/Aρ where F m is the interfcil gs flux (mol m - h -1 ), V is the internl ir volume (m ) in the chmber fter being plced, ΔM (h -1 ) is the chnge in gs concentrtion in the continer, A is the surfce re of the soil (m ) nd ρ is the volume of per mol gs (m mol -1 ). During ech smpling, the open ir temperture ws simultneously mesured with mercury thermometer to clculte the ρ vlue. 1. Smpling nd nlysis of soil Soil prmeters were lso mesured t these smpling sites in summer to exmine their reltionship with gs fluxes s the fluxes hve been found to be higher in summer in subtropicl mngroves (Chen et l., 01) which is conducive this exmintion. Soil redox potentil (E h ) under the chmber ws mesured using ph/e h meter (WP-1, TPS, Austrli) fter gs smpling, by inserting the pltinum probe directly into the soil t depth of cm from the surfce. A soil smple to depth ~cm ws collected t ech plot using steel tube (i.d. 1.cm) with the open end shrpened, nd the bulk density ws estimted from the soil volume nd o C oven-dried weight. Independent soil cores to depth of 1 cm ( cores for ech mngrove site) were then collected using hnd-held PVC corers. Soil orgnic crbon (OC) concentrtion ws nlyzed using rpid dichromte oxidtion procedure. Totl Kjeldhl nitrogen (TKN) content fter Kjeldhl digestion nd NH + -N nd NO -N contents in the KCl (M) extrcts were mesured by the Continuous Flow Anlyzer (CFA, Futur II, Allince Instruments). All soil nlyses were bsed on the stndrd methods for soil nlyses described by Pge et l. (), nd the dt were expressed in terms of o C oven-dried weight. In ddition to the soil nlysis, slinity of the soil porewter ws only mesured t the sewrd fringe of ech mngrove site (three replictes for ech site) s porewter smple ws not vilble for ll smple sites. The slinity ws mesured using pocket refrctometer (0 0 prts per thousnds,

8 Atgo PAL-0 S, Jpn). Such mesurement does not revel the slinities within the mngrove wetlnds, but could reflect the slinity grdient mong the three mngrove sites.. Plnt CO sequestrtion rte Plnt CO sequestrtion rte ws clculted from the NPP, the crbon content nd the formul weights of CO nd C. Mngrove NPP ws estimted using the litter fll technique proposed by Tes (), which postultes tht 1/ of mngrove NPP is returned s litter fll. A globl extrpoltion by Bouillon et l. (00) lso showed cler reltionship between litter fll nd wood production nd further suggested tht litter production mounts to ~% of the totl mngrove NPP including root production. This rpid nd direct method ws lso pplied in other studies (e.g. Lee, 0; Alongi, 00), but its ccurcy depends on the vilbility of good conversion fctor (Odum et l., ). In this study, conversion fctor. ws pplied for the estimtion of NPP, which ws clculted from previously reported NPP (including root production) nd the concurrent litter fll production of K. obovt mngrove in the Jiulong River Estury (Lin et l., ). The men crbon content in vrious plnt frctions ws % for K. obovt in the Jiulong River Estury (Zheng et l., ). Litter fll smples were collected using metl-frmed litter trps (Φ=0 cm for surfce re, 0 cm depth) with -mm mesh. Nine trps were plced rndomly under cnopies t similr height bove the mximum tide level (1.m bove the sediment) t ech mngrove site. Trp contents were collected monthly nd sorted into the ctegories of leves, woods nd reproduction (flowers nd propgules), nd were then dried t 0 C to constnt weight nd weighed. The totl litter fll production ws expressed s the sum of these components... Mitigting effect of the mngrove ecosystem on tmospheric wrming The gs fluxes were converted to CO -equivlent fluxes to indicte their respective contributions to globl wrming using the GWP vlue of ech gs (1, nd for CO, CH nd N O, respectively, over 0-yer timefrme) ccording to Myhre et l. (01). The nnulized wrming effect of gs emissions t ech site ws then compred ginst the CO sequestrtion rte of plnts to estimte the ecosystem mitigtion effect. Net ecosystem productions of the three mngrove sites were lso estimted by subtrcting soil respirtion rte from NPP, nd the soil respirtion rte expressed s the totl crbon-gs flux ws clculted s the sum of CO -C nd CH -C fluxes.

9 The nnul fluxes of the three gses nd their wrming effects were clculted from the fluxes mesured in the four sesons during exposure periods for ech site (n=) or the three sites (n=). This estimtion ws subjected to the ssumptions tht the fluctutions in soil-tmosphere fluxes were insignificnt during exposure period nd the wter-tmosphere fluxes during inundtion were similr to those during exposure. The ssumption ws bsed on the following findings from previous studies (Chng nd Yng, 00; Bouillon et l., 00; Tong et l., 01). Although tidl effect on gs flux ws observed during the exposure in previous study (Chng nd Yng, 00), the results were inconsistent cross different mesurement cmpigns. The study by Chng nd Yng (00) showed tht gs fluxes in K. obovte wetlnd hd significntly more emission fter ebb tide thn before flooding in August, but the fluxes before flood were significntly higher thn tht fter ebb tide in My nd August. Our preliminry study lso showed tht the temporl vrition in gs flux ws insignificnt during the exposure (unpublished dt). On the other hnds, gses relesed from soils could be dissolved in tides during the flood, prtil of which is relesed to tmosphere from the sewter (Tong et l., 01). Bouillon et l. (00) reported tht there ws no significnt difference in the CO emission between exposed nd inundted periods. A diurnl mesurement of CH nd N O fluxes in n esturine mrsh in Fujin Province lso showed no cler difference between the inundtion nd exposure periods (Tong et l., 01). Therefore, the clcultions of nnul emissions from fluxes during exposure time obtined from imitted mesurement would not ffect the findings of the present study. Since the crbon sequestrtion by mngrove plnts is estimted bsed on net primry production, the CO relesed due to utotrophic respirtion of mngrove roots should not be included. Although CO emissions from some soils include the CO efflux from plnt roots nd heterotrophic respirtion (Lovelock, 00; Bulmer et l., 01), Komiym et l. (00) concluded tht most metbolic respirtion from mngrove roots is considered to be relesed through the lenticels nd underground roots of mngroves my only mke smll contribution to the soil respirtion when soil respirtion chmbers re plced where there is no peumtophore, becuse the erenchym tissues of underground roots re connected with lenticels on pneumtophores, prop roots, nd buttresses bove the ground (Tomlinson, ). In the present study, K. obovte develops no pneumtophore. The smpling points locted between the trees, nd there ws no obvious root biomss observed in the soil under the

10 chmbers. Thus, the CO flux ws more likely to represent metbolism of microbes (including microlge) in this study.. Sttisticl nlysis 1 The normlity of vribles ws checked using the Kolmogorov-Smirnov test, nd the gs fluxes tht did not follow norml distribution were trnsformed to improve normlity nd homoscedsticity prior to nlysis. Two-wy ANOVA ws used to test the 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 then used to determine wht the difference ws. Differences in litter fll production nd soil chrcteristics mong different mngroves were compred by using one-wy ANOVA. Person correltion coefficients were clculted to determine the reltionships between soil properties nd greenhouse gs fluxes in the summer. All sttisticl nlyses were performed using SPSS.0 for Windows (SPSS Inc., USA). 1 1 Results.1 Soil to tmosphere greenhouse gs fluxes The soil to tmosphere N O fluxes rnged from -1. to 0.0 μg m - h -1 in Jiulong River Estury (Fig. ), with nnulized CO -equivelent flux rnging from. to. g CO m - yr -1 in the three mngrove sites. According to the two-wy ANOVAs, N O flux nd its CO -equivelent flux (proportionl to gs flux) vried significntly mong the three mngrove sites (F=., p=0.000) nd mong the four sesons (F=.1, p<0.001). However, no significnt interction ws found between these two fctors (F=1., p>0.0). The highest N O flux ws mesured in the summer, while the lowest ws observed in the winter nd utumn. XG mngrove hd higher N O flux thn the other two sites with similr fluxes. The CH flux nd its CO -equivelent flux showed significntly sptil (F=1., p<0.001) nd sesonl (F=.0, p<0.001) vritions. The lowest flux ws -1. ug m - h -1 (mesured in HIM in winter), while positive fluxes in other mesurements indicted sources of CH in the mngroves. Significnt interction ws lso found between the two fctors (F=., p<0.001). The flux ws significntly higher in summer while the winter flux ws generlly the lowest. However, the highest

11 vlue of CH flux ws mesured in utumn (in XG), when the CH flux hd gretly sptil vrition (0.-0. ug m - h -1 ). For CO, the flux lso vried significntly mong the mngrove sites (F=., p<0.001) nd the four sesons (F=., p<0.001), nd the interction between these two fctors ws lso significnt (F=., p<0.01). Sinks of CO were mesured in the winter in the three mngrove sites; however, mngrove soils in the wrmer sesons cted s significnt CO sources. Significntly higher CO flux ws mesured in the summer, vrying from.0 to. mg m - h -1, irrespectively the mngrove sites The nnul men CO. g m - yr -1 fluxes were 1. g m yr, 0. g m yr nd 0 in CPT, XG nd HMI, respectively.. Soil chrcteristic in summer nd their reltionship with gs fluxes HMI mngrove hd slightly higher porewter slinity while there ws no difference in slinity between the other two sites (Fig. ). Soil chrcteristics, except NO - -N concentrtion, bulk density nd E h, vried significntly mong the three mngrove sites in Jiulong River Estury (Fig. ). Lower soil wter content ws mesured in CPT thn in other two sites (p<0.01). Soil NH + -N content ws lower in CPT nd HMI (p<0.0). XG mngrove site hd the highest soil OC nd TKN concentrtions nd the lowest concentrtions were mesured t HMI. Among the mesured soil prmeters mesured, NH + -N, OC nd TKN concentrtions were positively correlted with fluxes of the three gses nd the totl CO - equivelent flux (Tble ). No significnt effect ws detected for other soil prmeters on the gs fluxes.. Litter fll nd net primry productions 0 Litter fll productions rnged from 1 gdw m - yr -1 to 1 gdw m - yr -1 (Tble ) in Jiulong River 1 Estury mngroves. Lef fll nd reproduction components were 0 nd 1 gdw m - yr -1, comprising % nd 1% of the totl litter fll production, respectively. Using the conversion fctor., the net primry production of mngrove clculted from litter fll production ws -0 - gdw m in the three mngrove sites. Due to its lower lef nd twig productions, the litter fll production nd NPP mesured in HMI were lower compred to the other two mngrove sites,.. Mitigting effect of the mngrove ecosystem on tmospheric wrming In cse of high primry productions nd low soil crbon gs emissions, the mngrove wetlnds in this study hd NEP rtes rnging from 1 to g C m - yr -1 (Tble ), with men s g C m - yr -1.

12 The crbon gs emission ccounted for.-. % of the totl mngrove NPP, nd the CH mde negligible contribution (0. %-. %) to the totl crbon gs emission. Bsed on the CO -equivelent fluxes of the three gses (Fig. ), the totl CO -equivlent fluxes indicting the wrming effect of gs emission, were, 00 nd 0 g CO m yr 1, respectively, in the three sites (Tble ). The two trce gses, CH nd N O, contributed s much s.% of the totl CO -equivlent flux in XG, but contributed less thn % in the other two sites. When blncing the wrming effect of the gses nd the concurrent CO -sequestrtion rte of the mngrove plnts, the effect of the mngrove ecosystem on tmospheric wrming ws equl to -0 g CO m - yr -1 (Tble ), further indicting the mngrove wetlnd s n ffirmtive role in mitigting globl wrming. Discussion The subtropicl K. obovt mngrove forest in Jiulong River Estury hd high net primry productivity, close to or higher thn mounts reported in tropicl regions, nd higher thn the globl men production (Bouillon et l., 00). This is consistent with the summry by IPCC (01b), which shows tht some subtropicl mngroves hve higher growth rtes thn the tropicl. This high NPP nd low crbon gs emissions from soil in the present study indicted tht the mngrove wetlnds hve strong sequestrtion cpbility of tmospheric crbon on the ecosystem scle. The NEP in Jiulong River Estury (1- gc m - yr -1 ) ws lso higher thn the globl men vlue of 10 g C m - yr -1 reported by Bouillon et l. (00), nd those estimted in Rhizophor mngle forest (1 gc m - yr -1 ) in Puerto Rico (Golley et l., ) nd in the mngrove in western Florid Evergldes (0 gc m - yr -1, Brr et l., 0). Although CH emission ws lso significnt in the esturine mngrove wetlnds in this study, it ccounted for smll proportion (0.-.%) of the soil gseous crbon emission. The soil to tmosphere gs fluxes in the Jiulong River Estury fell within the rnges previously reported for other mngrove wetlnds (Chuhn et l., 00; Chen et l., 0). The results further demonstrted tht mngrove soils cn be sources of greenhouse gses which contribute to the wrming effect. With both plnt CO sequestrtion (showed in Tble ) nd soil gs emissions considered, mngrove wetlnds were smll sources for CH nd N O ( g N O m - yr -1 nd 0.. g CH m - yr -1 ) nd significnt CO sinks t rtes from -0 g CO m - yr -1 to - g CO m - yr -1. However, when considering their wrming effect, soil greenhouse gs emissions ccounted for.-. 1

13 % of the plnt CO sequestrtion rte in this study, indicting tht greenhouse gs emissions from mngrove soils could reduce the benefit of mngrove plnts. The net mitigting effect of the mngrove ecosystem on tmospheric wrming ws estimted to be from - g CO m - yr -1 to -1 g CO m - yr -1 in the three mngrove sites. As the three sites in this study locte t different res (north-shore mngrove nd islnd mngrove) in the estury nd cover both the rehbilitted nd nturl sites in this region, we considered they re representtive of the lrger entire estury. The mitigtion effect of the mngroves in Jiulong River Estury could be estimted s 0 g CO m - yr -1, suggesting tht mngrove wetlnd in this region, in term of the rdioctive forcing, is importnt sinks of tmospheric CO. Given tht the CO sequestrtion cpbility of globl mngrove is equls to g CO m - yr -1 nd tht soil CO flux offsets 0% of the CO sequestrtion rte (Bouillon et l., 00), the mitigting effect of globl mngrove is ssumed to be less -000 g CO m - yr -1 when the wrming effect of non- CO emission is considered. In the present study, the greenhouse gs fluxes were mesured t the cler surfce soils, nd the fluxes were minly derived from soil metbolisms. If Tke into ccount of the CO emissions from other source like decompositions of litter fll nd ded wood s importnt crbon pools in the mngroves (IPCC, 01b), the contribution of greenhouse gs emissions would be more significnt. Alongi (01) suggested tht the CO loss to ir due to funl respirtion could lso be considerble. Further studies re therefore needed with considertion of CO emissions from these sources. Globlly, mngrove NPP decreses with incresing ltitude nd the highest litter fll rtes occur in the tropicl res (Bouillon et l., 00; Alongi, 00). Some studies on the other hnd reported low greenhouse gs emissions from soils in tropicl mngroves (Chen et l., 01; Nóbreg et 1 l., 01). These suggest tht the tropicl mngrove could be more relevnt in mitigtion globl 0 wrming, nd their roles deserve detiled studies s the tropicl mngroves (e.g. Indonesin mngrove) comprise the mjority of globl mngroves (Giri et l., 0). Despite their low fluxes compred to CO, the contributions of the trce CH nd N O gses re lso relevnt (up to.%) to globl wrming in the mngrove wetlnds considering their wrming effect. When subjected to nthropogenic nutrient inputs, the emissions of these two gses nd CO, could be more considerble (Muñoz-Hincpié et l., 00; Chen et l., 0), which would lrgely enhnce their contributions to the wrming effect. High gs emission rtes hve been reported from mngrove soils, nd N O nd CH contributed twice the globl wrming potentil s CO in the Futin mngrove in South Chin which receives dischrges nd nthropogenic nutrient inputs from Perl River Delt nd 1

14 nerby polluted rivers (Chen et l., 0). As the fluxes of the CH nd N O re not still poorly quntified, their fluxes from mngrove soils therefore should receive more ttentions nd should lso be documented in ddition to tht of CO to quntify the contribution of greenhouse gs emissions from mngrove soil, especilly for those receiving exogenous nutrients. Liu nd Grever (00) hve lso suggested tht lthough the ddition of N incresed the globl terrestril C sink, CO sequestrtion could be lrgely offset by N stimultion of globl CH nd N O emissions. N O ws found to dominte the totl wrming effect of gs emissions in some gro-ecosystems (Mosier et l., 00). Mngrove production, gs fluxes nd the ecosystem mitigtion effect in this study vried sptilly with mngrove sites, with lower fluxes nd mitigtion effect observed t HMI due to much lower plnt CO sequestrtion rte. The vrition ws greter for gs fluxes, with CO flux rnging between s low s 0 g m - yr -1 nd up to 0 g m - yr -1, nd even greter sptil vrition ws found in CH flux. Wrming effect of the gs emissions in XG ws bout times of tht in HMI. Moreover, gs fluxes lso vried sesonlly. Such sptil nd sesonl vritions in gs fluxes, which re suggested to be minly due to fluctutions in temperture in subtropicl mngroves nd moisture in tropicl mngroves (Chen et l., 01), therefore should be tken into ccount for the inventory of greenhouse gs emissions. We lso mesured lower primry production ccompnied by low gs emission rtes in this study. Similrly, the soil respirtion rte ws found to be correlted with litter fll production on lrge rnge of ltitude extending from N to S (Lovelock, 00). This pttern suggested tht the more CO is sequestrted by mngroves, the more substntil the effect of the soil greenhouse gs emissions might be, nd their wrming effect should not be ignored. The sptil vritions of greenhouse gs fluxes could be prtly ttributed to the differences in soil chrcteristics mong the study sites s the gs fluxes re relted to mngrove soil properties including concentrtions of orgnic crbon, totl nd inorgnic nitrogen, bulk density, slinity nd redox potentil (Purvj nd Rmesh 001; Allen et l., 00; Chen et l., 0, 01). The higher gs fluxes were ttributed to higher soil orgnic crbon, nitrogen nd NH + -N concentrtions in mngrove soils (Tble ). This is similr to the findings in our previous studies in other subtropicl K. obvot-dominted wetlnds in South Chin (Chen et l., 0). Positive soil E h in the mngrove soil nd significnt correltion between N O flux nd soil NH + -N concentrtion indicted the importnce of nitrifiction process in mngrove soil tht is responsible for the N O production. Nevertheless, the results didn t exclude the potentil of denitrifiction for N O production s the soil E h in this study ws below 0 1

15 mv, below which denitrifiction usully strts (Pitty, ). Similrly to some other studies (e.g. Allen et l., 00; Chen et l., 0), high soil NH + -N concentrtion lso enhnced the CH emission into the tmosphere in this study, probbly due to the inhibition effect of soil NH + -N on CH oxidtion under high concentrtion (Bosse et l., ). Methne emission from the costl soils hs been known to be limited by high slinity s the presence of high sulphte in costl soils llows sulphte-reducing bcteri to outcompete methnogens for energy sources (Bisws et l., 00; Poffenbrger et l., 0; IPCC, 01b). Lower soil CH flux nd higher porewter slinity in HMI ws lso consistent with such inhibition effect. Soil temperture nd soil moisture were the two key environmentl fctors ffecting soil greenhouse gses fluxes nd driving their sesonl nd sptil vritions (Lovelock, 00; Poungprn et l., 00; Chen et l., 01). The CO flux cn be suppressed by elevted soil moisture (Poungprn et l., 00; Chen et l., 01; Lewis et l., 01), becuse the high degree of soil sturtion reduces the exposure of soil to ir nd decomposition rte of orgnic mtter. On the opposite, the high moisture cn stimulte nerobic respirtion in soils nd enhnce the CH flux (Lu et l., ). However, in this study, the soil wter moisture fluctuted in nrrow rnge nd hd no significnt impct on gs fluxes. No significnt correltions were found between soil E h (indictor of oxidtion-reduction potentil) nd the gs fluxes in the present study, nd flux vribilities were more relted to the C/nutrient vilbilities. Vritions in soil temperture hve been reported to influence gs fluxes (Lovelock, 00; Poungprn et l., 00; Chen et l., 01; Leopold et l., 01), nd higher temperture generlly induce higher gs fluxes. Although not mesured in this study, we consider tht soil temperture drives the sesonl vrition in gs fluxes in the mngroves in Jiulong River Estury. Some other studies in sltmrshes lso quntified the potentil globl wrming feedbcks bsed on the soil crbon sequestrtion rte nd non-co gs emission rtes (e.g. Chmur et l., 0; Yun et l., 01). Considering the rpid soil ccumultion rte in the mngrove wetlnd in Jiulong River Estury (. mol C m - yr -1, equivlent to. g CO m - yr -1, Alongi et l., 00), the globl wrming potentil of this mngrove re is determined to be ~0 g CO m - yr -1 (the CO -equivelent flux of CH nd N O fluxes hd sum of 0 g CO m - yr -1 ). This vlue ws higher thn those in northern nd northwestern Atlntic sltmrshes estimted in the growing seson (-00 g CO m - yr -1, Chmur et l., 0) nd in the mrshes in estern Chin (-1 g CO m - yr -1, Yun et l., 01). Unlike the slt mrsh, the crbon ccumultion of which through plnt growth is roughly blnced by 1

16 losses through grzing, decomposition nd fire (IPCC, 00, 01b), mjority of C cptured by mngrove plnt is stored in their biomss nd s detritus in soil. Tking these crbon sequestrtions into ccount, it cn be suggested tht the mngrove wetlnd plys more substntilly potentil role in mitigting globl wrming. Mngrove ecosystem is open nd dynmic in the crbon processes. Mjority of mngrove NPP is stored in plnt biomss; prtil litter fll production cn be decomposed, retined nd buried in the mngrove soil, while the rest is exported to the djcent costl wter. On the other hnd, mngrove ecosystem could lso bury the exogenous crbon during flooding periods (Twilley et l.,, Bouillon et l., 00). Mngrove ecosystem lso loses significnt orgnic crbon in dissolved (DOC) nd prticulte forms with tidl wter (Dittmr et l., 00; Bouillon et l., 00; Ye et l., 0), while the mjority of crbon export from mngroves might occur s dissolved inorgnic crbon (DIC, Bouillon et l., 00; Mher et l., 01). Alongi (01) recently suggested tht loss of DIC in mngrove soils vi subsurfce pthwys to djcent wterwys is lrge, t potentil rte up to 0% of nnul primry production. These processes determine the crbon sequestrtion potentil within mngrove wetlnd, which is relted to the potentil of mngrove wetlnd in reducing crbon gs emissions nd mitigting globl wrming, s the loss of crbon pool is equivlent to relevnt crbon dioxide emission to tmosphere (IPCC 01b). The present study ssessed the role of mngrove wetlnd in mitigting tmospheric wrming bsed on the greenhouse gs exchnge between mngrove ecosystem nd tmosphere. Considering the potentil of crbon sequestrtion of mngrove ecosystem in reducing crbon gs emissions, we further propose ssessment of the potentil of mngrove wetlnd in mitigting globl wrming by considertions of both the greenhouse gs emissions nd the crbon sequestrtion potentil s synthesis of the bove comprehensive crbon processes. Conclusions The present study showed tht mngrove soils re significnt sources of greenhouse gses, nd the wrming effect of gs emissions could prtilly offset the benefit of plnt CO sequestrtion to mitigting tmospheric wrming. We therefore propose tht ny ssessment of the mitigtion effect on tmospheric wrming should tke into ccount soil greenhouse gs emissions. The contributions of trce mounts of CH nd N O gses to the wrming effect re lso significnt nd should not be 1

17 ignored in mngrove wetlnds, especilly in those nutrient-enriched. Moreover, the temporl nd sptil vritions in gs fluxes nd plnt CO sequestrtion rte should be tken into ccount to improve the ccurcy of inventory of greenhouse gs emissions nd the estimtes of mitigting effect of mngroves on tmospheric wrming. Author contribution G. Chen designed the experiments, nd S. Chen nd D. Yu crried out the field smpling nd lbortory nlysis. B. Chen performed the dt nlysis. G. Chen wrote the first drft of the mnuscript, nd ll uthors contributed substntilly to revisions. Acknowledgements The work described in this pper ws supported by the Ntionl Nturl Science Foundtion of Chin () nd the Fujin Province Science nd Technology Pln Project (01Y00). The Progrm (01CB0) nd Science Reserch Foundtion of the Third Institute of Ocenogrphy, SOA (0), 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 lbortory nlysis, s well s Mr. Z.Y. Xue for ssistnce with mngrove site selection. We lso thnk Dr. Chnghu Weng for English edit. References Allen, D.E., Dll, R.C., Rennenberg, H., Meyer, R.L., Reeves, S., nd Schmidt, S.: Sptil nd 0 1 temporl vrition of nitrous oxide nd methne flux between subtropicl mngrove sediments nd the tmosphere, Soil Biol. Biochem.,, -1, 00. Alongi, D.M.: Crbon cycling nd storge in mngrove forests, Annu. Rev. Mr. Sci., :, 01. Alongi, D.M.: Crbon sequestrtion in mngrove forests, Crbon Mngement, (), 1, 01b. Alongi, D.M., Pfitzner, J., Trott, L.A., Tirendi, F., Klumpp, D.W.: Rpid sedimenttion nd microbil minerliztion in mngrove forests of the Jiulongjing estury, Chin, Estur. Cost. Shelf Sci.,, 0, 00.

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21 understnding of the role of vegetted costl hbitts in sequestering CO, Front. Ecol. Environ.,, 0, 0 Moore, T.R., nd Roulet, N.T.: A comprison of dynmic nd sttic chmbers for methne emission mesurements from subrctic fens. Atmosphere-Ocen, :1, -, 1. Mosier, A.R., Hlvorson, A.D., Peterson, G.A., Robertson, G.P., nd Sherrod, L.: Mesurement of net globl wrming potentil in three groecosystems, Nutr. Cycl. Agroecosys.,,, 00. Muñoz-Hincpié, M., Morell, J.M., nd Corredor, J.E.: Increse of nitrous oxide flux to the tmosphere upon nitrogen ddition to red mngroves sediments, Mr. Pollut. Bull.,, -, 00. Myhre, G., Shindell, D., Bréon, F.-M., Collins, W., Fuglestvedt, J., Hung, J., Koch, D., Lmrque, J.- F., Lee, D., Mendoz, B., Nkjim, T., Robock, A., Stephens, G., Tkemur T., nd Zhng, H.: Anthropogenic nd nturl rditive forcing, in: Climte Chnge 01: the Physicl Science Bsis Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmentl Pnel on Climte Chnge (eds. Stocker, T.F., Qin, D., Plttner, G.K., Tignor, M., Allen, S.K., Boschung, J., Nuels, A., Xi, Y., Bex V., nd Midgley P.M.), Cmbridge University Press, Cmbridge, 01. Nóbreg, G.N., Ferreir, T.O., Siqueir Neto, M., Queiroz, H.M., Artur, A.G., De S. Mendonç, E., De O. Silv, E., Otero., X.L.: Edphic fctors controlling summer (riny seson) greenhouse gs emissions (CO nd CH ) from semirid mngrove soils (NE-Brzil), Sci. Totl Environ.,,, 01. O dum, W.E., McInvor, C.C., nd Smith III, T.J.: The Ecology of the Mngroves of South Florid: Community Profile, United Sttes Fish nd Wildlife Service, Office of Biologicl Services, Wshington D.C.,. Pge, A.L., Miller, R.H., nd Keeney, D.R. (Eds.): Methods of Soil Anlysis Prt Chemicl nd Microbiologicl Properties, Wisconsin, USA: Americn Society of Agronomy,. Pitty, A.F. (Ed.): Geogrphy nd Soil Properties, Methuen, London, pp.,. Poffenbrger, H.J., Needelmn, B.A., nd Megonigl, P.J.: Slinity influence on methne emissions from tidl mrshes, Wetlnds, 1, 1, 0. Po ungprn, S., Komiym, A., Tnk, A., Sngtien, T., Mknul, C., Kto, S., Tnpermpool, P., nd Ptnponpiboon, P., Crbon dioxide emission through soil respirtion in secondry mngrove forest of estern Thilnd, J. Tropic. Ecol.,, -00, 00. 1

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23 Tble 1. Litter fll production nd net primry production (gdw m - yr -1 ) in the three mngrove sites in the Jiulong River Estury. Mngrove Lef Twig Reproduction Totl NPP CPT ±1 1± 1± 1± 0± XG ± ±1 ± ± ± HMI ±b ± b ±10 1±1 b ± b JRE 0± ± 1±0 ± 1± CPT: Coputou; XG: Xiguo; HMI: Himen Islnd; JRE: Jiulong River Estury; NPP: Net primry production. Different letters in one column indicte significnt difference mong the three mngrove sites. Dt re men ± SE of ech site or the three sites (n = for ech site nd n= for JRE, the sme s for Tble )

24 Tble. Person correltion coefficient vlues (r) between soil properties nd summer fluxes of greenhouse gses in Jiulong River Estury. Soil prmeter Fluxes of gses Totl CO - N O CH CO equivelent flux Redox potentil Bulk density Wter content NH + -N 0.* 0.0** 0.* 0.0** NO - -N OC 0.*** 0.*** 0.1** 0.1*** TKN 0.1*** 0.1* 0.** 0.*** OC: orgnic crbon, TKN: totl Kjeldhl nitrogen. *, ** nd *** indicte significnt r vlue t p<0.0, 0.01 nd 0.001, respectively (n=). No correltion ws done between porewter slinity nd gs flux s the porewter smples were collected out of the smpling res.

25 Tble. Net ecosystem production nd the mitigting effects of wetlnds on globl wrming in the Jiulong River Estury Net primry Net ecosystem Plnt CO Ecosystem mitigtion Study Soil C-gs flux CO equivlent flux A production production sequestrtion rte effect B site (g C m - yr -1 ) (g CO (g C m - yr -1 ) (g C m - yr -1 ) (g CO m - yr -1 m - yr -1 ) ) (g CO m - yr -1 ) CPT ±1 0± 0± ±00 (. %) (1.%) XG 1± ± ± 00± 0 (. %) (.%) HMI ±1 ± 1 ± 0± 1(. %) 1 (.%) JRE ± ±1 0± 1± (. %) 0 (0.%) CPT: Coputou; XG: Xiguo; HMI: Himen Islnd; JRE: Jiulong River Estury. Dt re mens ±SD for ech site or for the JRE (for gs flux, n= for ech site nd n= for JRE). Net primry production ws derived from litter fll production (Tble ) nd the crbon content in plnts ( %). Net ecosystem production ws estimted through NPP minus soil respirtion rte, i.e. soil C-gs flux (the sum of CO -C nd CH -C fluxes). The ecosystem mitigtion effect ws estimted by compring the nnulized wrming effect of gs emissions ginst the CO sequestrtion rte of plnts. A: Vlue in the brcket represents the proportion of N O nd CH gses to the totl CO -equivelent flux. B: Vlue in the brcket represents the proportion of wrming effect of gs emissions to the plnt CO sequestrtion rte.

26 Figure cptions Fig. 1 Mp of the Jiulong River Estury, Chin nd the typicl scene of the mngrove forest (A nd B). Numbers 1- indicte the positions of the three smpling sites in this study, 1: Coputou; : Xiguo; : Himen Islnd; Fig. Soil to tmosphere greenhouse gs flux (men±se, n= for the sesonl fluxes nd for the nnul men fluxes) t the mngrove sites in Jiulong River Estury. Sme bbrevition 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. Soil chrcteristics (men±se, n=) t the mngrove sites in Jiulong River Estury. Sme bbrevition s Fig. 1. Different letters indicted significnt difference mong the three mngrove sites ccording to ANOVA test.

27 Fig. 1