Typhoons exert signiﬁcant but differential impacts on net ...lees.geo.msu.edu/usccc/resources/paper/tu_typhoons_chen.pdf · Revised: 27 August 2014 – Accepted: 27 August 2014

Biogeosciences 11 5323ndash5333 2014wwwbiogeosciencesnet1153232014doi105194bg-11-5323-2014copy Author(s) 2014 CC Attribution 30 License

Typhoons exert significant but differential impacts on net ecosystemcarbon exchange of subtropical mangrove forests in China

H Chen12 W Lu12 G Yan12 S Yang1 and G Lin23

1Key Laboratory of the Ministry of Education for Coastal and Wetland Ecosystems School of Life Sciences XiamenUniversity Xiamen Fujian 361005 China2Division of Ocean Science and Technology Graduate School at Shenzhen Tsinghua University Shenzhen 518055 China3Ministry of Education Key Laboratory for Earth System Modelling Center for Earth System Science Tsinghua UniversityBeijing 100084 China

Correspondence toG Lin (linghmailtsinghuaeducn or linguanghuisztsinghuaeducn)

Received 15 April 2014 ndash Published in Biogeosciences Discuss 17 June 2014Revised 27 August 2014 ndash Accepted 27 August 2014 ndash Published 2 October 2014

Abstract Typhoons are very unpredictable natural distur-bances to subtropical mangrove forests in Asian countriesbut little information is available on how these disturbancesaffect ecosystem level carbon dioxide (CO2) exchange ofmangrove wetlands In this study we examined short-termeffect of frequent strong typhoons on defoliation and netecosystem CO2 exchange (NEE) of subtropical mangrovesand also synthesized 19 typhoons during a 4-year periodbetween 2009 and 2012 to further investigate the regu-lation mechanisms of typhoons on ecosystem carbon andwater fluxes following typhoon disturbances Strong windand intensive rainfall caused defoliation and local cool-ing effect during the typhoon season Daily total NEE val-ues decreased by 26ndash50 following some typhoons (egW28-Nockten W35-Molave and W35-Lio-Fan) but signif-icantly increased (43ndash131 ) following typhoon W23-Babjand W38-Megi The magnitudes and trends of daily NEE re-sponses were highly variable following different typhoonswhich were determined by the balance between the variancesof gross ecosystem production (GEP) and ecosystem respira-tion (RE) Furthermore results from our synthesis indicatedthat the landfall time of typhoon wind speed and rainfallwere the most important factors controlling the CO2 fluxesfollowing typhoon events These findings indicate that dif-ferent types of typhoon disturbances can exert very differenteffects on CO2 fluxes of mangrove ecosystems and that ty-phoon will likely have larger impacts on carbon cycle pro-cesses in subtropical mangrove ecosystems as the intensity

and frequency of typhoons are predicted to increase underfuture global climate change scenarios

1 Introduction

Although mangrove ecosystems only cover a small fractionof world forests they are highly important components incoastal and global carbon cycle (Bouillon et al 2008 Kris-tensen et al 2008 Donato et al 2011) They also provideother numerous ecological services such as coastal protec-tion fishery production biodiversity maintenance and nutri-ent cycling (Tomlinson 1986 Gilbert and Janssen 1998)However the global mangrove area has been reduced by1ndash2 per year and the mangrove area in China has beengreatly lost since the 1980s with only 22 700 ha remainingdue to aquaculture urbanization and other human activities(Alongi 2002 Duke et al 2007 Chen et al 2009)

Changes in tropical cyclone activities are an importantcomponent of global climate change and the characteristicsof tropical cyclones are likely to change in a warming climate(Webster et al 2005 Emanuel 2007 IPCC 2013 Knutsonet al 2010) Knutson et al (2010) predicted that the globalmean maximum wind speed of tropical cyclones would in-crease by 2ndash11 in 2100 and the frequency is likely todecrease by 6ndash34 Coastal mangrove ecosystems are es-pecially vulnerable to tropical cyclones due to their locationalong coastlines (Kovacs et al 2004 Milbrandt et al 2006Amiro et al 2010 Barr et al 2012) Although mangrove

Published by Copernicus Publications on behalf of the European Geosciences Union

5324 H Chen et al Typhoon impact on CO2 flux of mangrove ecosystems

ecosystems exhibit a high degree of ecological stability tothese disturbances the increased intensity and frequency ofstorms may increase damage to mangroves through defolia-tion and tree mortality (Alongi 2008 Gilman et al 2008)Dietze and Clark (2008) investigated the detailed dynamicsof vegetation to hurricane disturbance using designed exper-imental gaps and found that sprouts which constitute 26ndash87 of early gap regeneration played an important role inthe maintenance of diversity However little information isavailable on how these disturbances affect carbon dioxide(CO2) exchange of mangrove ecosystems partly due to fewdirect measurements of canopy level CO2 fluxes of mangroveecosystems before and after tropical cyclone disturbances(Amiro et al 2010 Barr et al 2010 Barr et al 2012)

A synthesis of the FLUXNET database underscored theimportance of stand-replacing disturbance regulation on car-bon budgets of ecosystems (Baldocchi 2008) Running(2008) also illustrated the less extreme disturbances shouldbe incorporated in future climate change studies Distur-bances such as tropical cyclones (typhoons hurricanes orcyclones) which have strong impacts on forest structuresand functions are very common but unpredictable to coastalecosystems (Turner and Dale 1998 Greening et al 2006)The most fundamental impact of such disturbances is the re-distribution of organic matter from trees to the forest floor in-cluding defoliation and uprooting stems (Kovacs et al 2004Milbrandt et al 2006 Li et al 2007 Barr et al 2012) De-foliation could not only greatly reduce LAI (leaf area index)and the daytime carbon uptake but also increase litter de-composition and result in large ecosystem respiration (RE)following this disturbance (Ostertag et al 2003 Ito 2010)

In recent years several studies examined possible im-pacts of typhoon or hurricane disturbances on net ecosys-tem CO2 exchange (NEE) (Li et al 2007 Ito 2010 Barret al 2012) After 10 typhoons struck Japan the canopycarbon gain of forests decreased by 200 g C mminus2 yrminus1 (Ito2010) Li et al (2007) reported a 22 decrease of GPP(gross primary production) and a 25 decrease of RE of ascrub-oak ecosystem after Hurricane Frances resulting in nosignificant change in NEE Stand-replacing hurricane distur-bances generally cause large defoliation and tree mortalityand hence large reduction in CO2 uptake over a long timeperiod (Amiro et al 2010 Barr et al 2012) whereas lessextreme disturbances that do not have significant damage tostems have negligible effects on NEE (Li et al 2007 Powellet al 2008)

The complex variations of NEE depend on the balance be-tween two interactive processes GEP (gross ecosystem pro-duction) and RE (Valentini et al 2000 Wen et al 2010Zhang et al 2010) GEP is mainly controlled by PAR (pho-tosynthetically active radiation) high VPD (vapor pressuredeficit) andTa (air temperature) that limit daily photosyn-thetic rates (Goulden et al 2004 Powell et al 2008 Keithet al 2012) GEP and RE respond independently to micro-climate but RE is regulated byTs (soil temperature) soil

water content and debris on the forest floor (Li et al 2007Kwon et al 2010 Barr et al 2012) Kwon et al (2010) ob-served that NEE depression occurred with different timingmagnitude and mechanism in a deciduous forest and farm-land during the Asian monsoon These results indicate thatthe relative effects of these microclimatic factors determinethe balance between GEP and RE and hence the differenttrends and magnitudes in NEE responses following distur-bances However the relationships among different tropicalcyclone disturbances microclimates and the carbon budgetsof ecosystems are not well understood Moreover it is essen-tial to investigate the regulations of typhoon characteristics(including wind speed landfall point frequency and dura-tion) on CO2 exchange of mangrove ecosystems

The main objective of this study was to examine short-term effects of frequent strong typhoons on microclimatedefoliation and net ecosystem CO2 exchange of two subtrop-ical mangroves in China We also synthesized 19 typhoonsduring a 4-year period between 2009 and 2012 to further in-vestigate possible mechanisms for the regulations of typhooncharacteristics on variations of ecosystem carbon dynamicsfollowing typhoon disturbances

2 Materials and methods

21 Site description

The measurements were made in two subtropical mangroveecosystems located in gulf of Gulei Fujian Province andYingluo Bay Guangdong Province in southern China Thefirst site Yunxiao mangrove study site (thereafter YX) issituated in the Zhangjiangkou National Mangrove NatureReserve (2355prime1459primeprimeN 11725prime490primeprimeE) This nature re-serve was established in 1997 as a provincial nature re-serve and was included in the Ramsar List in 2008 Thissite is dominated byKandelia obovata Avicennia marinaand Aegiceras corniculatum with the canopy height of 3ndash4 m Based on China Meteorological Administration the1981ndash2011 mean annual temperature and precipitation were211C and 1285 mm respectively For YX tides are irreg-ular semidiurnal and the high tides can reach up to 10 mabove the sediment with tidal water salinity ranging between1 and 22 ppt The second site Gaoqiao mangrove studysite (thereafter GQ) is located in the Zhanjiang NationalMangrove Nature Reserve (2134prime304primeprimeN 10945prime2233primeprimeE)This nature reserve is the largest mangrove nature reservein China and it was included into the Ramsar List in 2002This site is dominated byBruguiera gymnorrhiza A cornic-ulatumand A marina and the canopy height was about 3 mThe 1981ndash2011 mean annual temperature and precipitationwere 229C and 1770 mm respectively The tides of GQare regular diurnal and the high tides can reach up to 18 mabove the sediment with tidal water salinity ranging between1 and 30 ppt

Biogeosciences 11 5323ndash5333 2014 wwwbiogeosciencesnet1153232014

H Chen et al Typhoon impact on CO2 flux of mangrove ecosystems 5325

22 Eddy covariance and microclimatic measurements

The eddy covariance measurement systems were establishedin 2008 and 2009 at the YX and GQ sites respectivelyEach system was equipped with a three-dimensional sonicanemometer (CSAT3 Campbell Scientific Inc USA) andan open-path infrared gas analyzer (LI-7500 Li-Cor IncUSA) The CSAT3 and LI-7500 were mounted at heights of54 m for YX and 86 m for GQ The footprint was in the di-rection of the local prevailing winds which is southeast windfor YX and northeast wind for GQ The eddy flux data weresampled at 10 Hz and their mean variance and covariancevalues were calculated and logged at 30 min intervals usinga data logger (CR1000 for YX CR3000 for GQ CampbellScientific Inc USA)

Air temperatures and relative humidities were measuredwith temperature and relative humidity probes (HMP45ACVaisala Inc Finland) at heights of 30 m and 126 m for YXand 26 m 74 m 86 m and 140 m for GQ Soil tempera-tures were measured using temperature probes (109 Camp-bell Scientific Inc USA) at three sediment layers (5 cm10 cm 20 cm) for YX and at two sediment layers (10 cm20cm) for GQ and the average soil temperatures were alsomeasured using an averaging soil TC probe (TCAV Camp-bell Scientific Inc USA) at 10ndash20 cm sediment layer So-lar radiation PAR and net radiation were determined with apyranometer sensor (LI-200SZ Li-Cor Inc USA) a PARquantum sensor (LI-190SZ Li-Cor Inc USA) and a four-component net-radiation sensor (NR01 Hukseflux ThermalSensors Inc USA) respectively Soil heat flux was mea-sured with soil heat flux plate (HFP01SC Hukseflux Ther-mal Sensors Inc USA) Wind speeds (010C Met One In-struments Inc USA) and wind direction (020C Met OneInstruments Inc USA) were measured at heights of 30 mand 126 m for YX and 26 m 74 m and 140 m for GQ Pre-cipitation was measured using a tipping bucket rain gauge(TE525MM Texas Electronics Inc USA) The meteorolog-ical data were sampled at 1 s intervals and averaged valueswere recorded at 30 min intervals with a CR1000 data logger(Campbell Scientific Inc USA)

23 Flux data processing and gap filling

The eddy covariance data were processed with theEC_PROCESSOR software package (httpwww4ncsuedu~anoormeECP) (Noormets et al 2007) using the two-axis rotation and the WebbndashPearmanndashLeuning expression(Paw et al 2000 Mauder and Foken 2006) Sonic temper-atures were corrected for changes in humidity and pressure(Schotanus et al 1983) The 30 min fluxes were correctedfor the warming of IRGA (infrared gas analyzer) accord-ing to Burba et al (2006) We also removed anomalous orspurious data that were caused by rainfall events instrumentmalfunction power failure or IRGA calibration These in-troduced data gaps that were filled following the methods

Figure 1 (a) Paths of the 19 typhoons that passed over Yunxiao(YX) and Gaoqiao (GQ) mangrove sites during a 4-year period be-tween 2009 and 2012 and(b) category of each typhoon and itsdistancemin (the minimum distance from mangrove sites) during2009 and 2012

of Falge et al (2001) The mean diurnal variation methodwas used to fill short gaps by calculating the mean values ofthe same half-hour flux data with a 14-day moving windowLarger data gaps were filled using look-up tables For eachsite daytime and nighttime look-up tables were created foreach 2-month interval which was sorted by photosyntheticphoton flux density andTa After gap filling data were ex-tracted and analyzed with the micrometeorological data

24 Typhoon impacts on mangrove ecosystem

In this study we selected typhoons that were stronger thanCategory 8 (wind speed gt 172 m sminus1) and landed at a dis-tance less than 300 km from the YX or GQ sites based on datafrom China Meteorological Agency which resulted in a totalof 19 typhoons that passed over the YX and GQ site (Fig 1)during a 4-year period between 2009 and 2012 The charac-teristics of each typhoon including typhoon name DOYLand(the time of year that typhoon made landfall) duration (thelength of time when the typhoon occurred at a distance less

wwwbiogeosciencesnet1153232014 Biogeosciences 11 5323ndash5333 2014


than 300 km from our study site) category (Beaufort windforce scale) windLand (the maximum wind speed of typhoonwhen made landfall) windmindistance(the maximum windspeed near mangrove ecosystem when the typhoon was thenearest to it) distancemin (the minimum distance from man-grove study site during the typhoon period) and rainfall aresummarized in Supplement Table S1 If the dates of typhoonwere very close to each other (less than 7 days) or evenoverlapped we combined them as a single typhoon For ex-ample typhoon Lionrock Namtheum Meranti and Fanapiformed around late August and middle September and thenwe combined them as Lio-Fan To categorize the selected ty-phoons quantitatively we used the corresponding maximumwind speed and typhoon name to represent each typhoon Forexample the maximum wind speed of typhoon Lio-Fan was35 m sminus1 and then we used W35-Lio-Fan to represent thistyphoon

For each typhoon 5 clear days before and after the ty-phoon made landfall were selected to calculate the dailymean air and sediment temperature (Ta Ts) maximum airand sediment temperature (Tamax Tsmax) and photosynthet-ically active radiation (PAR) The daily gap-filled fluxes(NEE GEP RE and ET (evapotranspiration)) were calcu-lated the same way as these microclimatic factors For NEEvalues negative values represent net carbon uptake and pos-itive values represent net carbon release The light responsewas estimated with a form of MichaelisndashMenten equation(Barr et al 2010)

NEE= minusαPAR(1minus(PAR2000)+(αPARGEP2000))+Rd

Where α is the ecosystem quantum yield (micromol CO2(micromol PARminus1)) GEP2000 is the gross ecosystem productiv-ity (micromol CO2 mminus2 sminus1) when photosynthetically active radi-ation reaches 2000 micromol mminus2 sminus1 andRd is ecosystem res-piration (micromol CO2mminus2 sminus1) Delta values (1NEE 1GEP1RE 1ET 1α 1GEP2000 and 1 Rd) were estimated astheir differences between before and after each typhoonmade landfall For delta values negative values indicate de-crease following typhoon and positive values indicate in-crease after typhoon

The residuals of NEE (NEEresidual) from the light responsefunction (Barr et al 2010) were regressed against VPD andTa before and after the typhoon to quantify the magnitudethey regulate daytime NEE A more positive NEEresidual in-dicates less photosynthesis or more respiration To quantifytyphoon impacts on daily carbon and water fluxes we thenanalyzed the regulatory characteristics of typhoon on themusing data from 2009 to 2012 for YX and GQ

25 Litterfall measurements

To quantify litterfall production we randomly installed 5 Ltraps which were baskets constructed by 10 mm mesh sizenylon mesh under the canopy of each mangrove speciesaround the eddy tower with litter collected monthly oven-dried sorted and weighted as leaf twig flower and fruit (in-cluding hypocotyl)

26 Statistical analysis

The eddy covariance data were processed using softwareSAS version 90 (SAS Institute Inc USA) All measuredparameters before and after typhoon were presented asmeanplusmn standard deviation for five replicates The differencesin microclimatic factors carbon and water fluxes betweenbefore and after typhoon were tested using independent sam-ple t test The differences in daily carbon and water fluxesamong typhoons were analyzed by one-way analysis of vari-ance (ANOVA) Then Duncan post hoc tests were appliedto examine the differences after ANOVA The relationshipsbetween typhoon characteristics and microclimatic factorscarbon and water fluxes were also analyzed by linear regres-sion The statistical analyses were conducted with softwareSPSS version 160 (SPSS Inc USA)

3 Results

31 Typhoons and meteorological data

From 1945 to 2012 the annual typhoon initiation frequencywas 2527plusmn 610 and the frequency of landfalls on Chinawas 926plusmn 265 During 2009 and 2012 the typhoon initi-ation and landfall frequency was not very high There werethree and one typhoon that made landfall particularly nearYX and GQ (Fig 1a Supplement Table S1) Among them theminimum distance from YX and GQ was 9 km and 29 kmrespectively (Supplement Table S1) The duration of the ty-phoons that occurred at a distance less than 300 km from YXor GQ was 2879plusmn 1544 h on average ranging from 9 to74 h

From June to October typhoon brought strong wind ac-companied by torrential rain (Fig 2 Supplement Table S1)The monthly total rainfall showed significant correlationwith monthly maximum wind speed for our study sites (y =

1629x minus 15579 R2= 047 P lt 0001 for YX andy =

1105x minus 5066 R2= 019 P = 0004 for GQ) During the

typhoon period the strongest wind speed of typhoon reached40 m sminus1 and the strongest observed wind speed near ourstudy site can exceed 35 m sminus1 The magnitude of total rain-fall during the typhoon period ranged from 3 to 858 mmfor YX and from 02 to 1158 mm for GQ during 2009and 2012 Rainfall showed significant correlation with dura-tion of typhoon for our study sites (y = 212x minus1640R2

=

060 P = 0014 for YX andy = 159x + 019 R2= 047



Table 1Daily average microclimatic factors before and after typhoon made landfall for Yunxiao (YX) and Gaoqiao (GQ) in 2010 includingdaily means of air temperature (Ta) maximum air temperature (Tamax) soil temperature (Ts) maximum soil temperature (Tsmax) and totalphotosynthetically active radiation (PAR)

Typhoon Ta (C) Tamax(C) Ts (C) Tsmax(C) PAR (mol mminus2 dminus1)

W23-Parma Before 2829plusmn 065 3205plusmn 137 2768plusmn 028 2790plusmn 014 2881plusmn 835After 2757plusmn 080 3211plusmn 221 2641plusmn 051 2686plusmn 053 2965plusmn 668

W23-Babj Before 2928plusmn 030 3376plusmn 090 2765plusmn 013 2781plusmn 012 3865plusmn 194After 2755plusmn 029 3110plusmn 067 2654plusmn 013 2668plusmn 012 2867plusmn 413

W28-Nockten Before 2945plusmn 029 3334plusmn 095 2815plusmn 028 2841plusmn 034 3708plusmn 337After 2849plusmn 086 3237plusmn 131 2847plusmn 032 2873plusmn 029 2928plusmn 721

W35-Molave Before 2938plusmn 073 3343plusmn 134 2771plusmn 056 2864plusmn 051 4740plusmn 512After 2912plusmn 014 3296plusmn 118 2799plusmn 025 2886plusmn 028 4072plusmn 811

W35-Lio-Fan Before 2910plusmn 049 3399plusmn 084 2791plusmn 028 2941plusmn 032 3412plusmn 649After 2652plusmn 051 3295plusmn 092 2626plusmn 018 2791plusmn 038 2831plusmn 736

W38-Megi Before 2498plusmn 056 2851plusmn 088 2465plusmn 015 2486plusmn 024 2078plusmn 616After 1908plusmn 138 2294plusmn 080 2205plusmn 090 2242plusmn 089 2881plusmn 535

Figure 2 (a c) Maximum wind speed(b d) total weekly rain-fall for Yunxiao (YX) and Gaoqiao (GQ) during a 4-year periodbetween 2009 and 2012 The name and occurrence date of each ty-phoon are also shown

P = 0029 for GQ) Both daily mean and maximumTa sig-nificantly decreased after most of strong typhoon landfallswhile their variations were larger than those before typhoon(Table 1) The cooling effect of typhoon was less apparent inTs which led to smaller differences inTs andTsmax follow-ing typhoon With a few exceptions significant decreases indaily mean total PAR were observed (Table 1)

Figure 3 Monthly (a c e g)leaf litter and twig litter(b d f h)production for Yunxiao (YX) and Gaoqiao (GQ) in 2010 YX-AmAvicennia marinaat YX YX-Ko Kandelia obovataat YX GQ-BgBruguiera gymnorrhizaat GQ GQ-AcAegiceras corniculatumatGQ The name and occurrence date of each typhoon are also shown

32 Litterfall production

Mean annual litterfall production was84844 g DW mminus2 yrminus1 and 72862 g DW mminus2 yrminus1 forYX and GQ from 2009 to 2012 Leaf and twig litter were



Figure 4 Average daily(a) net ecosystem CO2 exchange (NEE)(b) gross ecosystem production (GEP)(c) ecosystem respiration(RE) and(d) evapotranspiration (ET) before and after six typhoonsmade landfall Dark grey bars represent the values during the ty-phoons that occurred at Yunxiao and light grey bars are for thoseduring the typhoons that occurred at Gaoqiao and standfor significant levelP lt 005 P lt 001 andP lt 0001 respec-tively

the largest components of total litterfall accounting formore than 75 of total litterfall for our mangrove sitesExcept leaf litter of A corniculatum monthly litterfallvaried seasonally with two peaks one in April to Mayand the other in July to August (Fig 3) Typhoon withstrong wind and heavy rain could cause defoliation Inthe typhoon season the highest monthly litter productionaccounted for 30 and 13 of annual litterfall for YXand GQ Moreover about 5 to 25 green leaves andtwigs appeared in litter traps after typhoon made landfallFor K obovata at YX site monthly twig litter produc-tion was significantly correlated with monthly maximumwind speed (y = 163x minus 1268 R2

= 014 P = 0015)and monthly total rainfall (y = 006x + 662 R2

= 010P = 0041) ForB gymnorrhizaat GQ site monthly leaflitter production was significantly correlated with monthlymaximum wind speed (y = 201x + 2429 R2

= 022P = 0004) and monthly twig litter production also showedsignificant correlation with monthly maximum wind speed(y = 077xminus521R2

= 026P = 0001) and monthly totalrainfall (y = 003x + 281 R2

= 021 P = 0005) ForAcorniculatumat GQ site only monthly twig litter productionshowed significant correlation with monthly maximum windspeed (y = 074x minus 134R2

= 011P = 0045)

33 Net ecosystem CO2 exchange

For typhoon effect on carbon and water flux values of man-grove ecosystems only six strong typhoons that made signif-icant changes on them were taken into account (Fig 4) Dailytotal NEE values were reduced following typhoon W28-Nockten (26 ) W35-Molave (39 ) and W35-Lio-Fan

(50 ) but significantly increased following typhoon W23-Parma (12 ) W23-Babj (43 ) and W38-Megi (131 )(Fig 4a) Daily total GEP values were all reduced signif-icantly following typhoon W28-Nockten (15 ) and W35-Molave (8 ) but no change in daily total GEP was observedfollowing the typhoon W23-Babj (Fig 4b) Typhoon W23-Parma and W38-Megi significantly suppressed daily totalRE values but typhoon W23-Babj increased the daily RE(Fig 4c) Typhoon W23-Parma also reduced daily total ETafter typhoon landfalls but typhoon W23-Parma caused theopposite change in ET (Fig 4d)

Table 2 summarized light response curve parameters be-fore and after strong typhoons made landfall near our studysites during the 4-year period between 2009 and 2012 Theapparent quantum yields (theαvalue) slightly decreased fol-lowing typhoon but there was no significant difference inα before and after each typhoon After typhoon W38-Megimade landfall GEP2000 value was smaller than before ty-phoon values (P lt 0001) RE rate (theRd value) before ty-phoon was more than twice the value after typhoon W38-Megi made landfall However after typhoon W23-BabjGEP2000 value was greater than before typhoon values (P =

0035) During the 4-year period between 2009 and 2012 theannual NEE ranged fromminus53998 tominus86580 g C mminus2 yrminus1

andminus69186 tominus73774 g C mminus2 yrminus1 for YX and GQ re-spectively (Table 4) The mean annual GEP was 1871 and1763 g C mminus2 yrminus1 respectively for YX and GQ during thesame period with corresponding mean annual total RE of1287 and 1096 g C mminus2 yrminus1 and REGEP of 069 and 063respectively

PAR was the most important control over daytime NEEalthough VPD andTa also exerted strong controls over day-time NEE (Fig 5 6) VPD above 15 kPa suppressed day-time NEE (Fig 5a e) After typhoon W28-Nockten landeddaytime NEE values were reduced by high VPD while theywere not affected by VPD before the typhoon (Fig 5e) Al-though highTa also reduced daytime NEE values after ty-phoon W28-Nockten it had little effect on daytime NEEbefore this typhoon made landfall (Fig 5f) After typhoonW38-Megi landed significant reduction inTa increased day-time NEE (Fig 5l)

34 Relationships of carbon and water fluxes withtyphoon properties

Variations in daily carbon fluxes and the model parameterswere explained by variations in typhoon properties (Table3) 1GEP values did not show significant relationships withtyphoon properties for YX and GQ However1NEE val-ues were strongly correlated with DOYLand (P = 0025) in-dicating that a typhoon that made landfall later in the yearcould increase daily NEE1α values were negatively cor-related with DOYLand (P = 0039) and rainfall (P = 0022)1RE values were also negatively related to windmindistance



Table 2Model parameters of light response curves before and after each typhoon landfall during 2009 and 2012α is the ecosystem quantumyield GEP2000 indicates the gross ecosystem productivity when photosynthetically active radiation reach 2000 micromol mminus2 sminus1 Rd representsecosystem respiration andP represents significant difference in model parameters comparing before and after typhoon

Typhoon α P GEP2000 P Rd P

(micromol CO2 (micromol PARminus1)) (micromol CO2 mminus2 sminus1) (micromol CO2 mminus2 sminus1)

W23-Parma Before 003plusmn 001 0538 2146plusmn 315 0085 253plusmn 106 0462After 002plusmn 001 1786plusmn 261 192plusmn 142

W23-Babj Before 003plusmn 003 0988 2257plusmn 416 0035 343plusmn 192 0775After 003plusmn 001 3074plusmn 592 380plusmn 196

W28-Nockten Before 003plusmn 001 0884 1765plusmn 209 0654 450plusmn 142 0218After 003plusmn 002 1708plusmn 176 270plusmn 265

W35-Molave Before 004plusmn 002 0182 1542plusmn 108 0651 491plusmn 202 0363After 002plusmn 001 1607plusmn 290 397plusmn 085

W35-Lio-Fan Before 003plusmn 002 0613 2538plusmn 209 0434 564plusmn 311 0294After 003plusmn 002 2434plusmn 193 358plusmn 268

W38-Megi Before 003plusmn 001 0079 2818plusmn 142 lt 0001 343plusmn 119 0009After 002plusmn 001 2085plusmn 143 146plusmn 047

Table 3 Linear regression coefficient (Coef) and significance probability (P) between daily ecosystem carbon fluxes change (1NEE1GEP and1RE) model parameters change of light response curves (1α 1GEP2000and1Rd) before and after typhoon made landfall andtyphoon characteristics (DOYLand duration category windLand windmindistance distancemin rainfall) The daily data from 2009 to 2012for Yunxiao (YX) and Gaoqiao (GQ) were used Thep value less than 005 is marked as bold number

Factor 1NEE 1GEP 1RE 1α 1GEP2000 1Rd

Coef P Coef P Coef P Coef P Coef P Coef P

DOYLand 0816 0025 0547 0204 minus0621 0137 minus0779 0039 minus0600 0154 minus0684 0090Duration minus0196 0674 0041 0931 0147 0752minus0481 0275 minus0099 0832 minus0303 0509Category 0160 0732 minus0165 0724 minus0536 0214 minus0287 0533 minus0516 0235 minus0307 0503WindLand 0100 0831 minus0226 0626 minus0506 0246 minus0238 0608 minus0501 0252 minus0289 0530Windmindistance 0314 0493 minus0281 0541 minus0802 0030 minus0043 0927 minus0514 0238 minus0320 0485Distancemin minus0371 0412 minus0301 0511 0381 0399 0518 0233 0274 0552 0507 0245Rainfall 0006 0989 0111 0813 minus0061 0897 minus0826 0022 minus0473 0284 minus0627 0132

(P = 0030) showing that typhoons with strong wind led tolower daily RE

4 Discussion

41 Impact of typhoons on defoliation of mangroveforests

We observed significant increase in litter production in bothmangrove forests in China following most typhoon events(Fig 3) suggesting that great defoliation occurred due to ty-phoon disturbances The immediate impacts of typhoon dis-turbance on canopy included defoliation and twig losses (Xuet al 2004 Li et al 2007 Ito 2010) which led to obvi-ous changes in LAI and albedo values (Barr et al 2012OrsquoHalloran et al 2012) The positive relationship betweenmonthly litter productions and monthly mean wind speedobserved here for GQ (Fig 3) also indicated a strong im-pact of wind disturbance on defoliation This is consistentwith the results from several previous studies which demon-

Table 4 Mean annual net ecosystem CO2 exchange (NEE) grossecosystem production (GEP) ecosystem respiration (RE) for Yunx-iao (YX) and Gaoqiao (GQ) during 2009 and 2012

Year NEE GEP RE(g C mminus2 yrminus1) (g C mminus2 yrminus1) (g C mminus2 yrminus1)

YX site2009 ndash53998 176255 1238462010 ndash588051 187507 1336702011 ndash75110 192832 1296842012 ndash85680 191933 127591

GQ site2009 N A N A N A2010 ndash73774 188972 1214822011 ndash69186 169819 1026892012 ndash73534 170314 104525



Figure 5Residuals of daytime net ecosystem CO2 exchange (NEE)at photosynthetically active radiation (PAR) as a function of vaporpressure deficit (VPD) and air temperature (Ta) before and after atyphoon made landfall Residual NEE was calculated by subtractingthe NEE expected based on light response function using observa-tions (PAR gt 500) from the observed NEE

strated higher monthly litter production during the typhoonseason (Tam et al 1998 Zheng et al 2000) Milbrandtet al (2006) observed no significant differences of hurri-cane impacts on litter production among mangrove speciesbut they found a negative correlation between canopy lossand the distance to hurricane eyewall Moreover typhoon-derived litter could immediately decompose on the forestfloor which increases litter decomposition and nutrient in-puts (Ostertag et al 2003) Thus significant increases inmangrove litter production following typhoon events are verycommon and will increase ecosystem respiration and nutri-ent supply for mangrove forest recovery At the same timeLi et al (2007) reported that lower LAI following wind dis-

Figure 6Light response curves before (grey circles) and after (darkcircles) six typhoons made landfall

turbances could result in lower soil respiration The intensiveand consecutive rainfalls also caused the reduced respirationduring the summer monsoon (Kwon et al 2010) Thereforethe positive correlation between rainfall and maximum windspeed for our study sites indicated strong winds control onRE

42 Impacts of typhoons on mangrove daytime NEE

We found inconsistent changes in daytime NEE follow-ing typhoon events with some typhoons (eg W23-BabjW38-Megi) increasing daytime NEE some typhoons (W28-Nockten W35-Molave W35-Lio-Fan) having the oppo-site effect and one typhoon (W23-Parma) having no effect(Fig 4) Ito (2010) observed that defoliation caused by ty-phoon greatly reduced CO2 uptake of a deciduous broadleafforest Li et al (2007) also reported a decrease in GPP be-cause of the reduction in LAI after hurricane disturbanceIn our study after typhoon W28-Nockten W35-Molave andW35-Lio-Fan made landfall the decrease in GEP was largerthan that of RE which resulted in significant decrease inNEE Although typhoon W38-Megi caused a reduction inGEP the large reduction of RE resulted in increased NEEKwon et al (2010) also reported that intensive rainfalls couldreduce respiration during the Asian monsoon GEP and REalso controlled the NEE values after typhoon W23-Parmaand W23-Babj (Fig 4) However Barr et al (2012) demon-strated that local heating effect following stand-replacinghurricane disturbances caused high respiration Thereforepossible effects of typhoons on daytime NEE depend on



forest types forest locations and various changes in microm-eteorological conditions due to typhoon events

For our subtropical mangrove forest sites the mean an-nual NEE values were smaller than those reported for tropicalmangrove ecosystems (Barr et al 2010) But the annual NEEvalues for our study site were substantially greater than thoseobserved in other temperate forest ecosystems in China (egWen et al 2010 Zhang et al 2010) Lower RE in mangroveecosystems was largely responsible for relatively high NEEvalues which also has been reported by Barr et al (20102012) At the same time tidal events generally result in sub-stantial lateral fluxes of particulate organic carbon dissolvedorganic carbon and dissolved inorganic carbon which mightoverestimate the NEE values observed by eddy covariancemeasurement (Bouillon et al 2008 Barr et al 2010)

VPD andTa were important secondary factors controllingdaytime NEE values especially after typhoon made land-fall (Fig 5) The less negative GEP2000 values following ty-phoon were likely due to carbon assimilation suppressed byhigh VPD andTa Our results for VPD also have been re-ported in previous studies (Goulden et al 2004 Powell etal 2008 Keith et al 2012) Daytime photosynthetic ratesof leaves could be limited by lower stomatal conductanceas a result of high VPD (Sano et al 2010) Additionallythe daytime NEE was much more sensitive to VPD follow-ing typhoon W28-Nockten AlthoughTa values were reducedfollowing typhoon highTa also could cause depression indaytime NEE This regulation can be explained by tempera-ture controls on both photosynthesis and respiration (Powellet al 2008) Goulden et al (2004) also demonstrated posi-tive correlation between NEEresidualandTa in the afternoonwhich was likely caused by highTa high VPD or a circadianrhythm

The large amount of rainwater from the rains induced bythe typhoons could significantly reduce the salinity in thetidal water surrounding the mangrove forest within the foot-print of the eddy flux tower which could exert a significanteffect on daytime CO2 flux by increasing light use efficiencyas shown in Table 3 The negative effects of salinity on lightuse efficiency of mangrove forests also have been reportedby Barr et al (2010) who observed small but significant lin-ear decreases in light use efficiency with increasing salin-ity during either wet or dry season Thus although rainfallfrom the typhoons plays a minor role in controlling CO2 fluxin terms of water availability the reduction in tidal watersalinity could influence the daytime CO2 flux of mangroveecosystems during the typhoon season

43 Regulation mechanisms of typhoons on ecosystemcarbon and water fluxes in mangrove forests

Although many studies have examined the impacts of ty-phoon or hurricane disturbances on CO2 fluxes in variousecosystems few have explored the regulation mechanismsof typhoon characteristics on mangrove carbon fluxes (Li et

al 2007 Ito 2010 Sano et al 2010 Barr et al 2012 Var-gas 2012) Results from our synthesis indicated that varia-tions of carbon fluxes following typhoon were strongly con-trolled by DOYLand windmindistanceand rainfall (Table 3)Rainfall control on RE was consistent with the finding ofKwon et al (2010) that intensive and consecutive rainfall re-duced respiration during summer monsoon Windmindistanceregulations on RE could be explained by wind damage oncanopy loss immediately after typhoon (Ito 2010) Althoughwe did not measure the changes in leaf area following ty-phoon the large litter production and their correlations withwind speed and rainfall during the typhoon season demon-strated the damage of typhoon on mangrove forest Thesediffer from the findings of extreme disturbance in whichstand-replacing damages cause significant large RE in thelong term (Amiro et al 2010 Barr et al 2012) However nodifference in RE after typhoon W28-Nockten W28-Molaveand W35-Lio-Fan observed in this study was consistent withthe findings of Li et al (2007) who found that less extremedisturbance did not increase respiration of forest ecosystem

The dynamics of daily NEE before and after typhoon werecomplex because NEE depends on both photosynthesis andrespiration processes They interact with each other and arecontrolled by relatively independent environmental factors(Li et al 2007 Wen et al 2010) Extreme hurricane distur-bances generally caused significant defoliation and plant up-rooting and then resulted in significant reduction in GEP andincrease in RE of mangrove ecosystems (Barr et al 2012)Reduced NEE values also have been reported by Lindroth etal (2008) who observed the reduction of NEE was causedby increased RE However less extreme disturbances havenegligible effects on NEE (Li et al 2007) Hurricane distur-bance has no significant effects on NEE due to the compen-satory reduction in GEP and RE (Li et al 2007) Actuallythere is great agreement between our results and those fromprevious studies which indicate climatic drivers on the bal-ance between carbon and uptake (Powell et al 2008 Wenet al 2010 Zhang et al 2010) These indicated typhoondisturbances reduced NEE or did not have significant impacton our mangrove study sites However a significant increasein NEE was observed at our study site after typhoon W38-Megi made landfall in early autumn which was due to thedecrease inTa and RE In this case the strong correlation be-tween1NEE values and DOYLand confirmed that the timingthat the typhoon made landfall also had an important con-trol on carbon exchange of mangrove ecosystems Althoughonly six typhoons caused significant changes in carbon fluxof mangrove ecosystems these results indicated that carbonflux dynamics were highly variable following typhoons

5 Conclusions

Typhoon disturbances frequently influence the subtropicalmangrove ecosystems in China Strong wind and intensive



rainfall caused defoliation and local cooling effect during ty-phoon periods The magnitudes and trends of daily NEE re-sponses were highly variable following different typhoonswhich were dependent on the balance between the changes ofGEP and RE Furthermore the results from our synthesis of19 typhoons demonstrated that DOYLand windmindistanceandrainfall were the most important factors controlling the car-bon fluxes following typhoon These findings indicated thatthe CO2 exchange of mangrove ecosystems responds differ-ently to various types of typhoon disturbances and futuretyphoons with increasing frequency and intensity will likelyhave large influence on carbon cycle processes of subtropicalmangrove ecosystems

The Supplement related to this article is available onlineat doi105194bg-11-5323-2014-supplement

AcknowledgementsThis study was supported financially bythe National Basic Research Program (973 Program) of China(2013CB956601) and the National Natural Science Foundation ofChina (30930017) We thank the Zhangjiangkou and ZhanjiangMangrove National Nature Reserve for allowing the study inthe field We appreciate Jiquan Chen Bin Zhao Haiqiang Guoand Dan Yakir for their help with eddy tower construction andflux data processing We also thank Jingfeng Xiao Yihui ZhangLuzhen Chen Wenjiao Zheng and Yue-Joe Hsia for their valuablesuggestions on our earlier version of the manuscript

Edited by J Xiao

References

Alongi D M Present state and future of the worldrsquosmangrove forests Environ Conserv 29 331ndash349doi101017s0376892902000231 2002

Alongi D M Mangrove forests Resilience protection fromtsunamis and responses to global climate change Estuar CoastShelf Sci 76 1ndash13 doi101016jecss200708024 2008

Alongi D M The energetics of mangrove forests Springer Dor-drecht 2009

Amiro B D Barr A G Barr J G Black T A BrachoR Brown M Chen J Clark K L Davis K J and De-sai A R Ecosystem carbon dioxide fluxes after disturbancein forests of North America J Geophys Res 115 G00K02doi1010292010jg001390 2010

Baldocchi D ldquoBreathingrdquo of the terrestrial biosphere lessonslearned from a global network of carbon dioxide flux measure-ment systems Aust J Bot 56 1ndash26 doi101071bt071512008

Barr J G Engel V Fuentes J D Zieman J C OrsquoHalloranT L Smith III T J and Anderson G H Controls onmangrove forest-atmosphere carbon dioxide exchanges in west-ern Everglades National Park J Geophys Res 115 G02020doi1010292009jg001186 2010

Barr J G Engel V Smith T J and Fuentes J D Hur-ricane disturbance and recovery of energy balance CO2fluxes and canopy structure in a mangrove forest of theFlorida Everglades Agr Forest Meteorol 153 54ndash66doi101016jagrformet201107022 2012

Bouillon S Borges A V Castantildeeda-Moya E Diele K DittmarT Duke N C Kristensen E Lee S Y Marchand C andMiddelburg J J Mangrove production and carbon sinks a re-vision of global budget estimates Glob Biogeochem Cycl 22GB2013 doi1010292007gb003052 2008

Burba G G Anderson D J Xu L and McDermitt D K Cor-recting apparent off-season CO2 uptake due to surface heating ofan open path gas analyzer progress report of an ongoing study27th Confercence on Agricultural and Forest Meteorology P44San Diego California 24 May 2006

Chen L Z Wang W Q Zhang Y H and Lin G H Recentprogresses in mangrove conservation restoration and research inChina J Plant Ecol 2 45ndash54 doi101093jpertp009 2009

Donato D C Kauffman J B Murdiyarso D Kurnianto SStidham M and Kanninen M Mangroves among the mostcarbon-rich forests in the tropics Nat Geosci 4 293ndash297doi101038ngeo1123 2011

Dietze M and Clark J S Changing the gap dynamics paradigmvegetative regeneration control on forest response to disturbanceEcol Monogr 78 331ndash347 doi10189007-02711 2007

Duke N C Meynecke J O Dittmann S Ellison A MAnger K Berger U Cannicci S Diele K Ewel K C andField C D A world without mangroves Science 317 41ndash42doi101126science317583441b 2007

Emanuel K Environmental factors affecting tropical cy-clone power dissipation J Climate 20 5497ndash5509doi1011752007jcli15711 2007

Falge E Baldocchi D Olson R Anthoni P Aubinet M Bern-hofer C Burba G Ceulemans R Clement R and Dol-man H Gap filling strategies for long term energy flux datasets Agr Forest Meteorol 107 71ndash77 doi101016S0168-1923(00)00235-5 2001

Gilbert A J and Janssen R Use of environmental functionsto communicate the values of a mangrove ecosystem un-der different management regimes Ecol Econ 25 323ndash346doi101016s0921-8009(97)00064-5 1998

Gilman E L Ellison J Duke N C and Field CThreats to mangroves from climate change and adap-tation options A review Aquat Bot 89 237ndash250doi101016jaquabot200712009 2008

Goulden M L Miller S D Da Rocha H R Menton M Cde Freitas H C Silva Figueira A M and de Sousa C A DDiel and seasonal patterns of tropical forest CO2 exchange EcolAppl 14 S42ndashS54 doi10189002-6008 2004

Greening H Doering P and Corbett C Hurricane im-pacts on coastal ecosystems Estuar Coast 29 877-879doi101007bf02798646 2006

IPCC Climate Change 2013 The Physical Science Basis Contri-bution of Working Group I to the Fifth Assessment Report of theIntergovernmental Panel on Climate Change Cambridge Univer-sity Press Cambridge and New York 2013

Ito A Evaluation of the impacts of defoliation by tropical cy-clones on a Japanese forestrsquos carbon budget using flux data



and a process-based model J Geophys Res 115 G04013doi1010292010jg001314 2010

Keith H van Gorsel E Jacobsen K and Cleugh H Dynam-ics of carbon exchange in a Eucalyptus forest in response to in-teracting disturbance factors Agr Forest Meteorol 153 67ndash81doi101016jagrformet201107019 2012

Knutson T R McBride J L Chan J Emanuel K Holland GLandsea C Held I Kossin J P Srivastava A and Sugi MTropical cyclones and climate change Nat Geosci 3 157ndash163doi101038ngeo779 2010

Kovacs J M Malczewski J and Flores-Verdugo F Exam-ining local ecological knowledge of hurricane impacts in amangrove forest using an analytical hierarchy process (AHP)approach J Coastal Res 20 792ndash800 doi1021121551-5036(2004)20[792elekoh]20co2 2004

Kristensen E Bouillon S Dittmar T and Marchand C Organiccarbon dynamics in mangrove ecosystems A review AquatBot 89 201ndash219 doi101016jaquabot200712005 2008

Kwon H Kim J Hong J and Lim J H Influence of theAsian monsoon on net ecosystem carbon exchange in twomajor ecosystems in Korea Biogeosciences 7 1493ndash1504doi105194bg-7-1493-2010 2010

Li J H Powell T L Seiler T J Johnson D P Ander-son H P Bracho R Hungate B A Hinkle C R andDrake B G Impacts of Hurricane Frances on Florida scrub-oakecosystem processes defoliation net CO2 exchange and interac-tions with elevated CO2 Glob Change Biol 13 1101ndash1113doi101111j1365-2486200701358x 2007

Lindroth A Lagergren F Grelle A Klemedtsson L LangvallO Weslien P and Tuulik J Storms can cause Europe-widereduction in forest carbon sink Glob Change Biol 15 346ndash355doi101111j1365-2486200801719x 2008

Mauder M and Foken T Impact of post-field data processing oneddy covariance flux estimates and energy balance closure Mete-orol Z 15 597-609 doi1011270941-294820060167 2006

Milbrandt E C Greenawalt-Boswell J M Sokoloff P D andBortone S A Impact and response of southwest Florida man-groves to the 2004 hurricane season Estuar Coast 29 979ndash984doi101007BF02798659 2006

Noormets A Chen J and Crow T R Age-dependent changes inecosystem carbon fluxes in managed forests in northern Wiscon-sin USA Ecosystems 10 187ndash203 doi101007s10021-007-9018-y 2007

OrsquoHalloran T L Law B E Goulden M L Wang ZBarr J G Schaaf C Brown M Fuentes J D GoumlckedeM and Black A Radiative forcing of natural forest distur-bances Glob Change Biol 18 555-565 doi101111j1365-2486201102577x 2012

Ostertag R Scatena F N and Silver W L Forest floor decom-position following hurricane litter inputs in several Puerto Ricanforests Ecosystems 6 261ndash273 doi101007s10021-002-0203-8 2003

Paw U K T Baldocchi D D Meyers T P and Wilson K BCorrection of eddy-covariance measurements incorporating bothadvective effects and density fluxes Bound-Lay Meteorol 97487ndash511 doi101023a1002786702909 2000

Powell T L Gholz H L Clark K L Starr G CROPPER WP and Martin T A Carbon exchange of a mature naturallyregenerated pine forest in north Florida Glob Change Biol 142523ndash2538 doi101111j1365-2486200801675x 2008

Running S W Ecosystem disturbance carbon and climate Sci-ence 321 652-653 doi101126science1159607 2008

Sano T Hirano T Liang N Hirata R and FujinumaY Carbon dioxide exchange of a larch forest after a ty-phoon disturbance Forest Ecol Manag 260 2214ndash2223doi101016jforeco201009026 2010

Tam N F Y Wong Y S Lan C Y and Wang L N Lit-ter production and decomposition in a subtropical mangroveswamp receiving wastewater J Exp Mar Biol Ecol 226 1ndash18 doi101016s0022-0981(97)00233-5 1998

Tomlinson P B The botany of mangroves Cambridge UniversityPress New York USA 1986

Turner M G and Dale V H Comparing large infrequent dis-turbances what have we learned Ecosystems 1 493ndash496doi101007s100219900045 1998

Valentini R Matteucci G Dolman A Schulze E D RebmannC Moors E Granier A Gross P Jensen N and PilegaardK Respiration as the main determinant of carbon balance inEuropean forests Nature 404 861-865 doi101038350090842000

Vargas R How a hurricane disturbance influences extreme CO2fluxes and variance in a tropical forest Environ Res Lett 7035704 doi1010881748-932673035704 2012

Webster P J Holland G J Curry J A and Chang HR Changes in tropical cyclone number duration and in-tensity in a warming environment Science 309 1844ndash1846doi101126science1116448 2005

Wen X F Wang H M Wang J L Yu G R and Sun X MEcosystem carbon exchanges of a subtropical evergreen conifer-ous plantation subjected to seasonal drought 2003ndash2007 Bio-geosciences 7 357ndash369 doi105194bgd-6-8691-2009 2010

Xu X N Hirata E Enoki T and Tokashiki Y Leaf lit-ter decomposition and nutrient dynamics in a subtropicalforest after typhoon disturbance Plant Ecol 173 161ndash170doi101023bvege00000293190598070 2004

Zhang Y P Tan Z H Song Q H Yu G R and Sun X MRespiration controls the unexpected seasonal pattern of carbonflux in an Asian tropical rain forest Atmos Environ 44 3886ndash3893 doi101016jatmosenv201007027 2010

Zheng F Z Lu C Y Zheng W J and Lin P Seasonal dynamicsof litter fall and energy flow through the leaf litter ofKandeliacandelmangrove in Jiulongjiang estuary Fujian province ChinaJ Xiamen University 39 693ndash698 2000



ecosystems exhibit a high degree of ecological stability tothese disturbances the increased intensity and frequency ofstorms may increase damage to mangroves through defolia-tion and tree mortality (Alongi 2008 Gilman et al 2008)Dietze and Clark (2008) investigated the detailed dynamicsof vegetation to hurricane disturbance using designed exper-imental gaps and found that sprouts which constitute 26ndash87 of early gap regeneration played an important role inthe maintenance of diversity However little information isavailable on how these disturbances affect carbon dioxide(CO2) exchange of mangrove ecosystems partly due to fewdirect measurements of canopy level CO2 fluxes of mangroveecosystems before and after tropical cyclone disturbances(Amiro et al 2010 Barr et al 2010 Barr et al 2012)

A synthesis of the FLUXNET database underscored theimportance of stand-replacing disturbance regulation on car-bon budgets of ecosystems (Baldocchi 2008) Running(2008) also illustrated the less extreme disturbances shouldbe incorporated in future climate change studies Distur-bances such as tropical cyclones (typhoons hurricanes orcyclones) which have strong impacts on forest structuresand functions are very common but unpredictable to coastalecosystems (Turner and Dale 1998 Greening et al 2006)The most fundamental impact of such disturbances is the re-distribution of organic matter from trees to the forest floor in-cluding defoliation and uprooting stems (Kovacs et al 2004Milbrandt et al 2006 Li et al 2007 Barr et al 2012) De-foliation could not only greatly reduce LAI (leaf area index)and the daytime carbon uptake but also increase litter de-composition and result in large ecosystem respiration (RE)following this disturbance (Ostertag et al 2003 Ito 2010)

In recent years several studies examined possible im-pacts of typhoon or hurricane disturbances on net ecosys-tem CO2 exchange (NEE) (Li et al 2007 Ito 2010 Barret al 2012) After 10 typhoons struck Japan the canopycarbon gain of forests decreased by 200 g C mminus2 yrminus1 (Ito2010) Li et al (2007) reported a 22 decrease of GPP(gross primary production) and a 25 decrease of RE of ascrub-oak ecosystem after Hurricane Frances resulting in nosignificant change in NEE Stand-replacing hurricane distur-bances generally cause large defoliation and tree mortalityand hence large reduction in CO2 uptake over a long timeperiod (Amiro et al 2010 Barr et al 2012) whereas lessextreme disturbances that do not have significant damage tostems have negligible effects on NEE (Li et al 2007 Powellet al 2008)

The complex variations of NEE depend on the balance be-tween two interactive processes GEP (gross ecosystem pro-duction) and RE (Valentini et al 2000 Wen et al 2010Zhang et al 2010) GEP is mainly controlled by PAR (pho-tosynthetically active radiation) high VPD (vapor pressuredeficit) andTa (air temperature) that limit daily photosyn-thetic rates (Goulden et al 2004 Powell et al 2008 Keithet al 2012) GEP and RE respond independently to micro-climate but RE is regulated byTs (soil temperature) soil

water content and debris on the forest floor (Li et al 2007Kwon et al 2010 Barr et al 2012) Kwon et al (2010) ob-served that NEE depression occurred with different timingmagnitude and mechanism in a deciduous forest and farm-land during the Asian monsoon These results indicate thatthe relative effects of these microclimatic factors determinethe balance between GEP and RE and hence the differenttrends and magnitudes in NEE responses following distur-bances However the relationships among different tropicalcyclone disturbances microclimates and the carbon budgetsof ecosystems are not well understood Moreover it is essen-tial to investigate the regulations of typhoon characteristics(including wind speed landfall point frequency and dura-tion) on CO2 exchange of mangrove ecosystems

The main objective of this study was to examine short-term effects of frequent strong typhoons on microclimatedefoliation and net ecosystem CO2 exchange of two subtrop-ical mangroves in China We also synthesized 19 typhoonsduring a 4-year period between 2009 and 2012 to further in-vestigate possible mechanisms for the regulations of typhooncharacteristics on variations of ecosystem carbon dynamicsfollowing typhoon disturbances

2 Materials and methods

21 Site description

The measurements were made in two subtropical mangroveecosystems located in gulf of Gulei Fujian Province andYingluo Bay Guangdong Province in southern China Thefirst site Yunxiao mangrove study site (thereafter YX) issituated in the Zhangjiangkou National Mangrove NatureReserve (2355prime1459primeprimeN 11725prime490primeprimeE) This nature re-serve was established in 1997 as a provincial nature re-serve and was included in the Ramsar List in 2008 Thissite is dominated byKandelia obovata Avicennia marinaand Aegiceras corniculatum with the canopy height of 3ndash4 m Based on China Meteorological Administration the1981ndash2011 mean annual temperature and precipitation were211C and 1285 mm respectively For YX tides are irreg-ular semidiurnal and the high tides can reach up to 10 mabove the sediment with tidal water salinity ranging between1 and 22 ppt The second site Gaoqiao mangrove studysite (thereafter GQ) is located in the Zhanjiang NationalMangrove Nature Reserve (2134prime304primeprimeN 10945prime2233primeprimeE)This nature reserve is the largest mangrove nature reservein China and it was included into the Ramsar List in 2002This site is dominated byBruguiera gymnorrhiza A cornic-ulatumand A marina and the canopy height was about 3 mThe 1981ndash2011 mean annual temperature and precipitationwere 229C and 1770 mm respectively The tides of GQare regular diurnal and the high tides can reach up to 18 mabove the sediment with tidal water salinity ranging between1 and 30 ppt























3 Results







=

060 P = 0014 for YX andy = 159x + 019 R2= 047

























= 011P = 0045)


























4 Discussion

























5 Conclusions







Edited by J Xiao

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3 Results







=

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= 011P = 0045)


























4 Discussion

























5 Conclusions







Edited by J Xiao

References






























































3 Results







=

060 P = 0014 for YX andy = 159x + 019 R2= 047

























= 011P = 0045)


























4 Discussion

























5 Conclusions







Edited by J Xiao

References











































































= 011P = 0045)


























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Edited by J Xiao

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= 011P = 0045)


























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Edited by J Xiao

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Edited by J Xiao

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5 Conclusions







Edited by J Xiao

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5 Conclusions







Edited by J Xiao

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Edited by J Xiao

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Documents

Typhoons exert signiﬁcant but differential impacts on net ...lees.geo.msu.edu/usccc/resources/paper/tu_typhoons_chen.pdf · Revised: 27 August 2014 – Accepted: 27 August 2014