Biogeochemical reSpoNSeS iN the SoutherN eaSt chiNa Sea after typhooNS

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To understand the biogeochemical impact of typhoons in marginal seas, 16 sea-going expeditions were conducted from 2007 to 2009, covering all four seasons and including periods following the passage of several typhoons in the southern East China Sea (SECS).Higher surface nitrate and chlorophyll a (Chl a) concentrations were measured in winter and spring, but surface nitrate (< 0.1 μM) and Chl a (0.47 ± 0.17 mg m -3 ) concentrations were low in summer under nontyphoon conditions.In comparison, elevated surface nitrate (0.2-2.3 μM) and Chl a concentrations (1.11 ± 0.40 mg m -3 ) were recorded in the SECS several days after the passage of each of three typhoons in 2008.The results demonstrate that nutrientrich waters are brought to the surface after the passage of typhoons, after which phytoplankton flourish.Most importantly, elevated particulate organic carbon (POC) fluxes (552 ± 28 mg C m -2 d -1 ) were observed after Typhoon Jangmi, about a threefold increase from the monthly mean value (184 ± 37 mg m -2 d -1 ).These field investigations demonstrate that typhoons can have a profound effect on nutrient supply, phytoplankton growth, and POC fluxes in marginal seas.(Liu et al., 2000).Walsh (1989)  to early winter (Sassa et al., 2008;Wang et al., 2008).Elevated phytoplankton biomass on the SECS shelf break has been documented (Gong et al., 1995(Gong et al., , 2000;;Chen, et al., 2001) and likely provides a good source of food for both adult and larval mackerels (Sassa et al., 2008).Researchers have found recurring upwelling off northeast Taiwan in the SECS (Chern et al., 1990;Liu et al., 1992;Jan et al., 2011, in this issue), and with it, transport of nutrients, mainly from subsurface Kuroshio waters, onto the shelf.However, some reports suggest that phytoplankton production in the ECS is limited in summer due to nitrogen deficiency (Chen et al., 2001;Liu et al., 2010).Satellite-derived average sea surface temperature (SST) in the SECS is about 28°C from July to September (Wang et al., 2008), suggesting that SECS surface water is likely nitrate-limited, based on the relationship between nitrate and temperature (Gong et al., 1995).The results of fishing catches (Figure 1) also suggest that nutrient supply may not support high biological productivity in the SECS in summer.
Elevated biogeochemical concentrations (e.g., nutrients, chlorophyll a [Chl a]) and new and primary production (NP and PP) in the SECS have been reported after an upwelling event (Chen et al., 2001;Gong et al., 2003).

Nitr ate Supply aNd phytopl aNktoN BiomaSS duriNg NoNt yphooN periodS
Under nontyphoon conditions, SST in the SECS shows great seasonal variation, ranging from 18.4° to 29.0°C, with the highest SST in summer, followed by autumn and spring, and the coldest value in January (Figure 3a).Surface nitrate concentrations in the SECS also exhibit significant seasonal variation, ranging from below the detection limit (~ 0.1 μM) to 4.1 μM, with maximum value in January, median value in spring, and lowest value in summer (Figure 3b).  1 and 2).Previous monthly and intensive investigations show similar values for the seasonal variation of SST and surface nitrate values in the SECS (Gong et al., 1995(Gong et al., , 2003;;Liu et al., 1992;Chen et al., 2001).Liu et al. (1992) and Gong et al. (1995) reported that the cold, nitrate-rich water brought to the SECS shelf area is mainly from bottom intrusion of Kuroshio water during autumn, winter, and spring.Despite the persistent southwest monsoon during summer over Taiwan Strait (June to September), nitrate-rich upwelled water at the surface has seldom been observed in the SECS (Liu et al., 1992;Gong et al., 1995).
Generally, the nitrate inventory in the SECS water column in summer is lower than that in other seasons.For example, the integrated nitrate inventory (I-NO 3 ) down to the bottom of the euphotic zone (defined as 1% of surface light intensity) in summer ranged from 0.05 to 0.293 (average = 0.161) mol-N m -2 (Table 2) measured in the euphotic zone (Table 2; Chen and Chen, 2008;Hung et al., 2009).
Based on field surveys, our current understanding of the summer nutrient supply in the SECS is that it cannot support the high biological activity that Hung et al. (2000) reported or that Chen et al. (2001) reported These concentrations imply that any agreement with previous studies, particularly the low Chl a concentrations during summer under good weather conditions.
The seasonal pattern of surface Chl a concentration in the SECS is similar to that of nitrate, suggesting that nitrate supply is directly related to phytoplankton growth (Figure 3c).
Because the study area is approximately 70 km from Taiwan, it could be argued that particle composition has been influenced by bottom resuspension or lateral advection from terrestrial inputs.As mentioned earlier, the bottom sediments in the study area are relic sand with low organic carbon content (< 0.3%; Liu et al., 1992).No large river is located near the study area, so the recent satellite ocean color data likely represent sea surface conditions that are unaffected by the influx of terrestrial materials (Hung et al., 2010a).Consequently, sediment resuspension and lateral particle transport are unlikely to have occurred in the study area (as suggested by Hung et al. [2003], the lateral transport occurred in deep depths).

chaNge S iN water-columN propertieS after t yphooNS
Satellite-derived SSTs and field data used in the present study show cooling after the passage of Typhoons Kalmaegi (no field data), Fungwong, Sinlaku, and Jangmi (Figure 2, Table 2).This cooling phenomenon near the SECS after the table 2. data on mixed layer depth (mld), euphotic zone (eZ: 1% of surface light intensity), surface nitrate (No 3 ), surface chlorophyll (chl a), integrated nitrate (i-No 3 ), integrated chl a (i-chl a), integrated particulate organic carbon (i-poc), and poc flux in the southern east china Sea, covering four seasons, including periods before and after typhoon events.passage of a typhoon has been observed frequently (Chang et al., 2008;Tsai et al., 2008;Zhao et al., 2008;Siswanto et al., 2007Siswanto et al., , 2009;;Hung et al., 2010a;Jan et al., 2011, in this issue).

Date
The greater level of wind mixing associated with Typhoon Jangmi likely increased the mixed layer depth (MLD, defined as the depth at which density increased by 0.1 kg m −3 compared with the density at the surface) to an extent greater than that associated with Typhoons Fungwong and Sinlaku (Table 1).Figure 2 shows that SST after passage of Typhoon Jangmi was colder than that after Typhoons Fungwong and Sinlaku.Additionally, the MLD after passage of Typhoon Fungwong (45 m) was deeper than the MLD zone (14-37 m) in summer when no typhoons occur.When nontyphoon conditions were prevalent in summer, the depth of the euphotic zone ranged from 38-65 m (Table 2).However, five to seven days after the Fungwong and Sinlaku typhoon events, the euphotic zones (EZ) became shallower, ranging from 30 to 34 m, respectively (Table 2), and the depth was only about half that of the mean euphotic zone depth reported by Gong et al. (2000) for this region (60 ± 10 m).
The shallow EZ after a typhoon may be a good indicator of higher phytoplankton biomass induced by nitrate supply.
eNhaNced Biogeochemical reSpoNSeS after t yphooNS Surface nitrate concentrations in the study area four to seven days after the passage of Typhoons Fungwong, Sinlaku, and Jangmi were 0.3, 0.2-0.3, and 1.9-2.3μM, respectively (Table 1).In comparison, surface nitrate concentrations during summer under pretyphoon conditions were generally below the detection limit (< 0.1 μM;  2).The data collected before and after the typhoon suggest that the strong winds and slow speed of Typhoon Jangmi led to upwelling of cold, nutrient-rich waters (Table 1).Babin et al. (2004) and Zheng and Tang (2007)  and internal tides (Tsai et al., 2008;Siswanto et al., 2009;Hung et al., 2010a).
Indeed, the strong correlation between integrated POC and nitrate concentration in the study area supports that concept (Figure 4).When nitrate supply in the water column reaches a certain threshold, the POC inventory is elevated, " iNteNSiVe field oBSerVatioNS coVeriNg four SeaSoNS, iNcludiNg periodS Before aNd Shortly after the paSSage of typhooNS, are proVidiNg eVideNce that typhooNS iNflueNce NutrieNt Supply, phytoplaNktoN dyNamicS, aNd carBoN export iN a coNtiNeNtal Shelf Break regioN." demonstrating that nitrate is an important source for phytoplankton growth.
As mentioned earlier, phytoplankton production in the East China Sea is likely limited by nitrogen in summer (Chen et al., 2001).The data suggest that the nitrate supplied through episodic typhoon events in the SECS contributes to phytoplankton growth, and thus is also important for zooplankton and larval fish.
Alternately, Babin et al. (2004) propose that the mixing of the subsurface Chl a maximum layer with low-Chl a surface water (e.g., phytoplankton dilution theory) can explain such increased surface phytoplankton biomass.

implicatioNS for poc fluxeS after t yphooN eVeNtS
The biogenic carbon flux to the deep ocean is one of the main factors affecting CO 2 partial pressure in the atmosphere.
Therefore, the amount of POC flux is crucial for understanding the global carbon cycle and its response to climate change (Emerson et al., 1997).Typhoons S p e c i a l i S S u e o N t h e o c e a N o g r a p h y o f ta i wa N The diatom Chaetoceros sp. is one of the dominant phytoplankton in the southern east china Sea in april and June.Biogeochemical reSpoNSeS iN the SoutherN eaSt chiNa Sea after typhooNS B y c h i N -c h a N g h u N g a N d g w o -c h i N g g o N g inventories as compared to the open ocean.Thus, marginal seas are believed to have crucial influence on marine carbon biogeochemical cycling (Liu et al., 2010, and references therein).Indeed, one of the major objectives of the international research project Land-Ocean Interaction in the Coastal Zone (LOICZ) is to quantify the exchange of carbon among continental shelves, marginal seas, and the open ocean.In addition, the coastal upwelling zones of marginal seas, among the most productive regimes of the marine food chain, contribute significantly to global fishery resources and catches (FAO, 2002).The East China Sea (ECS) is one of the largest marginal seas in the western Pacific Ocean.The southern East China Sea (SECS), a major ECS fishing ground, is located near the northern tip of Taiwan.Mackerel and swordtip squid are two of the most important fishery resources in the SECS, with a production season from approximately spring historical typhoon records, eight to ten typhoons pass the Asian continental marginal seas each year (see http://www.cwb.gov.tw).To better understand the biogeochemical impacts of typhoons on marginal seas, we present hydrographic information (e.g., temperature, nitrate concentration, and Chl a) and POC flux measurements in the SECS from 2007 to 2009, covering all four seasons and including periods following the passage of several typhoons (Figure 2, Table Field surveys from 2007 to 2009 indicate that surface nitrate concentration was below detection levels in the SECS during the summer months when no typhoons occurred (Tables figure 2. Satellite-observed (using advanced Very high resolution radiometer) sea surface temperature before (left panels) and after (right panels) typhoons in the southern east china Sea.typhoons include kalmaegi (a, b), fungwong (c, d), Sinlaku (e, f), and Jangmi (g, h).Solid lines on panels b, d, f, and g represent typhoon tracks in the western pacific ocean in 2008.red stars in panels d, f, and h represent sediment trap deployment locations.
this issue).Chen (2000) reported that the dominant phytoplankton composition in the SECS in April and June is diatoms (including Nitzschia sp., Thalassionema nitzschioides, Chaetoceros sp., Rhizosolenia fragilissima, and Leptocylindrus minimus), dinoflagellates (including Prorocentrum and Protoperidinium), Trichodesmium sp., and coccolithophores (Chen, 2000).Recent work of C.C. Chung of the Center for Marine Bioenvironment and Biotechnology, National Taiwan Ocean University, Keelung, Taiwan, and authors Gong and Hung shows that small dinoflagellates, such as Gymnodinium spp.and diazotrophic filamentous cyanobacteria Trichodesmium spp., were the dominant phytoplankton in summer under good weather conditions.poc fluxeS iN the SecS wheN No t yphooNS occur POC fluxes in the SECS, measured by floating sediment traps at 70 m depth, approximately 10 m below the bottom of the euphotic zone, at 25.40°N, 122.45°E, ~ 70 km northeast of Taiwan (Hung et al., 2003; 2010a) during nontyphoon periods did not show any remarkable seasonal variation, ranging from 140 ± 22 to 236 ± 25 mg-C m -2 d -1 , respectively (Table2 and Figure3).The trapping efficiency of floating sediment traps was 75% in the East China Sea(Li, 2009) and 80% in the oligotrophic waters of the Northwest Pacific Ocean(Hung and Gong, 2007), based on the 234 Th/ 238 U disequilibrium model ofHung et al. (2004) andHung et al. (2010b).Hung et al. (2003)  reported that POC fluxes measured by moored sediment traps in a region(i.e., 25.41°N, 122.35°E   and 25.34°N, 122.30°E)  similar to that of the present study ranged from 390 (at 325 m) to 730 mg-C m -2 d -1 mg-C m -2 d -1 , which are still lower than values reported byHung et al.   (2003).Normally, sinking material is remineralized or consumed by bacteria below the euphotic zone, decreasing figure 3. field-measured (a) sea surface temperature (t), (b) nitrate (No 3 ), (c) chlorophyll a (chl a) concentrations, and (d) particulate organic carbon (poc) flux in the southern east china Sea under nontyphoon conditions (black dashed line boxes) and after typhoon conditions (red box) from 2007 to 2009.Note: There are no surface nitrate concentrations during nontyphoon periods because they fall below the detection limit (< 0.1 μm).f = typhoon fungwong.S = typhoon Sinlaku.J = typhoon Jangmi.
cantly contributed to the measured POC fluxes, resulting in an overestimate of the vertical flux.Chen et al. (2001) reported that new production (down to 0.6% of surface light intensity) in the SECS was approximately 320 mg-C m -2 d -1 , and Hung et al. (2000) found that nitrate uptake rate (down to 10% of surface light intensity) in similar regions (i.e., 25.41°N, 122.35°E and 25.34°N, 122.30°E) was 226 mg-C m -2 d -1 .In other words, the POC fluxes measured by floating sediment traps are in agreement with those values measured by Chen et al. (

I
figure 4. relationship between integrated particulate organic carbon (i-poc) inventory and integrated nitrate (i-No 3 ) concentrations covering four seasons, including periods before and after typhoons.
figure 5. a simple diagram showing enhanced biological responses before and after typhoons in the summer.left panel: little cold, nutrient-rich water supports a marine food chain where dinoflagellates and cyanobacteria are the dominant phytoplankton species generating appropriate sinking particles under nontyphoon conditions.right panel: a robust supply of cold, nutrient-rich water supports a marine food chain where pinnate diatoms and centric diatoms are the dominant phytoplankton species generating elevated sinking particle fluxes after the passage of a typhoon.

Typhoon Wind Speed (m s -1 ) Landfall (mm/dd) Affecting Time (days) Cruise (mm/dd) SST (°C) Nitrate (μM) Chl a (mg m -3 ) Max Near ECS Before After Before After Before After
: SSt and chl a data for 25.2°N-25.7°N,122.1°e-122.6°ebeforetyphoon passage were derived using advanced Very high resolution radiometer (aVhrr) infrared sensors and moderate resolution imaging Spectroradiometer (modiS) ocean color, respectively.Nitrate concentrations before the typhoon were derived by the relationship between nitrate (nitrate = 33-1.25 x SSt; hung et al., 2010a) and SSt.SSt, nitrate, and chl a data were measured in the field shortly after typhoon passage at the trap station located at 25.40°N, 122.45°e.
vations for Chl a distribution patterns during nontyphoon conditions are in Chin-ChangHung (cchung@mail.nsysu.edu.tw)isProfessor,Institute of Marine Geology and Chemistry, National Sun Yat-sen University, Kaohsiung, Taiwan, and Professor, Institute of Marine Environmental Chemistry and Ecology, National Taiwan Ocean University, Keelung, Taiwan.Gwo-Ching Gong is Distinguished Professor and Director, Institute of Marine Environmental Chemistry and Ecology, Center of Excellence for Marine Bioenvironment and Biotechnology, National Taiwan Ocean University, Keelung, Taiwan.table 1. Sea surface temperature (SSt), nitrate concentration, and chlorophyll a (chl a) concentration before and after 2008 typhoons.Notemax = maximum wind speed ecS = east china Sea affecting time: time period in the southern east china Sea affected by typhoons.cruise: The field cruise was conducted four to eight days after typhoon landfall.Some SSt and chl a data before the typhoons were not available (na) due to cloud cover.