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Continental Shelf Research 68 (2013) 123–132

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Continental Shelf Research

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Research papers Biological response to typhoon in northern South China Sea: A case study of “Koppu”

Huaxue Liu a,b, Zifeng Hu a, Liangmin Huang a, Honghui Huang b, Zuozhi Chen b, Xingyu Song a,c,n, Zhixin Ke a, Linbin Zhou a a Laboratory of Marine Bio-resource Sustainable Utilization, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China b South China Sea Fisheries Research Institute, Chinese Academy of Fisheries Sciences, Guangzhou 510300, China c Marine Biology Research Station at Daya Bay, Chinese Academy of Science, Shenzhen 518121, China article info abstract

Article history: Obviously increased phytoplankton biomass and primary production was observed via both in situ investigation Received 24 May 2012 and remote sensing analysis in the northern South China Sea during typhoon Koppu′s intrusion in Received in revised form September 2009. Sea surface temperature declined in both coastal and offshore area when Koppu 31 May 2013 arrived. In the offshore waters, stratiﬁcation was weakened due to vertical mixing and sea surface Accepted 24 August 2013 temperature distribution pattern changed after the Koppu′s arrival. The in situ data showed that extreme Available online 2 September 2013 high primary production (PP) value (35 mgC m3 h1) appeared near the Dan′gan Island indicating a Keywords: potential algal bloom around the southern coastal waters of Hong Kong. Obviously increased nutrient Bloom loadings were also observed in the near-shore surface waters shortly after the typhoon′s arrival. Typhoon According to both in situ observation and remote sensing results, it is suggested that PP in the offshore South China Sea water was stimulated by extra vertical nutrient transport induced by Koppu; while the enhanced phytoplankton biomass and potential bloom along the coastal was mostly contributed by the increased Pearl River discharge after rainfall, which was also regulated by the typhoon event. & 2013 Elsevier Ltd. All rights reserved.

1. Introduction on the biological effects of typhoons on phytoplankton biomass in the offshore waters basically using ocean-color satellite data, while Tropical storms, also known as typhoons, hurricanes or cyclones, in situ studies, especially the possible responses of in situ primary are among the most extreme weather events affecting marine and production (PP) and related vertical biological profilestotyphoonsin coastalareasinthetropicalocean(Price, 1981). In addition to the SST an aquatic ecosystem have seldom been reported (Fogel et al., 1999). cooling, hurricane-induced vertical mixing can also bring up the Koppu was a category 1 typhoon that passed over the northern nutrient-rich water to the upper euphotic zone and thus stimulate SCS during September 11–15, 2009. Around this typhoon period, biological production. The processes of entrainment and upwelling an in situ investigation was conducted in the near-shore waters of bring up nutrients such as nitrate and phosphate from deeper layer the northern SCS. In addition, remote sensing data is also available to the upper euphotic zone and can stimulate phytoplankton blooms at that time, which provides us an opportunity to study the (Wu et al., 2007). Many studies have been carried out on biological typhoon impact on PP in the SCS with the coupled data. In present effect induced by typhoons, such as those in the East China Sea (Son study, we aimed to find out how the typhoon “Koppu” affected the et al., 2006; Chang et al., 2008), in the South China Sea (Lin et al., aquatic environment and further exerted influence on phytoplank- 2003; Zhao et al., 2008) and in the Northwest Atlantic (Babin et al., ton primary production based on both remote sensing and in situ 2004; Davis and Yan, 2004; Platt et al., 2005). Typhoons or tropical observation in the northern SCS. cyclones occurs frequently in the South China Sea (SCS), bringing sea surface cooling and phytoplankton blooms near their paths in the SCS, through strong vertical mixing (Chang et al., 1996; Zheng and Tang, 2007; Zhao et al., 2009). Previous studies were mostly focused 2. Material and methods

Koppu was a category 1 typhoon (Safﬁr-Simpson hurricane n Corresponding author at: Laboratory of Marine Bio-resource Sustainable Utili- scale), originated from the tropical depression in the Northwest zation, South China Sea Institute of Oceanology, Chinese Academy of Sciences, ﬁ 1 1 Guangzhou 510301, China. Tel.: þ86 20 890 23 201. Paci c (13.9 N, 129.6 E) at 0600 UTC on September 11, 2009, E-mail address: [email protected] (X. Song). strengthened to be a typhoon at 1200 UTC on September 14 with

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Fig. 1. Track of Typhoon Koppu. (Download from Hong Kong Weather Watch).

2 1 the strongest wind speed near continental shelf of the northern where IPPeu is the daily euphotic zone-IPP (mgC m d ), Csat 3 b SCS (Fig. 1). It has a relatively slow moving speed of 19.3 mph from the surface chlorophyll concentration (mgChl m ), Popt is the 0000 UTC on September 11 to 0000 UTC on September 13, and a optimal speciﬁc primary productivity, Dirr the daily photoperiod (h), relatively fast moving speed of 70 mph from 1200 to 1800 UTC on E0 the sea surface daily photosynthetically active radiation (PAR) (mol 2 1 September 14 near the Pearl River Estuary (PRE). Koppu reached quantna m d ), Zeu is physical depth (m) of the euphoric zone its peak intensity with estimated maximum wind speed of calculated from the satellite surface Chl a concentration (Cao and 140 mph near its center on 15 September. It landed at Taishan in Yang, 2002). Compared with other algorithms for retrieva1 of the western Guangdong Province in the morning and then euphotic depth based on the satellite surface Chl a concentration, weakened into a severe tropical storm. this has higher precision (Tang et al., 2007). The vertically integrated Chl a stock in the euphotic zone was derived from the SeaWiFS surface Chl a concentration following the algorithm of Behrenfeld b 2.1. Satellite data and Falkowski (1997). Popt was calculated from the empirical equa- tion provided by Behrenfeld and Falkowski (1997). Aside from surface To better understand the impact of typhoon, satellite observa- Chl a concentration, the major input data for the VGPM include sea tions were separated into three periods in 2009: before the surface daily PAR, SST, and length of solar radiation (Wang et al., typhoon′s arrival (September 4–10), under Koppu′s impact (Sep- 2008). The composites of PAR derived from SeaWiFS are taken from tember 14–20) and after the typhoon (October 1–7). Satellite data the web site (http://seadas.gsfc.nasa.gov). The lengths of solar radia- during the same periods in 2008 were also analyzed for compar- tion are taken from the data bank of IMCS Ocean Primary Productiv- ison. Satellite sea surface temperature (SST) and chlorophyll a (Chl ity Team (http://marine.rutgers.edu/opp/). a) data were acquired from the Moderate Resolution Imaging Spectroradiometer (MODIS) onboard Aqua via NASA‘s Ocean Color Working Group (http://oceancolor.gsfc.nasa.gov/). Daily MODIS 2.2. Typhoon track data standard Level 3 SST (4 4 km; nighttime) and chlorophyll (4 4 km) data were processed, and the composite images were The typhoon track data used in this study were available from based on the daily averages within different periods. the Unisys Weather Web site, which is based on the hurricane Chl a data derived from ocean-color images were used to track data issued from the Joint Typhoon Warning Center (Shang calculate the primary production with the VGPM algorithm et al., 2008). The data include the maximum sustained surface (Behrenfeld and Falkowski, 1997).The VGPM algorithm for estima- wind speed and the location of the hurricane center every 6 h. tion of the depth-integrated primary production (IPP) is expressed below: 2.3. In situ data

Locations of sampling sites were shown in Fig. 2. Station C1–C5 ¼ : b ½ =ð þ : Þ IPPeu 0 66125Popt E0 E0 4 1 CsatZeuDirr was investigated by the “Shiyan3” RV in August 16–17, 2008 and Author's personal copy

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SCS during that period (Zhao et al., 2009); then it increased to 30.01 1C during September 14–20 (Fig. 3e). During September 14–20, the mean SST in 2009 was about 0.6 1C lower than that in the same date period in 2008. During October 1–7, northeast monsoon prevailed in the SCS, and the mean SST decreased obviously in both the year of 2008 (26.95 1C, Fig. 3f) and 2009 (27.90 1C, Fig. 3c). Chl a always showed higher concentrations in the near-shore regions than offshore regions in the northern SCS. In 2008, the mean Chl a concentration was 2.72 mg m3 (Fig. 4d) during September 3–9whentyphoonT.Nuriinfluenced the northern SCS. It decreased to 0.81 mg m3 during September 14–20 (Fig. 4e). In 2009, the mean Chl a concentration was 0.85 mg m3 (Fig. 4a) before Koppu′s arrival, and increased to 2.01 mg m3 when the typhoon passed through the northern SCS (Fig. 4a and b). During October 1–7, Mean Chl a concentration was 0.65 mg m3 Fig. 2. Location of sampling sites in northern South China Sea. D: Dangan Island; 3 E1 and E2: monitoring station of Hong Kong Environmental Protection Department. (Fig. 4f) in 2008 and 1.0 mg m in 2009, respectively (Fig. 4c). The temporal variation of IPP showed similar distribution pattern with that of Chl a in 2008 and 2009. IPP averaged 1030 mgC m2 d1 (Fig. 5d) during September 3–9, 2008, and September 19, 2009 respectively, initiated by the South China Sea then decreased rapidly to 562 mgC m2 d1 during September Institute of Oceanology, CAS. Station D near the Dan′gan Island 14–20 (Fig. 5b). Conversely, in 2009, the mean IPP was was also investigated during the 2009 cruise. 517 mgC m2 d1 before Koppu′s arrival while it increased to Discrete samples were collected at various depths using a Rosette 652 mgC m2 d1 when the typhoon passed through the study sampler at four sites in 2008 (prior to the typhoon event) and six area, and then decreased (Fig. 5a–c). sites in 2009 (influenced by the typhoon event). Seawater salinity and temperature were determined by CTD (Seabird, USA). Seawater samples for Chl a analysis were immediately filtered through GF/F 3.2. Field observations filters,andstoredat20 1C. Chl a concentration was measured with a fluorometer (Turner-10-AU) according to Parsons et al. (1984). In Hong Kong, the wind was moderate and blew easterly on the PP incubation experiments were carried out in 2008 (C3) and 2009 night of September 13. The wind direction changed to be northeast (C5andD). PP was measured by the 14C assimilation method on the morning of September 14. As Koppu continued to move according to Knap et al. (1996) and Liu et al. (2011).Theincorporated closer to Hong Kong, the northeast wind became stronger in the radiocarbon was detected using a Beckman L6500 liquid scintillation afternoon. Thereafter, the wind direction gradually changed to be counter. southeast in the small hours of September 15 (Fig. 6). Free air The water quality data of station E1 and E2 were obtained from temperature decreased obviously during the passage of Koppu the Hong Kong Environmental Protection Department (http://epic. (Fig. 6). It was sunny in Hong Kong on September 13 but squally epd.gov.hk/ca/uid/marinehistorical). These two sites was close to thunderstorms affected Hong Kong in the evening. It was cloudy each other; in addition, based on correlation analysis results with squally showers on September 14. Heavy squally showers between them on salinity (E2¼0.9864 E1, r¼0.796, n¼108, affected Hong Kong on September 15 and more than 100 mm of Po0.001), temperature (E2¼1.0213 E1, r¼0.940, n¼108, rainfall were recorded in many meteorological stations of Hong Kong. Po0.001) and nitrate concentration (E2¼0.9766 E1, r¼0.806, Table 1 shows the main environmental characters in station E1 n¼103, Po0.001), they had very similar environmental distribu- and E2 in September, 2009. These 2 stations showed very similar tions during the year of 2007–2009. During the monthly investi- environmental distribution patterns according to the historical gations on September, 2009, E1 was sampled on September observation data (http://epic.epd.gov.hk/ca/uid/marinehistorical, 7 before the Koppu′s arrival; while E2 was sampled on September as suggested in section 1.3). Station E2 was investigated shortly 18 after the typhoon event. Therefore, in this study, we compare after the Koppu′s arrival (September 18), and showed 0.3–0.5 1C the differences between these two sites to indicate the typhoon lower on temperature than station E1, which was investigated impacts on environmental distributions. before the Koppu′s arrival (September 7). Obviously higher nitrate Data from the Hong Kong observatory (about 20 km away from concentration in the upper water layer was also observed in E2in station D) were also used (http://www.hko.gov.hk/informtc/tcMai- contrast with E1. Salinity and turbidity were similar between the n_uc.htm) for further analysis. two sites in the upper layer, but were obviously higher in the bottom water of E2 than that of E1. The surface Chl a of station E2 was nearly equal to Station D, and appeared to be much higher than that of E1. The difference on Chl a was little in the middle and 3. Results bottom water layers between E1 and E2. The vertical distribution of seawater temperature, salinity and Chl 3.1. Satellite observations a concentration along stations C1–C4wereshowninFig. 7. At station C1, low salinity water dominated the upper water layer SST generally decreased from near-shore to offshore waters in in both years, with both SSS values lower than 32. At C2, SSS was the northern SCS. When the Koppu affected the northern SCS in lower than 32 in 2008 but higher than 32 in 2009. At C3andC4, 2009, SST decreased around the typhoon-affected area in contrast salinity in water column was higher than 33. In 2009, the thermo- with that before Koppu′s arrival, despite the mean SST within the cline intensity in the investigated offshore area was weaker than that whole northern SCS appeared to be similar (Fig. 3a and b). in 2008, and the vertical stratification was less obvious than in 2008. In 2008, the mean SST within the study area was 28.97 1C In 2008, surface Chl a concentration decreased seaward from during September 3–9(Fig. 3d), since typhoon T. Nuri influenced the coastal waters, and the maximum record appeared at C1 Author's personal copy

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Fig. 3. Comparison on composed satellite image of SST between 2009 and 2008. (A) SST in September 3–9, 2009 (before Koppu′s arrival); (B) SST September 14–20, 2009 (during Koppu′s arrival); (C) SST in October 1–7, 2009 (after Koppu′s arrival); (D) SST in September 3–9, 2008; (E) SST September 14–20, 2008; (F) SST in October 1–7, 2008;

(Fig. 7). Subsurface Chl a maximum (SCM) were found at 10 m The distribution of PP and IPP were shown in Table 2. The depth at station C2, 50 m depth at station C3 and C4, respectively. surface PP at C3 was close to C5. An extreme high surface PP record In 2009, a near-surface phytoplankton bloom occurred at 10 m (35.00 mgC m3 h1) was found at the adjacent waters of Dan′gan depth of C1, with a maximum Chl a concentration of 3.11 mg m3. Island (Station D). If the column-integrated primary production in Chl a concentration at station C3 and C4 in 2009 was also the whole euphotic layer is concerned, IPP at station C5 reached obviously higher than in 2008. 1053 mgC m2 d1, which was more than twice of the value at C3. Author's personal copy

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Fig. 4. Comparison on composed satellite image of Chl a concentration between 2009 and 2008. (A) Chl a in September 3–9, 2009 (before Koppu′s arrival); (B) Chl a in September 14–20, 2009 (during Koppu′s arrival); (C) Chl a in October 1–7, 2009 (after Koppu′s arrival); (D) Chl a in September 3–9, 2008; (E) Chl a in September 14–20, 2008; (F) Chl a in October 1–7, 2008.

4. Discussion (Emanuel, 1999; Lee and Niller, 2003). Koppu decreased SST and weakened stratification in the northern SCS in 2009. Remote 4.1. Impact of SST cooling and vertical mixing on PP sensing result suggested that SST variation was influenced by typhoon and monsoon transition in 2008 (T. Nuri) and 2009 The SST cooling depends on many factors, such as the mixed (Koppu). In situ data also showed obviously different distribution layer depth, the thermocline depth and the air-sea heat fluxes patterns on SST in the year of 2008 and 2009. SST increased from Author's personal copy

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Fig. 5. Comparison on composed satellite image of IPP between 2009 and 2008. (A) IPP in September 3–9, 2009 (before Koppu′s arrival); (B) IPP in September 14–20, 2009 (during Koppu′s arrival); (C) IPP in October 1–7, 2009 (after Koppu′s arrival); (D) IPP in September 3–9, 2008; (E) IPP September 14–20, 2008; (F) IPP in October 1–7, 2008. near-shore to offshore in 2007 (Liu et al., 2011), which was similar accompanying variation of nutrient supply was probably the key to that in 2008; in contrast, the spatial variation of SST in 2009 via which coupled the physical and biological processes, and those confirmed that Koppu decreased SST in the northern SCS. physical processes which brought more nutrients to the euphotic Nutrients are often deficient in the upper layer of SCS and layer were important driving factors that could stimulate primary limits phytoplankton growth (Chen and Chen, 2006). In this study, production in this sea area. both in situ and remote sensing results suggested that the varia- According to the vertical profile of environmental factors when tion of SST during the typhoon event did not have a direct Koppu passed through, stratification in the upper layer along relationship with PP or phytoplankton biomass; therefore, the the relatively offshore waters (C1–C5) was weakened during the Author's personal copy

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Fig. 6. Temporal change of wind speed (m/s), precipitation (mm) and temperature of Hong Kong (near the Dangan Island) from September 3 to October 7, 2009.

Table 1 Comparison on environmental characters between E1 and E2.

Parameters Surface water Middle water Bottom water

E1 E2 E1 E2 E1 E2

Salinity (PSU) 31.5 31.4 31.6 31.8 32.2 33.1 Temperature (1C) 29.7 29.4 29.5 29 29 28.6 Turbidity (NTU) 1.6 2.7 1.7 3.7 2.1 14.7 Nitrate nitrogen (mg dm3) o0.002 0.023 0.004 0.019 0.011 0.008 Chlorophyll a (mg m3) 1.2 2.2 0.9 0.9 0.6 0.5

typhoon event, especially at C2 and C3, which was caused by waters (Fogel et al., 1999). Similarly, phytoplankton bloom occurred vertical mixing induced by Koppu. The distinctly increased phy- in Gulf of Mexico after the passage of the hurricane Katrina, and the toplankton biomass and IPP based on in situ and remote sensing mean Chl a concentration increased about 42%, which was attrib- data also suggested the contribution of nutrient supplement via uted to enhanced nutrient supply brought up by the wind-driven vertical mixing during the typhoon event. upwelling and vertical mixing (Shi and Wang, 2007; Liu et al., 2009). The ecological process in coastal waters may also be affected However, in this study, nutrient supply in the coastal waters was not by meteorological forcing such as storms and hurricanes via vertical contributed mainly by the vertical transport, since the bottom water mixing. For example, hurricane Gordon resulted in signiﬁcant had much lower nutrient concentration than the upper layer during change in primary production in the Atlantic coastal and Gulf Stream the typhoon event (Table 1). Author's personal copy

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Fig. 7. Vertical distributions of temperature, salinity and chlorophyll a concentration in August 2008 and September 2009. Author's personal copy

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Table 2 to the high phytoplankton biomass and potential algal bloom in the Phytoplankton biomass and production at the incubation site. near-shore waters.

Site 2008 2009

C3 DC5 Acknowledgements

Chlorophyll a ( mg m3) 0.14 1.93 0.09 IB (mg m2) 17.44 nd 47.0 This research was supported by the CAS Strategic Pilot Science 3 1 PPsur (mgC m h ) 1.74 35 1.91 and Technology under contract No. XDA10020200 and IPP (mgC m 2 d 1) 471 nd 1053 XDA05030403; the National Project of basic Sciences and Technol- ogy under contract No. 2012FY112400 and 2013FY111200; the Financial Fund of the Ministry of Agriculture (NO.NFZX2013); the 4.2. Impact of river discharge on primary production during the Special Fund of Basic Research for Centre Commonweal Scientific typhoon event Research Institute (NO. 2013TS07); and the National Nature Science Foundation of China (41276161, 41130855 and 41276162). Typhoon-associated precipitation often increased river runoff, The in situ research work was supported by the South China Sea resulted in an export of dissolved and particulate matter to coastal Open Cruise by R/V Shiyan 3, South China Sea Institute of waters after the typhoon, and stimulated phytoplankton growth Oceanology, CAS. The authors thank the Hong Kong Environmental (Herbeck et al., 2011). In this study, typhoon Koppu passed Protection Department, the Hong Kong Observatory and the through the Pear River estuary, where the second largest river in NASA‘s Ocean Color Working Group for their data support. China releases its discharge. The Pearl River discharge has been proved to have great impacts on phytoplankton distribution around the estuary and its adjacent waters (e.g. Yin et al., 2004; References Song et al., 2011). 3 1 High PP near the Dangan Island (35 mgC m h ) indicated a Babin, S.M., Carton, J.A., Dickey, T.D., Wiggert, J.D., 2004. 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