Response of Dissolved Oxygen and Related Marine Ecological Parameters to a Tropical Cyclone in the South China Sea

Available online at www.sciencedirect.com ScienceDirect

Advances in Space Research xxx (2014) xxx–xxx www.elsevier.com/locate/asr

Response of dissolved oxygen and related marine ecological parameters to a tropical cyclone in the South China Sea

Jingrou Lin a,b,c, Danling Tang a,b,⇑, Werner Alpers d, Sufen Wang a

a Research Center for Remote Sensing of Marine Ecology and Environment (RSMEE), State Key Laboratory of Tropical Oceanography, South China Sea Institute of Oceanology, Chinese Academy of Sciences, 164 West Xingang Road, Guangzhou 510301, PR China b Graduate University of Chinese Academy of Sciences, 19A Yuquan Road, Beijing 100049, PR China c South China Sea Marine Engineering and Environment Institute of State Oceanic Administration, Guangzhou 510300, PR China d Center for Marine and Atmospheric Sciences, Institute of Oceanography, University of Hamburg, Bundesstr. 53, D-20146 Hamburg, Germany

Received 5 April 2013; received in revised form 29 December 2013; accepted 7 January 2014

Abstract

It is well known that tropical cyclones can cause upwelling, decrease of sea surface temperature, increase of chlorophyll-a (Chl-a) concentration and enhancement of primary production. But little is known about the response of dissolved oxygen (DO) concentration to a typhoon in the open ocean. This paper investigates the impact of a typhoon on DO concentration and related ecological parameters using in situ and remote sensing data. The in situ data were collected 1 week after the passage of the super-typhoon Nanmadol in the northern South China Sea in 2011. An increase in DO concentration, accompanied by a decrease in water temperature and an increase in salinity and Chl-a concentration, was measured at sampling stations close to the typhoon track. At these stations, maximum DO concentration was found at a depth of around 5 m and maximum Chl-a concentration at depths between 50 and 75 m. The layer of high DO concentration extends from the surface to a depth of 35 m and the concentrations stay almost constant down to this depth. Due to the passage of the typhoon, also a large sea level anomaly (21.6 cm) and a high value of Ekman pumping velocity (4.0 104 ms1) are observed, indicating upwelling phenomenon. At the same time, also intrusion of Kuroshio waters in the form of a loop current into the South China Sea (SCS) was observed. We attribute the increase of DO concentration after the passage of the typhoon to three eﬀects: (1) entrainment of oxygen from the air into the upper water layer and strong vertical mixing of the water body due to the typhoon winds, (2) upwelling of cold nutrient-rich water which stimulates photosynthesis of phytoplankton and thus the generation of oxygen, which also increases the DO concentration due to cold water since the solubility of oxygen increase with decreasing water temperature, and, possibly, (3) transport of DO enriched waters from the Western Paciﬁc to the SCS via the intrusion of Kuroshio waters. Ó 2014 COSPAR. Published by Elsevier Ltd. All rights reserved.

Keywords: Dissolved oxygen; Tropical cyclone; South China Sea; Upwelling; Remote sensing; Kuroshio

1. Introduction upper ocean dynamics and the ecosystem, in particular upwelling, water temperature, salinity, chlorophyll-a Tropical cyclones, typhoons or hurricanes are strong (Chl-a) concentration, primary production (Price, 1981; wind events in the weather system, which inﬂuence the Price et al., 1994; Liu et al., 2002; Xu et al., 2005; Chang et al., 2006; Shi and Wang, 2007; Chen et al., 2009; Siswan- to et al., 2008, 2009; Smitha et al., 2006; Yang and Tang, ⇑ Corresponding author at: Research Center for Remote Sensing of 2010; Hung et al., 2010; Hung and Gong, 2011; Chung Marine Ecology and Environment (RSMEE), State Key Laboratory of et al., 2011) and ﬁsh abounce (Yu et al., 2013). Typhoons Tropical Oceanography, South China Sea Institute of Oceanology, can induce upwelling and thus transport nutrient-rich Chinese Academy of Sciences, 164 West Xingang Road, Guangzhou water to near-surface water levels (Zheng and Tang, 510301, PR China. Tel.: +86 13924282728. E-mail address: [email protected] (D. Tang). 2007; Chen et al., 2007; Chang et al., 2008; Siswanto

Please cite this article in press as: Lin, J., et al. Response of dissolved oxygen and related marine ecological parameters to a tropical cyclone in the South China Sea. J. Adv. Space Res. (2014), http://dx.doi.org/10.1016/j.asr.2014.01.005 2 J. Lin et al. / Advances in Space Research xxx (2014) xxx–xxx

Fig. 1. (a) Location of the study area (box S). (b) Track of the super-typhoon Nanmadol between 22 and 30 August 2011, location of the 17 sampling stations in the study area during the 2011 cruise, and the near-surface wind ﬁeld retrieved from ASCAT data acquired on 28 August. The Stations 1–5 are aligned along the transect A (marked by a black line).

Fig. 2. Horizontal distribution of DO concentration (in mg l1) at different depths at 19–22°N, 116–120°E (a–g). Location map (h). et al., 2008; Su and Pohlmann, 2009; Pun et al., 2011). Fur- DO in sea water is critical to marine life and primary thermore, they cause strong vertical mixing of the upper productivity. It is mainly influenced by composition and water layers above the thermocline (Dickey et al., 1998; decomposition of organic matter, by dynamic processes Jacob et al., 2000; Lin et al., 2003a,b; Lin, 2012; Shang in sea water, and by air–sea interactions (Han, 1995). et al., 2008). Previous studies mainly have focused on the The depth of maximum DO concentration is usually lies effect of typhoons on phytoplankton bloom (i.e., strong above the depth of maximum Chl-a concentration (Lin increase of Chl-a concentration), increase in primary pro- et al., 2001, 2003a,b). Furthermore, there is an inverse rela- ductivity, and decrease in water temperature (Cione and tionship between DO concentration and water temperature Uhlhorn, 2003; Smitha et al., 2006; Chen et al., 2007; Zhao (Long et al., 2006; Ning et al., 2009). et al., 2009; Sanford et al., 2011). But we know of no paper There exist several papers dealing with the response of dealing with the response of dissolved oxygen (DO) con- DO concentration to hurricanes or typhoons in estuaries. centration to typhoons in the open ocean. In estuaries, DO concentration can decrease in a short time

Please cite this article in press as: Lin, J., et al. Response of dissolved oxygen and related marine ecological parameters to a tropical cyclone in the South China Sea. J. Adv. Space Res. (2014), http://dx.doi.org/10.1016/j.asr.2014.01.005 J. Lin et al. / Advances in Space Research xxx (2014) xxx–xxx 3

a. Chlorophyll-a (mg/m3) b. Temperature (℃) c. Salinity (psu) 1 m

a1b1 c1 25 m

a2 b2 c2 50 m

a3 b3 c3

Fig. 3. Horizontal distribution of Chl-a concentration (a1–a3), temperature (b1–b3) and salinity (c1–c3) at depths of 1, 25 and 50 m. The units are: mg m3 in panels a, °C in panels b, and psu in panels c.

due to intrusion of saline water (Mitra et al., 2011a, 2011b; 2. Data and data analysis Van Dolah and Anderson, 1991; Stevens et al., 2006; Tom- asko et al., 2006). But it also can increase due to enhanced Since 2004, the South China Sea Institute of Oceanol- water exchange between upper and lower water layers. ogy, Chinese Academy of Sciences, Guangzhou, has been Chen et al. (2012) found that the DO concentration after conducting yearly cruises in the SCS, called “Northern the passage of the super typhoon Muifa was at a high level South China Sea Open Cruise”. The area, where oceano- for about 6–8 days and then returned to the normal values graphic measurements were carried out during the 2011 in about 11–13 days in the Changjiang (Yangtze) Estuary cruise (19–22.5°N, 116–120°E), is marked by the box S in 2011. inserted in Fig. 1, panel a. Its eastern section is located west During the cruise of the research vessel SHIYAN 3 of of the Luzon Strait, which connects the Western Pacific the South China Sea (SCS) Institute of Oceanology Ocean with the SCS. The sampling stations are marked between 19 August and 12 September 2011, the tropical by red stars in panel b. The five stations with the numbers cyclone Nanmadol passed over the northern SCS, which 1–5 are aligned along the transect A (19.5–21.5°N, 120°E). provided a rare opportunity to explore the response of Depth profiles of temperature and salinity (from the sur- DO concentration to a typhoon event. In this paper we face to a depth of 200 m) were measured by a Seabird con- present in situ measurements of DO and Chl-a concentra- ductivity-temperature-depth (CTD) sensor and depth tions as well as water temperature and salinity at sampling profiles of the DO concentration (from the surface to a stations close to the typhoon track 1 week after the passage depth of 50 m) by a multi-parameter water quality measure- of the tropical cyclone. In addition, satellite remote sensing ment instrument YSI 6600. Chl-a samples (from the surface data are used to supplement the shipboard data. to a depth of 200 m) having volumes between 0.5 and 2 l

Please cite this article in press as: Lin, J., et al. Response of dissolved oxygen and related marine ecological parameters to a tropical cyclone in the South China Sea. J. Adv. Space Res. (2014), http://dx.doi.org/10.1016/j.asr.2014.01.005 4 J. Lin et al. / Advances in Space Research xxx (2014) xxx–xxx (a) DO (mg/l) ) 3 -a Depth (m) Depth (m) (mg/m (b) Chl (b) Depth (m) (c) Temperature (c) Temperature Depth (m) (psu) (d) Salinity

120°E 543 2 1 19.5 20 20.5 21 21.5°N

Fig. 4. Depth profiles of the DO (a) and Chl-a concentrations (b), temperature (c), and salinity (d) along the transect A 1 week after the passage of the typhoon. Note that the depth scales in panel a reaches to 60 m, in panel b to 100 m, and in panels c and d to 200 m. were collected, filtered, and analyzed by a fluorescence spec- (ASCAT) onboard the European MetOp satellite (http:// trophotometer. In the present study, we measured Chl-a manati.star.nesdis.noaa.gov). Sea surface Chl-a concentra- concentration only down to a depth of 100 m, because the tion and sea surface temperature (SST) data (8-day com- Chl-a concentration was very low below this depth. posites with 4 km resolution) were derived from data of the Moderate Resolution Imaging Spectroradiometer 2.1. Typhoon track data (MODIS) onboard the Aqua satellite, which was launched in 1999. The data were downloaded from the Distributed The track data of the typhoon Nanmadol were obtained Active Archive Centre (DAAC) of NASA (http://oceancol- from the Unisys Weather Website (http://weather.uni- or.gsfc.nasa.gov). The sea level anomaly (SLA) and sea sys.com), which is based on typhoon data provided by surface height data (spatial resolution: 1/3° 1/3°, tempo- the Joint Typhoon Warning Center (JTWC). The data ral resolution: 7 days) were downloaded from the AVISO includes maximum sustained surface wind speed and longi- website (http://www.aviso.oceanobs.com). The SLA data tude and latitude of the center of the typhoon every 6 h. are merged data from the radar altimeters onboard the The category of the tropical cyclone is based on the Saf- ERS1/2, TOPEX/Poseidon, and Jason satellites. fir–Simpson scale. We also use the SLA data (or sea surface height g) downloaded from the AVISO website) to calculate geo- 2.2. Satellite data strophic velocities u =(u,v) and wind stress data downloaded from the NOAA website (http:// The near-surface wind field (25 km resolution) was manati.star.nesdis.noaa.gov) to calculate the geostrophic retrieved from data of the Advanced Scatterometer Ekman pumping velocity (EPV).

Please cite this article in press as: Lin, J., et al. Response of dissolved oxygen and related marine ecological parameters to a tropical cyclone in the South China Sea. J. Adv. Space Res. (2014), http://dx.doi.org/10.1016/j.asr.2014.01.005 J. Lin et al. / Advances in Space Research xxx (2014) xxx–xxx 5

Fig. 5. Depth proﬁles of the DO concentration (a), the Chl-a concentration (b), the temperature (c) and the salinity (d) at the Stations 1–5 along the transect A 1 week after the passage of the typhoon. Note that the depth scales in panel a reaches to 60 m, in panel b to 100 m, and in panels c and d to 200 m.

The geostrophic current is defined by: 3. Results g @g g @g u ¼ ; v ¼ ; 3.1. Characteristics of the tropical cyclone Nanmadol f @y f @x where g is the gravitational acceleration, f the Coriolis The tropical cyclone Nanmadol evolved from a tropical parameter, and g sea surface height. depression in the Western Pacific Ocean, then strength- The EPV is defined by: ened, moved northward and became a super-typhoon around 0000 UTC on 26 August 2011. It crossed the Luzon EPV ¼ curlðswind =qwf Þ; Strait between 0000 UTC on 27 August and 1800 UTC on where 28 August. After having crossed Taiwan, it decayed into a tropical depression and hit the Fujian Province on Main- s q C wind ¼ air DUU land China around 0000 UTC on 31 August. Nanmadol is the wind stress, qw the density of water, qair the density of crossed the Luzon Strait approximately 1 week before air, CD the wind drag coefficient, U the near-surface wind our research vessel arrived. Panel b of Fig. 1 shows the vector, and U the near-surface wind speed (absolute value track of the typhoon and its near-surface wind field on of U). 28 August 2011, when Nanmadol was located over the All remote sensing data were processed by using MAT- Luzon Strait. The wind speed reached 20 m s1 on 28 LAB, Surfer and SigmaPlot. August. The location of the sampling stations along the

Please cite this article in press as: Lin, J., et al. Response of dissolved oxygen and related marine ecological parameters to a tropical cyclone in the South China Sea. J. Adv. Space Res. (2014), http://dx.doi.org/10.1016/j.asr.2014.01.005 6 J. Lin et al. / Advances in Space Research xxx (2014) xxx–xxx

Fig. 6. Horizontal distribution of the Chl-a concentration (a1–a4), the sea surface temperature (SST) (b1–b4), and the merged sea level anomaly (SLA) (c1–c4), 1 week before, during the week, 1 week after, and 2 weeks after the passage of the typhoon. The Chl-a concentration (mg m3) and SST (°C) maps are 8-day composites retrieved from MODIS data and the SLA (cm) maps are weekly composites retrieved from altimeter data of several satellites.

transect A (120°E) near the Luzon Strait, marked 1–5, are high DO concentration is present at depths between the depicted in Fig. 1. Depth proﬁles of DO and Chl-a concen- surface and 40 m (marked by red boxes in Fig. 2, panels tration, water temperature and salinity were taken at 5 sta- a–f). At 50 m depth, the high DO concentration zone is tions 1 week after the passage of Nanmadol. Station 2 was absent. located closest to the typhoon track, and Station 5 farthest The horizontal distribution of Chl-a concentration, away from it. In the following, we shall concentrate dis- water temperature and salinity at depths of 1, 25, and cussing the data collected at Station 2, since they are the 50 m in the study area are plotted in Fig. 3. These plots ones most aﬀected by the typhoon. show that in the same area where the DO concentration is enhanced (20.5–21.5°N, 119.0–120.0°E, marked by red 3.2. Horizontal distributions of the marine parameters boxes), the Chl-a concentration, water temperature, and salinity also exhibit anomalies. Panels a1–a3 show that The horizontal distribution of DO concentration (in the Chl-a concentration increases with depth from an aver- mg l1) at depths of 1, 5, 10, 20, 30, 40, and 50 m in the age value of about 0.07 mg m3 at the surface to area S (19.0–21.5°N, 116.5–120.0°E) after the passage of 0.22 mg m3 at 50 m depth. The high value of the Chl-a the typhoon are depicted in Fig. 2. The DO concentration concentration at 50 m depth may suggest phytoplankton ranges from 6.17 to 6.72 mg l1, and has an average value bloom at this level. Simultaneously, the water temperature of 6.35 mg l1. The average DO concentration at 5 m depth decreases with depth from 29.55 to 27.27 °C (panels b1– is 6.46 mg l1, which is higher than at other depths. In the b3), while the salinity increases slightly with depth from eastern section (20.5–21.5°N, 119.0–120.0°E), a zone of 33.27 to 34.02 psu (panels c1–c3).

Please cite this article in press as: Lin, J., et al. Response of dissolved oxygen and related marine ecological parameters to a tropical cyclone in the South China Sea. J. Adv. Space Res. (2014), http://dx.doi.org/10.1016/j.asr.2014.01.005 J. Lin et al. / Advances in Space Research xxx (2014) xxx–xxx 7

Fig. 7. Daily averaged Ekman pumping velocity (m s1) of 28 August in 2011.

3.3. Vertical profiles along the Transect A The depth profiles of salinity (panel c) shows high salinity at Station 2 above 50 m, and a strong halocline at a The vertical profiles of DO and Chl-a concentrations, depth of 50 m. Note that at Station 2, there is a sharp hal- water temperature, and salinity measured along the tran- ocline at 50 m depth. Panel d shows higher water tempera- sect A (19.5–21.5°N, 120°E) between 3 and 4 September tures in the mixed layer at Stations 2 and 3 than at the 2011 are depicted in Figs. 4 and 5. The red dotted boxes other stations. Panel d shows lower water temperatures at inserted in Fig. 4 mark the area most affected by the Stations 2 and 3 in the upper layer (down to a depth of typhoon. At Station 2, which is closest to the typhoon 200 m) than at the other stations. track, the DO concentration reaches its highest value at 5 m depth, while the Chl-a concentration is highest at 3.4. Remote sensing observations of Chl-a, SST and SLA 50 m depth. At this station, the water temperature is lower and the salinity is higher than at other stations. Remote sensing data have been used widely in studies of Fig. 5 shows the same data collected at Stations 1–5 in the ecological response of water bodies to tropical cyclones another presentation. At Station 2, the DO concentration (Lin, 2012). The 8-day composite Chl-a concentration and is at all depths higher than at all other stations. At 5 m SST maps, as well as weekly SLA maps are depicted in depth, it is 6.50 mg l1 and at 35 m it is 6.45 mg l1. The Fig. 6. The three maps in the first column refer to the week depth profile of the DO concentration at Station 2 differs before the passage of the typhoon, the ones in the second significantly from the ones at all other stations. It stays column to the week when the typhoon was nearest to the almost constant at depths between the surface and 35 m, sampling stations, and the ones in the third and fourth col- while the depth profiles at all other stations sharply umns refer to 1 week and 2 weeks after the passage of the decrease with depth. Maximum DO concentration typhoon, respectively. (6.50 mg l1) is located at all stations at a depth of about The ellipse inserted into the SLA map (panel c3) shows a 5 m (panel a). The depth profiles of the Chl-a concentration strong negative SLA, indicating a strong cyclonic eddy, (panel b) show that at Stations 2 and 3 pronounced max- which is prone to cause upwelling of cold water. The area ima at 50 m depth. The maximum value measured at Sta- marked by an ellipse in panel b3 referring to 1 week after tion 2 is 0.4 mg m3, which is about four times the value the passage of the typhoon is cooler by approximately measured at Stations 1 and 5. This increase shows that 3 °C than 1 week before (panel b2). However, the Chl-a the typhoon triggered phytoplankton bloom at this layer. concentration map (panel a3) valid for the first week after Note that at Stations 2 and 3 not only the maximum value the passage of the typhoon is of poor quality due to cloud of the Chl-a concentration is higher than at the other sta- coverage. The map valid for the second week after the pas- tions, but also the layer of increased Chl-a concentration sage of the typhoon (panel a4) is of slightly better quality is thicker. and shows a slight increase in Chl-a concentration.

Please cite this article in press as: Lin, J., et al. Response of dissolved oxygen and related marine ecological parameters to a tropical cyclone in the South China Sea. J. Adv. Space Res. (2014), http://dx.doi.org/10.1016/j.asr.2014.01.005 8 J. Lin et al. / Advances in Space Research xxx (2014) xxx–xxx

(a) (b)

Fig. 8. Sea surface current (m s1) 1 week before (a), during (b), 1 week after (c) and 2 weeks after (d) the passage of the typhoon in Luzon Strait.

3.5. Ekman pumping velocity (EPV) visible east of the Luzon Strait. Panel a shows that 10 days before the passage of the typhoon, the Kuroshio was flow- The daily averaged EPV of 28 August is depicted in ing northward east of the Luzon Strait. Also a weak cyclo- Fig. 7. During the time the typhoon crossed the Luzon nic eddy located around 120°E, 22°N is visible. During the Strait, the EPV was negative along the typhoon track, indi- passage of the typhoon, this cyclonic eddy continuously cating strong upwelling. The EPV highest value reached its strengthened and interacted with the northward flowing highest value of 4.0 104 ms1 on that day. Kuroshio (panels b and c). Part of the Kuroshio waters followed the path of the cyclonic eddy, moved westward and intruded into the SCS as a loop current where it modified 3.6. Sea surface geostrophic currents the characteristics of the SCS waters (panel c). On 7 Sep- tember, i.e., 2 weeks after the passage of the typhoon, the The weekly composite sea surface geostrophic currents eddy had weakened (panel d). 1 week before, during, 1 week after and 2 weeks after the passage of the typhoon are depicted in Fig. 8. On all four 4. Discussion maps, a strong western boundary current (Kuroshio) is 4.1. Increase of DO concentration and entrainment

Typhoon The maps depicted in Fig. 2 clearly show that near the Station 2, at depths between the surface and 40 m, the horizontal distribution of the DO concentration is significantly Entrainment enhanced relative to the surrounding stations. This is also confirmed by the depth profiles of the DO concentration DO Kuroshio depicted in panels a of Figs. 4 and 5. Vertical Nutrient Increase mixing increase The fact that the DO concentration is enhanced at Sta- + tion 2 and is almost constant down to a depth of 35 m Upwelling Chl-a Temperature increase + decrease (Fig. 5, panel a) is a clear indication that (1) the increase of DO concentration in the upper layers after the passage of the typhoon is caused by the entrainment of oxygen Fig. 9. Schematic diagram showing the biochemical and physical processes induced by the typhoon Nanmadol causing increase in DO from the air and that (2) the water body is strongly mixed concentration. down to a depth of 35 m.

Please cite this article in press as: Lin, J., et al. Response of dissolved oxygen and related marine ecological parameters to a tropical cyclone in the South China Sea. J. Adv. Space Res. (2014), http://dx.doi.org/10.1016/j.asr.2014.01.005 J. Lin et al. / Advances in Space Research xxx (2014) xxx–xxx 9

Noted that the depth of maximum DO concentration between the Kuroshio and the eddy was strongest 1 week measured at all stations along the transect A (Fig. 1, panel after the passage of the typhoon. Since at Station 2, the b) is 5 m (Fig. 5, panel a), which is different from the depth salinity was higher than that at the other stations (panel of maximum DO concentration usually encountered in the dofFig. 4), we suspect that indeed Kuroshio waters SCS. According to Liu et al. (2005, 2011), the depth of intruded into the northern SCS since Kuroshio waters in maximum DO concentration in the SCS ranges from 20 the upper layers are more saline than SCS waters (Qu, to 75 m. In summer the average depth is 55 m, but in winter 2002). it is lower due the impact of strong winter monsoon with The advection of the surface waters from the western high winds. Our measurements show that after the passage North Pacific into the SCS caused by westward propagat- of the typhoon, maximum DO concentration is located at ing meso-scale eddies may also contribute to this effect. 5 m depth, which is well above the depth of the pycnocline Meso-scale eddies were present in this area from at least (around 50 m, see panels c and d of Fig. 5). Thus, we con- 1 week before and 2 weeks after the typhoon passed this clude that the typhoon winds, like the strong winter mon- area (Fig. 6c). soon winds, might give rise to an uplift of the layer of The different processes causing an increase in DO con- maximum DO concentration. centration by the passage of a typhoon are summarized in Fig. 9. 4.2. Increase of DO concentration and upwelling 5. Conclusions The increase of DO concentration induced by the typhoon is accompanied by an increase of Chl-a concentra- The ship-borne measurements carried out 1 week after tion and a decrease of water temperature with depth (Figs. 2 the passage of the typhoon Nanmadol in the northern and 3). At Station 2, which is closest to the typhoon track, South China Sea show that at the station closest to the upwelling of cold water and an increase in salinity is typhoon track a strong increase in DO concentration is observed (Panels c and d in Fig. 4), as well as an increase observed which reaches from the sea surface down to depth in Chl-a concentration in the subsurface layer. Further- of 35 m and which varies very little with depth. We have more, the occurrence of a negative SLA and a large EPV discussed three different mechanisms that can contribute (Figs. 6 and 7) shows that upwelling is quite strong in this to this increase, but we suspect that the entrainment of oxy- area. gen from the air into the upper water layer combined with Note that all our measurements were carried out at left strong vertical mixing of the water body due to the side of the typhoon track. In accordance with previous typhoon winds is the dominant mechanism. studies (Yang and Tang, 2010) the response of is here less We interpret the increase of DO concentration after the less strong than on the right side (see Fig. 6). passage of the typhoon being caused by the following three Upwelling of cold nutrient-rich waters contributes to the effects: increase of DO concentration after the passage of the typhoon by two effects: (1) enhancement of primary pro- (1) Entrainment of oxygen from the air caused by strong ductivity and thus increased generation of oxygen, and winds giving rise to enhanced vertical mixing in the (2) decrease of water temperature which increases the solu- upper water layers; bility of oxygen in water and thus the DO concentration. (2) Upwelling of cold nutrient-rich water to the upper layers, which stimulates photosynthesis of phyto- 4.3. Increase of DO concentration and Kuroshio intrusion plankton leading to generation of oxygen, and which also leads to an increase in DO concentration due to Intrusion of Kuroshio waters into the SCS frequently colder waters since the solubility of oxygen increase occurs in winter caused by high northeastern monsoon with decreasing water temperature; winds. In summer, the southwestern monsoon winds (3) Transport of DO enriched waters from the West Paci- restrain this intrusion. Previous investigations have shown fic to the South China Sea via Kuroshio intrusion. that typhoons can cause Kuroshio intrusion into the SCS via the interaction of the Kuroshio with typhoon-generated However, one has to keep in mind that the measure- cyclonic eddies (Sun et al., 2009; Miyazawa et al., 2008). ments reported in this paper were carried out in a com- Thus, we suspect that also during our cruise Kuoshio plex hydrological environment close to the Luzon Strait, waters had intruded into the SCS. where the Asian monsoon, the intrusion of Kuroshio The weekly maps of sea surface currents (Fig. 8) indicate waters into the SCS, and mesoscale eddies shed by the that indeed Kuroshio waters had intruded into the SCS Kuroshio affect the water body. Therefore it is difficult through the Luzon Strait, which might be partially caused to assess the effect of a single process on the ecology in by the northwestern typhoon winds. Part of the northward this region. Thus, more measurements at different loca- flowing Kuroshio waters followed the track of the typhoon tions and times have to be conducted, in order to get a and might have given rise to the generation of a cyclonic full understanding of the effect of typhoons on the DO eddy propagating into the northern SCS. The interaction concentration in the northern SCS.

Please cite this article in press as: Lin, J., et al. Response of dissolved oxygen and related marine ecological parameters to a tropical cyclone in the South China Sea. J. Adv. Space Res. (2014), http://dx.doi.org/10.1016/j.asr.2014.01.005 10 J. Lin et al. / Advances in Space Research xxx (2014) xxx–xxx

Acknowledgments Lin, H., Cheng, S., Han, W., Wang, H., 2003a. Seasonal features of the dissolved oxygen maximum in vertical distribution in the Nansha This work is jointly supported by research projects Islands. Acta Oceanol. Sin. 22, 9–15 (in Chinese). Lin, I.I., Liu, W.T., Wu, C.C., et al., 2003b. New evidence for enhanced awarded to D.L. Tang: (1) National Natural Sciences ocean primary production triggered by tropical cyclone. Geophys. Res. Foundation of China (31061160190, 40976091, NSFC– Lett. 30, 1718. RFBR Project -41211120181,Tang and Dmitry); (2) Liu, K.-K., Chao, S.Y., Shaw, P.T., et al., 2002. Monsoon-forced Guangdong Sciences Foundation (2010B031900041, chlorophyll distribution an primary production in the South China 8351030101000002); (3) Group Program of State Key Lab- Sea: observations and a numerical study. Deep-Sea Res. I 49, 1387– 1412. oratory of Tropical Oceanography (LTOZZ-1201) ; (4) Liu, X., Pan, J., Zhang, H., Yao, L., 2005. Horizontal and vertical Yang Scientist Research Projects of NSFC of China distributions of DO content and its flux of ocean-atmosphere exchange (41006068, 41106105), Knowledge Innovation Program of in the South China Sea. J. Mar. Sci. 23, 41–48 (in Chinese). the Chinese Academy of Sciences (SQ201302) and the Dra- Liu, Y., Bao, X., Wu, D., 2011. Analysis of vertical structure and seasonal gon 3 Project of ESA and NRSCC (Tang & Alpers, Project variation of the dissolved oxygen in the South China Sea. Period. Ocean Univ. China 41, 25–32 (in Chinese). 10705). We thank Thomas Pohlmann and Andreas Moll of Long, A., Chen, S., Zhou, W., et al., 2006. Distribution of macro- the Institute of Oceanography of the University of Ham- nutrients, dissolved oxygen, PH and Chl a and their relations in burg for their help in interpreting the data, and Weijie northern South China Sea. Mar. Sci. Bull. 25, 9–16 (in Chinese). Li, Haijun Ye, and Qingyang Sun of the South China Mitra, A., Banerjee, K., Sengupta, K., 2011a. Impact of AILA, a tropical Sea Institute of Oceanology for their revisions and sugges- cyclone on salinity, pH and dissolved oxygen of an aquatic sub-system of Indian Sundarbans. Proc. Natl. Acad. Sci. India Sect. B-Biol. Sci. tions to this paper. 81, 198–205. Mitra, A., Halder, P., Banerjee, K., 2011b. Changes of selected hydro- References logical parameters in Hooghly estuary in response to a severe tropical cyclone (Aila). Indian J. Geo-Mar. Sci. 40, 32–36. Chang, Y., Shimada, T., Lee, M.A., et al., 2006. Wintertime sea surface Miyazawa, Y., Kagimoto, T., Guo, X., Sakuma, H., 2008. The Kuroshio temperature fronts in the Taiwan strait. Geophys. Res. Lett. 33 (23), large meander formation in 2004 analyzed by an eddy-resolving ocean L23603. forecast system. J. Geophys. Res. 113, C10015. http://dx.doi.org/ Chang, Y., Liao, H.T., Lee, M.A., et al., 2008. Multisatellite observation 10.1029/2007JC004226. on upwelling after the passage of typhoon Hai-Tang in the southern Ning, X., Lin, C., Hao, Q., Liu, C., Le, F., Shi, J., 2009. Long term East China Sea. Geophys. Res. Lett. 35 (3), L03612. changes in the ecosystem in the northern South China Sea during Chen, Y.L., Chen, H.Y., Lin, I.I., Lee, M.A., Chang, J., 2007. Effects of 1976–2004. Biogeosciences 6, 2227–2243. cold eddy on phytoplankton production and assemblages in Luzon Price, J.F., 1981. Upper ocean response to a hurricane. J. Phys. Oceanogr. strait bordering the South China Sea. J. Oceanogr. 63, 671–683. 11, 153–175. Chen, Y.L.L., Chen, H.Y., Jan, S., Tuo, S.H., 2009. Phytoplankton Price, J.F., Sanford, T.B., Forristall, G.Z., 1994. Forced stage response to productivity enhancement and assemblage change in the upstream a moving hurricane. J. Phys. Oceanogr. 24, 233–260. Kuroshio after typhoons. Mar. Ecol. Prog. Ser 385, 111–126. Pun, I.F., Chang, Y.T., Lin, I.I., et al., 2011. Typhoon-ocean interaction Chen, J., Ni, X., Mao, Z., et al., 2012. Remote sensing and buoy based in the western north Pacific, Part 2. Oceanography 24 (4), 32–41. effect analysis of typhoon on hypoxia off the Changjiang (Yangtze) Qu, T.D., 2002. Evidence of water exchange between the South China Sea Estuary. Proc. SPIE 8532, Remote Sensing of the Ocean, Sea Ice, and the Pacific through the Luzon strait. Acta Oceanol. Sin. 21, 175– Coastal Waters, and Large Water Regions 2012, 853211. http:// 185. dx.doi.org/10.1117/12.974398. Sanford, T.B., Price, J.F., Girton, J.B., 2011. Upper ocean response to Chung, C.C., Gong, G.C., Hung, C.C., 2011. Effect of typhoon Morakot Hurricane Frances (2004) observed by profiling EM-APEX floats. J. on microphytoplankton population dynamics in the subtropical Phys. Oceanogr. 41, 1041–1056. Northwest Pacific. Mar. Ecol. Prog. Ser. 448, 39–49. Shang, S., Li, L., Sun, F., et al., 2008. Changes of temperature and bio- Cione, J.J., Uhlhorn, E.W., 2003. Sea surface temperature variability in optical properties in the South China Sea in response to typhoon hurricanes: implications with respect to intensity change. Mon. Lingling, 2001. Geophys. Res. Lett. 35, L10602. Weather Rev. 131, 1783–1796. Shi, W., Wang, M., 2007. Observations of a hurricane Katrina induced Dickey, T., Frye, D., McNeil, J., et al., 1998. Upper-ocean temperature phytoplankton bloom in the Gulf of Mexico. Geophys. Res. Lett. 34, response to hurricane Felix as measured by the Bermuda Testbed L11607. mooring. Mon. Weather Rev. 126, 1195–1201. Siswanto, E., Ishizaka, J., Morimoto, A., et al., 2008. Ocean physical and Han, W., 1995. Marine Chemistry of the Nansha Islands and South China biogeochemical responses to the passage of typhoon Meari in the East Sea. China Ocean Press (in Chinese). China Sea observed from Argo float and multiplatform satellites. Hung, C.C., Gong, G.C., 2011. Biogeochemical responses in the southern Geophys. Res. Lett. 35, L15604. East China Sea after typhoons. Oceanography 24, 42–51. Siswanto, E., Morimoto, A., Kojima, S., 2009. Enhancement of phyto- Hung, C.C., Gong, G.C., Chou, W.C., et al., 2010. The effect of typhoon plankton primary productivity in the southern East China Sea on particulate organic carbon flux in the southern East China Sea. following episodic typhoon passage. Geophys. Res. Lett. 36, Biogeosciences 7, 3007–3018. L11603. Jacob, S.D., Shay, L.K., Mariano, A.J., Black, P.G., 2000. The 3D Smitha, A., Rao, K.H., Sengupta, D., 2006. Effect of May 2003 tropical oceanic mixed layer response to Hurricane Gilbert. J. Phys. Oceanogr. cyclone on physical and biological processes in the Bay of Bengal. Int. 30, 1407–1429. J. Remote Sens. 27, 5301–5314. Lin, I.I., 2012. Typhoon-induced phytoplankton blooms and primary Stevens, P.W., Blewett, D.A., Casey, J.P., 2006. Short-term effects of a low productivity increase in the western North Pacific subtropical ocean. J. dissolved oxygen event on estuarine fish assemblages following the Geophys. Res.-Oceans (1978–2012) 117. passage of Hurricane Charley. Estuar. Coast. 29, 997–1003. Lin, H., Han, W., Wang, H., Cheng, S., 2001. Intensity of vertically Su, J., Pohlmann, T., 2009. Wind and topography influence on an distributed maximum DO in Nansha Islands sea area. J. Trop. upwelling system at the eastern Hainan coast. J. Geophys. Res. 114, Oceanogr. 23 (5), 65–69 (in Chinese). C06017.

Please cite this article in press as: Lin, J., et al. Response of dissolved oxygen and related marine ecological parameters to a tropical cyclone in the South China Sea. J. Adv. Space Res. (2014), http://dx.doi.org/10.1016/j.asr.2014.01.005 J. Lin et al. / Advances in Space Research xxx (2014) xxx–xxx 11

Sun, L., Yang, Y., Fu, Y., 2009. Impacts of typhoons on the Kuroshio Yang, X., Tang, D.L., 2010. Location of sea surface temperature cooling large meander: observation evidences. Atmos. Oceanic Sci. Lett. 2, 45– induced by typhoons in the South China Sea. J. Trop. Oceanogr. 29, 50. 26–31 (in Chinese). Tomasko, D., Anastasiou, C., Kovach, C., 2006. Dissolved oxygen Yu, J., Tang, D.L., Li, Y.Z., Huang, Z., Chen, G.B., 2013. Increase in fish dynamics in Charlotte Harbor and its contributing watershed, in abundance during two typhoons in the South China Sea. Adv. Space response to Hurricanes Charley, Frances, and Jeanne – impacts and Res. 51 (2013), 1734–1749. recovery. Estuar. Coast. 29, 932–938. Zhao, H., Tang, D.L., Wang, D., 2009. Phytoplankton blooms near the Van Dolah, R.F., Anderson, G.S., 1991. Effects of Hurricane Hugo on Pearl River Estuary induced by Typhoon Nuri. J. Geophys. Res. 114, salinity and dissolved oxygen conditions in the Charleston Harbor C12027. http://dx.doi.org/10.1029/2009JC005384. Estuary. J. Coastal Res., 83–94, 8(special issue). Zheng, G.M., Tang, D.L., 2007. Offshore and nearshore chlorophyll Xu, D., Liu, Z., Xu, X., Xu, J., 2005. The influence of typhoon on the sea increases induced by typhoon winds and subsequent terrestrial surface salinity in the warm pool of the western Pacific. Acta Oceanol. rainwater runoff. Mar. Ecol.-Prog. Ser. 333, 61–74. Sin. 27, 9–15 (in Chinese).