A subsurface chlorophyll a bloom induced by typhoon in the South China Sea

A subsurface chlorophyll a bloom induced by typhoon in the South China Sea
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  A subsurface chlorophyll a bloom induced by typhoon in the South China Sea H.J. Ye  a,b , Y. Sui  c , D.L. Tang  a,b, ⁎ , Y.D. Afanasyev  c a Research Center for Remote Sensing and Marine Ecology & Environment, State Key Laboratory of Tropical Oceanography, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, China b Graduate University of the Chinese Academy of Sciences, Beijing, China c Department of Physics & Physical Oceanography, Memorial University, Newfoundland, Canada a b s t r a c ta r t i c l e i n f o  Article history: Received 8 February 2013Received in revised form 18 April 2013Accepted 22 April 2013Available online xxxx Keywords: SubsurfaceChlorophyll a bloomTyphoonSouth China Sea Previous studies showed that typhoons often induce chlorophyll a (Chl-a) blooms in the surface waters. Thispaper shows that Chl-a blooms can occur not only on the surface but also in the interior just above the ther-mocline after the passage of a typhoon. We used satellite and cruise survey data to analyze physical andbiological characteristics in the South China Sea after the passage of the typhoon Nuri in August 2008. Thispaper shows that a subsurface (20 to 100 m depth) Chl-a bloom (1.31 ± 0.47 mg m − 3 ) occurred and lastedfor three weeks, stronger and longer than the surface Chl-a bloom (0.48 ± 0.23 mg m − 3 ). The maximumvalue of Chl-a of 2.10 mg m − 3 was detected at 50 m depth. This value was approximately 4 – 5 times higherthan the background value of 0.48 mg m − 3 measured at non blooming areas at the same time and about 7.5times higher than the mean Chl-a value of 0.28 ± 0.13 mg m − 3 measured over the period of   fi ve years. Themixed layer depth and the thickness of the Chl-a bloom increased after the typhoon. Our analysis clearlyshows that a subsurface upwelling caused by the passage of the typhoon, transported nutrients to the eupho-tic zone and supported the Chl-a bloom. These observations provide some insight on the effect of typhoonson marine ecosystems, especially as related to the Integrated Primary Production.© 2013 Elsevier B.V. All rights reserved. 1. Introduction Recently, subsurface chlorophyll has received a lot of attention inmodeling studies as well as in primary production studies becauseof its signi fi cant contribution to ecology (Fennel and Boss, 2003; Luet al., 2010; Perry et al., 2008; Sarma and Aswanikumar, 1991). As aresult of physical processes occurring on different time scales (Price,1981; Tang et al., 2004a,b; Wang et al., 2010), nutrients are pumpedfrom the deep waters of the ocean to the surface and subsurface wherethey initiate a sequence of biological processes. In the open ocean, thesubsurface chlorophyll maximum depth remains relatively stable. In thenearshore waters, the subsurface chlorophyll maximum shoals andweakens when the surface layer is affected by river discharges (Lu et al.,2010). In the northern part of the South China Sea (SCS), the depthwhere the maximum value of chlorophyll a (Chl-a) concentration is ob-served is lowest (20 – 30 m) in the winter, intermediate in May and isthe deepest (50 – 90 m) in other months (Chen et al., 2006).Recent studies showed that typhoons, hurricanes or tropical cy-clones can cause signi fi cant increase of Chl-a concentration in surfacewaters. A tropicalcyclone “ Kai-Tak ”  triggereda 30 fold increasein thesurface Chl-a concentration in the SCS in 2000 (Lin, 2003). Otherexamples where the increase of Chl-a concentration was observedoffshore include typhoons  “ Damrey ”  in 2005 (Zheng and Tang, 2007)and Nuri in 2008 (Zhao et al., 2009). In 2007, typhoon “ Hagibis ”  causedanotableeffectonChl-aconcentrationswiththeforcingtimemuchlon-gerthanthegeostrophicadjustmenttimeinthemiddleoftheSCS(Sunet al., 2010). Tropical cyclone  “ Linfa ”  in 2009 triggered an eddy-likeChl-a bloom (Walker et al., 2005). Typhoon  “ Morakot ”  changed thediatom abundance and species composition due to strong winds andcaused nutrient entrainment from upwelling and nutrient-enriched fl oodwaters (Chung et al., 2012). In the above studies the surfaceChl-a blooms were detected using satellite data for surface Chl-a.Typhoons alsoaffectparticulateorganic carbon fl ux in subsurfacewaters (Chen et al., 2009; Hung et al., 2010), suspended matterconcentration, re-suspension and terrestrial runoff, entrainment of riverine-mixing, Integrated Primary Production (IPP), (Chen et al.,2009; Gautam et al., 2005; Hung et al., 2010; Kundu et al., 2001;Shiah et al., 2000) and  fi sh abundance (Yu et al., 2013). However,Shiahetal.(2000)mentionedthatthespatialandtemporalvariationpatterns of Chl-a were quite heterogeneous, and that a detailed in-formation on Chl-a variations in the subsurface was lacking. Thereclearlyremainsacertainlackofinformationonsubsurfacephytoplank-ton,ontheoccurrenceofbloomsinsubsurfacewatersandonthemech-anisms of blooming. In August 2008, the typhoon Nuri passed over thenorthernpart of SCSandprovided uswithanopportunity to study bio-logicalandphysicalchangesinthesubsurfacewaters.Severaldaysafterthe passage of Nuri, a research cruise was conducted to obtain in situ  Journal of Marine Systems xxx (2013) xxx – xxx ⁎  Corresponding author at: Research Center for Remote Sensing and Marine Ecology& Environment, State Key Laboratory of Tropical Oceanography, South China Sea Insti-tute of Oceanology, Chinese Academy of Sciences, Guangzhou, China. E-mail address: (D.L. Tang). MARSYS-02361; No of Pages 8 0924-7963/$  –  see front matter © 2013 Elsevier B.V. All rights reserved. Contents lists available at SciVerse ScienceDirect  Journal of Marine Systems  journal homepage: Please citethis article as: Ye, H.J., et al.,Asubsurfacechlorophylla bloom induced bytyphoonin theSouthChinaSea,J.Mar. Syst.(2013), http://  data in this region. The results documented a subsurface Chl-a bloomthat lasted for a long time even after the surface Chl-a bloom hasdisappeared. 2. Data and methods  2.1. Study area The northwest Paci fi c is the region with the most numerous andviolent typhoons in the world (Fumin et al., 2002), and the SCS isthe largest semi-enclosed marginal sea in the northwest Paci fi c withan area of about 3.5 × 10 6 km 2 (Fig. 1). On average more than 10 ty-phoons pass through this region annually, and the typhoon tracks aremostly in the westward direction over the northern SCS (Elsner andLiu, 2003; Wu et al., 2005; Zheng and Tang, 2007). Compared withother ocean ecosystems, the summer SCS is notable for its shallowMixed Layer Depth (MLD) which is typically less than 50 m (Chenet al., 2006; Karl and Lukas, 1996). During the summer season, thenorthern SCS shows generally strati fi ed and oligotrophic conditions(Chen et al., 2003).  2.2. In situ data In situ data of Chl-a, temperature and salinity were measured at14 stations (Fig. 1) during a Research Cruise of the South China SeaInstitute of Oceanology, Chinese Academy of Science from 18 Augustto the 6 September 2008 after typhoon Nuri (Table 1). 1 – 2 L watersamples from  fi ve depths (0, 25, 50, 75, 100 m) were collected ateach station in order to measure the Chl-a concentrations. Seawater was  fi ltered through a GF/F  fi lter (Whatman, 25 mm) andthe fi lter paper was wrapped in aluminum foil and stored at temper-ature − 20 °C pending analysis. Chl-a concentrationwas determinedby  fl uorescence with a Turner Design 10  fl uorometer following theequations given by Parsons et al. (1984). Temperature and salinitydata were obtained by a Conductivity – Temperature – Depth probe.The MLD was determined based on a 0.125 unit potential densitycriterion (Levitus, 1982). In order to obtain information about meanMLDinpreviousyearsweusedCTDdataobtainedincruisesconductedin 2004, 2005, 2006, and 2007 (Table 2). Vertical pro fi les of Chl-a,temperature and salinity were obtained along the Transect North (TN)(Stations 2 – 9) and the Transect South (TS) (Stations 10 – 13) (Fig. 1).Relevant published information on Chl-a concentration in the SCS wasused in this study and is summarized in Table 3.  2.3. Typhoon track The typhoon Nuri track, based on the best track data issued by the Joint Typhoon Warning Center (JTWC), was obtained from the UnisysWeather Web ( fi c/ index.html). Theinformationsuchastyphooncenterlocations,centralpressure and Maximum Sustained Wind (MSW) was gathered every 17192123 SE PREHainan Island 1413121211846AUG/21/00AUG/20/00910AUG/22/00 China NLuzon IslandTai Wan 15109112115118121124 ° E753 B   A B Pacific Ocean South China Sea Indian Ocean TNTS 9080706050403020100MSW(Knots)Central Press(hPa)94495296096897698499210001008 Typhoon Nuri 25 ° N Fig. 1.  (A) Location of the South China Sea. (B) Study area (Box S) and the track of typhoon Nuri. The typhoon center positions for every 6 h are indicated by the colored circles. Thecircle color and size represent the central pressure [hPa] and the maximum sustained wind speeds [MSW, knots, 1 knot = 0.514 m s − 1 ], respectively. Box E is typhoon effect area(1.46 × 10 5 km 2 ; clockwise from the top, 116°W – 22.5 °N, 119.5 °W – 20.5 °N, 118.5 °W – 18.5 °N and 115 °W – 20.5 °N); TN: Transect North (Stations 2 – 9); TS: Transect South(Stations 10 – 13); PRE: Pearl River Estuary; the black triangle: Dongsha Island. All times are in Coordinated Universal Time (UTC). (For interpretation of the references tocolor in this  fi gure legend, the reader is referred to the web version of this article.)  Table 1 Information on in situ measurements at different stations in the SCS during 2008.Station Station locations Date/time1 114.00 °E, 21.00 °N 0248 Sep 62 114.50 °E, 20.50 °N 2041 Sep 53 115.00 °E, 20.50 °N 2045 Sep 54 115.50 °E, 20.50 °N 1623 Sep 55 116.00 °E, 20.50 °N 1255 Sep 56 116.50 °E, 20.50 °N 0830 Sep 57 117.00 °E, 20.50 °N 0615 Sep 58 117.50 °E, 20.50 °N 0215 Sep 59 120.00 °E, 20.50 °N 2033Aug 1810 120.00 °E, 20.00 °N 0033Aug 1911 117.00 °E, 20.00 °N 1519 Sep 412 116.00 °E, 20.00 °N 1326 Sep 313 115.00 °E, 20.00 °N 0541 Sep 314 116.00 °E, 19.00 °N 0305 Sep 22  H.J. Ye et al. / Journal of Marine Systems xxx (2013) xxx –  xxx Please citethis article as: Ye, H.J., et al.,Asubsurfacechlorophylla bloom induced bytyphoonin theSouthChinaSea,J.Mar. Syst.(2013), http://  6 h.Thetranslationspeedofthetyphoonwasestimatedusingtheposi-tionsofitscenterrecordedevery6 h.TheMSWandthecentralpressureof the typhoon are shown in Fig. 1.  2.4. Satellite data The daily, merged 8 day Chl-a concentration and sea surface tem-perature (SST) data Level 3, with a spatial resolution of 4 km, from theocean color sensor Moderate Resolution Imaging Spectroradiometer(MODIS) were obtained from the Distributed Active Archive Center(DAAC) of the US National Aeronautics and Space Administration(NASA) ( Sea level anomaly(SLA) data gathered from the TOPEX/Poseidon and JASON altime-ters ( ) was used to analyze surfacecirculations.The microwave scatterometer SeaWinds (QuikScat) data (http:// was used to obtain wind vectors at the sea surfacefor the periods before, during and after typhoon Nuri. The wind  fi elddata allows us to estimate wind stress  τ  → on the ocean surface usingthe conventional formula: τ  → ¼  ρ a C  D j U → 10 j U → 10 ;  ð 1 Þ where  ρ a  is the density of air andU → 10  is wind vector, and the drag co-ef  fi cient  C  D  ( Jarosz et al., 2007), is expressed as: C  D  ¼  2 : 229 þ 0 : 2983  U  10 − 0 : 00468  U  210    10 − 3 :  ð 2 Þ In order to estimate the rate of exchange between the deep layersand the top layer we calculated the Ekman pumping velocity  W  E   asfollows: W  E   ¼  curl  τ  → =  ρ  f    ;  ð 3 Þ where  ρ  is the density of seawater and  f   is the Coriolis parameter.Thermocline displacement  Δ  η   due to a typhoon can be estimatedusing the formula given by Δη   ¼ τ  → =  ρ  fU  t  ð Þ ;  ð 4 Þ (Price et al., 1994) where  U  t   is the translation speed of the typhoon.Alternatively, the thermocline displacement can be estimated fromthe SLA data. Assuming purely baroclinic response such that the ther-mocline displacement compensates for the surface displacement andis of opposite sign, we have a simple relation Δη   g  0 ¼ −  g  Δ h  ð 5 Þ (Shay et al., 2000) where  g  ′  =  g  Δ  ρ /   ρ  is the reduced gravity,  Δ  ρ  is thedensity difference between the upper and lower layers and  Δ h  is theSLA. The thermocline displacement is then Δη   ¼ − Δ h  ρ = Δρ :  ð 6 Þ 3. Results  3.1. Surface Chl-a bloom during typhoon Nuri in the SCS  Nuri (2008) was a Category 2 (based on Saf  fi r-Simpson scale) ty-phoon that impacted a wide area from Luzon Strait to Pearl RiverEstuary. It was developed as a tropical depression in the northernPaci fi c, and strengthened to a typhoon status on the 18 August 2008.The typhoon migrated towards the northwest, as its center passedthrough the DongSha Island on the 21 August 2008 and then movednorthwesttowardsPRE(Fig.1).Beforethetyphoon,onthe9 – 16August2008 the wind in the northern SCS was weak (~7 m s − 1 ) (Fig. 2Aa).During the passage of Nuri the winds were strong, in excess of 30 m s − 1 (Fig. 2Ab). After the typhoon, the wind speed returned to alow value of approximately 5 m s − 1 (Fig. 2Ac). According to the JTWC, the maximum sustained winds reached 51 m s − 1 on the 20August in the Luzon Strait. In the study area, the average windspeed was 35 m s − 1 from 1800 UTC on the 20 August to 0000 UTCon the 22 August. In the same period the translation speed of the ty-phoon was  U  t   = 4.2 m s − 1 . Although Nuri was a weak, fast movingtyphoon, a heavy rain brought by Nuri led to a signi fi cant direct eco-nomic impact of about ¥400 million (http://  fi roll/20080827/09172394980.shtml).In the period of 12 – 19 August before Nuri's passage, the map of SST shows that the study area was dominated by warm water withSST exceeding 29 °C (Fig. 2Ba). The SST map obtained during thepassage of Nuri demonstrates that a signi fi cant cooling occurredalong the track of the typhoon with  Δ SST =  − 2.0 °C, approximately(Table 4). The lateral extent of the low SST patch was approximately100 km. The low temperature patch persisted for about two weeksafter the passage of Nuri (Fig. 2Bc). It is interesting to note a clearrightward bias of in Δ SST distribution. The low SST patch was locatedmainly to the right of the typhoon track such that its centerline wasshifted by approximately 50 km from the track. The rightward biaswas observed previously by many authors (Fedorov et al., 1979;Sanford et al., 1987) and was discussed by Price (1981), Greatbatch (1983)and Priceet al. (1994). The bias occurs becauseof the effective coupling between the wind stress of the moving typhoon and theupper ocean inertial current. The current turns to the right and so doesthewindstressontherighthandsideofthetrack.Thiscausesapositivefeedbackonthecurrent.Asaresultthecurrentsarestrongertotherightof the track. Surface horizontal divergence and hence the pumping of cold water to the surface in this area become stronger as well.The sea surface Chl-a concentrations were signi fi cantly enhancedafter Nuri's passage. Pre-typhoon Chl-a concentration was in the rangefrom 0.09 to 0.10 mg m − 3 (Fig. 2Ca). The concentration increased up  Table 2 The mixed layer depth (MLD) in our study area at different sampling years.(Aug – Sep) Year Number of observations MLD (m)2004 10 30.5 ± 7.582005 6 36.0 ± 7.592006 7 41.4 ± 17.542007 4 33.5 ± 3.112008 10 63.0 ± 9.49Values were presented as mean ± standard deviation.  Table 3 The number of Chl-a data in our study area and data sources.Date Number of observationsData was obtainedwithin 15 days aftertyphoon passedSources12 Jun – 7 Jul, 1998 2 No Ning et al. (2005)Sep, 1998 1 No Chen et al. (2006)14 – 18 Sep, 1998 3 No Liu et al. (2002)18 – 20 Sep, 2004 6 No Present study6 – 7 Sep, 2005 2 No He et al. (2009)14 Aug, 2007 1 No Liu et al. (2009)2 – 6 Sep, 2008 5 Yes (12 – 16 days) Present study16 – 17 Sep, 2010 4 No Present study3 H.J. Ye et al. / Journal of Marine Systems xxx (2013) xxx –  xxx Please citethis article as: Ye, H.J., et al.,Asubsurfacechlorophylla bloom induced bytyphoonin theSouthChinaSea,J.Mar. Syst.(2013), http://  to 0.24 mg m − 3 two days later and up to 0.50 mg m − 3 four days later.However, only one week after the passage of the typhoon the Chl-aconcentration on the surface returned to its pre-typhoon value of 0.11 mg m − 3 (Fig. 2Cc). Further note that the patch of enhancedChl-a concentration approximately coincided with the low SST patch(compare Fig. 2Bb and Cb). This suggests that the enhanced Chl-aconcentrationwasduetotheintroductionofnutrientsfromthedeeperwaters accompany with cool SST.The comparison of the SLA images before and immediately afterthetyphoon(Fig.2DaandDb)showsadepressionofthesurfacecenteredatthelatitudeofapproximately20.5°N.Associatedwiththisdepression,the cyclonic cold eddy persisted for almost three weeks (Fig. 2Dc).  3.2. Variations of hydrographic conditions The changes of physical hydrography in the upper ocean were ex-amined using temperature and salinity measured at 14 stations in theperiod of 12 to 16 days after the typhoon (Fig. 3). The results showedthat the highest temperature and the lowest salinity occurred at seasurface as one might expect. A peak in isolines of temperature and sa-linity centered at Station 7 indicates a region of upwelling. Comparedwith surrounding stations, this region is associated with a sharp dropof temperature by 3 – 4 °C and increase in salinity by approximately0.2 psu between 60 m and 120 m depth. A region of equally strongdownwelling was observed at Station 5. We will discuss the physicalmechanism of this phenomenon in Section 4. The greatest tempera-ture and salinity change occurred at the 60 m depth. The sharp dropof temperature and sharp rise of salinity indicated that the typhoonhas induced a subsurface upwelling. The upwelling lifted deeperwater from approximately 140 m to 20 m depth and was sustainedfor at least 16 days before returning to the normal climatology level.The MLD in this region is typically about 35 m at this time of yearas data from previous years indicates (Table 2). Station 2, located atthe extreme left of the typhoon track where the in fl uence of typhoon    C   h   l  -  a a . 12-19 Augb. 20-27 Aug 182022 c . 27 Aug 1010.10.01    S   S   T a . 12-19 Aug c . 28 Aug-4 Sepb. 20-27 Aug 30.524.526.528.5    S   S   T   (   o    C   ) 182022 a . 14-20 Aug b . 28 Aug-3 Sep c . 4-10 Sep    S   L   A   (  c  m   ) 3010200-10    S   L   A 182022 c . 24-30 Aug a . 10-16 Aug b . 21 Aug 3001020    W   i  n   d   S  p  e  e   d 182022 Before typhoonDuring typhoonAfter typhoon ABCD -- 116114118120116114118120116114118120    W   i  n   d   S  p  e  e   d   (  m  s   -   1    )   C   h   l  -  a   (  m  m  g   -   3    ) 25°N25°N25°N25°N122°E Fig. 2.  Optical and biological responses of the ocean to the passage of typhoon Nuri. (A) QuikScat wind-vector  fi elds, (B) sea surface temperature, (C) MODIS-derived ocean colorproducts for Chl-a concentration, (D) sea level anomaly from AVISO. Rectangles in panels Bb, Cb, Db and Dc indicate the study area. Red crosses show the track of typhoon Nuri inpanel Bb. (For interpretation of the references to color in this  fi gure legend, the reader is referred to the web version of this article.)  Table 4 Comparisons of environmental variables between surface and subsurface and the potential mechanism induced by Nuri.Variables Nuri induced Chl-a (mg m – 3 ) Climatology Chl-a (mg m – 3 ) Tem change (°C)Maximum Mean Lasted time Bloom size (10 5 km 2 ) Maximum Mean Maximum MeanSurface 1.10 a 0.48 ± 0.23 a 1 week 0.60 a,b (Chl-a  ≥  0.50 mg m − 3 ) 0.20 c 0.10 ± 0.07 c 3.40 a 1.70 a subsurface 2.10 c 1.31 ± 0.47 c ~3 weeks 1.00 b,c (Chl-a  ≥  1.00 mg m − 3 ) 1.00 c 0.28 ± 0.13 c 3.50 c 2.00 c Mechanism Short-lasting vertical mixing and long-lasting subsurface upwelling a Remote sensing data. b Bloom size calculated from Figs. 2Cb and 4c. c In situ data.4  H.J. Ye et al. / Journal of Marine Systems xxx (2013) xxx –  xxx Please citethis article as: Ye, H.J., et al.,Asubsurfacechlorophylla bloom induced bytyphoonin theSouthChinaSea,J.Mar. Syst.(2013), http://  was minimal, shows a similar value of approximately 40 m. Howeverin the area affected by the mixing induced by the typhoon, the meanMLD increased signi fi cantly to approximately 70 m.  3.3. Subsurface Chl-a bloom after the typhoon Nuri The Chl-a concentration at the sea surface returned to the normalclimatology level after about two weeks after the Nuri's passage(Fig. 4A and B). However, high subsurface Chl-a concentrationswith average value of 1.31 ± 0.47 mg m − 3 at 50 m depth were ob-served in the vicinity of the Nuri's track (Fig. 4C, D, E and Table 4). The maximum Chl-a value of 2.10 mg m − 3 (Fig. 4C, D and Table 4) was observed at 50 m depth (Station 8). The maximum Chl-a valueat the stations away from the typhoon track (Stations 1, 2, 13 and 14)was less than 0.60 mg m − 3 . Vertically, the Chl-a values decreasedsharply in both upward and downward directions away from the A Tem 04080120160200    D  e  p   t   h   (  m   ) 92345678 Station 33.533.433.333.233.933.833.733.634.334. Psu N 141618202224262830 Station 8 (2008) 33.633.634.234.534.8 TemSal C Temperature( O C )Salinity (Psu) B SalStation 92345678    d  e  p   t   h   (  m   ) 04080120160200 D Sampling stations along TN 113115117119121E 182022 8 TN 92 O C Fig. 3.  Vertical distribution of temperature (A) and salinity (B) in the upper 200 m at the TN Transect North, with contour intervals of 1 °C and 0.10 Psu, respectively. Temperature(black) and salinity (red) pro fi les after Nuri's passage (C). The circles on the top of (A) and (B) indicate Nuri's track. The black rectangles show the area where decrease in temper-ature or increase in salinity is observed. (D) Sampling locations along the transect TN. (For interpretation of the references to color in this fi gure legend, the reader is referred to theweb version of this article.) Chl-a (mg m -3 )°N A MODIS chl-a ( Sep 2-6) 1112 E Chl-a in Transect TS 2 D Chl-a in Transect TN 020406080100    d  e  p   t   h   (  m   ) 468 StationStation 13111117119°E171921113115 C Chl-a at 50 m depth (Sep 2-6) TNTS 171921 B Chl-a on surface (Sep 2-6) TNTS 23°N23°N TNTS Fig. 4.  The Chl-a contours at the surface (A, B) and at 50 m (C) depth after Nuri's passage. The vertical distribution of Chl-a at the transect TN (Stations 2, 4, 6 and 8) (D) and thetransect TS (Stations 11 – 13) (E) after Nuri's passage. The black circles on top of (D) and (E) indicate the locations of typhoon Nuri. The black triangle indicates the Dongsha Island.5 H.J. Ye et al. / Journal of Marine Systems xxx (2013) xxx –  xxx Please citethis article as: Ye, H.J., et al.,Asubsurfacechlorophylla bloom induced bytyphoonin theSouthChinaSea,J.Mar. Syst.(2013), http://
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