Harmful Algae 30S (2013) S75–S88

Red tides in Masan Bay, Korea in 2004–2005: I. Daily variations in theabundance of red-tide organisms and environmental factors

Hae Jin Jeong a,*, Yeong Du Yoo a, Kyung Ha Lee a, Tae Hoon Kim b, Kyeong Ah Seong c,Nam Seon Kang a, Sung Yeon Lee a, Jae Seong Kim d, Shin Kim c, Won Ho Yih c

a School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University, Seoul 151-747, Republic of Koreab IGD Corporation, 499 Gunja-dong, Siheung-si, Gyeonggi-do 429-823, Republic of Koreac Department of Oceanography, College of Ocean Science and Technology, Kunsan National University, Kunsan 573-701, Republic of Koread Water and Eco-Bio Corporation, Kunsan National University, Kunsan 573-701, Republic of Korea

A R T I C L E I N F O

Keywords:

Diatom

Dinoflagellate

Harmful algal bloom

Mixotroph

Protist

Raphidophyte

Red tide

A B S T R A C T

To investigate red tides in Masan Bay, Korea, in which red tides have frequently occurred, we measured

the abundance of red-tide organisms at a fixed station daily from June 2004 to May 2005. We daily

measured physical, chemical, and biological properties. During the study period, 36 red-tide events

occurred. Of these, 7 events were overwhelmingly dominated by cryptophytes, 5 by phototrophic

dinoflagellates, 2 by diatoms, 2 by raphidophytes, 1 by a mixotrophic ciliate, and the rest by mixtures of

several taxonomic groups. The durations of the red-tide events ranged from 1 to 40 days and total

duration was 195 days. Most of the red tides occurred between June and September 2004 and between

January and March 2005. The maximum abundance and biomass of total phototrophic dinoflagellates

were 27,183 cells ml�1 and 3516 ng C ml�1, respectively, while those of total diatoms were

71,538 cells ml�1 and 10,981 ng C ml�1, respectively. Furthermore, the maximum abundance and

biomass of total raphidophytes were 90,010 cells ml�1 and 10,177 ng C ml�1. The biomass of total

phototrophic dinoflagellates had significant positive correlations with salinity, pH, dissolved oxygen,

euglenophytes, raphidophytes, cyanobacteria, and heterotrophic bacteria, but negative correlations with

temperature, nitrite plus nitrate and phosphate concentrations. In addition, the biomass of

raphidophytes had a significant positive correlation with temperature, pH, and heterotrophic bacteria,

but a negative correlation with salinity and the phosphate concentration. This evidence suggests that

red-tide dynamics dominated by these phototrophic dinoflagellates and raphidophytes may be mainly

affected by potential prey concentrations rather than inorganic nutrient concentrations. Daily sampling

is necessary to explore red-tide dynamics in Masan Bay because the generation time of the causative

species is �0.5–3 days.

� 2013 Elsevier B.V. All rights reserved.

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Harmful Algae

jo u rn al h om epag e: ww w.els evier .c o m/lo cat e/ha l

1. Introduction

Red tides, discoloration of the surface of the sea due to planktonblooms, have occurred in the coastal and offshore waters of manycountries and in oceanic waters (Holmes et al., 1967; Eppley andHarrison, 1975; ECOHAB, 1995; Jeong, 1995; Horner et al., 1997;Imai et al., 2001; Sordo et al., 2001; Anderson et al., 2002; Jeonget al., 2003, 2008; Alonso-Rodriguez and Ochoa, 2004; Seong et al.,2006; Kang et al., 2013; Lee et al., 2013). Red tides have oftencaused large-scale mortalities of fish and shellfish and great lossesto the aquaculture and tourist industries of many countries(Smayda, 1990; Glibert et al., 2005; Anderson et al., 2012; Fu et al.,

* Corresponding author. Tel.: +82 2 880 6746; fax: +82 2 874 9695.

E-mail address: hjjeong@snu.ac.kr (H.J. Jeong).

1568-9883/$ – see front matter � 2013 Elsevier B.V. All rights reserved.

http://dx.doi.org/10.1016/j.hal.2013.10.008

2012; Park et al., 2013b). Therefore, understanding the processesassociated with red tides and predicting the outbreak, persistence,and decline of red tides are important concerns to scientists,industry, and the public.

Phototrophic and heterotrophic dinoflagellates, raphidophytes,cryptophytes, euglenophytes, diatoms, and ciliates are known tobe causative organisms of red tides (Smayda, 1997; Parrow andBurkholder, 2003; Jeong et al., 2005b, 2011, 2013; Mason et al.,2007; Park et al., 2013a; Yih et al., 2013). Originally, phototrophicflagellates were treated as exclusively autotrophic organisms likediatoms. Thus, light and nutrient conditions were thought to be themost important factors affecting the dynamics of red tides(Cembella et al., 1984; Smayda, 1997; Uchida et al., 1999).However, recently, many phototrophic dinoflagellates that hadpreviously been thought to be exclusively autotrophic have beenrevealed to be mixotrophic (i.e., capable of both photosynthesis

Fig. 1. The sampling station (SNUMS) in Masan Bay, Korea. The number is

bathymetry (meter) during high tide.

H.J. Jeong et al. / Harmful Algae 30S (2013) S75–S88S76

and ingesting prey) (Jacobson and Anderson, 1986; Bockstahlerand Coats, 1993a; Graneli et al., 1997; Stoecker et al., 1997;Smalley et al., 1999; Stoecker, 1999; Skovgaard, 2000; Jeong et al.,2004, 2005c, 2010c, 2012; Burkholder et al., 2008; Hansen, 2011).These organisms have been shown to prey on diverse species,including heterotrophic bacteria (Seong et al., 2006; Seong andJeong, 2011; Jeong et al., 2012), cyanobacteria (Jeong et al., 2005a;Glibert et al., 2009), nano- and microflagellates (Li et al., 2000;Berge et al., 2008), other phototrophic dinoflagellates (Jeong et al.,2005b,c), diatoms (Bockstahler and Coats, 1993a; Yoo et al., 2009),heterotrophic dinoflagellates (Jeong et al., 1997, 1999), and ciliates(Bockstahler and Coats, 1993b; Smalley et al., 1999). In addition,the raphidophyte genera Heterosigma, Chattonella, and Fibrocapsa

have also been identified as mixotrophic organisms which are ableto feed on heterotrophic bacteria and cyanobacteria (Seong et al.,2006; Jeong et al., 2010b; Jeong, 2011). Therefore, manyphototrophic red-tide organisms are likely to be influenced bythe availability of prey in addition to nutrients.

To understand the dynamics of red tides in a specific area, thefollowing basic questions should be answered: (1) how many redtides occur in a year, (2) what are the causative phototrophicspecies of these red tides, (3) what are the growth factors for eachcausative phototrophic species, (4) what are the mortality factorsfor each causative phototrophic species, and (5) what is the patternof succession in serial red-tide events? To answer these questions,time series data (growth factors, mortality factors, and succession)are necessary.

The generation times of most red-tide organisms are �0.5–3days and detection of those requires high frequency measurements(Smayda, 1997; Jeong et al., 2010a). Furthermore, the mixotrophicgrowth rates of phototrophic dinoflagellates are generally higherthan the autotrophic growth rates (Jeong et al., 2010a; Yoo et al.,2010; Kang et al., 2011). Thus, time series with short samplingintervals are necessary to understand the dynamics of red tidesdominated by mixotrophic and heterotrophic flagellates. Deter-mining the sampling interval appropriate for a specific area is thefirst step in investigating the dynamics of the red tides that occurthere. There have been several time-series studies (Varela et al.,2002; Yin, 2002; Nishikawa et al., 2010). However, the samplingintervals used (i.e., weekly or monthly) may have been too long todetect short red-tide events.

Masan Bay, a highly eutrophied bay in southern Korea,experiences frequent red tides. Masan Bay is a semi-enclosedembayment in which advection is minimal and water circulation isrestricted, and thus is a suitable location for time-series studies.However, previously, only monthly data on red-tide dynamicshave been collected (Yoo, 1991; Kwak et al., 2001). To explore theprocesses associated with red tides in Masan Bay, we measured theabundance of red-tide organisms and related plankton in samplescollected daily from June 2004 to May 2005. In addition, wemeasured physical, chemical, and biological properties andinvestigated the relationships among these properties. Further-more, the roles of heterotrophic protists such as ciliates, heterotro-phic dinoflagellates, and heterotrophic flagellates (Yoo et al., 2013)as well as mesozooplankton such as copepods, cladocerans, andinvertebrate larvae (Kim et al., 2013) in red-tide dynamics wereexplored. The results of the present study provide a foundation forunderstanding red tides in eutrophic bays and relationships amongred-tide organisms and environmental factors.

2. Materials and methods

Masan Bay is located in southeast Korea (Fig. 1). The bay is oval-shaped (5 km long, 2 km wide, 1 km mouth). A large city,Changwon, surrounds the bay and three streams enter the bay.Water depth at the sampling station (SNUMS) in 2004–2005 was

1.2–2.4 m, depending on the tide and thus the tide range was�1.2 m. The water is mixed year-round except in summer.

Water samples were taken at the surface from a pier (StationSNUMS) with water samplers daily at 10:00 from June 2004 to May2005. On August 17, 2004 when the water column was stratified,near-bottom samples were also taken to investigate differences inwater temperature, salinity, and concentrations of chlorophyll-aand phototrophic plankton between the surface and bottomwaters. Plankton samples for counting were poured into 500-mlpolyethylene bottles and preserved with acidic Lugol’s solution fordiatoms, phototrophic dinoflagellates, cryptophytes, raphido-phytes, and euglenophytes, Bouin solution for ciliates, andglutaraldehyde for phototrophic nanoflagellates, picoeukaryotes,and bacteria. Dominant species were single cell isolated and grownin clonal culture for morphological and DNA sequencing identifi-cation.

To determine the abundance of diatoms, phototrophic dino-flagellates, and flagellates (cryptophytes, raphidophytes, eugleno-phytes, etc.), the samples preserved with acidic Lugol’s solutionwere concentrated by 1/5 to 1/10 using the settling and siphoningmethod (Welch, 1948). After thorough mixing, all or a minimum of100 cells of each phototrophic plankton species in one to ten 1-mlSedgwick–Rafter counting chambers were counted under anepifluorescent microscope.

To determine bacterial and nanoflagellate abundance, aliquotsof the water samples were poured into 100-ml polyethylene

Fig. 2. Physical and chemical properties of Masan Bay (SNUMS) from June 1, 2004 to

May 31, 2005. (A) Water temperature (T, 8C), (B) precipitation (Prec., mm), (C)

salinity (S), (D) ammonium (NH4, mM), (E) nitrite plus nitrate (NO3, mM), (F)

phosphate (PO4, mM), (G) silicate (SiO2, mM), (H) pH, (I) dissolved oxygen (DO,

mg l�1), and (J) chlorophyll-a (Chl-a, mg l�1).

H.J. Jeong et al. / Harmful Algae 30S (2013) S75–S88 S77

bottles and preserved with glutaraldehyde (final concentration, 1%,v/v). Three to twelve 1-ml fixed aliquots were stained with 40,6-diamidino-2-phenylindole (DAPI; final concentration, 1 mM) andthen filtered through 0.2-mm-pore-sized polycarbonate (PC) blackmembrane filters. Bacteria were enumerated under an epifluor-escent microscope with UV light excitation (Porter and Feig, 1980).Additionally, three 1- to 5-ml fixed aliquots were stained with DAPIand then filtered through 0.2-mm-pore-sized PC black membranefilters. Phototrophic nanoflagellates (PNFs; 3–6 mm cell length) thatexhibited orange autofluorescence under an epifluorescent micro-scope with blue light excitation were also enumerated.

We measured the carbon content for each species of manyphototrophic plankton species cultured in our laboratory usingCHN analyzer. For non-culturing species or taxon, the length andwidth of cells preserved in 5% acid Lugol’s solution were measuredusing a light microscope and then cell volume was calculated usinggeometry. The carbon content for each species of phototrophicplankton was calculated from the cell volume according toMenden-Deuer and Lessard (2000).

Water temperatures and salinities of the surface water weremeasured on a daily basis using a YSI 30 (YSI, Inc., Baton Rouge, LA,USA), and pH and DO were measured using a Handylab pH 11(Schott Instruments, Mainz, Germany) and Oxi 197i (WTW GmbH,Weilheim, Germany), respectively. Water samples for analyzingnutrient concentrations were gently filtered through GF/F filtersand stored frozen at �20 8C until the concentrations of ammonium(NH4), nitrate plus nitrite (NO3 + NO2, hereafter NO3), phosphate(PO4), and silicate (SiO2) were measured using a nutrient auto-analyzer system (Quattro; Seal Analytical Gmbh, Norderstedt,Germany). The chlorophyll-a of phototrophic protists was mea-sured as in APHA (1995). Precipitation data were obtained from theKorea Meteorological Administration (http://web.kma.go/kr). Wetested weather filtering is necessary and did not find a significantdifference (Menden-Deuer and Fredrickson, 2010). The correlationcoefficients between phototrophic plankton and physical, chemi-cal, and biological properties were calculated using the Pearson’scorrelation (Conover, 1980; Zar, 1999).

During the study period, red-tide patches were generally visiblewhen the biomass of causative species exceeded 200 ng C ml�1. Inaddition, when the biomass of red-tide organisms exceed200 ng C ml�1, red-tide warning is announced by National Fisher-ies Research and Development Institute, Korea (NFRDI, 2012).Thus, we defined here red tides as biomass of phototrophicplankton �200 ng C ml�1.

3. Results

3.1. Physical and chemical properties in Masan Bay

From June 1, 2004 to May 31, 2005, water temperature (T) atstation SNUMS ranged from 4.2 to 28.6 8C (Fig. 2A; Table 1); thehighest T was observed on August 9, 2004, while the lowest T wasobserved on February 1, 2005. In addition, daily precipitation rangedfrom 0.0 to 116.5 mm, while salinity ranged from 4.1 to 33.3 (Fig. 2Band C; Table 1). Precipitation showed a significant positivecorrelation with T and a negative correlation with salinity (Table 2).

The NH4 concentration ranged from 0.1 to 129.5 mM, while theNO3 concentration ranged from not detectable to 105.2 mM(Fig. 2D and E; Table 1). In addition, the PO4 concentration rangedfrom not detectable to 11.9 mM and the SiO2 concentration rangedfrom not detectable to 239.7 mM (Fig. 2F and G; Table 1). The NO3

and SiO2 concentrations showed significant negative correlationswith salinity, while pH and DO showed significant positivecorrelations (Table 2).

pH values were 7.1–8.7 (Fig. 2H; Table 1). pH showed significantpositive correlations with dissolved oxygen concentration (DO), T,

and salinity, but negative correlations with NO3 and PO4

concentrations (Table 2). DO ranged from 0.4 to 14.9 (Fig. 2I),and showed a significant positive correlation with salinity andsignificant negative correlations with T, precipitation, NO3, PO4,and SiO2 (Table 2). The chlorophyll-a concentration (chl-a) rangedfrom 0.02 to 514.7 mg m�3. Chl-a showed significant positivecorrelations with T, SiO2, pH, and DO and a significant negativecorrelation with salinity.

3.2. Number of phototrophic plankton species

During the study period, 50 diatom species, 23 phototrophicdinoflagellate species, 3 raphidophyte species, 2 cryptophyte

Table 1The range of physical and chemical properties in Masan Bay, Korea from June 2004

to May 2005.

Components Min Max AV SD n

T 4.2 28.6 16.6 7.4 337

Prec 0 116.5 4.9 16.7 337

S 4.1 33.3 25.9 5.8 337

NH4 0.1 129.5 19.5 22.6 335

NO3 ND 105.2 14.9 17.1 335

PO4 ND 11.9 1.9 1.6 335

SiO2 ND 239.7 38.2 30.1 334

pH 7.1 8.7 7.9 0.3 336

DO 0.4 14.9 7.0 2.6 336

Chl-a 0.02 514.7 18.5 49.1 332

Min: minimum, Max: maximum, AV: average, SD: standard deviation, n: number of

data, T: temperature (8C), Prec: precipitation (mm), S: salinity, NH4: ammonium

(mM), NO3: nitrate plus nitrate (mM), PO4: phosphorus (mM), SiO2: silicate (mM),

DO: dissolved oxygen (mg l�1), Chl-a: chlorophyll-a (mg m�3). ND: not detectable.

Fig. 3. Biomass of phytoplankton groups in Masan Bay (SNUMS) from June 1, 2004

to May 31, 2005. (A) Total phototrophic plankton, (B) diatoms, (C) phototrophic

dinoflagellates (PTDs), (D) raphidophytes, (E) cryptophytes, (F) euglenophytes, (G)

phototrophic nanoflagellates, (H) picoeukaryotes, (I) cyanobacteria, and (J)

heterotrophic bacteria. Numbers indicate the sequence of each red tide event.

H.J. Jeong et al. / Harmful Algae 30S (2013) S75–S88S78

species, 2 dictyochophyte species, 1 euglenophyte species, and 1mixotrophic ciliate were found at station SNUMS (SupplementaryTable 1).

3.3. Biomass and abundance of the major taxa of phototrophic

plankton

The biomass of total phototrophic plankton (other than themixotrophic ciliate Mesodinium rubrum) was high from June toSeptember 2004 and intermediate from January to March 2005,but low in other months (Fig. 3A). The maximum biomass andabundance were 11,634 ng C ml�1 and 427,800 cells ml�1, respec-tively (Fig. 3A; Table 3).

From June 1, 2004 to May 31, 2005, the biomass and abundance oftotal diatoms ranged from 0 to 10,981 ng C ml�1 and from 0 to71,538 cells ml�1, respectively (Fig. 3B; Table 3); red tides dominat-ed by diatoms (i.e., >200 ng C ml�1) occurred 6 times (July–September 2004 and April–May 2005). In addition, the biomassand abundance of total phototrophic dinoflagellates (PTDs) rangedfrom 0 to 3516 ng C ml�1 and from 0 to 27,183 cells ml�1,respectively (Fig. 3C; Table 3); red tides dominated by PTDs (i.e.,>200 ng C ml�1) occurred 17 times (June–September 2004 andDecember 2004–March 2005). Furthermore, the biomass andabundance of total raphidophytes ranged from 0 to10,177 ng C ml�1 and from 0 to 90,010 cells ml�1, respectively(Fig. 3D; Table 3); red tides dominated by raphidophytes (i.e.,>200 ng C ml�1) occurred 12 times (June–September 2004 and May2005) (Figs. 3D and 4).

The biomass and abundance of total cryptophytes ranged from0 to 6679 ng C ml�1 and from 0 to 392,440 cells ml�1, respectively

Table 2Correlations among physical and chemical properties in Masan Bay, Korea from June 2004 to May 2005.

Components T P S NH4 NO3 PO4 SiO2 pH DO Chl-a LI

T

P 0.174**

S �0.569** �0.291**

NH4 �0.201**

NO3 0.132* �0.341** 0.144**

PO4 �0.136* 0.266**

SiO2 0.347** 0.234** �0.353** 0.192** 0.248** 0.160*

pH 0.127* �0.122* 0.148** �0.230** �0.261**

DO �0.449** �0.134* 0.289** �0.175** �0.165** �0.261** 0.408**

Chl-a 0.243** �0.198** 0.135* 0.237** 0.198**

LI 0.210** �0.283** �0.143** �0.307** �0.108*

T: temperature, P: precipitation, S: salinity, NH4: ammonium, NO3: nitrite plus nitrate, PO4: phosphate, SiO2: silicate, DO: dissolved oxygen, Chl-a: chlorophyll-a, LI: light

intensity.* p < 0.05.** p < 0.01.

Table 3The abundance (cells ml�1) of phototrophic plankton in Masan Bay, Korea from June 2004 to May 2005. Values in the parentheses are biomass (ng C ml�1). Min: minimum.

Max: maximum; AV: average; SD: standard deviation.

Components Min Max AV SD n

Total phototrophic plankton 5.0 (0.4) 427,800 (11,634) 15,666 (909) 38,371 (1688) 322

Diatoms 0 (0) 71,538 (10,981) 1449 (117) 6577 (694) 322

Phototrophic dinoflagellates 0 (0) 27,183 (3516) 1849 (299) 3784 (564) 322

Raphidophytes 0 (0) 90,010 (10,177) 2125 (241) 9176 (1036) 322

Cryptophytes 0 (0) 392,440 (6679) 9866 (199) 32,886 (631) 322

Euglenophytes 0 (0) 17,029 (2384) 376 (53) 1548 (217) 322

Phototrophic nanoflagellates 0 (0) 73,978 (537) 1579 (12) 4782 (35) 291

Picoeukaryotes 0 (0) 134,746 (288) 9823 (21) 19,727 (42) 295

Cyanobacteria 0 (0) 53,645 (11) 2390 (1) 5333 (1) 292

Mixotrophic ciliates 0 (0) 1014 (1217) 21 (25) 91 (109) 332

H.J. Jeong et al. / Harmful Algae 30S (2013) S75–S88 S79

(Fig. 3E; Table 3); red tides dominated by cryptophytes (i.e.,>200 ng C ml�1) occurred 20 times (June–November 2004). Inaddition, the biomass and abundance of total euglenophytesranged from 0 to 2384 ng C ml�1 and from 0 to 17,029 cells ml�1,respectively (Fig. 3F; Table 3); red tides dominated by eugleno-phytes (i.e., >200 ng C ml�1) occurred 7 times (June–August,December 2004 and January and May 2005). Furthermore, thebiomass and abundance of total small phototrophic nanoflagel-lates (PNFs; 3–6 mm cell length) ranged from 0 to 537 ng C ml�1

and from 0 to 73,978 cells ml�1, respectively (Fig. 3G; Table 3);both abundance and biomass of the PNFs were highest in July 2004.

The biomass and abundance of total picoeukaryotes (PE) rangedfrom 0 to 288 ng C ml�1 and from 0 to 134,746 cells ml�1,respectively (Fig. 3H; Table 3); both abundance and biomass ofthe PE were highest in April 2005. In addition, the biomass andabundance of total cyanobacteria (CYA) ranged from 0 to11 ng C ml�1 and from 0 to 53,645 cells ml�1, respectively(Fig. 3I; Table 3); both abundance and biomass of the CYA werehighest in July 2004. Furthermore, the biomass and abundance ofheterotrophic bacteria (HB) ranged from 12.6 to 548.4 ng C ml�1

and from 4.4 � 105 to 1.9 � 107 cells ml�1, respectively; bothabundance and biomass of the HB were highest in May 2005(Fig. 3J).

The biomass and abundance of the mixotrophic ciliateMesodinium rubrum ranged from 0 to 1217 ng C ml�1 and from 0to 1014 cells ml�1, respectively (Table 3); both abundance andbiomass of the mixotrophic ciliates were highest in May 2005 (Yihet al., 2013).

Phototrophic dinoflagellates were dominant among the photo-trophic plankton in mid-June 2004 and December 2004–March2005, while diatoms were dominant in September 2004 and April2005 (Fig. 4). In addition, raphidophytes were dominant duringsome periods of June–September 2004.

3.4. Correlations between major taxa of phototrophic plankton and

environmental factors

Correlations between biological variables and physical andchemical properties measured during the study period are shown

Fig. 4. Biomass compositions (%) of phytoplankton groups in Masan Bay (SNUMS) from J

raphidophytes, CRY: cryptophytes, EUG: euglenophytes, PNF: phototrophic nanoflagell

in Table 4. The biomass of total diatoms showed significant positivecorrelations with T, pH, and light intensity (LI). In addition, thebiomass of total PTDs showed significant positive correlations withsalinity, pH, DO, and chl-a, but negative correlations with T and theconcentrations of NO3 and PO4. Furthermore, the biomass of totalraphidophytes showed significant positive correlations with T, pH,and chl-a, but negative correlations with salinity and theconcentration of PO4.

The biomass of total euglenophytes showed significantpositive correlations with T, pH, and DO, but negative correlationswith the concentrations of NO3 and PO4. In addition, the biomassof total cryptophytes showed significant positive correlationswith T, pH, and chl-a, but negative correlations with salinity andthe concentration of PO4. Furthermore, the biomass of total PNFsshowed significant positive correlations with T and the concen-tration of SiO2, but a negative correlation with salinity. Thebiomass of total picoeukaryotes showed a significant positivecorrelation with LI.

The biomass of total cyanobacteria showed significantpositive correlations with T and pH. In addition, the biomassof total HB showed significant positive correlations with T, pH,DO, chl-a, and LI, but negative correlations with the concentra-tions of NO3 and NH4.

3.5. Correlations among major taxa

Correlations among biological variables are shown in Table 5.The biomass of total diatoms showed a significant positivecorrelation with the biomass of total PNFs. In addition, thebiomass of total PTDs showed significant positive correlations withthe biomass of total euglenophytes, raphidophytes, HB, andcyanobacteria, but a negative correlation with the biomass ofPE. Furthermore, the biomass of total raphidophytes showedsignificant positive correlations with the biomass of PNFs and HB.The biomass of total euglenophytes showed significant positivecorrelations with the biomass of PTDs, cryptophytes, raphido-phytes, cyanobacteria, and HB. The biomass of total cryptophytesshowed significant positive correlations with the biomass ofeuglenophytes, raphidophytes, PNFs, PE, and HB. In addition, the

une 1, 2004 to May 31, 2005. DIA: diatoms, PTD: phototrophic dinoflagellates, RAP:

ates, PE: picoeukaryotes, and CYA: cyanobacteria.

Table 4Correlations between the biomass of phototrophic plankton (PP) and bacteria and physical and chemical properties in Masan Bay, Korea from June 2004 to May 2005.

Component PP

DIA PTD RAP EUG CRY PNF PE CYA TP HB

T 0.143** �0.200** 0.243** 0.112* 0.314** 0.173** 0.162** 0.274** 0.294**

P

S 0.186** �0.141* �0.243** �0.177** �0.142**

NH4 �0.130*

NO3 �0.120* �0.114* �0.142** �0.114*

PO4 �0.190** �0.127* �0.140* �0.145** �0.245**

SiO2 0.124*

pH 0.220** 0.189** 0.269** 0.164** 0.138* 0.112* 0.390** 0.201**

DO 0.269** 0.210** 0.208** 0.157**

Chl-a 0.197** 0.443** 0.341** 0.470** 0.238**

LI 0.126* 0.126* 0.151**

T: temperature, P: precipitation, S: salinity, NH4: ammonium, NO3: nitrite plus nitrate, PO4: phosphate, SiO2: silicate, DO: dissolved oxygen, Chl-a: chlorophyll-a, LI: Light

intensity, DIA: diatoms, PTD: phototrophic dinoflagellates, RAP: raphidophytes, EUG: euglenophytes, CRY: cryptophytes, PNF: phototrophic nanoflagellats, PE:

picoeukaryotes, CYA: cyanobacteria, HB: heterotrophic bacteria, TP: total phototrophic plankton.* p < 0.05.** p < 0.01.

Table 5Correlations among major phototrophic plankton groups and heterotrophic bacteria in Masan Bay, Korea from June 2004 to May 2005.

Components DIA PTD RAP EUG CRY PNF PE CYA TP HB

DIA

PTD

RAP 0.146** 0.127* 0.158**

EUG 0.128*

CRY 0.175**

PNF 0.152** 0.148** 0.201**

PE �0.116* 0.139* 0.421** 0.217**

CYA 0.132* 0.113*

TP 0.417** 0.423** 0.725** 0.314** 0.546** 0.254** 0.264**

HB 0.126* 0.195** 0.244** 0.153** 0.214**

DIA: diatoms, PTD: phototrophic dinoflagellates, RAP: raphidophytes, EUG: euglenophytes, CRY: cryptophytes, PNF: phototrophic nanoflagellats, PE: picoeukaryotes, CYA:

cyanobacteria, HB: heterotrophic bacteria, TP: total phototrophic plankton.* p < 0.05.** p < 0.01.

H.J. Jeong et al. / Harmful Algae 30S (2013) S75–S88S80

biomass of total PNFs showed a significant positive correlationwith the biomass of total diatoms, cryptophytes, raphidophytes,PE, and HB. Furthermore, the biomass of total PE showedsignificant positive correlations with the biomass of cryptophytes,PNFs, and HB, but a significant negative correlation with thebiomass of PTDs. The biomass of total cyanobacteria showedsignificant positive correlations with the biomass of PTDs andeuglenophytes, while that of total HB showed significant positivecorrelations with the biomass of PTDs, raphidophytes, eugleno-phytes, cryptophytes, PNFs, and PE.

3.6. Abundance and biomass of red-tide organisms

From June 1, 2004 to May 31, 2005, there were 36 red-tideevents (Fig. 3; Supplementary Table 2); 7 events were overwhelm-ingly dominated by cryptophytes, 5 events by PTDs, 2 by diatoms, 2by raphidophytes, and 1 by a mixotrophic ciliate, while theremaining red-tide events were dominated by mixtures of 2–4different taxa (Supplementary Table 2).

Most red tides occurred in June–September 2004 or January–March 2005 (Fig. 3; Supplementary Table 2). The PTDs Akashiwo

sanguinea, Ceratium furca, Cochlodinium polykrikoides, Dinophysis

acuminata, Prorocentrum micans, and P. triestinum, and the diatomsThalassiosira decipiens and T. gravida formed red tides only insummer, while the PTD Heterocapsa triquetra caused red tides inthe winter (Fig. 5; Supplementary Table 3). The PTD P. minimum

caused red tides in both summer and winter (Fig. 5). Furthermore,the raphidophyte Heterosigma akashiwo, the diatoms Skeletonema

costatum and T. rotula, and cryptophytes caused red tides in 2–3seasons (Fig. 5).

In general, the physical, chemical, and biological propertiesmeasured when each red-tide species was present and its red-tideoccurred differed from those of the other species. Thus, we havedescribed these properties for each species below.

Akashiwo sanguinea. This dinoflagellate formed red tides 5times from June to August 2004 (Fig. 5A; Supplementary Table 3).The maximum abundances (biomass) of A. sanguinea during thered tides were 280–519 cell ml�1 (409–757 ng C ml�1). Watertemperatures at the initial and terminal stages of these red tideswere 21.2–28.1 8C. In addition, salinities at the initial and terminalstages of these red tides were 17.2–28.8.

The NH4 concentration was 9.9–29.4 mM at the initial stages ofthe red tides and 1.2–29.4 mM at the terminal stages (Supplemen-tary Table 3). In addition, NO3 concentrations at the initial andterminal stages of these red tides were 0.2–8.0 mM. Furthermore,the PO4 concentration was 0.3–1.9 mM at the initial stages and 0.1–1.9 mM at the terminal stages. The SiO2 concentration at the initialstages was 34.5–76.3 mM and 22.8–76.3 mM at the terminalstages.

During these red tides, Heterosigma akashiwo, cryptophytes,Eutreptiella gymnastica, Prorocentrum triestinum, and/or Ceratium

furca were abundant (Supplementary Table 2).Prorocentrum minimum. This dinoflagellate formed red tides

4 times in June and December 2004 and January and February 2005(Fig. 5B; Supplementary Table 3). The maximum abundance(biomass) of P. minimum during the summer red tide was

Fig. 5. Biomass of the red-tide causative species or taxa in Masan Bay (SNUMS) from June 1, 2004 to May 31, 2005. (A) Akashiwo sanguinea, (B) Prorocentrum minimum, (C)

Eutreptiella gymnastica, (D) Heterosigma akashiwo, (E) cryptophytes, (F) Prorocentrum triestinum, (G) Dinophysis acuminata, (H) Cochlodinium polykrikoides, (I) Skeletonema

costatum, (J) Thalassiosira decipiens, (K) Thalassiosira gravida, (L) Thalassiosira rotula, (M) Prorocentrum micans, (N) Heterocapsa triquetra, and (O) Eucampia zodiacus. Numbers

indicate the sequence of each red tide event (i.e., 1 means the first red tide event during the study period).

H.J. Jeong et al. / Harmful Algae 30S (2013) S75–S88 S81

22,817 cell ml�1 (2936 ng C ml�1). The water temperatures at theinitial and terminal stages of the summer red tide were 21.2 and22.6 8C, respectively, while the salinities were 26.3 and 26.4,respectively. The NH4 concentrations at the initial and terminalstages were 19.9 mM and 0.4 mM, respectively, while the NO3

concentrations were 3.3 mM and 0.2 mM, respectively. The PO4

concentrations at the initial and terminal stages were 1.7 mM and0.3 mM, respectively, while the SiO2 concentrations were 41.8 mMand 44.7 mM, respectively. Eutreptiella gymnastica was abundantduring the summer red tide dominated by P. minimum (Supple-mentary Table 2).

The maximum abundances (biomass) of Prorocentrum mini-

mum during the winter red tides were 1693–27,157 cell ml�1

(218–3495 ng C ml�1), similar to that during the summer redtide (Supplementary Table 3). The water temperatures at theinitial and terminal stages of the winter red tides were 6.3–14.3 8C and 5.4–14.3 8C, respectively, while the salinities were29.9–30.2 and 29.1–30.1, respectively. The NH4 concentrationsat the initial and terminal stages were 7.9–14.2 mM and 7.9–123.1 mM, respectively, while the NO3 concentrations at theinitial and terminal stages were 10.2–19.2 mM and 19.2–38.5 mM, respectively. The PO4 concentrations at the initialand terminal stages were 0.9–1.8 mM and 1.8–3.1 mM, respec-tively, while the SiO2 concentrations were 15.8–21.0 mM and18.0–30.5 mM, respectively.

Eutreptiella gymnastica. This euglenophyte formed red tides 4times from June to August 2004 and May 2005 (Fig. 5C;Supplementary Table 3). The maximum abundances (biomass)

of E. gymnastica during the summer red tides were 7286–17,029 cell ml�1 (1020–2384 ng C ml�1). The water temperaturesat the initial and terminal stages of the summer red tides were21.6–27.4 8C and 21.8–28.4 8C, respectively, while the salinitieswere 22.1–29.3 and 22.8–28.5, respectively. NH4 concentrations atthe initial and terminal stages were 2.0–13.9 mM and 0.3–11.9 mM, while the NO3 concentrations were 0.4–21.9 mM and0.3–14.0 mM, respectively. The PO4 concentrations at the initialand terminal stages were 0.2–1.2 mM and 0.4–1.5 mM, respective-ly, while the SiO2 concentrations were 13.6–35.7 mM and 13.6–47.9 mM, respectively (Supplementary Table 3).

Eutreptiella gymnastica formed red tides 3 times from December2004 to January 2005 (Fig. 5; Supplementary Table 3). Themaximum abundances (biomass) of E. gymnastica during thewinter red tides were 1881–5000 cell ml�1 (263–700 ng C ml�1)The water temperatures at the initial and termination stages of thewinter red tides were 5.3–9.8 8C and 5.3–6.9 8C, while the salinitieswere 30.2–31.4 and 29.1–31.4, respectively. The NH4 concentra-tions at the initial and terminal stages were 0.9–22.7 mM and 0.9–123.1 mM, respectively, while the NO3 concentrations at the initialand terminal stages were 6.3–13.7 mM and 6.3–24.8 mM, respec-tively. The PO4 concentrations at the initial and terminal stageswere 0.7–1.2 mM and 0.7–1.9 mM, respectively, while the SiO2

concentrations were 18.7–23.2 mM and 18.0–23.2 mM, respec-tively (Supplementary Table 3).

Heterosigma akashiwo. This raphidophyte formed red tides 12times from June to September in 2004 and May 2005 (Fig. 5D;Supplementary Table 3). The maximum abundances (biomass) of

H.J. Jeong et al. / Harmful Algae 30S (2013) S75–S88S82

H. akashiwo during the red tides were 2238–90,000 cell ml�1 (252–10,148 ng C ml�1). The water temperatures at the initial andterminal stages of these red tides were 21.2–28.1 8C and 21.6–28.1 8C, respectively, while the salinities were 12.2–28.8 and 16.2–28.8, respectively. The NH4 concentrations at the initial andterminal stages were 2.0–35.3 mM and 2.0–109.5 mM, respective-ly, while the NO3 concentrations were both 0.2–105 mM. The PO4

concentrations at the initial and terminal stages were 0.1–1.9 mMand 0.1–10.7 mM, while the SiO2 concentrations were 13.6–144.6 mM and 5.9–144.6 mM.

During these red tides, Akashiwo sanguinea, cryptophytes,Ceratium furca, Prorocentrum triestinum, and/or Eutreptiella gym-

nastica were abundant (Supplementary Table 2).Cryptophytes. Cryptophytes (<10 mm in size) formed red tides

21 times in June–November 2004 (Fig. 5E; Supplementary Table 3).The maximum abundances (biomass) of cryptophytes during thered tides were 11,862–392,000 cell ml�1 (202–6664 ng C ml�1).The water temperatures at the initial and terminal stages of thesered tides were 17.5–28.1 8C and 17.5–28.4 8C, respectively, andsalinities were 8.3–29.3 and 8.3–29.8, respectively. The NH4

concentrations at the initial and terminal stages were 0.4–45.8 mMand 0.3–42.9 mM, respectively, while the NO3 concentrations wereboth 0.2–105 mM. PO4 concentrations at the initial and terminalstages were both 0.0–5.8 mM, while the SiO2 concentrations wereboth 0.0–144.6 mM.

During these red tides, Akashiwo sanguinea, Ceratium furca,Eutreptiella gymnastica, Heterosigma akashiwo, Mesodinium rubrum,Prorocentrum triestinum, Skeletonema costatum, Thalassiosira dec-

ipiens, T. gravida, T. rotula, and/or were abundant (SupplementaryTable 2).

Prorocentrum triestinum. This dinoflagellate formed red tides7 times in June, August, and September 2004 (Fig. 5F; Supplemen-tary Table 3). The maximum abundances (biomass) of P. triestinum

during the red tides were 2020–20,331 cell ml�1 (290–2907 ng C ml�1). The water temperatures at the initial andterminal stages of the red tides were 22.6–27.5 8C and 22.6–26.7 8C, respectively, while the salinities were 16.4–26.0 and 17.0–28.0 psu, respectively. The NH4 concentrations at the initial andterminal stages were 3.0–29.7 mM and 1.2–29.7 mM, respectively.The NO3 concentrations at the initial and terminal stages were 0.8–105 mM and 0.3–105 mM, respectively. The PO4 concentrations atthe initial and terminal stages were both 0.1–2.2 mM, while theSiO2 concentrations were 43.1–144.6 mM and 22.8–144.6 mM,respectively.

During these red tides, cryptophytes, Heterosigma akashiwo,Cochlodinium polykrikoides, and/or Dinophysis acuminata wereabundant (Supplementary Table 2).

Dinophysis acuminata. This dinoflagellate formed a red tideonce with Cochlodinium polykrikoides as described above (Fig. 5G;Supplementary Table 3). The maximum abundance (biomass) of D.

acuminata during the red tide was 68 cell ml�1 (215 ng C ml�1).During this red tide, Cochlodinium polykrikoides and Prorocen-

trum triestinum were abundant (Supplementary Table 2).Cochlodinium polykrikoides. This dinoflagellate formed a red

tide once in June 2004 (Fig. 5H; Supplementary Table 3). Themaximum abundance (biomass) of C. polykrikoides during the redtide was 207 cells ml�1 (192 ng C ml�1). Water temperatureduring the one-day red tide was 23.0 8C, while the salinity was17.0. In addition, the NH4 concentration was 16.5 mM, while theNO3 concentration was 0.8 mM. Furthermore, PO4 concentrationduring the red tide was 2.1 mM, while the SiO2 concentration was84.2 mM.

During this red tide, Prorocentrum triestinum and Dinophysis

acuminata were abundant (Supplementary Table 2).Skeletonema costatum. This diatom formed red tides 4 times

from July to September 2004 and April 2005 (Fig. 5; Supplementary

Table 3). The maximum abundances (biomass) of S. costatum duringthe red tides were 15,500–59,143 cell ml�1 (403–1538 ng C ml�1).The water temperatures at the initial and terminal stages of thesered tides were 12.4–27.0 8C and 13.4–28.4 8C, respectively, while thesalinities were 16.4–28.8 and 18.2–28.5, respectively. The NH4

concentrations at the initial and terminal stages were 20.1–44.1 mMand 0.3–24.3 mM, respectively, while the NO3 concentrations were0.3–4.2 mM and 0.3–10.1 mM, respectively. The PO4 concentrationsat the initial and terminal stages were 0.1–1.6 mM and 0.0–2.6 mM,respectively, while the SiO2 concentrations were 14–137 mM and7.7–37.5 mM, respectively.

During these red tides, cryptophytes were abundant (Supple-mentary Table 2).

Thalassiosira spp. T. decipiens and T. gravida formed red tides2–3 times from July to September 2004, while T. rotula formed redtides 2 times in August 2004 and April 2005 (Fig. 5; SupplementaryTable 2). The maximum abundances (biomass) of T. decipiens, T.

gravida, and T. rotula during the red tides were 10,400–34,298(2089–6890), 520–3782 (278–2022), and 400–478 cell ml�1 (297–355 ng C ml�1), respectively.

Prorocentrum micans. This dinoflagellate formed red tidestwice in June and September 2004 (Fig. 5; Supplementary Table 3).The maximum abundances (biomass) of P. micans during the redtides were 557–1600 (555–1594 ng C ml�1).

Heterocapsa triquetra. This dinoflagellate formed red tides 4times in January–March 2005 (Fig. 5; Supplementary Table 3). Themaximum abundances (biomass) of H. triquetra during the redtides were 1321–10,243 cell ml�1 (297–2303 ng C ml�1). Thewater temperatures at the initial and terminal stages of the redtide were 5.3–6.9 8C and 5.3–8.0 8C, respectively, while thesalinities were 29.8–31.3 and 29.3–31.5, respectively. The NH4

concentrations at the initial and terminal stages were 0.9–30.9 mMand 0.9–15.4 mM, respectively, while the NO3 concentrations were8.2–20.5 mM and 6.6–30.8 mM, respectively. The PO4 concentra-tions at the initial and terminal stages were 0.0–1.6 mM and 0.7–2.4 mM, respectively, while the SiO2 concentrations were 7.4–23.2 mM and 7.4–38.1 mM, respectively.

Eucampia zodiacus. This diatom formed a red tide once in May2005 (Fig. 5; Supplementary Table 3). The maximum abundance(biomass) of Prorocentrum micans during the red tides was 3275(835 ng C ml�1).

Ceratium furca. This dinoflagellate formed a red tide once inJuly 2004 (Supplementary Table 3). The maximum abundance(biomass) of C. furca during the red tides was 134 cells ml�1

(167 ng C ml�1). The water temperatures at the initial and terminalstages of the red tide were 24.7 8C and 24.8 8C, respectively, whilethe salinities were 20.4 and 19.3, respectively. The NH4 concen-trations at the initial and terminal stages were 1.2 mM and11.3 mM, respectively, while the NO3 concentrations were 0.3 mMand 25.1 mM, respectively. PO4 concentrations at the initial andterminal stages were both 0.1 mM, while the SiO2 concentrationswere 22.8 mM and 30.0 mM, respectively.

During these red tides, Heterosigma akashiwo, cryptophytes,Prorocentrum triestinum, and/or Akashiwo sanguinea were abun-dant (Supplementary Table 2).

Mesodinium rubrum. This mixotrophic ciliate formed red tides3 times in July and September 2004 and May 2005 (SupplementaryTable 3). The maximum abundances (biomass) of M. rubrum duringthe red tides were 219–1014 cell ml�1 (262–1217 ng C ml�1). Thewater temperatures at the initial and terminal stages of the red tidewere 18.3–27.9 8C and 18.0–27.9 8C, respectively, while thesalinities were 23.5–25.6 and 20.5–26.9, respectively. Other relateddata can be found in Yih et al. (2013).

Other red-tide organisms. In addition to the species describedabove, the PTDs Alexandrium spp., Ceratium fusus, C. tripos,Gonyaulax polygramma, G. verior, Gymnodinium sp. (20-mm cell

Table 6Correlations between red-tide species and environmental factors in Masan Bay, Korea from June 2004 to May 2005.

Species T S NH4 NO3 PO4 SiO2 pH DO Chl-a LI

Sc 0.159** �0.126* 0.211**

Td 0.166**

Tg 0.126* 0.138**

As 0.236** �0.143** �0.154** 0.222** 0.280**

Asp

Cf 0.115* �0.111* 0.163** 0.332**

Cp �0.120* 0.122* 0.391**

Da 0.126* 0.347**

Ht �0.413** 0.232** �0.119* 0.280** �0.151**

Pmc 0.132*

Pmn �0.245** 0.255** �0.187** �0.179** 0.117* 0.202**

Pt 0.149* �0.153** 0.161* 0.438**

St 0.137* 0.127*

Ha 0.242** �0.127* 0.269** 0.442**

Eg 0.112* �0.114* �0.140* 0.164** 0.210**

Cry 0.314** �0.243** �0.145** 0.138* 0.341**

T: temperature, S: salinity, NH4: ammonium, NO3: nitrite plus nitrate, PO4: phosphate, SiO2: silicate, DO: dissolved oxygen, Chl-a: chlorophyll-a, LI: Light intensity, Sc:

Skeletonema costatum, Td: Thalassiosira decipiens, Tg: T. gravida, As: Akashiwo sanguinea, Asp: Alexandrium sp., Cf: Ceratium furca, Cp: Cochlodinium polykrikoides, Da: Dinophysis

acuminata, Ht: Heterocapsa triquetra, Pmc: Prorocentrum micans, Pmn: P. minimum, Pt: P. triestinum, St: Scrippsiella trochoidea, Ha: Heterosigma akashiwo, Eg: Eutreptiella

gymnastica, Cry: cryptophytes.* p < 0.05.** p < 0.01.

H.J. Jeong et al. / Harmful Algae 30S (2013) S75–S88 S83

length), Heterocapsa rotundata, and Scrippsiella trochoidea andthe raphidophytes Chattonella sp. and Fibrocapsa sp. were found,although they did not form red tides (Supplementary Tables 1and 3).

3.7. Correlations between red-tide organisms and environmental

factors

Using all of the data obtained in the present study, we analyzedcorrelations between red-tide organisms and physical–chemicalproperties (Table 6).

The biomass of Skeletonema costatum, Thalassiosira gravida,Akashiwo sanguinea, Ceratium furca, Dinophysis acuminata, Pro-

rocentrum micans, P. triestinum, Scrippsiella trochoidea, Heterosigma

akashiwo, Eutreptiella gymnastica, and cryptophytes had significantpositive correlations with water temperature, while those ofHeterocapsa triquetra and P. minimum had significant negativecorrelations with water temperature (Table 6). In addition, thebiomass of H. triquetra and P. minimum had significant positivecorrelations with salinity, while those of Cochlodinium polykri-

koides, P. triestinum, and cryptophytes had significant negativecorrelations with salinity (Table 6). Furthermore, the biomass of A.

sanguinea and E. gymnastica had significant negative correlationswith NO3 concentration, while those of S. costatum, A. sanguinea, C.

furca, P. minimum, H. akashiwo, E. gymnastica, and cryptophytes hadsignificant negative correlations with PO4 concentration. Thebiomass of P. triestinum had significant positive correlations withSiO2 concentration, while those of H. triquetra and P. minimum hadsignificant negative correlations with SiO2 concentration. Inaddition, the biomass of S. costatum, T. decipiens, T. gravida, A.

sanguinea, C. furca, C. polykrikoides, P. minimum, H. akashiwo, E.

gymnastica, and cryptophytes had significant positive correlationswith pH (Table 6). Furthermore, the biomass of H. triquetra, P.

minimum, and E. gymnastica had significant positive correlationswith DO (Table 6).

3.8. Correlations among red-tide organisms

A red-tide species can be a competitor, prey, or predator ofanother red-tide species. The biomass of Skeletonema costatum hadsignificant positive correlations with the biomass of Thalassiosira

decipiens, T. gravida, cryptophytes, and PNFs, while the biomass of

T. gravida had significant positive correlations with the biomass ofcryptophytes and PNFs. In addition, the biomass of Akashiwo

sanguinea had significant positive correlations with the biomass ofCeratium furca, Cochlodinium polykrikoides, Dinophysis acuminata,Prorocentrum micans, P. triestinum, Scrippsiella trochoidea, Hetero-

sigma akashiwo, cryptophytes, PNFs, and heterotrophic bacteria,while the biomass of C. furca had significant positive correlationswith the biomass of C. polykrikoides, D. acuminata, P. triestinum, H.

akashiwo, and cryptophytes (Table 7). Furthermore, the biomass ofC. polykrikoides had significant positive correlations with thebiomass of A. sanguinea, C. furca, D. acuminata, P. triestinum, H.

akashiwo, cryptophytes, PNFs, and heterotrophic bacteria, whilethat of D. acuminata had significant positive correlations withthe biomass of A. sanguinea, C. furca, C. polykrikoides, P. triestinum,H. akashiwo, cryptophytes, PNFs, and heterotrophic bacteria(Table 7). The biomass of H. triquetra showed a significant positivecorrelation with the biomass of P. minimum (Table 7). In addition,the biomass of P. micans showed a significant positive correlationwith the biomass of A. sanguinea, P. minimum, and heterotrophicbacteria, while the biomass of P. minimum showed a significantpositive correlation with the biomass of Alexandrium sp., H.

triquetra, P. micans, E. gymnastica, and cyanobacteria (Table 7).Furthermore, the biomass of P. triestinum showed a significantpositive correlation with the biomass of A. sanguinea, C. furca, C.

polykrikoidea, D. acuminata, H. akashiwo, PNFs, and heterotrophicbacteria, while the biomass of S. trochoidea showed a significantpositive correlation with the biomass of A. sanguinea, H. akashiwo,E. gymnastica, PNFs, and heterotrophic bacteria (Table 7). Thebiomass of H. akashiwo showed a significant positive correlationwith the biomass of A. sanguinea, C. furca, C. polykrikoides, D.

acuminata, cryptophytes, PNFs, and heterotrophic bacteria(Table 7).

3.9. Succession in the causative species of serial red tides

From June 1, 2004 to May 31, 2005, there were 36 red-tideevents. Successions occurred in the causative species of serial redtides as follows: (1) from June 1 to 15, 2004, Heterosigma akashiwo

and cryptophytes shifted to Prorocentrum minimum then toEutreptiella gymnastica; (2) from June 18 to July 3, 2004,cryptophytes shifted to H. akashiwo, to P. triestinum, to Cochlodi-

nium polykrikoides and Dinophysis acuminata, and finally to

Table 7Correlations among red-tide organisms in Masan Bay, Korea from June 2004 to May 2005.

Species Sc Td Tg As Asp Cf Cp Da Ht Pmc Pmn Pt St Ha

Sc

Td 0.372**

Tg 0.284**

As

Asp

Cf 0.404**

Cp 0.356** 0.447**

Da 0.467** 0.209** 0.707**

Ht

Pmc 0.179**

Pmn 0.150** 0.211** 0.131*

Pt 0.208** 0.247** 0.755** 0.569**

St 0.155**

Ha 0.618** 0.314** 0.143** 0.231** 0.189** 0.220**

Eg 0.127* 0.230**

Cry 0.193** 0.184** 0.248** 0.138** 0.115* 0.116* 0.158**

PNF 0.210** 0.369** 0.212** 0.125* 0.167** 0.117* 0.292** 0.148**

PE �0.124*

CYA 0.145** 0.261**

HB 0.191** 0.188** 0.232** 0.132* 0.182** 0.352** 0.194**

Sc: Skeletonema costatum, Td: Thalassiosira decipiens, Tg: T. gravida, As: Akashiwo sanguinea, Asp: Alexandrium sp., Cf: Ceratium furca, Cp: Cochlodinium polykrikoides, Da:

Dinophysis acuminata, Ht: H. triquetra, Pmc: Prorocentrum micans, Pmn: P. minimum, Pt: P. triestinum, St: Scrippsiella trochoidea, Ha: Heterosigma akashiwo, Eg: Eutreptiella

gymnastica, Cry: cryptophytes, PNF: phototrophic nanoflagellats, PE: picoeukaryotes, CYA: cyanobacteria, HB: heterotrophic bacteria.* p < 0.05.** p < 0.01.

H.J. Jeong et al. / Harmful Algae 30S (2013) S75–S88S84

Akashiwo sanguinea and C. furca; (3) from July 10 to August 12,2004, cryptophytes and Heterocapsa akashiwo shifted to Akashiwo

sanguinea; and (4) from January 8 to March 15, 2005, P. minimum

shifted to Heterocapsa triquetra.

3.10. Variations in vertical distribution in Masan Bay

On August 17, 2004 when the water column was stratified, the T

of the surface water at station SNUMS was 28.1 8C, while the T nearthe bottom was 27.5 8C. In addition, the DO concentrations atthe surface and near the bottom were 7.05 and 4.33 mg l�1,respectively. Furthermore, the chl-a concentrations at the surfaceand near the bottom were 20.1 and 14.4 mg l�3, respectively. Thebiomass of total phytoplankton at the surface and near the bottomwas 550 and 180 ng C ml�1, respectively. Thus, stratification of thewater column at SNUMS in August resulted in differences in DO,chl-a concentration, and the biomass of total phytoplanktonbetween the surface and bottom waters; values at the bottom were30–70% of the values measured at the surface.

4. Discussion

4.1. Physical and chemical properties of Masan Bay

NO3 and SiO2 concentrations showed significant negativecorrelations with salinity, suggesting that freshwater drainageafter rainfall from streams into Masan Bay may increase theconcentrations of NO3 and SiO2. In addition, total phototrophicdinoflagellates, raphidophytes, euglenophytes, and cryptophyteshad significant negative correlations with the concentrations ofPO4. Thus, PO4 may be not a critical factor limiting the growth ofthese algae in Masan Bay.

Significant positive correlations between pH and the abun-dances of total diatoms, phototrophic dinoflagellates, raphido-phytes, euglenophytes, cryptophytes, and cyanobacteria, suggestthat during red tides, CO2 uptake by diatoms, phototrophicdinoflagellates, raphidophytes, euglenophytes, cryptophytes, andcyanobacteria may increase pH. Thus, blooms or red tidesdominated by these algae may play an important role in reducingocean acidification.

4.2. Number of red-tide events in Masan Bay

There were 36 red-tide events in Masan Bay during the one-year study period, and the total duration of the red-tide period was195 days (i.e., �53% of 365 days). Previously, the National FisheriesResearch and Development Institute (NFRDI, 1996) reported thatin Masan Bay, red tides occurred 14 times in 1991, 4 times in 1992,10 times in 1993 and 1994, and 3 times in 1995. These NFRDI datawere based on weekly sampling. Thus, the number of red tidesreported per year in Masan Bay may have been affected by thefrequency of sampling. The generation times of the causativespecies for red tides in Masan Bay are short (Jeong et al., 2010a) andthus, daily samples may be needed to detect the occurrence anddynamics of red tides.

4.3. Causative species of red tide events in Masan Bay

During the study period, seven PTDs (Akashiwo sanguinea,Ceratium furca, Cochlodinium polykrikoides, Dinophysis acuminata,Heterocapsa triquetra, Prorocentrum minimum, and P. triestinum)predominantly formed red tides, while two diatom species(Skeletonema costatum and Thalassiosira decipiens), one raphido-phyte (Heterosigma akashiwo), one euglenophyte (Eutreptiella

gymnastica), and one mixotrophic ciliate (Mesodinium rubrum)predominantly formed red tides. In addition, cryptophytespredominantly formed several red tides.

Diatoms have been known to grow faster than similarly sizedPTDs or nano- and micro-flagellates when nutrient concentrationsare high (Banse, 1982). Furthermore, in the uptake (U) of eachnutrient, the values of K1/2 (the nutrient concentration sustaining(1/2)Umax) for diatoms are lower than those for PTDs; thus, diatomsare able to grow earlier than PTDs as nutrient concentrationsincrease (Smayda, 1997). During the study period, the means of theconcentrations of NH4, NO3, PO4, and SiO2 in the surface water inMasan Bay were 19.5 mM, 14.9 mM, 1.9 mM, and 38.2 mM,respectively. Thus, diatoms would be expected to cause red tidesmore frequently and dominate the phototrophic plankton biomasscompared to PTDs or flagellates. However, the results were theopposite of those expected based on nutrient concentrations alone,indicating that other factors must influence these patterns. Many

Table 8Predator–prey relationships among red tide organisms in Masan Bay, Korea from June 2004 to May 2005.

Prey PD

Sc As Asp Cf Cp Da Ht Pmc Pmn Pt St Ha Eg Ref.

Sc (+) (+) ? (+) ? (+) (+) (+) (+) (+) (�) 1, 2

As (�) (�) ? (�) ? (�) (�) (�) (�) (�) (�) 1, 3

Asp (�) (�) ? (�) ? (�) (�) (�) (�) (�) (�) 1, 3

Cf ? (�) ? ? ? (�) (�) (�) (�) (�) (�) 4

Cp (�) (�) (�) ? ? (�) (�) (�) (�) (�) (�) 1, 5

Da ? ? ? ? ? (�) ? ? ? ? ? 6

Ht (�) (+) (�) ? (�) ? (+) (�) (�) (�) (�) 1, 2, 3

Hr (�) (+) (�) ? ? ? ? ? ? ? ? (�) 1, 3

Pmc (�) (�) (�) ? (�) ? (�) (�) (�) (�) (�) 1, 3

Pmn (�) (+) (+) ? (�) ? (+) (+) (+) (+) (�) 1, 3

Pt (�) (+) (�) ? (�) ? (�) (+) (�) (�) (�) 1, 3

St (�) (+) (�) ? (�) ? (�) (�) (�) (�) (�) 1, 3

Cry ? (+) (+) ? (+) (�) (+) (+) (+) (+) (+) (�) 2, 3, 5, 6

Ha (�) (+) (+) ? (+) ? (+) (+) (+) (+) (+) 2, 3, 5, 6

PNF ? (+) ? ? ? ? ? ? ? ? ? ? 7

PE ? (+) ? ? ? ? ? ? ? ? ? ? 8

HB ? (+) (+) (+) (+) ? (+) (+) (+) (+) (+) (+) (+) 2, 10

CYA ? (+) (+) (+) (+) ? (+) (+) (+) (+) (+) (+) 2, 8, 9

(+): feeding; (�): non-feeding; ?: not-tested; PD: predator.

Sc: Skeletonema costatum, As: Akashiwo sanguinea, Asp: Alexandrium sp., Cf: Ceratium furca, Cp: Cochlodinium polykrikoides, Da: Dinophysis acuminata, Ht: Heterocapsa triquetra,

Hr: H. rotundata, Pmc: Prorocentrum micans, Pmn: P. minimum, Pt: P. triestinum, St: Scrippsiella trochoidea, Cry: cryptophytes, Ha: Heterosigma akashiwo, PNF: phototrophic

nanoflagellats, PE: picoeukaryotes, HB: heterotrophic bacteria, CYA: cyanobacteria, Eg: Eutreptiella gymnastica.

1: Yoo et al. (2009), 2: Jeong (2011), 3: Jeong et al. (2005b), 4: Smalley et al. (1999), 5: Jeong et al. (2004), 6: Park et al. (2006), 7: Jeong et al. (in preparation), 8: Lee (2006), 9:

Jeong et al. (2005a), 10: Seong et al. (2006).

H.J. Jeong et al. / Harmful Algae 30S (2013) S75–S88 S85

PTDs are known to feed on diverse prey such as bacteria,nanoflagellates, diatoms, other PTDs, and heterotrophic protists(e.g., Jeong et al., 2005a, 2010a, 2012; Burkholder et al., 2008),while raphidophytes feed on bacteria (Jeong et al., 2010b; Jeong,2011). The abundance of heterotrophic bacteria in Masan Bayduring this study was 4.4 � 105 to 1.9 � 107 cells ml�1, close to theabundance that supports the maximum ingestion rates of PTDs andraphidophytes (Seong et al., 2006; Jeong et al., 2010a). However,diatoms are not able to feed on prey and thus grow onlyphotosynthetically. The concentration of NO3 was near the K1/2

for diatoms. Thus, their mixotrophic nature may enable PTDs andraphidophytes to form red tides more frequently than diatoms,

Table 9Half-saturation constants (Ks, mM) for uptake of ammonium (NH4), nitrate (NO3), and p

2005.

Red-tide organisms NH4 NO3

Akashiwo sanguinea (PTD) 1.1 3.8

6.55

Alexandrium minutum (PTD) 1.18

Alexandrium tamarense (PTD) 2.72 3.21

Ceratium furca (PTD) 0.44

0.49

Chattonella antiqua (RAP) 2.2

0.23

2.81

2.8

0.65

Cochlodinium polykrikoides (PTD) 2.6

1.03

2.94

2.1

Eutreptiella gymnastica (EUG)

Euglena gracilis (EUG)

0.12

Heterocapsa triquetra (PTD)

Heterosigma akashiwo (RAP) 2.0–2.3

1.44

2.0–2.5

1.47

Prorocentrum minimum (PTD) 2.4–9.8 1.4–7.8

20.52

Skeletonema costatum (DIA) 0.8–3.6 0.4–0.5

Thalassiosira weissflogii (DIA)

NH4: ammonium, NO3: nitrite plus nitrate, PO4: phosphate.

DIA: diatoms, EUG: euglenophyte, PTD: phototrophic dinoflagellate, RAP: raphidophyte

particularly when nutrient concentrations are too low to supportdiatom growth or maintenance.

Some red-tide species such as Akashiwo sanguinea, Heterocapsa

triquetra, Prorocentrum minimum, P. triestinum, and Eutreptiella

gymnastica formed red tides several times (Supplementary Table 2)and have been revealed to be mixotrophic (Table 8). Thus, weexplore the environmental factors affecting each of these red-tideorganisms separately below.

Akashiwo sanguinea. The concentration of NO3 at the initialstages of these red tides (0.2–3.3 mM) except one was lower thanthe reported value for K1/2 (3.8–6.6 mM) (Table 9), while that ofNH4 (9.9–29.4 mM) was much greater than the reported value for

hosphate (PO4) by red-tide organisms in Masan bay, Korea from June 2004 to May

PO4 Ref.

Eppley et al. (1969)

Thomas and Dodsom (1974)

0.12 Ignatiades et al. (2007)

1.85

2.6

1.85

Leong et al. (2004)

Yamanoto and Tarutani (1999)

Yamamoto and Tarutani (1996)

0.17

0.05

Qasim et al. (1973)

Baek et al. (2008)

1.76

0.25

Nakamura and Watanabe (1983)

Nakamura (1985a)

Nakamura (1985b)

Burson (2009)

Kim et al. (2001)

0.7–2.8 Falkowski (1975)

Chisholm and Stross (1976)

3.1 Doremus (1982)

1.0–1.98 Tomas (1979)

Herndon and Cochlan (2007)

1.39

1.96

Fan et al. (2003)

Hu et al. (2011)

Cembella et al. (1984)

Eppley et al. (1969)

2.8 Lomas and Glibert (2000)

.

H.J. Jeong et al. / Harmful Algae 30S (2013) S75–S88S86

K1/2 (1.1 mM). Thus, Akashiwo sanguinea may acquire nitrogenmostly from NH4. Furthermore, A. sanguinea has been reported tofeed on heterotrophic bacteria (Seong et al., 2006), cyanobacteria(Jeong et al., 2005a), cryptophytes, Heterosigma akashiwo, Pro-

rocentrum donghaiense, P. minimum, P. triestinum, Heterocapsa

triquetra, Scrippsiella trochoidea, Alexandrium tamarense (Jeonget al., 2005b, 2010a), and ciliates (Bockstahler and Coats, 1993b).During the A. sanguinea red tides, heterotrophic bacteria,cryptophytes, H. akashiwo, E. gymnastica, P. triestinum, and C. furca

were abundant. A. sanguinea may acquire phosphorous partiallyfrom heterotrophic bacteria, which have low N:P ratios (3–9) (e.g.Goldman et al., 1987; Mozes et al., 1988), and carbon fromthese algal prey (Jeong et al., 2005b). This evidence suggests thatthe population dynamics of A. sanguinea is likely affected by theconcentration of NH4 and prey availability.

Prorocentrum minimum. Interestingly, this dinoflagellateformed red tides in both December–February and June whenwater temperatures were 6.3–14.3 and 21.2 8C, respectively. Thesequences of SSU, ITS1, 5.8 s, ITS2, and LSU rDNA of the summerstrain were 0.7% (12 of 1646), 0% (0/219), 0% (0/158), 0% (0/191),and 0.1% (1/907), respectively, different from those of the winterstrain (Kim, 2010). However, the morphologies of these twostrains were very similar. Thus, the summer strain is notgenetically identical to the winter strain and their eco-physiologymay be somewhat different. The concentrations of NO3 at theinitial stages of the winter red tides (10.2–19.2 mM) were muchhigher than those during the summer red tides (3.3 mM). Thisdifference may enable these two strains to inhabit differentecological niches. In addition, the winter strain may have anadvantage in dominance over PTDs other than Heterocapsa

triquetra in the winter season.The concentration of NH4 at the initial stages of the red tides

(7.9–19.9 mM) was comparable to or greater than the reportedvalues for K1/2 (2.4–9.8 mM) (Table 9), while the concentrations ofNO3 and PO4 (3.3–19.2 mM and 0.9–1.8 mM, respectively) compa-rable to or slightly lower than the reported values for K1/2 (1.4–20.5 mM and 1.4–2.0 mM, respectively) (Table 9). Thus, theconcentration of NH4 may be high enough to support the growthof Prorocentrum minimum. Just before the P. minimum red tide,cryptophytes had formed a red tide, and P. minimum is known tofeed on cryptophytes (Stoecker et al., 1997). In addition, theabundance of P. minimum had a significant positive correlationwith the abundance of Synechococcus spp. and P. minimum has beenknown to feed on Synechococcus spp. (Jeong et al., 2005a). Thus,cryptophytes and Synechococcus spp. may partially affect thepopulation dynamics of P. minimum.

Heterocapsa triquetra. This dinoflagellate formed red tides inJanuary and March when water temperatures were 5.3–6.9 8C,suggesting that in the colder seasons H. triquetra has an advantagein dominance over PTDs other than Prorocentrum minimum inMasan Bay. The abundance of H. triquetra showed a significantpositive correlation with the abundance of P. minimum. Further-more, just before the red tide dominated by H. triquetra, P.

minimum formed a red tide. H. triquetra is known to feed on P.

minimum (Jeong et al., 2005b); therefore, such feeding maypartially support the formation of red tides.

Ceratium furca. The concentrations of NO3 and PO4 at theinitial stage of the C. furca red tide (0.3 mM and 0.1 mM) wereslightly lower than or comparable to the reported values of K1/2

(0.4–0.5 mM and 0.1–0.2 mM, respectively) (Qasim et al., 1973;Baek et al., 2008). Thus, C. furca may form red tides using NO3 andPO4 as nutrient sources in Masan Bay.

Heterosigma akashiwo. The concentrations of NO3 and PO4 atthe initial stages of these red tides (0.2–105 mM and 0.1–1.9 mM,respectively) fell between the reported values of K1/2 (1.5–2.5 mM and 1.0–2.0 mM, respectively) (Table 9). Thus, this

raphidophyte may be able to form red tides in high concentra-tions of NO3 and PO4. During the study year, the abundance of H.

akashiwo showed a significant positive correlation with totalbacteria. H. akashiwo are known to feed on bacteria (Seong et al.,2006; Jeong, 2011). The percentage of heterotrophic bacteriacarbon acquired daily by H. akashiwo to use as body carbon was12.5% (Seong et al., 2006). Therefore, when nutrient concentra-tions were low, H. akashiwo may have formed red tides byfeeding on bacteria. From June to September, Akashiwo

sanguinea, Ceratium furca, and Prorocentrum triestinum wereabundant. These dinoflagellates are known to feed on H.

akashiwo (Jeong et al., 2005b). Therefore, high abundances ofH. akashiwo may enable PTDs to form red tides even whennutrient conditions were not favorable to photosynthesis.

5. Conclusions

The present study demonstrated that: (1) red tide events inMasan Bay from June 2004 to May 2005 occurred 36 times for a totalof 195 days and (2) daily sampling is necessary to detect all red-tideevents because some red tides persisted only one to a few days. (3)Prorocentrum minimum and Eutreptiella gymnastica caused red tidesin both summer and winter. Furthermore, Skeletonema costatum

caused red tides over a wide range of water temperatures. However,Akashiwo sanguinea, Ceratium furca, Cochlodinium polykrikoides,Dinophysis acuminata, P. triestinum, and Thalassiosira decipiens

formed red tides only in summer, while Heterocapsa triquetra

formed red tides only in winter. Thus, water temperature is likely toaffect the causative species of red tides in Masan Bay. (4) Some red-tide species formed red tides when inorganic nutrient concentra-tions were lower than the reported values of K1/2 and had asignificant positive correlation with bacteria and other algae. Theirmixotrophic nature may enable these species to grow and form redtides (Jeong et al., 2005b, 2010a).

Acknowledgements

We thank Dr. Ted Smayda for his valuable advice and Dr. JaeYeon Park for technical support. This paper was supported by theNational Research Foundation/MSICTFP (NRF-C1ABA001-2010-0020702), Mid-career Researcher Program (2012-R1A2A201-010987) and Ecological Disturbance Research Program andLong-term change of structure and function in marine ecosystemsof Korea program, Korea Institute of Marine Science & TechnologyPromotion/Ministry of Oceans and Fisheries award to HJ Jeong.[TS]

Appendix A. Supplementary data

Supplementary data associated with this article can be found, inthe online version, at http://dx.doi.org/10.1016/j.hal.2013.10.008.

References

Alonso-Rodriguez, R., Ochoa, J.L., 2004. Hydrology of winter-spring ‘‘red-tides’’ inBahia de Mazatlan, Sinaloa, Mexico. Harmful Algae 3, 163–171.

Anderson, D.M., Glibert, P.M., Burkholder, J.M., 2002. Harmful algal blooms andeutrophication: nutrient sources, composition, and consequences. Estuar.Coast. 25, 704–726.

Anderson, D.M., Alpermann, T.J., Cembella, A.D., Collos, Y., Masseret, E., Montresor,M., 2012. The globally distributed genus Alexandrium: multifaceted roles inmarine ecosystems and impacts on human health. Harmful Algae 14, 10–35.

APHA (American Public Health Association), 1995. Standard Methods for theexamination of Water and Wastewater, 19th ed. APHA, Washington.

Baek, S.H., Shimode, S., Han, M.S., Kikuchi, T., 2008. Growth of dinoflagellates,Ceratium furca and Ceratium fusus in Sagami Bay, Japan: the role of nutrients.Harmful Algae 7, 729–739.

Banse, K., 1982. Cell volumers maximal growth rates of unicellular algae andciliates, and the role of ciliates in the marine pelagial. Limnol. Oceanogr. 27,1059–1071.

H.J. Jeong et al. / Harmful Algae 30S (2013) S75–S88 S87

Berge, T., Hansen, P.J., Moestrup, Ø., 2008. Prey size spectrum and bioenergetics ofthe mixotrophic dinoflagellate Karlodinium armiger. Aquat. Microb. Ecol. 50,289–299.

Bockstahler, K.R., Coats, D.W., 1993a. Spatial and temporal aspects of mixotrophy inChesapeake Bay dinoflagellates. J. Eukaryot. Microbiol. 40, 49–60.

Bockstahler, K.R., Coats, D.W., 1993b. Grazing of the mixotrophic dinoflagellateGymnodinium sanguineum on ciliate population of Chesapeake Bay. Mar. Biol.116, 447–487.

Burkholder, J.M., Glibert, P.M., Skelton, H.M., 2008. Mixotrophy, a major mode ofnutrition for harmful algal species in eutrophic waters. Harmful Algae 8, 77–93.

Burson, A.M., 2009. The Role of Nitrogenous Nutrients in the Occurrence of theHarmful Dinoflagellate Blooms Caused by Cochlodinium polykrikoides in LongIsland Estuaries (NY, USA). Degree of Master of Science, Stony Brook University, ,pp. 37.

Cembella, A.D., Antia, N.J., Harrison, P.J., 1984. The utilization of inorganic andorganic phosphorus compounds as nutrients by eukaryotic microalgae: amultidisciplinary perspective: part I. CRC Crit. Rev. Microbiol. 10, 317–391.

Chisholm, S.W., Stross, R.G., 1976. Phosphate uptake kinetics in Euglena gracilis(Euglenophyceae) grown on light/dark cycles. I. Synchronized batch cultures. J.Phycol. 12, 210–217.

Conover, D., 1980. Practical Nonparametric Statistics, 2nd ed. John Wiley and Sons,New York, NY 493 pp.

Doremus, C., 1982. Geochemical control of dinitrogen fixation in the open ocean.Biol. Oceanogr. 1, 429–436.

ECOHAB, 1995. The Ecology and Oceanography of Harmful Algal Blooms. ANational Research Agenda. Woods Hole Oceanographic Institute, Woods Hole,MA, pp. 1–66.

Eppley, R.W., Rogers, J.N., McCarthy, J.J., 1969. Half-saturation constants for uptakeof nitrate and ammonitum by marine phytoplankton. Limnol. Oceanogr. 14,912–920.

Eppley, R.W., Harrison, W.G., 1975. Physiological ecology of Gonyaulax polyedrum, ared tide water dinoflagellate of southern California. In: Locicero, V.R. (Ed.),Proceedings First International Conference on Toxic Dinoflagellate Blooms,Massachusetts Science and Technology Foundation, Wakefield, MA, pp. 11–22.

Falkowski, P.G., 1975. Nitrate uptake in marine phytoplankton: comparison of half-saturation constants from seven species. Limnol. Oceanogr. 20, 412–417.

Fan, C., Glibert, P.M., Burkholder, J.M., 2003. Characterization of the affinity fornitrogen, uptake kinetics, and environmental relationships for Prorocentrumminimum in natural blooms and laboratory cultures. Harmful Algae 2, 283–299.

Fu, F., Tatters, A.O., Hutchins, D.A., 2012. Global change and the future of harmfulalgal blooms in the ocean. Mar. Ecol. Prog. Ser. 470, 207–233.

Glibert, P.M., Anderson, D.M., Gentein, P., Graneli, E., Sellner, K.G., 2005. The global,complex phenomena of harmful algal blooms. Oceanography 18, 136–147.

Glibert, P.M., Burkholder, J.M., Kana, T.M., Alexander, J., Skelton, H., Shilling, C., 2009.Grazing by Karenia brevis on Synechococcus enhances its growth rate and mayhelp to sustain blooms. Aquat. Microb. Ecol. 55, 17–30.

Goldman, J.C., Caron, D.A., Dennett, M.R., 1987. Regulation of gross efficiency andammonium regeneration in bacteria by substrate C:N ratio. Limnol. Oceanogr.32, 1239–1252.

Graneli, E., Anderson, D.M., Carlsson, P., Maestrini, S.Y., 1997. Light and dark carbonuptake by Dinophysis species in comparison to other photosynthetic andheterotrophic dinoflagellates. Aquat. Microb. Ecol. 13, 177–186.

Hansen, P.J., 2011. The role of photosynthesis and food uptake for the growth ofmarine mixotrophic dinoflagellates. J. Eukaryot. Microbiol. 58, 203–214.

Herndon, J., Cochlan, P., 2007. Nitrogen utilization by the raphidophyte Heterosigmaakashiwo: growth and uptake kinetics in laboratory cultures. Harmful Algae 6,260–270.

Holmes, R.W., Williams, P.M., Eppley, R.W., 1967. Red water in La Jolla Bay, 1964–1966. Limnol. Oceanogr. 12, 503–512.

Horner, R.A., Garrison, D.L., Plumely, F.G., 1997. Harmful algal blooms and red tideproblems on the U.S. west coast. Limnol. Oceanogr. 42, 1076–1088.

Hu, H., Zhang, J., Chen, W., 2011. Competition of bloom-forming marine phyto-plankton at low nutrient concentrations. J. Environ. Sci. 23, 654–663.

Ignatiades, L., Gotsis-Skretas, O., Metaxatos, A., 2007. Field and culture studies onthe ecophysiology of the toxic dinoflagellate Alexandrium minutum (Halim)present in Greek coastal waters. Harmful Algae 6, 153–165.

Imai, I., Sunahara, T., Nishikawa, T., Hori, Y., Kondo, R., Hiroishi, S., 2001. Fluctuationsof the red tide flagellates Chattonella spp. (Raphidophyceae) and thealgicidal bacterium Cytophaga sp. in the Seto Inland Sea, Japan. Mar. Biol.138, 1043–1049.

Jacobson, D.M., Anderson, D.M., 1986. Thecate heterotrophic dinoflagellates: feed-ing behavior and mechanisms. J. Phycol. 22, 249–258.

Jeong, H.J., 1995. The Interactions between Microzooplanktonic Grazers and Dino-flagellates Causing Red Tides in the Open Coastal Waters off Southern Califor-nia. Dissertation, Scripps Institution of Oceanography, University of California,San Diego 139 pp. (Available on microfilm from University of Michigan,Accession Number 223882).

Jeong, H.J., 2011. Mixotrophy in red-tide algae raphidophytes. J. Eukaryot. Micro-biol. 58, 215–222.

Jeong, H.J., Lee, C.W., Yih, W.H., Kim, J.S., 1997. Fragilidium cf. mexicanum, a thecatemixotrophic dinoflagellate, which is prey for and a predator on co-occurringthecate heterotrophic dinoflagellate Protoperidinium cf. divergens. Mar. Ecol.Prog. Ser. 151, 299–305.

Jeong, H.J., Shim, J.H., Lee, C.W., Kim, J.S., Kohm, S.M., 1999. The feeding by thethecate mixotrophic dinoflagellate Fragilidium cf. mexicanum on red tide andtoxic dinoflagellate. Mar. Ecol. Prog. Ser. 176, 263–277.

Jeong, H.J., Kim, J.S., Yoo, Y.D., Kim, S.T., Kim, T.H., Park, M.G., Lee, C.H., Seong, K.A.,Kang, N.S., Shim, J.H., 2003. Feeding by the heterotrophic dinoflagellate Oxyrrhismarina on the red-tide raphidophyte Heterosigma akashiwo: a potential biolog-ical method to control red tides using mass-cultured grazers. J. Eukaryot.Microbiol. 50, 274–282.

Jeong, H.J., Yoo, Y.D., Kim, J.S., Kim, T.H., Kim, J.H., Kang, N.S., Yih, W.H., 2004.Mixotrophy in the phototrophic harmful alga Cochlodinium polykrikoides (Dino-phycean): prey species, the effects of prey concentration and grazing impact. J.Eukaryot. Microbiol. 51, 563–569.

Jeong, H.J., Park, J.Y., Nho, J.H., Park, M.O., Ha, J.H., Seong, K.A., Jeng, C., Seong, C.N.,Lee, K.Y., Yih, W.H., 2005a. Feeding by red-tide dinoflagellates on the cyano-bacterium Synechococcus. Aquat. Microb. Ecol. 41, 131–143.

Jeong, H.J., Yoo, Y.D., Park, J.Y., Song, J.Y., Kim, S.T., Lee, S.H., Kim, K.Y., Yih, W.H.,2005b. Feeding by the phototrophic red-tide dinoflagellates: five species newlyrevealed and six species previously known to be mixotrophic. Aquat. Microb.Ecol. 40, 133–155.

Jeong, H.J., Yoo, Y.D., Seong, K.A., Kim, J.H., Park, J.Y., Kim, S.H., Lee, S.H., Ha, J.H., Yih,W.H., 2005c. Feeding by the mixotrophic dinoflagellate Gonyaulax polygramma:mechanisms, prey species, the effects of prey concentration, and grazingimpact. Aquat. Microb. Ecol. 38, 249–257.

Jeong, H.J., Kim, J.S., Yoo, Y.D., Kim, S.T., Song, J.Y., Kim, T.H., Seong, K.A., Kang, N.S.,Kim, M.S., Kim, J.H., Kim, S., Ryu, J., Lee, H.M., Yih, W.H., 2008. Control of theharmful alga Cochlodinium polykrikoides by the naked ciliate Strombidinopsisjeokjo in mesocosm enclosures. Harmful Algae 7, 368–377.

Jeong, H.J., Yoo, Y.D., Kim, J.S., Seong, K.A., Kang, N.S., Kim, T.H., 2010a. Growth,feeding, and ecological roles of the mixotrophic and heterotrophic dinoflagel-lates in marine planktonic food webs. Ocean Sci. J. 45, 65–91.

Jeong, H.J., Seong, K.A., Kang, N.S., Yoo, Y.D., Nam, S.W., Park, J.Y., Shin, W.G., Glibert,P.M., Johns, D., 2010b. Feeding by raphidophytes on the cyanobacteriumSynechococcus. Aquat. Microb. Ecol. 58, 181–195.

Jeong, H.J., Yoo, Y.D., Kang, N.S., Rho, J.R., Seong, K.A., Park, J.W., Nam, G.S., Yih, W.H.,2010c. Ecology of Gymnodinium aureolum. I. Feeding in western Korean waters.Aquat. Microb. Ecol. 59, 239–255.

Jeong, H.J., Kim, T.H., Yoo, Y.D., Yoon, E.Y., Kim, J.S., Seong, K.A., Kim, K.Y., Park, J.Y.,2011. Grazing impact of heterotrophic dinoflagellates and ciliates on commonred-tide euglenophyte Eutreptiella gymnastica in Masan Bay, Korea. HarmfulAlgae 10, 576–588.

Jeong, H.J., Yoo, Y.D., Kang, N.S., Lim, A.K., Seong, K.A., Lee, S.Y., Lee, M.J., Lee, K.H.,Kim, H.S., Shin, W., Nam, S.W., Yih, W., Lee, K., 2012. Heterotrophic feeding as anewly identified survival strategy of the dinoflagellate Symbiodinium. Proc. Natl.Acad. Sci. U.S.A. 109, 12604–12609.

Jeong, H.J., Yoo, Y.D., Lim, A.S., Kim, T.W., Lee, K., Kang, C.K., 2013. Raphidophyte redtides in Korean waters. Harmful Algae (in this volume).

Kang, N.S., Jeong, H.J., Yoo, Y.D., Yoon, E.Y., Lee, K.H., Lee, K., Kim, K.H., 2011.Mixotrophy in the newly described phototrophic dinoflagellate Woloszynskiacincta from western Korean waters: feeding mechanism, prey species, and effectof prey concentration. J. Eukaryot. Microbiol. 58, 152–170.

Kang, N.S., Lee, K.H., Jeong, H.J., Yoo, Y.D., Seong, K.A., Potvin, E., Hwang, Y.J., Yoon,E.Y., 2013. Red tides in Shiwha Bay, western Korea: a huge dike and tidal powerplant established in a semi-closed embayment system. Harmful Algae (in thisvolume).

Kim, H., Lee, C., Lee, S., Kim, H., Park, C., 2001. Physico-chemical factors on thegrowth of Cochlodinium polykrikoides and nutrient utilization. J. Korean Fish.Soc. 34, 445–456.

Kim, J.S., Jeong, H.J., Yoo, Y.D., Kang, N.S., Kim, S.K., Song, J.Y., Lee, M.J., Kim, S.T., Kang,J.H., Seong, K.A., Yih, W.H., 2013. Red tides in Masan Bay, Korea in 2004–2005:III. Daily variation in the abundance of mesozooplankton and their grazingimpact on red tide organisms. Harmful Algae (in this volume).

Kim, T.H., 2010. A Study of the Correlations between a HAB Species, Prorocentrumminimum (Pavillard) Schiller and Environmental Factors in Masan Bay, Korea.Kunsan National University 134 pp. (Ph.D. Thesis).

Kwak, S.K., Choi, M.Y., Cho, K.J., 2001. Distribution and occurrence frequency of red-tide causing flagellates in Masan-Jinhae Bay. Algae 16, 315–323.

Lee, C.K., Park, T.G., Park, Y.T., Lim, W.A., 2013. Monitoring and trends in red-tideevents in Korea with emphasis on Cochlodinium polykrikoides. Harmful Algae (inthis volume).

Lee, S.H., 2006. Feeding by Mixotrophic Red-Tide Algae on Photosynthetic Picoeu-karyotes. Degree of Master of Science, Seoul National University 55 pp.

Leong, S.C.Y., Murata, A., Nagashima, Y., Taguchi, S., 2004. Variability in toxicity ofthe dinoflagellate Alexandrium tamarense in response to different nitrogensources and concentrations. Toxicon 43, 407–415.

Li, A., Stoecker, D.K., Coats, D.W., 2000. Mixotrophy in Gyrodinium galatheanum(dinophyceae): grazing responses to light intensity and inorganic nutrients. J.Phycol. 36, 33–45.

Lomas, M.W., Glibert, P.M., 2000. Comparison of nitrate uptake, storage, andreduction in marine diatoms and flagellates. J. Phycol. 36, 903–913.

Mason, P.L., Litaker, R.W., Jeong, H.J., Ha, J.H., Reece, K.S., Vogelbein, W.K., Stokes,N.A., Park, J.Y., Steidinger, K.A., Vandersea, M.W., Kibler, S., Tester, P.A., Vogel-bein, W.K., 2007. Description of a new genus of Pfiesteria-like dinoflagellate,Luciella gen. nov. (dinophyceae), including two new species: Luciella masanensissp. nov. and Luciella atlantis sp. nov. J. Phycol. 43, 799–810.

Menden-Deuer, S., Lessard, E., 2000. Carbon to volume relationships for dinofla-gellates, diatoms, and other protist plankton. Limnol. Oceanogr. 45, 569–579.

Menden-Deuer, S., Fredrickson, K., 2010. Structure-dependent, protistan grazingand its implication for the formation, maintenance and decline of planktonpatches. Mar. Ecol. Prog. Ser. 420, 57–71.

H.J. Jeong et al. / Harmful Algae 30S (2013) S75–S88S88

Mozes, N., Leonard, A.J., Rouxhet, P.G., 1988. On the relations between the elementalsurface composition of yeasts and bacteria and their charge and hydrophobic-ity. Biochim. Biophys. Acta 945, 324–334.

Nakamura, Y., 1985a. Alkaline phosphatase activity of Chattonella antiqua andHeterosigma akashiwo. Res. Rep. Natl. Inst. Environ. Stud. 80, 67–72.

Nakamura, Y., 1985b. Kinetics of nitrogen- or phosphorus-limited growth andeffects of growth conditions on nutrient uptake in Chattonella antiqua. J.Oceanogr. Soc. Jpn. 41, 381–387.

Nakamura, Y., Watanabe, M.M., 1983. Nitrate and phosphate uptake kineticsof Chattonella antiqua grown in light/dark cycles. J. Oceanogr. Soc. Jpn. 39,167–170.

National Fisheries Research and Development Institute (NFRDI), 1996. Red Tides inKorea. National Fisheries Research and Development Institution, Korea.

National Fisheries Research and Development Institute (NFRDI), 2012. Data on RedTides.. http://www.nfrdi.re.kr/redtideinfo (written in Korean).

Nishikawa, T., Hori, Y., Nagai, S., Miyahara, K., Nakamura, Y., Harada, K., Tanda, M.,Mannabe, T., Tada, K., 2010. Nutrient and phytoplankton dynamics in Harima-Nada, eastern Seto Inland Sea, Japan during a 35-year period from 1973 to 2007.Estuar. Coast. 33, 417–427.

Park, J.Y., Jeong, H.J., Yoo, Y.D., Yoon, E.Y., 2013a. Mixotrophic dinoflagellate redtides in Korean waters: distribution and ecophysiology. Harmful Algae (in thisvolume).

Park, M.G., Kim, S., Kim, H.S., Myung, G., Kang, Y.G., Yih, W., 2006. First successfulculture of the marine dinoflagellate Dinophysis acuminata. Aquat. Microb. Ecol.45, 101–106.

Park, T.G., Lim, W.A., Park, Y.T., Lee, C.K., Jeong, H.J., 2013b. Economic impact,management and mitigation of red tides in Korea. Harmful Algae (in thisvolume).

Parrow, M.W., Burkholder, J.M., 2003. Reproduction and sexuality in Pfiesteriashumwayae (Dinophyceae). J. Phycol. 39, 697–711.

Porter, K.G., Feig, Y.S., 1980. The use of DAPI for identifying and counting aquaticmicroflora. Limnol. Oceanogr. 25, 943–948.

Qasim, S.Z., Bhattathiri, P.M.A., Devassy, V.P., 1973. Growth kinetics and nutrientrequirements of two tropical marine phytoplanktoners. Mar. Biol. 21, 299–304.

Seong, K.A., Jeong, H.J., Kim, S., Kim, G.H., Kang, J.H., 2006. Bacterivory by co-occurring red-tide algae, heterotrophic nanoflagellates, and ciliates on marinebacteria. Mar. Ecol. Prog. Ser. 322, 85–97.

Seong, K.A., Jeong, H.J., 2011. Interactions between the pathogenic bacterium Vibrioparahaemolyticus and red-tide dinoflagellates. Ocean Sci. J. 46 (2) 105–115.

Skovgaard, A., 2000. A phagotrophically derivable growth factor in the plastidicdinoflagellate Gyrodinium resplendens (Dinophyceae). J. Phycol. 36, 1069–1078.

Smalley, G.W., Coats, D.W., Adam, E.J., 1999. A new method using fluorescentmicrospheres to determine grazing on ciliates by the mixotrophic dinoflagellateCeratium furca. Aquat. Microb. Ecol. 17, 167–179.

Smayda, T.J., 1990. In: Graneli, E., Sundstrom, B., Edler, L., Anderson, D.M. (Eds.),Toxic Marine Phytoplankton. Elsevier Publishers B. V., Amsterdam, pp. 29–40.

Smayda, T.J., 1997. Harmful algal blooms: their ecophysiology and general rele-vance to phytoplankton blooms in the sea. Limnol. Oceanogr. 42, 1137–1153.

Sordo, I., Barton, E.D., Cotos, J.M., Pazos, Y., 2001. An inshore poleward current in theNW of the Iberian Peninsula detected from satellite images, and its relation withG. catenatum and D. acuminata blooms in the Galican Rias. Estuar. Coast. ShelfSci. 53, 787–799.

Stoecker, D.K., 1999. Mixotrophy among dinoflagellates. J. Eukaryot. Microbiol. 46,397–401.

Stoecker, D.K., Li, A., Coats, D.W., Gustafson, D.E., Nannen, M.K., 1997. Mixotrophy inthe dinoflagellate Prorocentrum minimum. Mar. Ecol. Prog. Ser. 152, 1–12.

Thomas, W.H., Dodsom, A.N., 1974. Effect of interactions between temperature andnitrate supply on the cell-division rates of two marine phytoflagellates. Mar.Biol. 24, 213–217.

Tomas, C.R., 1979. Olisthodiscus leteus (Chrysophyceae). III. Uptake and utilization ofnitrogen and phosphorus. J. Phycol. 15, 5–12.

Uchida, T., Toda, S., Matsuyama, Y., Yamaguchi, M., Kotani, Y., Honjo, T., 1999.Interactions between the red tide dinoflagellate Heterocapsa circularisquamaand Gymnodinium mikomotoi in laboratory culture. J. Exp. Mar. Biol. Ecol. 241,285–299.

Varela, M., Fernandez, E., Serret, P., 2002. Size-fractionated phytoplankton biomassand primary production in the Gerlache and south Bransfield Straits (AntarcticPeninsula) in Austral summer 1995–1996. Deep Sea Res. II 49, 749–768.

Welch, P.S., 1948. Limnological Methods. The Blaikston Co., Philadelphia, pp. 381.Yamamoto, T., Tarutani, K., 1996. Growth and phosphate uptake kinetics of Alex-

andrium tamarense from Mikawa ay, Japan. In: Yasumoto, T., Oshima, Y., Fukuyo,Y. (Eds.), Harmful and Toxic Algal Blooms. IOC/UNESCO, Paris, pp. 293–296.

Yamanoto, T., Tarutani, K., 1999. Growth and phosphate uptake kinetics of the toxicdinoflagellate Alexandrium tamarense from Hiroshima Bay in the Seto InlandSea, Japan. Phycol. Res. 47, 27–32.

Yih, W., Kim, H.S., Myung, G., Park, J.W., Yoo, Y.D., Jeong, H.J., 2013. The red-tideciliate Mesodinium rubrum in the Korean coastal waters. Harmful Algae (in thisvolume).

Yin, K., 2002. Monsoonal influence on seasonal variations in nutrients and phyto-plankton biomass in coastal waters of Hong Kong in the vicinity of the PearlRiver estuary. Mar. Ecol. Prog. Ser. 245, 111–122.

Yoo, K.I., 1991. Population dynamics of dinoflagellate community in Masan Baywith a note on the impact of environmental parameters. Mar. Pollut. Bull. 23,185–218.

Yoo, Y.D., Jeong, H.J., Kim, M.S., Kang, N.S., Song, J.Y., Shin, W.G., Kim, K.Y., Lee, K.T.,2009. Feeding by phototrophic red-tide dinoflagellates on the ubiquitousmarine diatom Skeletonema costatum. J. Eukaryot. Microbiol. 56, 413–420.

Yoo, Y.D., Jeong, H.J., Kang, N.S., Song, J.Y., Kim, K.Y., Lee, K.T., Kim, J.H., 2010. Feedingby the newly described mixotrophic dinoflagellate Paragymnodinium shi-whaense: feeding mechanism, prey species, and effect of prey concentration.J. Eukaryot. Microbiol. 57, 145–158.

Yoo, Y.D., Jeong, H.J., Kim, J.S., Kim, T.H., Kim, J.H., Seong, K.A., Lee, S.H., Kang, N.S., Park,J.W.,Yih,W.H.,2013.Redtides inMasanBay,Koreain2004–2005:II.Dailyvariationin the abundance of heterotrophic nanoflagellates and dinoflagellates and ciliatesand their grazing impact on red tide organisms. Harmful Algae (in this volume).

Zar, J.H., 1999. Biostatistical Analysis, 4th ed. Prentice Hall, Upper Saddle River, NJ.