Harmful Algae 30S (2013) S89–S101

Red tides in Masan Bay, Korea in 2004–2005: II. Daily variations inthe abundance of heterotrophic protists and their grazing impacton red-tide organisms

Yeong Du Yoo a, Hae Jin Jeong a,*, Jae Seong Kim b, Tae Hoon Kim c, Jong Hyeok Kim d,Kyeong Ah Seong d, Seung Hyun Lee a, Nam Seon Kang a, Jong Woo Park d, Jaeyeon Park e,Eun Young Yoon e, Won Ho Yih d

a School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University, Seoul 151-747, Republic of Koreab Water and Eco-Bio Corporation, Kunsan National University, Kunsan 573-701, Republic of Koreac IGD Corporation, 499, Gunja-dong, Siheung-si, Gyeonggi-do, 429-823, Republic of Koread Department of Oceanography, College of Ocean Science and Technology, Kunsan National University, Kunsan 573-701, Republic of Koreae Advanced Institutes of Convergence Technology, Suwon, Gyeonggi-do 443-270, Republic of Korea

A R T I C L E I N F O

Keywords:

Ciliate

Food web

Grazing

Harmful algal bloom

Heterotrophic dinoflagellate

Red tide

A B S T R A C T

To investigate the role of heterotrophic protists in the dynamics of red tides in Masan Bay, Korea, we

measured the abundance of heterotrophic dinoflagellates, ciliates, and heterotrophic nanoflagellates in

daily samples collected from June 2004 to May 2005. The abundance of heterotrophic dinoflagellates,

tintinnid ciliates, naked ciliates, and heterotrophic nanoflagellates were high when red tides occurred,

with maximum biomass of 1916, 1263, 1013, and 141 ng C ml�1, respectively. The HTDs Gyrodinium

dominans/Gyrodinium moestrupii, Gyrodinium glaucum, Protoperidinium bipes, and Pfiesteria-like

dinoflagellates (PLDs) as well as naked ciliates (�50 mm) were present nearly all year and their

maximum biomass was 235, 48, 298, 1020, and 1013 ng C ml�1, respectively. PLDs were the most

abundant taxa during red tides dominated by Akashiwo sanguinea, Heterocapsa rotundata, summer

populations of Prorocentrum minimum, Heterosigma akashiwo, Eutreptiella gymnastica, and cryptophytes,

while G. dominans/G. moestrupii were most abundant during red tides dominated by Ceratium furca and

Dinophysis acuminata. Naked ciliates were most abundant during red tides dominated by Cochlodinium

polykrikoides, Prorocentrum triestinum, and winter populations of P. minimum. The maximum calculated

grazing coefficients for each dominant heterotrophic protistan grazer on their respective co-occurring

red-tide organisms in Masan Bay ranged from 0.0 to 6.8 h�1. The results of the present study suggest that

populations of certain heterotrophic protistan grazers may have considerable potential grazing impact

on populations of red-tide organisms in Masan Bay.

� 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 occur in the coastal and offshore waters of manycountries and in oceanic waters (Jeong, 1995; Horner et al., 1997;Imai et al., 2001; Sordo et al., 2001; Anderson et al., 2002; Alonso-Rodriguez and Ochoa, 2004; Seong et al., 2006; Jeong et al.,2013a,b; Kang et al., 2013; Lee et al., 2013; J.Y. Park et al., 2013).They can alter the balance of food webs and cause large-scalemortalities of fish and shellfish (Smayda, 1990; Glibert et al., 2005;Anderson et al., 2012; Fu et al., 2012). Studies of red-tideformation and persistence suggest that grazing pressure mayplay an important role in bloom dynamics (Watras et al., 1985;

* Corresponding author.

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.2013.10.009

Turner, 2006; Jeong et al., 2011a; Kim et al., 2013). In particular,grazing by heterotrophic protists is believed to contribute to thedecline of red tides (Holmes et al., 1967; Eppley and Harrison,1975; Jeong, 1995, 1999; Kamiyama et al., 2000; Stoecker andGustafson, 2002; Johnson et al., 2003; Kim and Jeong, 2004;Tillmann, 2004).

Heterotrophic protists such as heterotrophic dinoflagellates(HTDs) and ciliates are known to be effective grazers on red-tideorganisms (Jeong and Latz, 1994; Hansen et al., 1997; Jeong et al.,1999, 2001a, 2003b, 2007, 2008, 2010, 2011b; Tillmann, 2004; Yooet al., 2010, 2013; T.G. Park et al., 2013). These heterotrophicprotists usually divide 1–3 times each day after feeding on optimalor sub-optimal red-tide organisms and thus are often abundantduring red tides (e.g. Jeong et al., 2010). They can have considerablegrazing impact on red-tide organisms, controlling their popula-tions (Lessard and Swift, 1985; Calbet et al., 2003; Jeong et al.,

Y.D. Yoo et al. / Harmful Algae 30S (2013) S89–S101S90

2003a, 2004, 2005; Irigoien et al., 2005; Yoo et al., 2010). Tounderstand their roles, the following basic issues should beinvestigated: (1) identify the potential predators of dominant red-tide organisms through correlations between red-tide organismsand dominant heterotrophic protists, (2) determine whether thepredators are able to feed on the red-tide organisms, and (3)estimate the grazing impact of populations of predators onpopulations of red-tide organisms.

To understand the roles of heterotrophic protistan grazers onthe dynamics of red-tide organisms in Masan Bay, Korea, wemeasured the abundance of HTDs, tintinnid ciliates, naked ciliates,and heterotrophic nanoflagellates (HNFs) on a daily basis for oneyear and correlations between the biomass of heterotrophicprotistan grazers and red-tide organisms. In addition, based ondata obtained from the literature and our experiments in thelaboratory, we identified the predators of each red-tide species andestimated their grazing impacts on populations of red-tideorganisms. The results of the present study provide a basis forunderstanding the roles of heterotrophic protistan grazers in red-tide dynamics in eutrophied bays.

2. Materials and methods

2.1. Abundance in Masan Bay, Korea

Masan Bay is located in southeast Korea (Jeong et al., 2013a).The bay is oval-shaped (5 km long, 2 km wide, 1 km mouth). Alarge city, Changwon, surrounds the bay and three streams enterthe bay.

Water samples were taken from the surface at a pier (StationSNUMS) every day at 10:00 from June 2004 to May 2005. Waterdepth at the sampling station (SNUMS) in 2004–2005 was 1.2–2.4 m, depending on the tide whose range was �1.2 m. The water ismixed year-round except in summer.

Plankton samples for counting were poured into 500-mlpolyethylene bottles and preserved with acidic Lugol’s solutionfor heterotrophic protists, Bouin solution for ciliates, andglutaraldehyde for heterotrophic nanoflagellates and bacteria. Inaddition, dominant species were single celled isolated and grownin clonal culture for morphological and DNA sequencing identifi-cation. To determine the abundance of HTDs and ciliates, samplespreserved with acidic Lugol’s solution were concentrated by 1/5–1/10 using the settling and siphoning method (Welch, 1948). Afterthorough mixing, all or a minimum of 100 cells of each protistspecies in 1–10 1-ml Sedgwick–Rafter counting chambers (SRCs)were counted under an epifluorescent microscope.

To determine the abundance of HNFs, aliquots of the watersamples were poured into 100-ml polyethylene bottles andpreserved with glutaraldehyde (final concentration, 1%, v/v). Three1–5-ml fixed aliquots were stained with 40,60-diamidino-2-phenylindole (DAPI; final concentration, 1 mM) and then filteredonto 0.2 mm-pore-sized polycarbonate (PC) black membranefilters. HNFs exhibiting blue fluorescence were numerated underan epifluorescent microscope with ultraviolet light excitation.HNFs were distinguishable from phototrophic nanoflagellates(PNFs), which exhibit orange autofluorescence with blue lightexcitation (Porter and Feig, 1980).

We measured the carbon content for each species of manyheterotrophic protist species cultured in our laboratory using CHNanalyzer. For non-culturable species or taxa, the length and widthof cells preserved in 5% acid Lugol’s solution were measured usinga light microscope and then cell volume was calculated usinggeometry. The carbon content for each species of heterotrophicprotist species was calculated from the cell volume according toMenden-Deuer and Lessard (2000). Water temperatures, salinities,pH, and dissolved oxygen (DO) were measured using a Handylab

pH 11 (Schott Instruments, Mainz, Germany) and Oxi 197i (WTWGmbH, Weilheim, Germany), respectively. Chlorophyll-a wasmeasured as in APHA (1995).

Data on the abundances of phototrophic plankton andheterotrophic bacteria were also obtained from Jeong et al.(2013a).

The correlation coefficients between heterotrophic protists andphysical, chemical, and biological properties were calculated usingthe Pearson’s correlation (Conover, 1980; Zar, 1999).

2.2. Grazing impact

Using certain assumptions, we estimated grazing coefficientsattributable to a dominant heterotrophic protist feeding on a co-occurring red-tide organism by combining field data on theabundance of the dominant heterotrophic protist and red-tideorganism with ingestion rates of the protistan grazer on the red-tide prey obtained from literature. Stoeckeria algicida, Pfiesteria

piscicida, and other similar heterotrophic dinoflagellates (so-calledPfiesteria-like dinoflagellates; PLDs) could not be distinguishedfrom one another under a light microscope because they are smalland morphologically very similar. Therefore, we estimated grazingcoefficients attributable to PLDs on co-occurring red-tide organ-isms assuming that these PLDs were S. algicida, or alternatively,that they were P. piscicida. In addition, we used data for theingestion rates of Strobilidium sp. on Eutreptiella gymnastica fornaked ciliate grazers (�50 mm; Jeong et al., 2011a) and data forStrombidinopsis sp. on red-tide organisms for naked ciliate grazers(>50 mm; Jeong et al., 1999, 2011a).

The grazing coefficient g (h�1) was calculated as:

g ¼ CR � GC (1)

where CR is the clearance rate (ml predator�1 h�1) for a predator ofa red-tide organism at a given prey concentration and GC is thepredator concentration (cells ml�1). CR values were calculated as

CR ¼ IR

X(2)

where IR is the ingestion rate (cells eaten predator�1 h�1) of thepredator on the prey and X is the prey concentration (cells ml�1).CR values were corrected using Q10 = 2.8 (Hansen et al., 1997)because the in situ water temperatures and the temperature usedin the laboratory for this experiment (20 8C) were sometimesdifferent.

3. Results

3.1. Physical and chemical properties of Masan Bay

From June 1, 2004 to May 31, 2005, the water temperature atStation SNUMS was 4.2–28.6 8C and the salinity was 4.1–33.3(Fig. 1A and B). The chlorophyll-a (chl-a) concentration was0.02–514.7 mg m�3 (Fig. 1C). Other physical (precipitation) andchemical (pH, DO, etc.) properties are reported in Jeong et al.(2013a).

3.2. Abundance and biomass of major heterotrophic protistan groups

The abundance (biomass) of total HTDs during the study periodwas 0–10,289 cells ml�1 (0–1916 ng C ml�1) (Fig. 1D; Table 1);they were abundant in June–September 2004 and February–April2005. In addition, the abundance (biomass) of tintinnid ciliates(TCs) was 0–216 cells ml�1 (0–1263 ng C ml�1) (Fig. 1E andTable 1); they were abundant in June–September 2004 andMarch–April 2005. The biomass of naked ciliates (NCs) was 0–1113 cells ml�1 (0–1013 ng C ml�1) (Fig. 1F and Table 1); they

Fig. 1. Physical and chemical properties and biomass (ng C ml�1) of the major

heterotrophic protist groups of Masan Bay, Korea (Station SNUMS) from June 1,

2004 to May 31, 2005. (A) Water temperature (T, 8C), (B) salinity (S), (C) chlorophyll-

a (chl-a, mg m�3), (D) total heterotrophic dinoflagellates (HTD), (E) tintinnids (TC),

(F) naked ciliates (NC), and (G) heterotrophic nanoflagellates (HNF).

Y.D. Yoo et al. / Harmful Algae 30S (2013) S89–S101 S91

were abundant in June–September 2004 and February–April 2005.The abundance (biomass) of HNFs was 0–19,446 cells ml�1 (0–141 ng C ml�1) (Fig. 1G and Table 1); they were abundant in June–September 2004 and February–April 2005.

3.3. Correlations between major heterotrophic protistan groups and

physical, chemical, and biological properties

The biomass of total HTDs had significant positive correlationswith pH, DO, and chl-a, but a negative correlation with theconcentration of PO4 (Table 2). In addition, the biomass of total TCshad significant positive correlations with pH and chl-a (Table 2).The biomass of total NCs had a significant positive correlation with

Table 1Range of abundance and biomass for each heterotrophic protist taxon and the water temp

to May 2005.

Taxa Temperature (8C) Salin

Total heterotrophic dinoflagellates 4.3–28.6 4.1–

Total tintinnid ciliates 4.6–28.1 8.1–

Total naked ciliates 4.3–28.4 5.7–

Total heterotrophic nanoflagellates 4.2–28.6 4.1–

water temperature, but a negative correlation with salinity(Table 2), while the biomass of total HNFs had a significantpositive correlation with the concentration of PO4 (Table 2).

The biomass of total HTDs had significant positive correlationswith cryptophytes, phototrophic nanoflagellates (PNFs), picoeu-karyotes, total phytoplankton, and heterotrophic bacteria(Table 2). Biomass of total TCs had significant positive correlationswith diatoms, phototrophic dinoflagellates, cryptophytes, raphi-dophytes, PNFs, picoeukaryotes, total phytoplankton, and hetero-trophic bacteria (Table 2). Biomass of total NCs had significantpositive correlations with diatoms, euglenophytes, cryptophytes,PNFs, and total phytoplankton (Table 2), and biomass of total HNFshad a negative correlation with heterotrophic bacteria (Table 2).

3.4. Temporal variations in the occurrence and biomass of

heterotrophic protist taxa

At station SNUMS from June 1, 2004 to May 31, 2005, 29 HTDtaxa, 16 TC taxa, and several NC taxa were found (SupplementaryTable S1).

Supplementary material related to this article can be found, inthe online version, at http://dx.doi.org/10.1016/j.hal.2013.10.009.

The HTDs Gyrodinium dominans/G. moestrupii, Gyrodinium

glaucum, Oxyphysis oxytoxoides, PLDs, and NCs were presentyear-round, while Gyrodinium spirale, Oblea rotunda, Protoperidi-

nium bipes, Protoperidnium claudicans, Protoperidnium minutum,and the TCs Tintinnopsis spp. were present year-round except for1–2 months (Supplementary Table S1).

The tintinnids (TCs) Eutintinnus perminatus and Helicostomella

longa were present in all seasons, while Tintinnopsis aperta andTintinnopsis tubulosoides were present in summer and fall(Supplementary Table S1). Helicostomella fusiformis was presentin winter and spring, but Amphorellopsis acuta and T. angustior werepresent only in summer (Supplementary Table S1).

Among HTDs, the abundance (biomass) of PLDs was 0–10,200 cells ml�1 (0–1020 ng C ml�1) (Fig. 2A and Table 3); theywere abundant in July–September 2004. Abundance (biomass) of P.

bipes was 0–1018 cells ml�1 (0–298 ng C ml�1) (Fig. 2B andTable 3); it was also abundant in July 2004. Abundance (biomass)of G. dominans/G. moestrupii was 0–748 cells ml�1 (0–235 ngC ml�1) (Fig. 2C and Table 3); these species were abundant inJune–August 2004 and February 2005. The abundance (biomass) ofG. glaucum was 0–85 cells ml�1 (0–48 ng C ml�1) (Fig. 2D andTable 3); it was abundant in June 2004 and October 2004–March2005. The abundance (biomass) of G. spirale was 0–25 cells ml�1

(0–44 ng C ml�1) (Fig. 2E and Table 3); it was abundant in June2004, September–December 2004, and March–May 2005.

Among TCs, the abundance of H. fusiformis was 0–107 cells ml�1

(0–871 ng C ml�1) (Fig. 2F and Table 3); it was abundant duringMarch–April 2005. The abundance (biomass) of Eutintinnus

tubulosus ranged from 0 to 210 cells ml�1 (0–790 ng C ml�1)(Fig. 2G and Table 3); it was abundant in August 2004.The abundance (biomass) of T. tubulosoides was 0–30 cells ml�1

(0–209 ng C ml�1) (Fig. 2H and Table 3); it was abundant duringJune–November 2004. The abundance of NCs (�50 mm) was0–1113 cells ml�1 (0–1013 ng C ml�1) (Fig. 2I and Table 3); they

erature and salinity when each taxon was found in Masan Bay, Korea from June 2004

ity (psu) Abundance (cells ml�1) Biomass (ng C ml�1)

33.3 0–10,289 0–1916

31.7 0–216 0–1263

31.8 0–1113 0–1013

31.8 0–19,446 0–141

Table 2Correlations between heterotrophic protist groups and physical, chemical, and biological properties in Masan Bay, Korea from June 2004 to May 2005.

A. Physical and chemical factors

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

HTD �0.140* 0.157** 0.150** 0.139*

TC 0.147** 0.270**

NC 0.154** �0.193**

HNF 0.233**

B. Biological factors

Components DIA PTD EUG CRY RAP HB CYA PNF PE TP

HTD 0.163** 0.166** 0.238** 0.355** 0.175**

TC 0.232** 0.124* 0.207** 0.142** 0.213** 0.262** 0.356** 0.305**

NC 0.137* 0.164** 0.170** 0.291** 0.161**

HNF 0.124*

T: temperature; P: precipitation; S: salinity; NH4: ammonium; NO3: nitrate plus nitrate; PO4: phosphorus; SiO2: silicate; DO: dissolved oxygen; Chl-a: chlorophyll-a; HTD:

heterotrophic dinoflagellates; TC: tintinnids ciliates; NC: naked ciliates; HNF: heterotrophic nanoflagellates; DIA: diatoms; PTD: phototrophic dinoflagellates; EUG:

euglenophytes; CRY: cryptophytes; RAP: raphidophytes; HB: heterotrophic bacteria; CYA: cyanobacteria; PNF: phototrophic nanoflagellates; PE: picoeukaryotes; TP: total

phototrophic protists.* p < 0.05.** p < 0.01.

Table 3Range of abundance and biomass for each species or taxon of dominant heterotrophic protists and water temperature and salinity when it was found in Masan Bay, Korea

from June 2004 to May 2005.

Species Temperature (8C) Salinity Abundance (cells ml�1) Biomass (ng C ml�1)

Pfiesteria-like-dinoflagellates (PLDs) 4.7–28.6 5.7–33.3 0–10,200 0–1020

Protoperidinium bipes 5.0–28.6 9.7–33.3 0–1018 0–298

Gyrodinium dominans/G. moestrupii 4.5–28.4 8.3–33.3 0–748 0–235

Gyrodinium glaucum 4.6–24.8 19.3–31.7 0–85 0–48

Gyrodinium spirale 7.1–27.6 16.4–31.1 0–25 0–44

Helicostomella fusiformis 5.2–13.6 24.6–30.8 0–107 0–871

Eutintinnus tubulosus 24.4–26.7 19.0–29.3 0–210 0–790

Tintinnopsis tubulosoides 14.8–26.7 16.4–30.1 0–30 0–209

Naked ciliates (�50 mm) 4.3–28.4 6.1–31.8 0–1113 0–1013

Naked ciliates (>50 mm) 4.3–27.7 9.1–31.8 0–57 0–648

Y.D. Yoo et al. / Harmful Algae 30S (2013) S89–S101S92

were abundant during July–September 2004 and April–May 2005.The abundance of NCs (>50 mm) was 0–57 cells ml�1 (0–648 ngC ml�1) (Fig. 2J and Table 3); they were abundant during June–September 2004 and January–April 2005.

3.5. Dominant heterotrophic protists during red tides dominated by

each causative species and their correlations

From June 1, 2004 to May 31, 2005, there were 36 red-tideevents in Masan Bay (Jeong et al., 2013a). PLDs were the mostabundant taxa during red tides dominated by Akashiwo sanguinea,the summer populations of Prorocentrum minimum, Heterosigma

akashiwo, E. gymnastica, and cryptophytes, while G. dominans/G.

moestrupii were most abundant during those dominated byCeratium furca and Dinophysis acuminata. NCs were the mostabundant taxa during red tides dominated by Cochlodinium

polykrikoides, Prorocentrum triestinum, and the winter populationsof P. minimum. During red tides dominated by each red-tideorganism, several heterotrophic protists were abundant and hadsignificant positive correlations with the red-tide organism duringthe study period. The dominant heterotrophic protists during redtides dominated by each red-tide organism are as follows. The term‘‘positively correlated’’ will be used to indicate the biomassrelationships were statistically significant.

H. akashiwo. During its red tides, PLDs, G. dominans/G.

moestrupii, P. bipes, and NC (�50 mm) were abundant. The biomassof Noctiluca scintillans, PLDs, A. acuta, E. perminatus, and H. longa

was positively correlated with that of H. akashiwo (SupplementaryTable S2).

Supplementary material related to this article can be found, inthe online version, at http://dx.doi.org/10.1016/j.hal.2013.10.009.

E. gymnastica. During its red tides, G. dominans/G. moestrupii,PLDs, and NC (�50 mm) were abundant. The biomass of G.

dominans/G. moestrupii, G. spirale, and O. oxytoxoides was positivelycorrelated with that of E. gymnastica (Supplementary Table S2).

P. minimum. During its red tides, PLDs, G. dominans/G.

moestrupii, and NC (�50 mm) were abundant. The biomass of G.

dominans/G. moestrupii, G. glaucum and O. oxytoxoides waspositively correlated with that of P. minimum (SupplementaryTable S2).

Skeletonema costatum. During its red tides, G. dominans/G.

moestrupii, PLDs, H. fusiformis, and NC (�50 mm) were abundant. Inaddition, the biomass of G. dominans/G. moestrupii, G. spirale, E.

tubulosus, T. angustior, and T. tubulosoides was positively correlatedwith S. costatum (Supplementary Table S2).

Heterocapsa triquetra. During its red tides, O. rotunda wasabundant, and the biomass of G. glaucum was positively correlatedwith H. triquetra (Supplementary Table S2).

A. sanguinea. During its red tides, PLDs, G. dominans/G.

moestrupii, Tintinnopsis sp. (90 mm), and NC (�50 mm) wereabundant and the biomass of G. dominans/G. moestrupii, N.

scintillans, O. oxytoxoides, PLDs, and E. perminatus significantlyand positively correlated with that of A. sanguinea (SupplementaryTable S2).

C. furca. During its red tides, G. dominans/G. moestrupii andTintinnopsis sp. (90 mm) were abundant, and the biomass of G.

dominans/G. moestrupii, N. scintillans, A. acuta, and H. longa

positively correlated with C. furca (Supplementary Table S2).

Fig. 3. Abundance (AB, cells ml�1) of (A) the raphidophyte Heterosigma akashiwo, (B)

heterotrophic Pfiesteria-like dinoflagellates, and (C) the ciliate Tiarina fusus in

Masan Bay, Korea from June 1, 2004 to May 31, 2005. Pfiesteria-like dinoflagellates

include Stoeckeria algicida, Pfiesteria piscicida, and other dinoflagellates with size

and shape similar to P. piscicida that could not be distinguished due to their small

sizes and morphological similarity under light microscopy. Calculated grazing

coefficients (g, h�1) for (D) S. algicida and (E) P. piscicida on H. akashiwo, based on

assumptions (see text). (F) Calculated grazing coefficients (h�1) for T. fusus on co-

occurring H. akashiwo. Data for H. akashiwo were obtained from Jeong et al.

(2013a).

Fig. 2. Biomass (ng C ml�1) of the heterotrophic protist species or taxa in Masan Bay,

Korea (Station SNUMS) from June 1, 2004 to May 31, 2005. (A) Pfiesteria-like

dinoflagellates, (B) Protoperidinium bipes, (C) Gyrodinium dominans/G. moestrupii,

(D) Gyrodinium glaucum, (E) Gyrodinium spirale, (F) Helicostomella fusiformis, (G)

Eutintinnus tubulosus, (H) Tintinnopsis tubulosoides, (I) naked ciliates (�50 mm), and

(J) naked ciliates (>50 mm).

Y.D. Yoo et al. / Harmful Algae 30S (2013) S89–S101 S93

C. polykrikoides. During its red tides in June, Tintinnopsis sp.(90 mm) and NC (�50 mm) were abundant, and the biomass of H.

longa positively correlated with C. polykrikoides (SupplementaryTable S2).

Cryptophytes. G. dominans/G. moestrupii, PLDs, and NC(�50 mm) were abundant, and the biomass of G. dominans/G.

moestrupii, N. scintillans, PLDs, and P. bipes was positivelycorrelated with cryptophytes (Supplementary Table S2).

P. triestinum. Naked ciliates (�50 mm) were abundant; andbiomass of T. angustior and H. longa positively correlated with P.

triestinum (Supplementary Table S2).

D. acuminata. During its red tides, G. dominans/G. moestrupii,Tintinnopsis sp. (90 mm), and NC (�50 mm) were abundant. Thebiomass of G. dominans/G. moestrupii, N. scintillans, O. oxytoxoides,A. acuta, E. perminatus, and T. tubulosoides was positively correlatedwith that of D. acuminata (Supplementary Table S2).

Other red-tide organisms. The biomass of G. spirale waspositively correlated with the biomass of S. costatum, Prorocentrum

micans, Scrippsiella trochoidea, E. gymnastica, and PNFs (Supple-mentary Table S2).

3.6. Grazing impacts on red-tide organisms

There was a wide range in grazing coefficients (g) of thedominant heterotrophic protists and co-occurring red-tide organ-isms in Masan Bay during the study period.

H. akashiwo. The PLDs S. algicida and P. piscicida and the ciliateTiarina fusus feed on H. akashiwo (Jeong et al., 2002, 2005, 2006). S.

algicida and P. piscicida could not be distinguished from on eachother under light microscopy because they are small andmorphologically very similar. The abundance of H. akashiwo

Table 4Calculated grazing impacts (GI, h�1) of the dominant heterotrophic protists on each red-tide organism observed in Masan Bay, Korea from June 2004 to May 2005 using each

predator’s maximum ingestion rate and K1/2 (half saturation) from the literature.

Red-tide organisms Predator GI aMIR KIR Ref.

Heterosigma akashiwo Stoeckeria algicida 0.00–2.45 0.8 45 Jeong et al. (2005)

Pfiesteria piscicida 0.00–0.45 0.8 839 Jeong et al. (2006)

Tiarina fusus 0.00–0.002 6.5 1850 Jeong et al. (2002)

Eutreptiella gymnastica Gyrodinium dominans 0.00–0.48 2.7 229 Jeong et al. (2011a)

Polykrikos kofoidii 0.00–0.004 2.7 472 Jeong et al. (2011a)

Protoperidinium bipes 0.00–1.10 2.0 109 Jeong et al. (2011a)

Strobilidium sp. (for naked ciliates �50 mm) 0.00–0.28 2.2 722 Jeong et al. (2011a)

Strombidinopsis sp. (for naked ciliates >50 mm) 0.00–0.06 156.0 6267 Jeong et al. (2011a)

Prorocentrum minimum Gyrodinium dominans 0.00–1.43 1.2 31 Kim and Jeong (2004)

Gyrodinium spirale 0.00–0.13 13.6 137 Kim and Jeong (2004)

Strombidinopsis sp. (for naked ciliates >50 mm) 0.00–6.77 267 82 Jeong et al. (1999)

Skeletonema costatum Protoperidinium bipes 0.00–0.52 2.9 355 Jeong et al. (2004)

Heterocapsa triquetra Gyrodinium dominans 0.00–0.76 4.7 220 Nakamura et al. (1995a,b)

Gyrodinium spirale 0.00–0.02 8.6 560 Hansen (1992)

Tiarina fusus 0.00–0.001 2.6 1180 Jeong et al. (2002)

Akashiwo sanguinea Strombidinopsis sp. (for naked ciliates >50 mm) 0.08–5.31 343.0 133 Jeong et al. (1999)

Ceratium furca Polykrikos kofoidii 0.01–0.05 9.8 55 Jeong et al. (2001b)

Cochlodinium polykrikoides Polykrikos kofoidii 0.00–0.11 14.5 47 Kim (2004)

Scrippsiella trochoidea Polykrikos kofoidii 0.00–0.003 2.9 355 Jeong et al. (2001b)

Tiarina fusus 0.00–0.001 10.2 6310 Jeong et al. (2002)

a MIR: maximum ingestion rate (ng C predator�1 d�1); KIR: prey concentration sustaining (1/2)MIR.

Fig. 4. Abundance (cells ml�1) of (A) the euglenophyte Eutreptiella gymnastica, (B) the heterotrophic dinoflagellates Gyrodinium dominans/G. moestrupii, (C) Protoperidinium

bipes, (D) Polykrikos kofoidii, (E) naked ciliates (�50 mm), and (F) naked ciliates (>50 mm) in Masan Bay, Korea from June 1, 2004 to May 31, 2005. Calculated grazing

coefficients (g, h�1) for (G) G. dominans/G. moestrupii, (H) P. bipes, (I) P. kofoidii, (J) naked ciliates (�50 mm), and (K) naked ciliates (>50 mm) on E. gymnastica and (L) total

combined grazing coefficients. Data for E. gymnastica were obtained from Jeong et al. (2013a).

Y.D. Yoo et al. / Harmful Algae 30S (2013) S89–S101S94

Fig. 5. Abundance (AB, cells ml�1) of (A) the red-tide dinoflagellate Prorocentrum

minimum, (B) the heterotrophic dinoflagellates Gyrodinium dominans/G. moestrupii,

(C) Gyrodinium spirale, and (D) naked ciliates (>50 mm) in Masan Bay, Korea from

June 1, 2004 to May 31, 2005. Calculated grazing coefficients (g, h�1) for (E) G.

dominans/G. moestrupii, (F) G. spirale, and (G) naked ciliates (>50 mm) on P.

minimum and (H) total combined grazing coefficients. Data for P. minimum from

Jeong et al. (2013a).

Y.D. Yoo et al. / Harmful Algae 30S (2013) S89–S101 S95

ranged from 1 to 87,677 cells ml�1, that of co-occurring S. algicida

and/or P. piscicida from 2 to 10,200 cells ml�1. Assuming thatthese PLDs were S. algicida, the grazing coefficients of PLDs on H.

akashiwo were 0.00003–2.45 h�1 (i.e., up to 91% of the populationH. akashiwo was consumed in 1 h) (Fig. 3 and Table 4). [Hereafter,the maximum hourly populations loss calculated will be indicatedby the percent value entered following the preceding g rate (e.g.91% loss).] However, assuming that these PLDs were P. piscicida,the grazing coefficients of PLDs on H. akashiwo were 0.00002–0.45 h�1 (36% loss) (Fig. 3 and Table 4). In addition, the abundanceof H. akashiwo and co-occurring T. fusus were 1–749 cells ml�1

and 0.9–13.6 cells ml�1, respectively. The grazing coefficientsof T. fusus on H. akashiwo were 0.0001–0.002 h�1 (0.2% loss) (Fig. 3and Table 4).

During this study, the combined grazing coefficients for S.

algicida (or P. piscicida) and T. fusus on H. akashiwo were 0.1–2.45 h�1 (0.00002–0.45 h�1) (Fig. 3 and Table 4).

E. gymnastica. The heterotrophic dinoflagellates G. dominans,Polykrikos kofoidii, and Protoperidinium bipes and the naked ciliatesStrobilidium sp. and Strombidinopsis sp. feed on E. gymnastica

(Jeong et al., 2011a). The abundance of E. gymnastica and co-occurring G. dominans/G. moestrupii in Masan Bay was 1–17,029 cells ml�1 and 0.7–748 cells ml�1, respectively. The graz-ing coefficients of the HTD Gyrodinium spp. on E. gymnastica were0.0001–0.48 h�1 (38% loss) (Fig. 4 and Table 4). In addition, whenthe abundance of E. gymnastica and co-occurring P. bipes were 1–11,714 cells ml�1 and 1–1018 cells ml�1, respectively, the grazingcoefficients of P. bipes on E. gymnastica were 0.0001–1.10 h�1 (67%loss) (Fig. 4 and Table 4). Furthermore, when the abundance ofE. gymnastica and P. kofoidii was 1–840 cells ml�1 and 1–332 cells ml�1, respectively, grazing coefficients of P. kofoidii onE. gymnastica were 0.00003–0.004 h�1 (0.4% loss) (Fig. 4 andTable 4). The abundance of E. gymnastica and co-occurring nakedciliates (�50 mm) was 1–17,029 cells ml�1 and 1–1113 cells ml�1, respectively, and the grazing coefficients of NC(�50 mm) on E. gymnastica were 0.00002–0.28 h�1 (24% loss)(Fig. 4 and Table 4). In addition, the abundance of E. gymnastica

and co-occurring NC (>50 mm) was 1–7857 cells ml�1 and 1–57 cells ml�1, respectively. The grazing coefficients of NC(>50 mm) on E. gymnastica were 0.0001–0.06 h�1 (6% loss)(Fig. 4 and Table 4).

During this study, the combined grazing coefficients for G.

dominans/G. moestrupii, P. bipes, P. kofoidii, and the NC on E.

gymnastica were 0.0001–1.15 h�1 (72% loss) (Fig. 4).P. minimum. G. dominans, G. spirale, and Strombidinopsis sp.

feed on P. minimum (Jeong et al., 1999; Kim and Jeong, 2004). Theabundance of P. minimum and co-occurring G. dominans/G.

moestrupii ranged from 1 to 16,068 cells ml�1 and 1–748 cells ml�1, respectively. The grazing coefficients of Gyrodinium

spp. on P. minimum were 0.00001–1.43 h�1 (76% loss) (Fig. 5 andTable 4). In addition, the abundance of P. minimum and co-occurring G. spirale ranged from 2 to 16,070 cells ml�1 and 0.8–24.5 cells ml�1, respectively; the grazing coefficients of the HTD G.

spirale on P. minimum were 0.0002–0.13 h�1 (12% loss) (Fig. 5 andTable 4). The abundance of P. minimum and co-occurring NC>50 mm ranged from 1 to 27,157 cells ml�1 and 1–57.0 cells ml�1,respectively; the grazing coefficients of NC >50 mm on P. minimum

were 0.002–6.77 h�1 (99% loss) (Fig. 5 and Table 4).During the study period, the combined grazing coefficients for

G. dominans/G. moestrupii, G. spirale and Strombidinopsis spp. on P.

minimum varied from 0.00001 to 6.95 h�1 (99% loss) (Fig. 5).S. costatum. P. bipes feeds on S. costatum (Jeong et al., 2004).

The abundance of S. costatum and P. bipes ranged from 4 to59,143 cells ml�1 and 1–1018 cells ml�1, respectively. The grazingcoefficients of P. bipes on S. costatum were 0.0001–0.52 h�1 (40%loss) (Fig. 6 and Table 4).

H. triquetra. G. dominans, G. spirale and T. fusus feed on H.

triquetra (Hansen, 1992; Nakamura et al., 1995a; Jeong et al., 2002).The abundance of H. triquetra and co-occurring G. dominans/G.

moestrupii ranged from 1 to 10,243 cells ml�1 and 0.7–748 cells ml�1, respectively. The grazing coefficients of Gyrodinium

spp. on H. triquetra were 0.001–0.76 h�1 (53% loss) (Fig. 7 andTable 4). The abundance of H. triquetra and G. spirale was 2–556 cells ml�1 and 0.2–24.5 cells ml�1, respectively; grazing coef-ficients of G. spirale on H. triquetra were 0.001–0.02 h�1 (2% loss)(Fig. 7 and Table 4). At the abundance of H. triquetra and co-occurring T. fusus was 1–5845 cells ml�1 and 0.7–22.3 cells ml�1,respectively, the grazing coefficients of T. fusus on H. triquetra were0.00001–0.001 h�1 (0.1% loss) (Fig. 7 and Table 4).

During this study, the combined grazing coefficients for G.

dominans/G. moestrupii, G. spirale and T. fusus on co-occurring H.

triquetra were 0.0001–0.76 h�1 (54% loss) (Fig. 7 and Table 4).A. sanguinea. The naked ciliate Strombidinopsis sp. feeds on A.

sanguinea (Jeong et al., 1999). The abundance of A. sanguinea andco-occurring NC >50 mm was 1.0–519 cells ml�1 and 1.0–57.0 cells ml�1, respectively, with the grazing coefficients of

Fig. 6. Abundance (AB, cells ml�1) of (A) the red-tide diatom Skeletonema costatum

and (B) the heterotrophic dinoflagellate Protoperidinium bipes and (C) the calculated

grazing coefficients (g, h�1) attributable to P. bipes on co-occurring S. costatum in

Masan Bay, Korea from June 1, 2004 to May 31, 2005. Data for S. costatum from Jeong

et al. (2013a).

Fig. 7. Abundance (AB, cells ml�1) of (A) the red-tide dinoflagellate Heterocapsa

triquetra, (B) the heterotrophic dinoflagellates Gyrodinium dominans/G. moestrupii

and (C) Gyrodinium spirale, and (D) the ciliate Tiarina fusus in Masan Bay, Korea from

June 1, 2004 to May 31, 2005. Calculated grazing coefficients (g, h�1) for (E) G.

dominans/G. moestrupii, (F) G. spirale, and (G) Tiarina fusus on H. triquetra and

(H) total combined grazing coefficients. Data for H. triquetra from Jeong et al.

(2013a).

Y.D. Yoo et al. / Harmful Algae 30S (2013) S89–S101S96

Strombidinopsis spp. on A. sanguinea were 0.08–5.31 h�1 (99% loss)(Table 4).

C. furca. P. kofoidii feeds on C. furca (Jeong et al., 2001b). Theabundance of C. furca and co-occurring P. kofoidii was 0.3–52.5 cells ml�1 and 0.8–6.4 cells ml�1, respectively. The grazingcoefficients of P. kofoidii on C. furca were 0.01–0.05 h�1 (5% loss)(Table 4).

C. polykrikoides. P. kofoidii and Strombidinopsis spp. feed on C.

polykrikoides (Jeong et al., 1999, 2008; Kim, 2004). The abundanceof C. polykrikoides and co-occurring P. kofoidii ranged from 6 to210 cells ml�1 and 0.8–6.4 cells ml�1, respectively. The grazingcoefficients of P. kofoidii on C. polykrikoides were 0.003–0.11 h�1

(10% loss) (Table 4).S. trochoidea. P. kofoidii feeds on S. trochoidea (Jeong et al.,

2001b). The abundance of S. trochoidea and co-occurring P. kofoidii

ranged from 1.3 to 110 cells ml�1 and 0.8–6.4 cells ml�1, respec-tively. The grazing coefficients of P. kofoidii on S. trochoidea were0.0002–0.003 h�1 (0.4% loss). Further, the abundance of S.

trochoidea and co-occurring T. fusus was 1–50 cells ml�1 and0.9–13.9 cells ml�1, respectively, with the grazing coefficients of T.

fusus on S. trochoidea 0.0001–0.001 h�1 (0.1% loss) (Table 4).The combined calculated grazing coefficients of P. kofoidii and T.

fusus on S. trochoidea were 0.0001–0.003 h�1 (0.4% loss) (Table 4).

4. Discussion

4.1. Abundance and biomass of major heterotrophic protistan

groups in Masan Bay

The maximum abundance and biomass of all heterotrophicdinoflagellates in Masan Bay during the study period(10,289 cells ml�1 and 1916 ng C ml�1, respectively) were muchgreater than reported for other regions (�200 cells ml�1 and�480 ng C ml�1, respectively) except in Albemarle-Pamlico Estu-ary, USA (Table 5). Pfiesteria-like dinoflagellates contributed themost abundance and biomass of all heterotrophic dinoflagellates inMasan Bay. However, among previous studies, only Glasgow et al.(2001) included Pfiesteria-like dinoflagellates, reporting a very highPfiesteria-like dinoflagellate abundance of 1,200,000 cells ml�1

in Albemarle-Pamlico Estuary, USA, but moderate abundance

(280–4300 cells ml�1) in Neuse, Pamlico Estuary, New River, andChesapeake Bay, USA. Thus, if Pfiesteria-like dinoflagellates hadbeen included, the maximum abundance and biomass of allheterotrophic dinoflagellates in other regions might have beenhigher than reported. We suggest that Pfiesteria-like dinoflagel-lates be included when measuring in heterotrophic dinoflagellates.

The maximum abundance and biomass of all heterotrophicdinoflagellates other than Pfiesteria-like dinoflagellates in MasanBay (1100 cells ml�1 and 1916 ng C ml�1, respectively) were stillgreater than in the other regions. Masan Bay may provide morefavorable conditions for growth of heterotrophic dinoflagellatesthan these other regions, with frequent red-tide events, diversered-tide causative species, lower abundance of mesozooplanktonand lower grazing pressure (Jeong et al., 2013a; Kim et al., 2013).Alternatively, daily sampling may produce a higher maximumabundance and biomass than less frequent sampling.

The maximum abundance and biomass of tintinnids in MasanBay (216 cells ml�1 and 1263 ng C ml�1, respectively) werecomparable to those in Narragansett Bay in the USA and coastalNorth Sea of Germany, lower than in Flødevigen Bay of Norway,

Table 5Comparison of the abundance and biomass of total heterotrophic dinoflagellates (HTDs), tintinnids, naked ciliates (NCs), and heterotrophic nanoflagellates (HNFs).

Taxon Area Abundance (cells ml�1) Biomass (ng C ml�1) Ref.

Total HTDs Masan Bay, Korea 1–10,289 0.1–1916 This study

Albemarle-Pamlico Estuarine, USA 300–1200,000 Glasgow et al. (2001)

Kiel Bight, Germany <1–25 Smetacek (1981)

Perch Pond, USA 0.2–480 Jacobson (1987)

Kattegat, Denmark 200a 162.7a Hansen (1991)

Gulf of Gdansk, Southern Baltic 100 Bralewska and Witek (1995)

Gyenggi Bay, Korea 0.4–94 0.6–71.2 Yang et al. (2008)

Seto Inland, Japan 4–90 Nakamura et al. (1995b)

Northern Strait of Georgia, Canada 30a Haigh and Taylor (1991)

Weddell Sea, Antarctica 0.2–20 Nothig and von Bodungen (1989)

Weddell Sea, Antarctica 0.06–64 <0.01–2.8 Garrison and Buck (1989)

Northeast Atlantic Ocean 2–67 0.9–18.3 Verity et al. (1993)

Northeastern Atlantic Ocean 0.1–10.3 Sleigh et al. (1996)

Weddell/Scotia Sea 9–44 0.5–6.0 Garrison et al. (1990)

South Atlantic 38a Hentschel (1932)

Coastal East Antarctica 4.5–34 10.6–114.5 Archer et al. (1996)

Sargasso Sea near Bermuda 0.9–29 0.1–2.1 Lessard and Murrell (1996)

McMurdo Sound, Antarctica 28a 4a Stoecker et al. (1993)

Dogger Bank, North Sea 0.4–27 >1a Nielsen et al. (1993)

North Atlantic 0.1–22 0.1–6.1 Lessard (1991)

Weddell/Scotia Sea 0.02–14 0.0–6.7 Garrison and Buck (1989)

Polar Front Region 3.1–11 1.5–4 Klass (1997)

Subarctic North Pacific 0.5–2.1 Gifford and Dagg (1991)

Antarctic Circumpolar Current 2–5.7 0.6–1.5 Klass (1997)

Igloolik (polar) 0.7 Bursa (1961)

McMurdo Sound (polar) 0.04–0.14 0.3–2 Lessard and Rivkin (1986)

Ellis Fjord, Eastern Antarctica 0.1a Grey et al. (1997)

Equatorial Pacific 0.02 0.06–0.09 Stoecker et al. (1996)

Total tintinnids Masan Bay, Korea 1–216 0.6–1263 This study

Flødevigen Bay, Norway 729a Dahl and Dahl (1987)

Narragansett Bay, Rhode Island 0.01–270 Verity (1987)

Coastal North Sea 118 Admiraal and Venekamp (1986)

Long Island Sound 0.3–12.6 Capriulo and Carpenter (1983)

Gulf of Naples 0–30.5 Modigh and Castaldo (2002)

Bay of Biscay, Spain 7.4a Urrutxurtu (2004)

Gulf of Naples 0–30.5 0–50.0 Modigh (2001)

Gyenggi Bay, Korea 0.06–7.1 0.1–40.5 Yang et al. (2008)

Buzzards Bay, Massachusetts 0–3.3 Pierce and Turner (1994)

Weddell Sea 3a Buck and Garrison (1983)

Inland Sea of Japan 2.4a Uye et al. (1996)

Arthur Harbor 0.5–2 Heinbokel and Coats (1985)

North Irish Sea 0–1.6 Graziano (1989)

Pacific Ocean 1.2 Tumantseva (1978)

Ise Bay, Japan 0.01–0.7 1–3.8 Uye et al. (2000)

Weddell Sea, Antarctica 0.001–0.4 0.01–0.9 Garrison and Buck (1989)

South Atlantic 0.01–0.2 Hentschel (1932)

Solent Estuary, England 0.09a Burkill (1982)

Total NCs Masan Bay, Korea 1–1113 1–1013 This study

Mediterranean 120a Rassoulzadegan (1977)

Long Island Sound 0.05–113 Capriulo and Carpenter (1983)

Inland Sea of Japan 16a Uye et al. (1996)

Gyenggi Bay, Korea 0.5–33 0.4–80.1 Yang et al. (2008)

Weddell Sea 1–9 Buck and Garrison (1983)

Coastal waters off California, USA 0.1–5.6 Beers and Stewart (1970)

Lime Cay, Kingston, Jamaica 0.001–3.9 0.3–2.1 Lynn et al. (1991)

Weddell Sea 0.003–2.1 0.0–3.8 Garrison and Buck (1989)

Weddell/Scotia Sea 0.3–1.9 0.1–1.1 Garrison et al. (1990)

Total HNFs Masan Bay, Korea (0.0–1.9) � 104 1–141 This study

Baltic Sea (North-Rugian Bodden) (0.8–1.0) � 105 Dietrich and Arndt (2000)

Baltic Sea, Finland (0.0–1.0) � 104 Kuuppo (1994)

NE Pacific Coast (0.3–6.7) � 103 Tanaka et al. (1997)

Funka Bay, Japan (0.5–5.6) � 103 Lee et al. (2001)

Rimov reservoir, Czech Republic (1.4–4.5) � 103 Simek et al. (1997)

Gyenggi Bay, Korea (0.4–4.4) � 103 1.3–15.4 Yang et al. (2008)

Lago Maggiore, Italy (1.8–3.8) � 103 Callieri et al. (2002)

New Zealand Safi and Hall (1997)

(Offshore West Coast) (0.2–0.5) � 103

(Inshore West Coast) (0.2–0.9) � 103

(Subantarctic) (0.2–0.6) � 103

(Convergence) (0.3–1.0) � 103

(Subtropical) (0.1–0.5) � 103

a Maximum abundance and biomass.

Y.D. Yoo et al. / Harmful Algae 30S (2013) S89–S101 S97

Table 6Heterotrophic dinoflagellates (HTDs) and tintinnid ciliates (TCs) measured in other locations reported in the literature.

Taxa Location Temperature (8C) Abundance (cells ml�1) Ref.

Gyrodinium dominans (HTD) Perch Pond, Massachusetts, USA 5–25 0.6–1.1 Jacobson (1987)

Gyrodinium spirale (HTD) Perch Pond, Massachusetts, USA 2–22 0.0–7.0 Jacobson (1987)

Oblea rotunda (HTD) Perch Pond, Massachusetts, USA 2–25 0.0–57.0 Jacobson (1987)

Protoperidinium bipes (HTD) Perch Pond, Massachusetts, USA 2–25 0.0–1.0 Jacobson (1987)

Protoperidinium claudicans (HTD) Perch Pond, Massachusetts, USA 5–23 0.0–2.1 Jacobson (1987)

Protoperidinium minutum (HTD) Perch Pond, Massachusetts, USA 10–23 0.0–18.0 Jacobson (1987)

Protoperidinium pyriforme (HTD) Perch Pond, Massachusetts, USA 5–20 0.0–1.0 Jacobson (1987)

Zygabikodinium lenticulatum (HTD) Perch Pond, Massachusetts, USA 2–25 0.0–1.0 Jacobson (1987)

Tintinnopsis beroidea (TC) Mediterranean, Gulf of Naples 13.3–28.6 0.0–6.2 Modigh and Castaldo (2002)

Eutintinnus tubulosus (TC) Mediterranean, Gulf of Naples 15.0–28.6 0.0–2.6 Modigh and Castaldo (2002)

Helicostomella subulata (TC) Mediterranean, Gulf of Naples 13.3–28.6 0.0–28.7 Modigh and Castaldo (2002)

Y.D. Yoo et al. / Harmful Algae 30S (2013) S89–S101S98

and greater than in other regions (Admiraal and Venekamp, 1986;Dahl and Dahl, 1987; Verity, 1987; Table 5). The maximumabundance and biomass of naked ciliates (1113 cells ml�1 and1013 ng C ml�1, respectively) were greater than those in otherregions (Table 5). Naked ciliates grow quickly on abundant prey,but die rapidly if starved (Jeong et al., 1999). Thus, bloomsdominated by favorable prey may result in a high maximumabundance of naked ciliates in Masan Bay. The maximumabundance and biomass of heterotrophic nanoflagellates in MasanBay (1.9 � 104 cells ml�1 and 141 ng C ml�1, respectively) werecomparable to, or lower than in the Baltic Sea, Finland (Kuuppo,1994; Dietrich and Arndt, 2000), but greater than in other regions(Table 5). The biomass of heterotrophic nanoflagellates had asignificant correlation with that of heterotrophic bacteria, but anegative correlation with that of cyanobacteria. The abundance ofheterotrophic bacteria in Masan Bay ranged from 4.4 � 105 to1.9 � 107 cells ml�1 (Jeong et al., 2013a). Thus, high heterotrophicbacterial abundance may support high maximum abundance andbiomass of heterotrophic nanoflagellates in Masan Bay.

4.2. Temporal variations in the occurrence and biomass of

heterotrophic protist taxa

During the study period, 17 of 29 heterotrophic dinoflagellatetaxa were present year-round, or nearly so. However, only a fewtintinnid taxa were so ubiquitous; most of these taxa were presentonly for a few months. One explanation may be that heterotrophicdinoflagellate taxa in Masan Bay are less likely to be affected bywater temperature than tintinnids. In general, heterotrophicdinoflagellate taxa are tolerant of wider temperature ranges thantintinnids (Jacobson, 1987; Modigh and Castaldo, 2002; Table 6). Inaddition, heterotrophic dinoflagellate taxa in Masan Bay are likely tofeed on more diverse prey than tintinnids. Heterotrophic dino-flagellates have diverse feeding mechanisms such as direct-engulfment feeding, pallium feeding, and peduncle feeding (e.g.Jeong et al., 2010). However, tintinnids are able to feed only on preywhose size is <41–45% of the mouth diameter of their lorica throughdirect-engulfment feeding (Spittler, 1973). Thus, prey availability fortintinnids in Masan Bay may be very low in some months.

4.3. Dominant heterotrophic protists during red tides dominated by

each causative species

Heterotrophic protists in Masan Bay were abundant during red-tide periods, but rare otherwise. Thus, the abundance ofheterotrophic protists in Masan Bay is likely affected by preyavailability. In addition, the biomass of most heterotrophic protisttaxa in Masan Bay were significantly and positively correlated withred-tide organisms (Supplementary Table S2). Thus, the popula-tion of heterotrophic protist taxa generally increased when redtides occurred.

During the study period, Pfiesteria-like dinoflagellates, G.

dominans/G. moestrupii, and naked ciliates were the most abundantheterotrophic protist taxa during red tides, except during H.

triquetra red tides. These three taxa were simultaneously mostabundant during red tides dominated by many causative speciessuch as A. sanguinea, the summer populations of P. minimum, P.

triestinum, D. acuminata, H. akashiwo, E. gymnastica, and crypto-phytes. Thus, these three taxa may compete with one anotherwhen they form red tides in Masan Bay. In addition, their relativeabundance changed depending on the red-tide taxa. Thus, therelative growth rates of these three taxa may be affected by thered-tide taxa present.

N. scintillans was abundant during C. furca red tides. It is a slowswimmer (Kiørboe and Titelman, 1998) and may be able to capturethe slow-swimming C. furca. During C. polykrikoides red tides, largeciliates Tintinnopsis sp. (90 mm) and NC (�50 mm) were abundant.The chain-forming C. polykrikoides is known to be preyed upon bylarge ciliates (Jeong et al., 1999, 2008).

4.4. Grazing impact

The heterotrophic protist species having the highest calculatedgrazing coefficient on red-tide organisms in Masan Bay nearlyalways differed among each other. For example, S. algicida had thehighest grazing impact on populations of H. akashiwo; G. dominans/G. moestrupii on P. minimum and H. triquetra; P. bipes on E.

gymnastica; naked ciliates >50 mm on A. sanguinea and P.

minimum, and P. kofoidii on C. polykrikoides and C. furca. Thus,heterotrophic protist species may be specialized to controlpopulations of specific red-tide species in Masan Bay.

The range of the calculated grazing coefficients (g) for eachheterotrophic protist species on co-occurring red-tide organismswas large. For example, the maximum grazing coefficients of S.

algicida, G. dominans/G. moestrupii, P. bipes, and naked ciliates>50 mm on H. akashiwo, P. minimum, E. gymnastica, and A.

sanguinea, respectively were as high as 1.1–6.8 h�1 (i.e., 64–99%of their prey populations were consumed in 1 h), while their lowestgrazing coefficients had negligible affects. When abundance of thepredator populations are very high, but those of the preypopulations are very low, the grazing impact can be so high thatit has the potential to remove almost all prey cells within hours.Thus, heterotrophic protistan grazers may at times have consider-able grazing impact on the populations of co-occurring red-tideorganisms.

Whereas most red-tide organisms are likely to have naturalenemies, S. trochoidea may not. The maximum calculated grazingcoefficient on co-occurring S. trochoidea was for P. kofoidii, it wasonly 0.003 h�1 (i.e., 0.4% of the S. trochoidea population wasconsumed in 1 h). When the abundance of the prey populations isvery high but that of the predator populations very low, the grazingimpact can be negligible. Furthermore, the maximum calculated

Table 7Comparison of the maximum measured or calculated grazing impacts (GI) of heterotrophic protists on each red-tide organism.

Red-tide organism Predator Area GI (h�1) Ref.

Heterosigma akashiwo Pfiesteria-like dinoflagellates Masan Bay, Korea 2.45 This study

H. akashiwo Microzooplankton Love Creek, USA 0.03 Demir et al. (2008)

H. akashiwo Microzooplankton Torquary Canal, USA 0.03 Demir et al. (2008)

H. akashiwo Microzooplankton Russell’s Canal, USA 0.01–0.08 Demir et al. (2008)

H. akashiwo Microzooplankton East Sound, Orcas Island 0.27 Graham and Strom (2010)

Prorocentrum minimum Naked ciliates >50 mm Masan Bay, Korea 6.77 This study

P. minimum Microzooplankton Chesapeake Bay, USA 0.22 Johnson et al. (2003)

Skeletonema costatum Protoperidinium bipes Masan Bay, Korea 0.52 This study

S. costatum Gyrodinium sp. Monterey Bay, USA 0.01 Buck et al. (2005)

Y.D. Yoo et al. / Harmful Algae 30S (2013) S89–S101 S99

grazing coefficient for T. fusus on co-occurring S. trochoidea was lessthan for P. kofoidii. Thus, the red-tide dynamics of S. trochoidea maynot be substantially affected by grazing pressure.

The maximum calculated grazing coefficients attributable todominant heterotrophic protists on co-occurring red-tide organ-isms in Masan Bay during the study period were higher than thoseon the same prey species in other regions (Table 7). The maximumgrazing coefficient of PLDs on H. akashiwo in the present study(2.45 h�1) was much higher than microzooplanktonic grazing onthe same prey in Love Creek, Torquary Canal, Russell’s Canal, andEast Sound of Orcas Island, USA (0.01–0.27 h�1; Demir et al., 2008;Graham and Strom, 2010). In addition, the maximum grazingcoefficients for naked ciliates >50 mm and G. dominans on P.

minimum in the present study (6.8 and 1.43 h�1, respectively) wasmuch higher than microzooplanktonic grazing on P. minimum inChesapeake Bay, USA (0.22 h�1) (Johnson et al., 2003). Further-more, the maximum grazing coefficient for P. bipes on S. costatum

(0.52 h�1) was higher than that for Gyrodinium sp. on the sameprey in Monterey Bay, USA (0.01 h�1; Buck et al., 2005).

5. Conclusions

The present study demonstrated that: (1) at the station SNUMSin Masan Bay from June 1, 2004 to May 31, 2005, 29 heterotrophicdinoflagellate taxa, 16 tintinnid taxa, and several naked ciliate taxawere found; (2) heterotrophic protists were abundant in red-tideperiods, but rare in non-red tide periods; (3) the range of thecalculated grazing coefficients attributable to a dominant hetero-trophic protist on a co-occurring red-tide organism in Masan Bay inthe study period was large, but the maximum grazing coefficientson red-tide organisms were quite high, other than for S. trochoidea.Thus, heterotrophic protistan grazers may at times have consider-able grazing impact on the populations of co-occurring red-tideorganisms.

Acknowledgements

We thank Moo Joon Lee and An Suk Lim for technical support.This paper was supported by the National Research Foundation/MSITCFP (NRF-C1ABA001-2010-0020702), Mid-career ResearcherProgram (2012-R1A2A201-010987) and Ecological DisturbanceResearch Program and Long-term change of structure and functionin marine ecosystems of Korea program, Korea Institute of MarineScience & Technology Promotion/Ministry of Oceans and Fisheriesaward to HJ Jeong.

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