Harmful Algae 30S (2013) S102–S113

Red tides in Masan Bay, Korea, in 2004–2005: III. Daily variations in theabundance of mesozooplankton and their grazing impacts on red-tideorganisms

Jae Seong Kim a, Hae Jin Jeong b,*, Yeong Du Yoo b, Nam Seon Kang b, Soo Kyeum Kim c,Jae Yoon Song d, Moo Joon Lee b, Seong Taek Kim e, Jung Hoon Kang f,Kyeong Ah Seong c, Won Ho Yih c

a Water and Eco-Bio Corporation, Kunsan National University, Kunsan 573-701, Republic of Koreab School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University, Seoul 151-747, Republic of Koreac Department of Oceanography, College of Ocean Science and Technology, Kunsan National University, Kunsan 573-701, Republic of Koread Korea Engineering Consultants Corporation, 546-1, Guui-dong, Gwangjin-gu, Seoul 143-715, Republic of Koreae B&G Eco Tech, 140 Top-ri, Chukdong-myeon, Sacheon-si, Gyeonnam 664-811, Republic of Koreaf South Sea Branch, Korea Ocean Research and Development Institute (KORDI), 391 Jangmok-ri, Jangmok-myon, Geoje, Gyungsangnam-do 656-830, Republic

of Korea

A R T I C L E I N F O

Keywords:

Cladocera

Copepod

Food web

Grazing

Harmful algal bloom

Larvae

A B S T R A C T

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

measured the abundance of mesozooplankton in daily samples collected from June 1, 2004 to May 31,

2005. Mesozooplankton were abundant in the winter, but rare in the summer, and had a range of

abundance of 3–52,843 ind. m�3. Similarly, both copepods and cladocerans were abundant in the winter,

but rare in the summer, and had ranges of abundance of 0–48,817 ind. m�3 and 0–10,951 ind. m�3,

respectively. Invertebrate larvae were abundant in the fall but not in other seasons. The biomass of

copepods was significantly positively correlated with salinity, dissolved oxygen, the biomass of the

phototrophic dinoflagellates Heterocapsa triquetra and Prorocentrum minimum, and the biomass of the

heterotrophic dinoflagellate Gyrodinium glaucum, but negatively correlated with water temperature and

the biomass of heterotrophic bacteria and small algae. In addition, the biomass of cladocerans was

significantly positively correlated with salinity and the biomass of euglenophytes and G. glaucum, but

negatively correlated with water temperature. The biomass of invertebrate larvae was significantly

positively correlated with water temperature, but negatively correlated with dissolved oxygen. These

observations suggest that copepods and cladocerans may increase their populations by feeding on large

phytoplankton in cold water, whereas invertebrate larvae may prefer warm water. The grazing

coefficients for the copepods Acartia spp. on co-occurring Pfiesteria-like dinoflagellates (PLDs), P.

minimum, Skeletonema costatum, H. triquetra, Heterosigma akashiwo, and Scrippsiella trochoidea were

0.104, 0.083, 0.042, 0.034, 0.033, and 0.030 d�1, respectively. These results suggest that grazing by

Acartia populations in Masan Bay can have a considerable impact on the populations of PLDs and P.

minimum, but only a moderate impact on S. costatum, H. triquetra, S. trochoidea, and H. akashiwo.

� 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 have occurred in the coastal and offshore waters ofmany countries as well as in the mid-ocean (Holmes et al., 1967;Jeong, 1995; Imai et al., 2001; Sordo et al., 2001; Alonso-Rodriguezand Ochoa, 2004; Seong et al., 2006; Lee et al., 2013; J.Y. Park et al.,

* 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.2013.10.010

2013a). They can alter the balance of food webs and cause large-scale mortality of fish and shellfish (ECOHAB, 1995; T.G. Park et al.,2013b). Studies of red-tide formation and persistence suggest thatgrazing pressure may play an important role inbloom dynamics(Watras et al., 1985; Turner, 2006). Grazing by mesozooplanktonis believed to sometimes contribute to the decline of red tides(Calbet et al., 2003; Tan et al., 2004).

Many mesozooplankters such as copepods, cladocerans, andinvertebrate larvae are known to feed on red-tide organisms(Houde and Roman, 1987; Turner et al., 1988, 2012; Carlsson et al.,

Fig. 1. Map of the sampling station (SNUMS) in Masan Bay, Korea (A). (B) Enlarged

from (A).

J.S. Kim et al. / Harmful Algae 30S (2013) S102–S113 S103

1995; Liu and Wang, 2002; Broglio et al., 2003; reviewed by Turner,2006; Cohen et al., 2007; Waggett et al., 2008; Jeong et al., 2004a,2010a). In turn, they are good prey for adult fish and shellfish(Sanders and Wickham, 1993; Lazareva and Kopylov, 2011). Thus,mesozooplankters play important roles in marine ecosystems.To understand the role of mesozooplankton in red-tidedynamics, we must examine four questions. First, whichmesozooplankton species are abundant during a red tide? Acorrelation between the abundances of the dominant mesozoo-plankton and the red-tide organism may give clues to theirpredator–prey relationship. Second, are the dominant meso-zooplankton able to feed on the red-tide organism? Manystudies have observed these predator–prey relationships inlaboratory experiments (Sanders and Wickham, 1993; Huskinet al., 2000; Jeong et al., 2001; Kim, 2005; Song, 2007). Third, atwhat rate do predators ingest red-tide species? Many studieshave also measured these rates (Sanders and Wickham, 1993;Ban et al., 1997; Hansen et al., 1997; Jeong et al., 2001; Kim,2005; Song, 2007). Finally, what is the impact of grazing bypredators on the red-tide species? The grazing impact can eitherbe measured directly or calculated (Turner and Graneli, 1992;Calbet, 2001; Calbet et al., 2003; Tan et al., 2004).

Masan Bay, Korea, is a highly eutrophicated bay withfrequent red tides (Han et al., 1991; Yoo, 1991; Kwak et al.,2001; Lee and Lim, 2006). To explore the role of mesozoo-plankton in red-tide dynamics in Masan Bay, we measured theabundance of mesozooplankton (i.e., copepods, cladocerans,invertebrate larvae, etc.) on a daily basis for 1 year. We alsolooked for correlations between the abundance of mesozoo-plankton and physical and chemical factors, the abundance ofco-occurring red-tide organisms (Jeong et al., 2013), andheterotrophic protists (Yoo et al., 2013). By combining fielddata on the abundances of mesozooplankton predators and thetarget red-tide organism with the ingestion rates of thepredators on the prey obtained from the literature, we estimatedthe grazing coefficients attributable to the predator on co-occurring red-tide prey. The results of the present study providea basis for understanding the role of mesozooplankton in red-tide dynamics in eutrophic bays.

2. Materials and methods

2.1. Abundance in Masan Bay, Korea

Masan Bay is located in the southeastern part of Korea (Fig. 1).This bay is long and semi-enclosed (5-km long and 2-km wide witha 1-km mouth). A large city, Changwon, surrounds the bay, andthree streams enter the bay.

Mesozooplankton samples were collected at a pier in MasanBay (Station SNUMS; 1.2–2.4-m deep depending on tide) by towinga 303-mm-mesh, 45-cm-diameter, conical plankton net with aflowmeter obliquely from the bottom to the surface every day fromJune 2004 to May 2005. Samples were taken at 10:00 h. Eachplankton sample was poured into a 500-ml polyethylene bottleand preserved with 4% formalin. Species identification anddetermination of the abundance of mesozooplankton wereperformed using dissecting and inverted microscopes at magni-fications of 40� and 200�. The calanoid copepods Acartia omorii

and Acartia hongi (Soh and Suh, 2000) which coexist in the coastalwaters off Korea are similar, and it is very difficult to distinguishbetween the two species. Thus, we used A. omorii/A. hongi for thesetaxa.

Simultaneously, surface water samples were taken from thepier to measure physical, chemical, and biological properties(Jeong et al., 2013; Yoo et al., 2013).

2.2. Biomass conversion

The biomass of each mesozooplankton taxon was obtainedfrom the literature, if known, or estimated from the taxon’sbiovolume according to Berggreen et al. (1988), Durbin and Durbin(1992), Hansen (1993), and Hansen et al. (1997).

2.3. Correlations

The correlation coefficients between mesozooplankton andphysical, chemical, and biological properties were calculated usingPearson’s correlation (Conover, 1980; Zar, 1999).

2.4. Grazing impact by mesozooplankton on red-tide organisms

Grazing coefficients for each predator–prey relationship wereestimated by combining field data on the abundances of themesozooplankton predators and the target red-tide organism, withthe ingestion rates of the predators on the prey obtained in theliterature, with some assumptions. Acartia hudsonica (Acartia

clausii) is known to feed on Skeletonema costatum (Deason, 1980). Itwas assumed that the ingestion rate for Acartia omorii, thedominant Acartia species in this study, was the same as that for A.

hudsonica. In addition, A. omorii/Acartia hongi are known to feed onthe heterotrophic dinoflagellates Pfiesteria piscicida, Stoeckeria

algicida, and Luciella masanensis (Jeong et al., 2007b). These 3

J.S. Kim et al. / Harmful Algae 30S (2013) S102–S113S104

dinoflagellate species are difficult to distinguish using a lightmicroscope. Thus, the grazing coefficients for Acartia spp. on co-occurring Pfiesteria-like dinoflagellates (PLDs) were calculated byassuming that the ingestion rate of Acartia spp. on the PLDs was thesame as that of A. omorii/A. hongii on S. algicida.

The grazing coefficients (g, d�1) were calculated as follows:

g ¼ CR � GC � 24; (1)

where CR is the clearance rate (ml predator�1 h�1) of a predator ona red-tide organism at a given prey concentration and GC is thepredator concentration (predators ml�1). CR values were calculat-ed as follows:

CR ¼ IR

X; (2)

where IR is the ingestion rate (cells predator�1 h�1) of the predatoron the prey and X is the prey concentration (cells ml�1). CR valueswere corrected using a Q10 of 3.2 for copepods and 3.4 forinvertebrate larvae (Hansen et al., 1997) because in situ watertemperatures sometimes differed from the temperature used inlaboratory experiments (20 8C).

3. Results

3.1. Physical and chemical properties of Masan Bay

From June 1, 2004 to May 31, 2005, water temperature at thestation SNUMS varied from 4.2 to 28.6 8C; the highest temperaturewas in August 2004, while the lowest temperature was in February2005 (Fig. 2A). Salinity was 4.1–33.3; the highest salinity was in

Fig. 2. (A) Water temperature (T, 8C), (B) salinity (S), (C) dissolved oxygen (DO,

mg l�1), (D) the concentration of chlorophyll-a (Chl-a, mg l�1), and (E) the biomass

of heterotrophic bacteria (HB, ng C ml�1) in Masan Bay, Korea from June 1, 2004 to

May 31, 2005.

December 2004, while the lowest salinity was in July 2004(Fig. 2B). Dissolved oxygen (DO) was 0.4–14.9 mg l�1 (Fig. 2C): thechlorophyll-a concentration (chl-a) was 0–514.7 mg l�1 (Fig. 2D).Other physical and chemical properties are provided in Jeong et al.(2013).

The biomass and abundance of heterotrophic bacteria (HB)ranged from 12.6 to 548.4 ng C ml�1 and from 4.4 � 105 to1.9 � 107 cells ml�1, respectively (Jeong et al., 2013); both biomassand abundance of the HB were highest in May 2005 (Fig. 2E).

3.2. Biomass and abundance of mesozooplankton

The total biomass of mesozooplankton was high from Decem-ber 2004 to March 2005, intermediate from September to October2004, and low in all other months (Fig. 3A). The maximum totalbiomass of mesozooplankton (113 mg C m�3) was observed inJanuary 2005 (Fig. 3A). Copepods were the predominant compo-nent of total mesozooplankton biomass in all months except fromJuly to September 2004 (Fig. 3B). The maximum biomass ofcopepods (107 mg C m�3) was observed in January 2005. Clado-cerans were the predominant component of total mesozooplank-ton biomass in August, but their maximum biomass (16 mg C m�3)was highest in January 2005 (Fig. 3C). Benthic invertebrate larvaepredominated in July and September 2004 (Fig. 3D) and theirmaximum biomass (16 mg C m�3) was observed in September2004. The biomass of all other mesozooplankton taxa was<1.3 mg C m�3 in every month (Fig. 3E).

The total abundance of mesozooplankton at the station SNUMSwas 3–52,843 ind. m�3 (mean � SE = 3344 � 414, n = 313), whilethe abundance of copepods was 0–48,817 ind. m�3 (mean� SE = 2830 � 390, n = 313) (Table 1). In addition, the abundanceof the cladocerans was 0–10,951 ind. m�3 (mean � SE = 289 � 49,

Fig. 3. The biomass of total mesozooplanton (A), copepods (B), cladocerans (C),

invertebrate larvae (D), other mesozooplankton (E) in Masan Bay, Korea from June

1, 2004 to May 31, 2005.

Table 1The range of abundance and biomass of each mesozooplankton group and the water temperature and salinity where each group was found in Masan Bay from June 2004 to

May 2005.

Taxa Temperature (8C) Salinity (psu) Abundance (ind. m�3) Biomass (mg C m�3)

Total mesozooplanton 4.2–28.6 4.1–33.3 2.6–52,843 0.001–113

Total copepods 4.2–28.6 4.1–33.3 0.1–48,817 0.001–107

Total cladocerans 4.2–28.6 4.1–33.3 0.01–10,951 0.002–16

Total larvae of invertebrates 4.2–28.6 4.1–33.3 0.01–3733 0.00003–16

Othersa 4.2–28.6 4.1–33.3 0.00004–1894 0.00004–1.3

a See supplementary Table S1.

J.S. Kim et al. / Harmful Algae 30S (2013) S102–S113 S105

n = 313), while that of the larvae of benthic invertebrates was 0–3733 ind. m�3 (mean � SE = 115 � 24, n = 313).

3.3. Species composition of mesozooplankton

During the study period, 16 copepod, 3 cladocera, 11 inverte-brate larvae, and 6 other mesozooplankton species or taxa werefound (Supplementary Table S1). These included the copepodsAcartia omorii/Acartia hongii, Acartia erythrea, Acartia pacifica,Calanopia thomsoni, Calanus sinicus, Centropages abdominalis,Corycaeus affinis, Labidocera rounta, Oithona similis, Paracalanus

indicus, Pontella fera, Psuedodiaptomus marinus, Temora turbinata,and Tortanus forcipatus, harpacticoids, copepodites; the cladocer-ans Evadne tergestina, Penilia avirostris, and Podon polyphemoides. Inaddition, barnacle larvae, decapod zoea, polychaete larvae, andchaetognaths were observed.

Fig. 4. The biomass of the copepods Acartia omorii/A. hongii (A), Calanus sinicus (B),

Centropages abdominalis (C), Oithona similis (D), Paracalanus indicus (E),

Pseudodiaptomus marinus (F), and harpacticoids (G) in Masan Bay, Korea from

June 1, 2004 to May 31, 2005.

Supplementary material related to this article can be found, inthe online version, at http://dx.doi.org/10.1016/j.hal.2013.10.010.

Of these mesozooplankters, Acartia omorii/Acartia hongii,Centropages abdominalis, Corycaeus affinis, Oithona similis, Para-

calanus indicus, Psuedodiaptomus marinus, copepodites, harpacti-coids, Podon polyphemoides, barnacle nauplii, polychaete larvae,amphipods, chaetognaths, and mysids were present in almost allseasons (Figs. 4 and 5; Supplementary Table S1). However, Acartia

erythrea, Calanopia thomsoni, Pontella fera, and siphonophores wereonly present in a single season.

The biomasses of Acartia omorii/Acartia hongii and Calanus

sinicus were the highest and second highest among copepods,respectively, while Podon polyphemoides had the highest biomassamong the cladocerans (Figs. 4 and 5; Table 2). The biomass ofpolychaete larvae was highest among the invertebrate larvae(Fig. 5). Dominant mesozooplankton species differed from otherspecies in their maximum abundance and biomass and themonths, water temperature, and salinity when they wereabundant.

Fig. 5. The biomass of the cladocerans Evadne tergestina (A), Penilia avirostris (B),

Podon polyphemoides (C), barnacle nauplii (D), polychaete larvae (E), and

chaetognatha (F) in Masan Bay, Korea from June 1, 2004 to May 31, 2005.

Table 2The range of the abundance and biomass of the dominant mesozooplankton species or taxon and the water temperature and salinity when found in Masan Bay from June 2004

to May 2005.

Species Temperature (8C) Salinity (psu) Abundance (ind. m�3) Biomass (mg C m�3)

Acartia omorii/A. hongii 4.2–28.6 4.1–33.3 0–45,671 0–81.8

Calanus sinicus 4.2–19.6 25.0–31.8 0–437 0–23.7

Centropages abdominalis 4.2–24.9 8.5–33.3 0–419 0–0.8

Oithona similis 4.4–28.6 4.1–33.3 0–5126 0–1.7

Paracalanus indicus 4.2–28.6 4.1–33.3 0–4355 0–8.0

Pseudodiaptomus marinus 4.3–27.0 9.7–31.8 0–891 0–4.8

Harpacticoid 4.2–28.4 4.1–31.5 0–177 0–0.2

Evadne tergestina 5.6–28.6 4.1–31.1 0–364 0–0.5

Penilia avirostris 8.6–28.6 4.1–31.1 0–914 0–1.5

Podon polyphemoides 4.2–27.9 4.1–33.3 0–10,951 0–16.1

Barnacle nauplius 5.0–28.6 4.1–33.3 0–524 0–0.4

Polychaete larvae 5.5–28.6 4.1–31.2 0–3575 0–16.1

Chaetognatha 4.2–28.6 4.1–33.3 0–664 0–0.4

J.S. Kim et al. / Harmful Algae 30S (2013) S102–S113S106

3.3.1. Acartia omorii/Acartia hongiiTheir abundance (and biomass) was 0–45,671 ind. m�3 (0–

81.8 mg C m�3), and they were present when the water tempera-ture was 4.2–28.6 8C and the salinity was 4.1–33.3 (Table 2). Thesecopepods were particularly abundant in January and February2005 when the water temperature was 4.2–7.2 8C and the salinity26.7–31.8 (Fig. 4A).

3.3.2. Calanus sinicusIts abundance (and biomass) was 0–437 ind. m�3 (0–

23.7 mg C m�3), and it was present at 4.2–19.6 8C and salinity25.0–31.8 (Table 2). This copepod was abundant in January andFebruary 2005 at 4.2–6.5 8C and salinity 28.7–31.7 (Fig. 4B).

3.3.3. Centropages abdominalisIts abundance (and biomass) was 0–419 ind. m�3 (0–

0.8 mg C m�3), and it was present when the water temperaturewas 4.2–24.9 8C and the salinity was 8.5–33.3 (Table 2). Thiscopepod was abundant from January to March 2005 at 4.2–8.6 8Cand salinity 28.7–31.4 (Fig. 4C).

3.3.4. Oithona similisIts abundance (and biomass) was 0–5126 ind. m�3 (0–

1.7 mg C m�3), and it was present when the water temperaturewas 4.4–28.6 8C and the salinity was 4.1–33.3 (Table 2). Thiscopepod was abundant in January 2005 at 4.6–6.1 8C and salinity29.2–31.7 (Fig. 4D).

3.3.5. Paracalanus indicusIts abundance (and biomass) was 0–4355 ind. m�3 (0–

8.0 mg C m�3), and it was present when the water temperaturewas 4.2–28.6 8C and the salinity was 4.1–33.3 (Table 2). Thiscopepod was abundant from January to March 2005 at 4.2–6.9 8Cand salinity 26.7–31.8 (Fig. 4E).

3.3.6. Pseudodiaptomus marinusIts abundance (and biomass) was 0–891 ind. m�3 (0–

4.8 mg C m�3), and it was present when the water temperaturewas 4.3–27.0 8C, and the salinity was 9.7–31.8 (Table 2). Thiscopepod was abundant in September 2004 and February 2005 at4.4–24.8 8C and salinity 22.4–31.7 (Fig. 4F).

3.3.7. Harpacticoids

Their abundance (and biomass) was 0–177 ind. m�3 (0–0.2 mg C m�3), and they were present when the water temperaturewas 4.2–28.4 8C and the salinity was 4.1–31.5 (Table 2). Thesecopepods were abundant in June and July 2004 and from December2004 to May 2005 at 4.2–24.8 8C and salinity 19.3–31.2(Fig. 4G).

3.3.8. Evadne tergestinaIts abundance (and biomass) was 0–364 ind. m�3 (0–

0.5 mg C m�3), and it was present at 5.6–28.6 8C and salinity4.1–31.1 (Table 2). This cladoceran was abundant in August andSeptember 2004 at 24.7–27.0 8C and salinity 19.0–29.8(Fig. 5A).

3.3.9. Penilia avirostrisIts abundance (and biomass) was 0–914 ind. m�3 (0–

1.5 mg C m�3), and it was present when the water temperaturewas 8.6–28.6 8C and the salinity was 4.1–31.1 (Table 2). Thiscladoceran was abundant in August and September 2004 at 16.8–28.6 8C and salinity 8.1–29.8 (Fig. 5B).

3.3.10. Podon polyphemoidesIts abundance (and biomass) was 0–10,951 ind. m�3 (0–

16.1 mg C m�3), and it was present at 4.2–27.9 8C and salinity4.1–33.3 (Table 2). This cladoceran was abundant in December2004 and January 2005 at 4.2–16.2 8C and salinity 29.0–31.6(Fig. 5C).

3.3.11. Barnacle larvae

Their abundance (and biomass) was 0–524 ind. m�3 (0–0.4 mg C m�3), and they were present at 5.0–28.6 8C and salinity4.1–33.3 (Table 2). These larvae were abundant in August andSeptember 2004 at 19.6–25.0 8C and salinity 11.5–29.1 (Fig. 5D).

3.3.12. Polychaete larvae

Their abundance (and biomass) was 0–3575 ind. m�3 (0–16.1 mg C m�3), and they were present at 5.5–28.6 8C and salinity4.1–31.2 (Table 2). These larvae were abundant in September 2004at 20.7–24.8 8C and salinity 19.6–29.1 (Fig. 5E).

3.3.13. Chaetognaths

Their abundance (and biomass) was 0–664 ind. m�3 (0–0.4 mg C m�3), and they were present at 4.2–28.6 8C and salinity4.1–33.3 (Table 2). They were abundant in September 2004 andfrom December 2004 to March 2005 at 4.3–25.4 8C and salinity10.4–31.8 (Fig. 5F).

3.4. Correlations between the biomass of the major mesozooplankton

taxa and environmental factors in Masan Bay

The biomass of copepods was significantly positively correlatedwith salinity, pH, DO, and the concentration of NH4, but negativelycorrelated with water temperature and the concentration of SiO2

(Table 3A). In addition, the biomass of cladocerans was signifi-cantly positively correlated with salinity and the concentration ofNH4, but negatively correlated with water temperature. However,

Table 3Correlations between mesozooplankton groups and physical, chemical, and biological factors in Masan Bay, Korea from June 1, 2004 to May 31, 2005.

A. Physical and chemical factors

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

Copepods �0.557** 0.324** 0.151** �0.227** 0.124* 0.329**

Cladocerans �0.149** 0.180** 0.125*

Larvae of invertebrates 0.168** 0.132* �0.277**

Others 0.185**

B. Biological factors

Components DIA PTD EUG CRY RAP HB CYA PNF PE TP HTD TC NC HNF

Copepods 0.342** �0.122* �0.217** �0.143*

Cladocerans 0.119* 0.116*

Larvae of invertebrates

Others

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

diatoms, PTD: phototrophic dinoflagellates, EUG: euglenophytes, CRY: cryptophytes, RAP: raphidophytes, HB: heterotrophic bacteria: CYA: cyanobacteria, PNF: phototrophic

nanoflagellats, PE: picoeukaryotes, TP: total phototrophic plankton, HTD: heterotrophic dinoflagellates, TC: tintinnid ciliates, NC: naked ciliates, HNF: heterotrophic

nanoflagellates.* p < 0.05.** p < 0.01.

J.S. Kim et al. / Harmful Algae 30S (2013) S102–S113 S107

the biomass of invertebrate larvae was significantly positivelycorrelated with water temperature and precipitation, but nega-tively correlated with DO.

The biomass of copepods was significantly positively correlatedwith the biomass of phototrophic dinoflagellates, but negativelycorrelated with the biomass of cryptophytes, picoeukaryotes, andheterotrophic bacteria (Table 3B). At the species level, the biomassof Acartia omorii/Acartia hongii, Calanus sinicus, Centropages

abdominalis, and Paracalanus indicus was significantly positivelycorrelated with the biomass of the phototrophic dinoflagellatesHeterocapsa triquetra and Prorocentrum minimum, whereas bio-mass of Oithona similis and Podon polyphemoides was significantlypositively correlated with the biomass of Prorocentrum minimum

(Table 4).The biomass of cladocerans was significantly positively

correlated with the biomass of phototrophic dinoflagellates andeuglenophytes. At the species level, the biomass of Evadne

tergestina was significantly positively correlated with that ofProrocentrum micans, Scrippsiella trochoidea, Eutrepsiella gymnas-

tica, cryptophytes, heterotrophoic bacteria, and phototrophicnanoflagellates (Table 4). Furthermore, the biomass of Penilia

avirostris was significantly positively correlated with that of thephototrophic dinoflagellate Akashiwo sanguinea and cryptophytes,but negatively correlated with that of Prorocentrum minimum.

3.5. Grazing impact by mesozooplankton on red-tide organisms

Acartia spp. and the polychaete larva Polydora sp. are known tofeed on Prorocentrum minimum (Kim, 2005; Song, 2007). When theabundances of P. minimum and co-occurring Acartia spp. were 1–27,157 cells ml�1 and 0.001–45.7 ind. l�1, respectively, the calcu-lated grazing coefficients attributable to Acartia spp. on co-occurring P. minimum were 0.00001–0.083 d�1 (i.e., up to 7.9% ofthe population of P. minimum was removed by Acartia in 1 day)(Fig. 6; Table 5). In addition, when the abundances of P. minimum

and co-occurring Polydora spp. were 1–16,068 cells ml�1 and0.001–3.4 ind. l�1, respectively, the calculated grazing coefficientsattributable to Polydora sp. on co-occurring P. minimum were0.000002–0.212 d�1 (i.e., up to 19.1% of the population of P.

minimum was removed by Polydora in 1 day) (Fig. 6). Therefore, thecombined calculated grazing coefficient attributable to Acartia spp.and Polydora sp. on co-occurring P. minimum was 0.00001–0.218 d�1 (i.e., up to 20.2% of the population of P. minimum wasremoved by Acartia and Polydora, combined, in 1 day) (Fig. 6).

Acartia spp. are known to feed on Skeletonema costatum

(Deason, 1980). When the abundances of S. costatum and co-occurring Acartia spp. were 4–59,143 cells ml�1 and 0.001–28.1 ind. l�1, respectively, the calculated grazing coefficientsattributable to Acartia spp. on co-occurring S. costatum were0.00001–0.042 d�1 (i.e., up to 4.1% of the population of S. costatum

was removed by Acartia in 1 day) (Fig. 7; Table 5).Acartia spp. are known to feed on Heterocapsa triquetra (Kim,

2005). When the abundances of H. triquetra and co-occurringAcartia spp. were 1–10,243 cells ml�1 and 0.001–45.7 ind. l�1,respectively, the calculated grazing coefficients attributable toAcartia spp. on co-occurring H. triquetra were 0.000003–0.034 d�1

(i.e., up to 3.3% of the population of H. triquetra was removed byAcartia in 1 day) (Fig. 8; Table 5).

Acartia spp. are also known to feed on Heterosigma akashiwo

(Kim, 2005). When the abundances of H. akashiwo and co-occurring Acartia spp. were 1–90,000 cells ml�1 and 0.002–12.0 ind. l�1, respectively, the calculated grazing coefficientsattributable to Acartia spp. on co-occurring H. akashiwo were0.000002–0.033 d�1 (i.e., up to 3.2% of the population ofHeterosigma was removed by Acartia in 1 day) (Fig. 9; Table 5).In addition, Polydora sp. is known to feed on H. akashiwo (Song,2007). When the abundances of H. akashiwo and co-occurringPolydora spp. were 1–90,000 cells ml�1 and 0.001–3.6 ind. l�1,respectively, the calculated grazing coefficients attributable toPolydora spp. on co-occurring H. akashiwo were 0.000001–0.011 d�1 (i.e., up to 1.1% of the population of H. akashiwo wasremoved by Polydora in 1 day) (Fig. 9; Table 5). Furthermore, thecombined calculated grazing coefficients attributable to Acartia

spp. and Polydora sp. on co-occurring H. akashiwo were 0.000002–0.033 d�1 (i.e., up to 3.2% of the population of H. akashiwo wasremoved by Acartia and Polydora, combined, in 1 day) (Fig. 9).

Acartia spp. are known to feed on Scrippsiella trochoidea (Kim,2005). When the abundance of S. trochoidea and co-occurringAcartia spp. were 1–243 cells ml�1 and 0.003–18.1 ind. l�1, respec-tively, the calculated grazing coefficients attributable to Acartia

spp. on co-occurring S. trochoidea were 0.00004–0.030 d�1 (i.e., upto 3.0% of the population of S. trochoidea was removed by Acartia in1 day) (Fig. 10; Table 5).

Acartia spp. are known to feed on Cochlodinium polykrikoides

(Kim, 2005). When the abundance of C. polykrikoides and co-occurring Acartia spp. were 2–207 cells ml�1 and 0.004–0.2 ind. l�1, respectively, the calculated grazing coefficients attrib-utable to Acartia spp. on co-occurring C. polykrikoides were

Table 4Correlations between mesozooplankton and potential prey (i.e., phototrophic and heterotrophic protists and bacteria) in Masan Bay, Korea from June 1, 2004 to May 31, 2005.

Components Sc Td Tg As Asp Cf Cp Da Hsp Ht Pmc Pmn

A.omorii/A. hongii 0.346** 0.321**

C. sinicus 0.526** 0.261**

C. abdominalis 0.282** 0.242**

O. similis 0.151**

P. indicus 0.407** 0.311**

P. marinus

Harpacticoid

E. tergestina 0.170**

P. avirostris 0.168** �0.129*

P. polyphemoides 0.211**

Barnacle nauplius 0.199** 0.424** �0.112*

Polychaete larvae 0.279**

Chaetognatha 0.148**

Components Pt St Eg Ha CRY DIA PTD RAP HB CYA PNF PE TP

A.omorii/A. hongii �0.112* 0.301** �0.214** �0.142*

C. sinicus �0.265* 0.340** �0.127*

C. abdominalis 0.228** �0.157**

O. similis 0.133*

P. indicus �0.124* 0.312** �0.201** �0.147** *

P. marinus 0.587**

Harpacticoid

E. tergestina 0.491** 0.242** 0.213** 0.171** 0.140*

P. avirostris 0.176**

P. polyphemoides 0.133* �0.129*

Barnacle nauplius

Polychaete larvae

Chaetognatha �0.113* �0.130* �0.120*

Components Gd + Gm Gg Gs Oo PLDs Pk Pb Et Hf Hl Ta Tt

A.omorii/A. hongii 0.284**

C. sinicus 0.254*

C. abdominalis 0.265**

P. indicus 0.304**

O. similis

P. marinus

Harpacticoid

E. tergestina

P. avirostris 0.119*

P. polyphemoides 0.176** 0.125*

Barnacle nauplius 0.242** 0.450**

Polychaete larvae 0.189** 0.116*

Chaetognatha 0.303** 0.164** 0.327**

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

Dinophysis acuminata, Hsp.: Heterocapsa sp. Ht: H. triquetra, Pmc: Prorocentrum micans, Pmn: P. minimum, Pt: P. triestinum, St: Scrippsiella trochoidea, Eg: Eutreptiella

gymnastica, Ha: Heterosigma akashiwo, CRY: cryptophytes, DIA: diatoms, PTD: phototrophic dinoflagellates, RAP: raphidophytes, HB: heterotrophic bacteria, CYA:

cyanobacteria, PNF: phototrophic nanoflagellats, PE: picoeukaryotes, TP: total phototrophic protists. Gd + Gm: Gyrodinium dominans/G. moestrupii, Gg: Gyrodinium glaucum,

Gs: Gyrodinium spirale, Oo: Oxyphysis oxytoxoides, PLDs: Pfiesteria-like dinoflagellates, Pk: Polyrkikos kofoidii, Pb: Protoperidinium bipes, Et: Eutintinnus tubulosus, Hf:

Helicostomella fusiformis, HI: Helicostomella longa, Ta: Tintinnopsis angustior, Tt: Tintinnopsis tubulosoides.* p < 0.05.** p < 0.01.

J.S. Kim et al. / Harmful Algae 30S (2013) S102–S113S108

0.00003–0.002 d�1 (i.e., up to 0.2% of the population of C.

polykrikoides was removed by Acartia in 1 day) (Fig. 11; Table 5).When the abundance of PLDs and co-occurring Acartia spp.

were 2 to 10,200 cells ml�1 and 0.001 to 20.7 ind. l�1, respectively,the calculated grazing coefficients attributable to Acartia spp. onco-occurring PLDs were 0.00002 to 0.104 d�1 (i.e., up to 9.9% of thepopulation of PLDs was removed by Acartia in 1 day) (Fig. 12;Table 5).

4. Discussion

4.1. Biomass and abundance of mesozooplankton in Masan Bay

The maximum abundance of total mesozooplankton in MasanBay between June 2004 and May 2005 (5.3 � 104 ind. m�3) iscomparable to that found in the northwestern Mediterranean(Calbet, 2001; Table 6). In addition, the maximum abundance ofcopepods in Masan Bay (4.9 � 104 ind. m�3) is comparable to thatin the Pearl River Estuary, China; lower than in Fukuyama Harbor,

Japan and the Newport River Estuary, UK; but higher than in theBalearic Sea off Mallorca (Fulton, 1984; Uye and Liang, 1998; Tanet al., 2004; Table 6). Furthermore, the maximum abundance ofcladocerans in Masan Bay (1.1 � 104 ind. m�3) is higher than in theBalearic Sea off Mallorca or the northeast Mediterranean (Calbet,2001; Puelles et al., 2003; Table 6). In addition, the maximumabundance of polychaete larvae (3.6 � 103 ind. m�3) is comparableto that in the northeast Mediterranean (Calbet, 2001; Table 6).Thus, the maximum abundances of total mesozooplankton and ofthe major subgroups in Masan Bay in the study period are notunusual compared to in other regions.

The peak abundances of total mesozooplankton, copepods, andcladocerans in Masan Bay during the study period were observedin the winter of 2005, unlike most temperate waters where thesetaxa have been observed to be the most abundant between thespring and fall after peaks of phytoplankton (Fulton, 1984; Uye andLiang, 1998; Calbet, 2001; Weikert et al., 2001; Puelles et al., 2003;Tan et al., 2004; Table 5). The physical-chemical properties inMasan Bay from June to August 2004, as compared to those in

Fig. 6. Abundance (AB) of the red-tide dinoflagellate Prorocentum minimum (A), the

copepods Acartia spp. (B), and polychaete larvae (C) in Masan Bay, Korea from June

1, 2004 to May 31, 2005; and the calculated grazing coefficients (g, d�1) attributable

to Acartia spp. (D) and polychaete larvae (E) on P. minimum and their combined

grazing coefficient (F). The data on P. minimum were obtained from Jeong et al.

(2013).

Fig. 8. Abundance (AB) of the red-tide dinoflagellate Heterocapsa triquetra (A) and

the copepods Acartia spp. (B) and the calculated grazing coefficient (g, d�1)

attributable to Acartia spp. on H. triquetra (C) in Masan Bay, Korea from June 1, 2004

to May 31, 2005. The data on H. triquetra were obtained from Jeong et al. (2013).

J.S. Kim et al. / Harmful Algae 30S (2013) S102–S113 S109

January and February 2005, were characterized by (1) higher watertemperature, (2) lower salinity, (3) lower DO concentration, and (4)a similar level of chlorophyll-a. In addition, the biologicalproperties in Masan Bay from June to August 2004, as comparedto those in January and February 2005, included (1) higher bacteriaconcentrations, (2) more diverse red-tide organisms (Akashiwo

Fig. 7. Abundance (AB) of the red-tide diatom Skeletonema costatum (A) and the

copepods Acartia spp. (B); and the calculated grazing coefficient (g, d�1) attributable

to Acartia spp. on co-occurring S. costatum (C) in Masan Bay, Korea from June 1, 2004

to May 31, 2005. The data on S. costatum were obtained from Jeong et al. (2013).

sanguinea, Ceratium furca, Cochlodinium polykrikoides, Dinophysis

acuminata, Prorocentrum triestinum, Prorocentrum minimum, andThalasiosira decipiens all formed red tides in summer 2004, whileonly Heterocapsa triquetra and P. minimum formed red tides inwinter 2005), and (3) a higher biomass of heterotrophic protists.

Many copepod species and taxa (e.g., Acartia omorii/Acartia

hongii, Centropages abdominalis, Corycaeus affinis, Oithona similis,Paracalanus indicus, Psuedodiaptomus marinus, copepodites, andharpacticoids) were present in almost all seasons, while a fewspecies or taxa (e.g., Acartia erythrea, Calanopia thomsoni, andTortanus forcipatus) were present in only one season. Thus, watertemperature may not have a large effect on the presence ofcopepods in Masan Bay. However, low salinity in the summer (4.1–8.5) may eliminate A. omorii/A. hongii, Acartia pacifica, P. indicus,and T. forcipatus, which cannot survive at salinities <10, and also C.

abdominalis and C. sinicus, which cannot survive at salinities <20(Kim et al., 2003). In addition, low DO may affect the abundance ofcopepods because the biomass of copepods had significant positivecorrelations with DO. The lowest DO in the surface water in MasanBay from June to September 2004 was 0.9 mg l�1. Watercirculation inside Masan Bay is known to be restricted becauseit is a semi-closed bay, and this can cause anoxia in water near thebottom (Park and Cho, 2002; Yim et al., 2005; Kim et al., 2012).Several copepods, such as Acartia spp., Centropages spp., Labidocera

spp., and Pseudodiaptomus spp., are known to die at a DO � 0.1–2.0 mg l�1 (Table 7). Thus, low DO in the summer may be partiallyresponsible for the low abundance of copepods. Most red tidesoccurred between June and September 2004 and between Januaryand March 2005 (Jeong et al., 2013) and heterotrophic protistswere also abundant from February to April 2005 (Yoo et al., 2013).In addition, the abundance of potential prey for copepods in thesummer and fall of 2004 was comparable to that in the winter andspring of 2005. Thus, prey availability may not be responsible forthe low abundance of copepods in the summer and fall of 2004, butonly for the high abundance in the winter and spring of 2005.However, red tides dominated by Akashiwo sanguinea, Ceratium

furca, Cochlodinium polykrikoides, Dinophysis acuminata, Prorocen-

trum triestinum, and Heterosigma akashiwo may be harmful to thedominant copepods in Masan Bay, whereas Heterocapsa triquetra

and Prorocentrum minimum may be excellent prey for thecopepods.

Table 5Calculated grazing impacts (GI, d�1) of Acartia spp. and the polychaete larva Polydora sp. 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. Clearance rates measured under the conditions provided in the present study

were corrected using Q10 of 3.2 for Acartia spp. and 3.4 for Polydora sp. (Hansen et al., 1997) because in situ water temperatures sometimes differed from the temperature used

in the laboratory for this experiment (20 8C).

Red-tide organisms Predator GI MIR K1/2 Ref

Prorocentrum minimum Acartia spp. 0.00–0.083 2310 118 Kim (2005)

Polydora sp. 0.00–0.212 1500# Song (2007)

Skeletonema costatum Acartia spp. 0.00–0.042 7618 178 Deason (1980)

Heterocapsa triquetra Acartia spp. 0.00–0.034 4830 1170 Kim (2005)

Heterosigma akashiwo Acartia spp. 0.00–0.033 2550 204 Kim (2005)

Polydora sp. 0.00–0.011 1600# Song (2007)

Scrippsiella trochoidea Acartia spp. 0.00–0.030 10,100 1050 Kim (2005)

Cochlodinium polykrikoides Acartia spp. 0.000–0.002 3040 549 Kim (2005)

PLDsa Acartia spp. 0.00–0.104 3070 140 Jeong et al. (2007b)

MIR: Maximum ingestion rate (ng C grazer�1 d�1). K1/2: prey concentration sustaining 1/2 MIR.a Stoeckeria algicida prey.# The highest ingestion rate at the given prey concentrations (linear regression).

J.S. Kim et al. / Harmful Algae 30S (2013) S102–S113S110

The pattern of seasonal variation in the abundance ofcladocerans in Masan Bay was similar to that for copepods. Atthe species level, Evadne tergestina and Penilia avirostris wereabundant in August and September 2004, whereas Podon poly-

phemoides was abundant in December 2004 and January 2005.Thus, E. tergestina and P. avirostris may tolerate low DO, while P.

polyphemoides may not. E. tergestina and P. avirostris likely have adifferent ecological niche than P. polyphemoides.

Larvae of benthic invertebrates were abundant in Septemberand October 2004. Unlike copepods and cladocerans, the biomass

Fig. 9. Abundance (AB) of the red-tide raphidophyte Heterosigma akashiwo (A), the

copepods Acartia spp. (B), and polychaete larvae (C) in Masan Bay, Korea from June

1, 2004 to May 31, 2005; and the calculated grazing coefficients (g, d�1) attributable

to Acartia spp. (D) and polychaete larvae (E) on H. akashiwo, and their combined

grazing coefficient (F). The data on H. akashiwo were obtained from Jeong et al.

(2013).

of invertebrate larvae was significantly negatively correlated withDO. Therefore, larvae of benthic invertebrates may also be tolerantof low DO.

4.2. Potential predator–prey relationships between the major taxa of

mesozooplankton and red-tide organisms

The biomass of copepods was significantly positively correlatedwith that of phototrophic dinoflagellates, but negatively correlatedwith cryptophytes, picoeukaryotes, and heterotrophic bacteria.This suggests that the copepods in Masan Bay may increase theirpopulations by feeding on phototrophic dinoflagellates, but not onsmall algae and bacteria. Dam et al. (1995) reported severalcopepods and cladocerans feed on prey with a cell size >2 mm. Inaddition, Acartia clausii was able to feed on prey >3 mm (Nival andNival, 1976). Thus, the dominant copepods in Masan Bay are notlikely to feed on these small algae and bacteria. However, smallalgae and bacteria are known to be eaten by diverse phototrophicand heterotrophic dinoflagellates, raphidophytes, and ciliates(Seong et al., 2006; Jeong et al., 2005, 2008, 2010b, 2012; Jeong,2011). Furthermore, these grazers are known to be prey forcopepods (Jeong et al., 2001, 2004b; Roman et al., 2006; Turner,2004, 2006). Thus, the biomass of bacteria and small algae may bepartially transferred to copepods via large, protistan grazers.

Fig. 10. Abundance (AB) of the red-tide dinoflagellate Scrippsiella trochoidea (A) and

the copepods Acartia spp. (B) and the calculated grazing coefficient (g, d�1)

attributable to Acartia spp. on co-occurring S. trochoidea (C) in Masan Bay, Korea

from June 1, 2004 to May 31, 2005. The data on S. trochoidea were obtained from

Jeong et al. (2013).

Fig. 11. Abundance (AB) of the red-tide dinoflagellate Cochlodinium polykrikoides (A)

and the copepods Acartia spp. (B) and the calculated grazing coefficient (g, d�1)

attributable to Acartia spp. on co-occurring C. polykrikoides (C) in Masan Bay, Korea

from June 1, 2004 to May 31, 2005. The data on C. polykrikoides were obtained from

Jeong et al. (2013).

Fig. 12. Abundance (AB) of the heterotrophic Pfiesteria-like dinoflagellates (PLDs, A)

and the copepods Acartia spp. (B) and the calculated grazing coefficients (g, d�1)

attributable to Acartia spp. on PLDs (C) in Masan Bay, Korea from June 1, 2004 to

May 31, 2005. We assumed the ingestion rate of Acartia spp. on the PLDs was the

same as that of A. omori on S. algicida (Jeong et al., 2007b). The data on PLDs were

obtained from Yoo et al. (2013).

J.S. Kim et al. / Harmful Algae 30S (2013) S102–S113 S111

However, the amount of bacterial and small algal biomasstransferred to copepods may not be sufficiently high enough tosupport population growth in copepods.

At the species level, the biomass of Acartia omorii/Acartia hongii,Calanus sinicus, and Paracalanus indicus was significantly positivelycorrelated with the biomass of Heterocapsa triquetra and/orProrocentrum minimum. In addition, the biomass of Centropages

abdominalis was significantly positively correlated with thebiomass of H. triquetra and P. minimum, while Oithona similis

was significantly positively correlated with the biomass of P.

minimum. Acartia spp. and Pseudodiaptomus spp. have been shownto consume these dinoflagellates during feeding experiments(Turner and Anderson, 1983; Uye and Takamatsu, 1990; Besiktepeand Dam, 2002). Thus, these copepods may increase or maintaintheir population by feeding on red-tide organisms in Masan Bay.However, feeding by C. abdominalis, C. sinicus, P. indicus, and O.

similis on H. triquetra and/or P. minimum has yet to be observed, andmerits further investigation.

Table 6The maximum abundance (MA) and biomass (MB) of the major mesozooplankton grou

Taxon Area MA (ind. m�3) MB (mg C

Mesozooplankton Masan Bay, Korea 5.3 � 104 113

Mesozooplankton Newport River Estuary, UK 2.2 � 105

Mesozooplankton NW Mediterraneae 7.8 � 104

Mesozooplankton Levantine Sea, Crete

Mesozooplankton NE Atalntic

Mesozooplankton Balearic Sea, Mallorca 9.0 � 103

Copepod Masan Bay, Korea 4.9 � 104 107

Copepod Fukuyama Harbor, Japan 6.4 � 105 165

Copepod Newport River Estuary, UK 2.2 � 104 48

Copepod NE Atlantic Ocean 1.5 � 105

Copepod Pearl River Estuary, China 4.4 � 104

Copepod NW Mediterranean 2.8 � 104

Copepod Balearic Sea, Mallorca 6.5 � 103

Copepod NE Atlantic Ocean

Cladocerans Masan Bay, Korea 1.1 � 104 16

Cladocerans Balearic Sea, Mallorca 1.0 � 103

Cladocerans NW Mediterraneae 5.7 � 103

Total larvae Masan Bay, Korea 3.7 � 103 16

Polychaete larvae Masan Bay, Korea 3.6 � 103 16

Polychaete larvae NW Mediterraneae 2.6 � 103

Mollusc larvae NW Mediterraneae 1.3 � 103

Cirriped larvae NW Mediterraneae 4.6 � 103

The biomass of cladocerans was significantly positivelycorrelated with that of phototrophic dinoflagellates. In particular,Penilia avirostris was significantly positively correlated withAkashiwo sanguinea, whereas Podon polyphemoides was signifi-cantly positively correlated with Prorocentrum minimum. Inaddition, Evadne tergestina was significantly positively correlatedwith Eutreptiella gymnastica, Prorocentrum micans, Scrippsiella

trochoidea, cryptophytes, heterotrophoic bacteria, and photo-trophic nanoflagellates. Kim et al. (1989) reported that phyto-plankton <35 mm in size, including Prorocentrum spp. andCeratium sp., were found in the guts of 5 marine cladoceranspecies—Evadne nordmanni, E. tergestina, P. avirostris, Pseudodaph-

nella leuckarti, and P. polyphemoides—in the Inland Sea of Japan. Inaddition, several studies reported feeding by cladocerans ondinoflagellates (Bainbridge, 1958; Morey-Gaines, 1979; White,1980). Thus, an abundance of phototrophic dinoflagellates mayincrease the population of cladocerans in Masan Bay.

ps in temperate waters and the month when the MA occurred.

m�3) MB (mg C m�2) Peak Ref

January This study

July Fulton (1984)

January Calbet (2001)

2.9 � 104 June Weikert et al. (2001)

2.8 � 104 Spring Koppelmann and Weikert (1999)

December Puelles et al. (2003)

January This study

Jun. Uye and Liang (1998)

July Fulton (1984)

July Gallienne and Robins (2001)

July Tan et al. (2004)

April Calbet (2001)

February Puelles et al. (2003)

2.4 � 104 Spring Koppelmann and Weikert (1999)

January This study

February Puelles et al. (2003)

August Calbet (2001)

September This study

September This study

January Calbet (2001)

January Calbet (2001)

January Calbet (2001)

Table 7The lower limits of dissolved oxygen concentration (mg l�1) at which mesozoo-

plankton species can survive.

Taxon DO Ref.

Acartia clausi <2.0 Kouassi et al. (2001)

Acartia tonsa 0.9 Stalder and Marcus (1997)

Acartia spp. <0.1 Saltzman and Wishner (1997)

Centropages hamatus <2.0 Stalder and Marcus (1997)

Centropages sp. <0.1 Saltzman and Wishner (1997)

Corycaeus spp. <0.1 Saltzman and Wishner (1997)

Labidocera aestiva 2.0 Stalder and Marcus (1997)

Oithona spp. <0.1 Saltzman and Wishner (1997)

Paracalanus sp. <0.1 Saltzman and Wishner (1997)

Pseudodiaptomus hessei <2.0 Kouassi et al. (2001)

J.S. Kim et al. / Harmful Algae 30S (2013) S102–S113S112

4.3. Grazing impact by mesozooplankton on red-tide organisms

The calculated grazing coefficient attributable to Acartia spp. onco-occurring Pfiesteria-like dinoflagellates (PLDs) was relativelyhigh (0.104 d�1), whereas that on co-occurring Prorocentrum

minimum was moderate (0.083 d�1), while grazing coefficientson Heterocapsa triquetra, Scrippsiella trochoidea, Skeletonema

costatum, and Heterosigma akashiwo were relatively low (0.030–0.042 d�1) (Table 5). Further, the calculated grazing coefficientsattributable to Acartia spp. on co-occurring Cochlodinium poly-

krikoides were almost negligible (0.002 d�1). Therefore, grazing byAcartia spp. copepods in Masan Bay may sometimes have aconsiderable impact on populations of P. minimum and PLDs, amoderate impact on populations of H. triquetra, S. trochoidea, S.

costatum, and H. akashiwo, and a negligible impact on populationsof C. polykrikoides. PLDs are known to feed on H. akashiwo (Jeonget al., 2005, 2006, 2007a) and are, in turn, prey for copepods (Jeonget al., 2007b). Thus, the biomass of H. akashiwo can be transferredto copepods via PLDs in Masan Bay. In addition, the calculatedgrazing coefficient attributable to Polydora spp. on co-occurring P.

minimum was high (0.212 d�1), while that on co-occurring H.

akashiwo was negligible (0.011 d�1). The results of this studysuggest that the mortality rate of P. minimum due to grazing bymesozooplankton in Masan Bay may sometimes be considerable,but that of H. akashiwo may be very low. Therefore, it is critical toexamine predation by mesozooplankton on red-tide dinoflagel-lates to understand the dynamics of red tides in Masan Bay.

Acknowledgements

We thank Kyung Ha Lee and Jong Woo Park for technicalsupport. This paper was supported by the National ResearchFoundation/MSICTFP (NRF-C1ABA001-2010-0020702), Mid-careerResearcher Program (2012-R1A2A201-010987) and EcologicalDisturbance Research Program and Long-term change of structureand function in marine ecosystems of Korea program, KoreaInstitute of Marine Science & Technology Promotion/Ministry ofOceans and Fisheries award to HJ Jeong.[TS]

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