INTRODUCTION
Marine benthic dinoflagellates have been paid attention in terms of microalgal monitoring due to potentially harmful benthic species which lead to the economic loss by killing fish/shellfish through toxic blooms and subsequently human health especially in subtropical to tropical coastal areas (Hallegraeff 1993; Gilbert et al. 2005). Benthic dinoflagellates are known to be present in tropical and subtropical regions of the Pacific Ocean, Indian Ocean, and the Caribbean where they are found to be associated with seagrasses, macroalgae and sediments (Fukuyo 1981; Morton and Faust 1997; Aligizaki et al. 2008; Almazán-Becerril et al. 2015). Recently some species are also found in temperate regions (Pistocchi et al. 2011; Selina and Levchenko 2011; Shah et al. 2013). Several benthic dinoflagellates species of the genera Ostreopsis, Coolia, Prorocentrum, and Amphidinium are known to be potentially toxic (Fukuyo 1981; Besada et al. 1982; Faust 1995; Mohammad-Noor et al. 2007).
Previously, the toxic dinoflagellates recorded from Korean temperate waters were planktonic, but potentially toxic benthic sand dwelling and epiphytic dinoflagellates have not been well documented. To date, no toxic event caused by a marine benthic dinoflagellate has been reported from Jeju Island. Since Kim et al. (2011), Jeong et al. (2012a, b), Kang et al. (2013) and Lim et al. (2013) described 6 benthic epiphytic dinoflagellates in the coast of Jeju Island, Shah et al. (2013) added 37 benthic dinoflagellates from the Jeju coastal beach through two years of intensive survey. A research searching for unrecorded indigenous species, which has not been described taxonomically in Korea, has been done as part of projects by NIBR from 2006. This study clarify additionally 5 species belonging to 4 genera with the respects of classification and easy taxonomical key based on Light Microscope (LM) criteria.
MATERIALS AND METHODS
Samplings were done at intertidal zone of sandy beach in Korea as well as Jeju Island from January 2015 to April 2017. Samples of sand sediment were collected on sandy beaches using a spatula. The samples were transferred to plastic bottles with seawater. The samples were incubated and then isolated by picking method and fixed with formaldehyde (final concentration of 1%) or glutaraldehyde (final concentration of about 1%). Benthic dinoflagellates were identified by using LM (Axioplan, Carl Zeiss, Oberkochen, Germany). To make slide specimens for one species, the dinoflagellate samples were washed with distilled water and then the method described in Kim et al. (2013) was followed.
For identification, a monograph of Hoppenrath et al. (2014) reported from different areas were mainly used. Classification for the new combinations of the family Dinophysiales familia incertae sedis, Gymnodiniaceae, Peridiniales incertae sedis and Prorocentraceae was cited from AlgaeBase (http:// www.algaebase.org) (Guiry and Guiry 2018).
RESULTS AND DISCUSSION
A total of 36 species of 4 genera (Sinophysis, Bispinodinium, Cabra and Prorocentrum) belonging to the family Dinophysiales familia incertae sedis, Gymnodiniaceae, Peridiniales incertae sedis and Prorocentraceae from Korean coastal beach were identified and classified in the checklist based on valid name as below. Five species were described as newly recorded species in Korean waters. The newly recorded are marked with asterisks (*), ‘C’ indicates a currently accepted name, ‘S’ a synonym based on the species database of AlgaeBase (Guiry and Guiry 2018), respectively.
Checklist of the genus Sinophysis, Bispinodinium, Cabra and Prorocentrum occurred in Korea Waters
Class Dinophyceae West et Fritsch
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Order Dinophysiales Kofoid
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Family Dinophysiales familia incertae sedis
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Genus Sinophysis Nie et Wang
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* Sinophysis canaliculata Quod, Ten-Hage, Turquet, Mascarell et Couté C
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Order Gymnodiniales Apstein
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Family Gymnodiniaceae Lankester
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Genus Bispinodinium Yamada et Horiguchi
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*Bispinodinium angelaceum Yamada et Horiguchi C
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Order Peridiniales Haeckel
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Family Peridiniales incertae sedis
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Genus Cabra Murray et Patterson
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*Cabra armorica Chomérat, Couté et Nézan C
Cabra matta Murray et Patterson C
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Order Prorocentrales Lemmermann
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Family Prorocentraceae Stein
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Genus Prorocentrum Ehrenberg
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Prorocentrum aporum (Schiller) Dodge C
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Prorocentrum arcuatum Issel C
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Prorocentrum balticum (Lohmann) Loeblich Ⅲ C
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*Prorocentrum bimaculatum Chomérat et Saburova C
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Prorocentrum clipeus Hoppenrath C
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Prorocentrum compressum (Bailey) Abé ex Dodge S =Tryblionella compressa (Bailey) Poulin C
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Prorocentrum concavum Fukuyo C
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Prorocentrum cordatum (Ostenfeld) Dodge C =Prorocentrum minimum (Pavillard) Schiller S
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Prorocentrum cornutum Schiller C
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Prorocentrum dactylus (Stein) Dodge C
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Prorocentrum dentatum Stein C
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Prorocentrum emarginatum Fukuyo C
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Prorocentrum fukuyoi Murray et Nagahama C
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Prorocenturm gracile Schütt C =Prorocentrum sigmoides Böhm S
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Prorocentrum hoffmannianum Faust C =Prorocentrum belizeanum Fasut S
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Prorocentrum koreanum Han, Cho et Wang C
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Prorocentrum leve Faust, Kibler, Vandersea, Tester et Litaker C
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Prorocentrum lima (Ehrenberg) Stein C
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Prorocentrum maculosum Faust C
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Prorocentrum mexicanum Osorio-Tafall C
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Prorocentrum micans Ehrenberg C
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Prorocentrum nanum Schiller C
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Prorocentrum oblongum (Schiller) Taylor C
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Prorocentrum rhathymum Loeblich III, Sherley et Schmidt C
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Prorocentrum rostratum Stein C
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Prorocentrum ruetzleranum Faust C
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Prorocentrum scutellum Schröder C
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Prorocentrum sipadanensis Mohammad-Noor, Daugbjerg et Moestrup C
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Prorocentrum triestinum Schiller C
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Prorocentrum tropicale Faust C
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* Prorocentrum tsawwassenense Hoppenrath et Leander C
Taxonomic description of unrecorded dinoflagellates
Genus Sinophysis Nie et Wang 1944
Holotype species:Sinophysis microcephala Nie et Wang.
Description: Medium-sized (35-45 μm) laterally compressed dinoflagellate, circular to subcircular in lateral view. Thecal plates are covered by many areolae. It has a very small epicone, separated by a well-developed cingulum from the large hypocone with a well-developed sulcus which does not reach the antapex. It has 2 pairs of channeled and paralled projections, possesses a large apical pore. No chloroplasts (Guiry and Guiry 2018).
Numbers of names and species: There are 9 species names in the database at present, of which 9 have been flagged as accepted taxonomically (Guiry and Guiry 2018).
Sinophysis canaliculata Quod, Ten-Hage, Turquet, Mascarell et Couté 1999 (Fig. 1a and b)
Synonym: No synonym.
References: Hoppenrath et al. 2014. p. 165. figs. 77A, 78A-C, 79A and B.
Specimen examined: Serial No. LJB2017001.
Description: Cells are almost spherical and compressed. The relatively large, dome shape epitheca has two parallel anterior projection. The hypotheca is slightly elongated and posteriorly rounded. Cingulum is relatively deep and wide. Sulcus is present on the right side and covers about twothirds of the cell length.
Size: 45-57 μm long, 37-51 μm wide in the apical view.
Sampling: Jan. 2015. Sa-gye beach in Jeju Island (33°13ʹ 53.12ʺ N, 126°18ʹ38.22ʺ E).
Habitat: Marine species.
Distribution: Atlantic Islands: Canary Islands (García- Portela et al. 2017); North America: Mexico (Caribbean) (Almazán-Becerril et al. 2015); South America: Brazil (Diniz et al. 2017); Asia: Japan (García-Portela et al. 2017). Note: This species was reported as an unrecorded indigenous species by NIBR in 2017 and reported as a newly recorded species in the coastal waters of Korea in the present study.
Genus Bispinodinium Yamada et Horiguchi 2013
Holotype species:Bispinodium angelaceum Yamada et Horiguchi.
Description:Amphidinium-like athecate photosynthetic dinonflagellate. Cells composed of a short epicone and a large hypocone. The cingulum completely encircling the cell. (Hoppenrath 2014).
Numbers of names and species: There is only one species or infraspecific name in the database at present, which has been flagged as accepted taxonomically (Guiry and Guiry 2018).
Bispinodinium angelaceum Yamada et Horiguchi 2013 (Fig. 1c)
Synonym: No synonym.
Specimen examined: Serial No. LJB2015003.
Description: Cells are almost oval and athecate dinoflagellates. The epicone is triangle and the hypocone is oval. The ventral and dorsal side is flattened. The cingulum is located at about one-third of the total cell length. The sulcus is straight, narrow and extends antapex. The nucleus is spherical and is located in the middle of the hypocone. Chloroplasts exist.
Size: 30-42 μm long, 25-33 μm wide in the lateral view.
Sampling: Jul. 2015. Hamduk beach in Jeju Island (33° 32ʹ36.11ʺ N, 126°40ʹ4.98ʺ E).
Habitat: Marine species.
Distribution: Japan (Yamada et al. 2013).
Note: This species was reported as an unrecorded indigenous species by NIBR in 2017 and reported as a newly recorded species in the coastal waters of Korea in the present study.
Genus Cabra Murray et Patterson 2004
Holotype species:Cabra matta Murray et Patterson.
Description: Medium sized (30-55 μm) sand-dwelling dinoflagellates. Cells are strongly compressed and asymmetric, appearing different from the left as compared to the right side. Heterotrophic thecal plates are more or less pentagonal and irregular in lateral view. The cingulum is markedly ascending (Hoppenrath et al. 2014).
Numbers of names and species: There are 4 species names in the database at present, of which 4 have been flagged as accepted taxonomically (Guiry and Guiry 2018).
Cabra armorica Chomérat, Couté et Nézan 2010 (Fig. 1d and e)
Synonym: No synonym.
References: Hoppenrath et al. 2014. p. 74, figs. 29A-C, 30A-F.
Specimen examined: Serial No. LJB2016011.
Description: Cells are polygonal. Thecal plates are areolate shallowly depressions. The hypotheca is larger than the epitheca. The plate of hypotheca 2’’’ and 4’’’ makes up 4 multidiscipline shaped cells, separated by ridges. The apical pore is hook shape but extends to the dorsal left side of cells.
Size: 37-40 μm long, 31-38 μm wide in the lateral view.
Sampling: Jul. 2016. Sinyang beach in Jeju Island (33° 26ʹ6.63ʺ N, 126°55ʹ30.07ʺ E).
Habitat: Marine species.
Distribution: France (Chomérat et al. 2010).
Note: This species was reported as an unrecorded indigenous species by NIBR in 2017 and reported as a newly recorded species in the coastal waters of Korea in the present study.
Genus Prorocentrum Ehrenberg 1834
Holotype species:Prorocentrum micans Ehrenberg.
Description: Small to medium sized (15-100 μm) bilateral thecate dinoflagellates with 2 apical heterodynamic flagella. The shape is globular, lanceolate or oval. Thecal plates are composed of two smooth valve-shaped plates with pores or spines. Both flagella emerge from one pore. In the flagellar region are an additional 7-14 small plates (Guiry and Guiry 2018).
Numbers of names and species: There are 119 species names in the database at present, as well as 4 infraspecific names. Of the species names, 75 have been flagged as accepted taxonomically (Guiry and Guiry 2018).
Prorocentrum bimaculatum Chomérat et Saburova 2012 (Fig. 1f and g)
Synonym: No synonym.
References: Hoppenrath et al. 2014. p. 135, figs. 62, 64A.
Specimen examined: Serial No. LJB2017010.
Description: Cells are long oval. The surface of the plate is exceptionally smooth with tiny pores. The two cingular areas are located above and below the center without a pore. The periflagellar area is wide V-shaped with a short collar. Size: 50-55 μm long, 38-43 μm wide in lateral view.
Sampling: Apr. 2017. Wangsan beach in Incheon (37° 27ʹ20.97ʺ N, 126°22ʹ17.67ʺ E).
Habitat: Marine species.
Distribution: South-west Asia: Kuwait (Chomérat et al. 2012).
Note: This species was reported as an unrecorded indigenous species by NIBR in 2017 and reported as a newly recorded species in the coastal waters of Korea in the present study.
Prorocentrum tsawwassenense Hoppenrath et Leander 2008 (Fig. 1h-k)
Synonym: No synonym.
References: Hoppenrath et al. 2014. p. 152, fig. 63.
Specimen examined: Serial No. LJB2017011.
Description: Cells are oval. The surface of thecal plate has large pores as radial row, and the center of the plate is smooth and pores don’t exist. The periflagellar area is wide U-shaped, with collar.
Size: 40-55 μm long, 30-48 μm wide in lateral view.
Sampling: Apr. 2017. Wangsan beach in Incheon (37° 27ʹ20.97ʺ N, 126°22ʹ17.67ʺ E).
Habitat: Marine species.
Distribution: North America: British Columbia (Hoppenenrath and Leander 2008; Chomérat et al. 2011).
Note: This species was reported as an unrecorded indigenous species by NIBR in 2017 and reported as a newly recorded species in the coastal waters of Korea in the present study.