Morphological study of the genus Eucampia (Bacillariophyceae) in Korean coastal waters

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http://dx.doi.org/10.4490/algae.2012.27.4.235 Open Access

Morphological study of the genus Eucampia (Bacillariophyceae) in Korean coastal waters

Jun Mo Lee

^1,2

and Jin Hwan Lee

^1,

*

1Department of Life Science, Sangmyung University, Seoul 110-743, Korea

2Global Bioresources Research Center, Korea Institute of Ocean Science & Technology, Ansan 426-744, Korea

Regardless of continuous researches, recent researches on the genus Eucampia (Bacillariophyceae) have focused mainly on E. zodiacus f. zodiacus In the present study, species of the genus Eucampia have been studied based on their morphological characteristics. Eucampia species were collected at 24 sites from July 2008 to June 2011 in Korean coastal waters. Species were mainly identified based on the shape of valve, ocellus, and aperture, along with the length and shape of the bipolar elevations. As a result, five Eucampia species were identified: Eucampia cornuta, E. groenlandica, E.

zodiacus f. zodiacus, E. zodiacus f. cylindrocornis, and E. zodiacus var. cornigera. E. cornuta and E. groenlandica have long pervalvar axis length, but the others display short or moderate length. Ocellus shape of E. cornuta, E. groenlandica and E. zodiacus f. cylindrocornis are linear ribs, whereas E. zodiacus f. zodiacus and E. zodiacus var. cornigera have radial ribs with central area. E. cornuta and E. zodiacus f. cylindrocornis have long and narrow cylindrical elevations. E. groenlandica and E. zodiacus f. zodiacus have short and broad elevations with blunt tips. E. zodiacus var. cornigera has long and broad conical elevations. In terms of aperture shape, E. cornuta has large elliptical form, E. groenlandica has almost circular to rounded rectangular form, E. zodiacus f. zodiacus has narrow and elliptical rounded rectangular to a narrow lanceolate form, E. zodiacus f. cylindrocornis has almost rectangular form, and E. zodiacus var. cornigera has rounded rhombic form.

On the basis of elevations in broad girdle view, 5 Eucampia taxa could be divided into 3 types: ‘narrow H type’, E. cornuta and E. groenlandica; ‘regular H type’, E. zodiacus f. cylindrocornis and E. zodiacus var. cornigera (partial); ‘wide H type’, E.

zodiacus f. zodiacus (almost).

Key Words: diagnosis; diatoms; distribution; Eucampia; morphology

INTRODUCTION

The genus Eucampia Ehrenberg is a common marine genus that was established by Ehrenberg in 1839 from the North Sea of Germany. The morphological features of this genus are as follows: bipolar frustules with elliptical valve face, without raphe or pseudoraphe (Hustedt 1930), discoid plastids (Round et al. 1990), bipolar elevations with ocellus (Syvertsen and Hasle 1983), and curved colony formations (Cupp 1943, Kokubo 1955, Hasle and

Syvertsen 1996). In general, aperture shape between cells is taken into consideration for the systematic delimita- tion of species when cells extend after an initial cell di- vision (Hustedt 1930). A single labiate process is located on the central or marginal inter-valve face. The areolae form on the cribra in valve face (Willis et al. 2010). The girdle consists of many intercalary bands (Hasle and Sy- vertsen 1996, Rivera et al. 2003). These are arranged into

Received September 8, 2012, Accepted November 10, 2012

*

Corresponding Author E-mail: jhlee@smu.ac.kr

Tel: +82-2-2287-5152, Fax: +82-2-2287-0098 This is an Open Access article distributed under the terms of the

Creative Commons Attribution Non-Commercial License (http://cre- ativecommons.org/licenses/by-nc/3.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

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MATERIALS AND METHODS

Samples were collected at 24 sites with 20 µm mesh- sized plankton nets and van Dorn Water Sampler from July 2008 to June 2011 in Korean coastal waters (Table 1).

For light microscopic (LM, Axioskop 40; Zeiss, Jena, Germany and Nikon E 80i; Nikon, Tokyo, Japan) and scanning electron microscopic (SEM, JSM-5600LV; Jeol, Ja- pan) examinations, field samples were rinsed and organic materials removed by a modified method (Hendey 1964, Hasle and Fryxell 1970, Hendey and Sims 1984). For LM observations, specimens were mounted on a slide glass using Pleurax. For SEM observations, specimens were placed on cleaned aluminum stubs and the stubs were subsequently sputter-coated with gold-palladium.

Terminology used herein is recommended by the first report of the working committee on Diatom Terminology from the 3rd Symposium on Recent and Fossil Marine Di- atoms, Kiel (Anonymous 1975), and recent terminology follows Hasle and Syvertsen (1996).

ligule-closed and linear-half bands with horizontal punc- tate striae. Only species from the polar regions have rest- ing spores, e.g., Eucampia antarctica (Fryxell and Prasad 1990, Hasle and Syvertsen 1996). The thickness of their cell wall changes with season (Fryxell 1991). Currently, eight species of the genus Eucampia have been reported around the world (Van Landingham 1969, Fryxell and Prasad 1990, Rivera et al. 2003).

Irrespective of these researches, many taxonomic problems have ensured. For instance, other species of genus Eucampia can be misidentified as E. zodiacus f.

zodiacus because there is the possibility of incorrectly discriminated in this genus during routine microscopic observations (Gómez and Souissi 2007). In Korea, previous studies have reported only the illustrations or species checklist without light micrographs, illustrations and de- scriptions for the species in this genus, although species were frequently recorded (Lee 1995).

Additionally, species of Eucampia isolated from Korea lack detailed and comparative study of their morphological features. Thus, the purpose of this study is to provide detailed morphological characteristics by means of numerical value for species identification.

Table 1.

Sample collection sites in Korean coastal waters

No. Date Location Latitude (N) Longitude (E)

1 Jul 26, 2008 Incheon coast 37°14.032 126°19.224

2 Jan 21, 2009 Yeong-il Bay 35°59.839 129°27.479

3 Jan 23, 2009 Jeongdongjin coast 37°41.163 129°02.570

4 Feb 16, 2009 Pusan Harbor 35°08.317 129°06.867

5 May 3, 2009 Daecheon coast 36°19.645 126°30.594

6 Jul 25, 2009 Oido Is. 37°20.730 126°41.181

7 Aug 17, 2009 Incheon coast 37°14.032 126°19.224

8 Aug 29, 2009 Geum River estuary 35°58.688 126°37.588

9 Sep 12, 2009 Jeju Is. 33°30.281 126°27.633

10 Jan 12, 2010 Mokpo Bay 35°05.359 126°09.441

11 Jan 28, 2010 Sumun coast 34°37.879 127°01.949

12 Jan 28, 2010 Deokheung coast 34°31.495 127°27.724

13 Jan 29, 2010 Yeoja Bay 34°47.981 127°33.527

14 Jan 29, 2010 Yeosu coast 34°44.339 127°39.008

15 Jan 30, 2010 Jinhae Bay 35°04.052 128°37.736

16 Jan 31, 2010 Pusan Harbor 35°06.659 129°04.182

17 Apr 23, 2010 Yeongnang Lake 38°12.530 128°34.140

18 Jul 22, 2010 Oido Is. 37°19.572 126°39.282

19 Jul 22, 2010 Asan Bay 37°06.951 126°40.618

20 Jul 24, 2010 Saemangeum Seawall 35°43.670 126°31.759

21 Oct 11, 2010 Jinhae Bay 35°04.052 128°37.736

22 Oct 14, 2010 Wolgot estuary 37°23.247 126°44.413

23 Oct 15, 2010 Man-gyeong River 35°53.180 126°43.653

24 Jun 9, 2011 Hoejin estuary 34°28.843 126°56.460

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Suborder Biddulphiineae Simonsen 1979 Family Biddulphiaceae Kützing 1844

Subfamily Hemiauloideae Jousé (Kiselev and Poretskii) 1949

Genus Eucampia Ehrenberg 1839

Eucampia cornuta (Cleve) Grunow in Van Heurck 1882

Eucampia groenlandica Cleve 1896

Eucampia zodiacus f. zodiacus Ehrenberg 1839

RESULTS

This research described the characteristics of the ge- nus Eucampia (Table 2). According to Simonsen (1979) system, the systematic accounts of five Eucampia taxa were as follows:

Class Bacillariophyceae Haeckel 1878 Order Centrales Hustedt 1930

Table 2.

Comparisons of the morphological and numerical characteristics of Eucampia species Characteristics

Species

E. cornuta E. groenlandica E. zodiacus E. zodiacus

f. cylindrocornis E. zodiacus var. cornigera Cell AA length (µm) 18.2 (11.5-27.1)

(n = 23) 21.3 (15.5-31.0)

(n = 11) 41.2 (21.8-67.9)

(n = 164) 30.3 (20.0-42.9)

(n = 37) 22.9 (10.7-32.2) (n = 42) PA length (µm) 34.6 (15.3-44.4)

(n = 22) 31.9 (27.5-42.2)

(n = 10) 16.9 (3.9-31.2)

(n = 151) 15.9 (7.1-27.7)

(n = 33) 13.3 (4.3-23.2) (n = 31) AA length, PA length

ratio 1 : 1.9 (1.3-2.8)

(n = 22) 1 : 1.5 (1.3-1.9)

(n = 10) 1 : 0.4 (0.1-1.1)

(n = 149) 1 : 0.5 (0.2-0.9)

(n = 33) 1 : 0.6 (0.2-0.9) (n = 26)

Valve face Concave Concave or

almost flat Slightly concave Almost flat Concave

Elevations Shape Narrow, long Broad, short Broad, short Narrow, long Broad, long

Characteristic Cylindrical Risen tips Risen blunt tips Cylindrical Truncated conical

Colony Form Most slightly

curved Most slightly

curved Helical coiled Comparatively

curved Most slightly

curved

Ocellus Shape Linear ribs Linear ribs Radial ribs with

large central area

Linear ribs Radial ribs with small central pore field

DM (µm) 2.3 (0.8-3.3)

(n = 28) 3.5 (1.8-5.2)

(n = 18) 6.0 (3.1-10.6)

(n = 197) 2.3 (0.7-3.8)

(n = 56) 3.2 (2.2-6.2) (n = 47) Rib length (µm) 0.9 (0.6-1.1)

(n = 5) 1.1 (1.0-1.3)

(n = 7) 1.3 (0.8-2.4)

(n = 43) 1.0 (0.8-1.3)

(n = 18) 0.9 (0.8-1.0) (n = 5) Rib count 26 (20-29)

(n = 5) 30.7 (27-38)

(n = 7) 53.9 (36-80)

(n = 42) 25.9 (20-36)

(n = 18) 29.2 (26-34) (n = 4) Labiate

process Location Depressed valve

central Central Depressed valve

central Central Central

Aperture Shape Large elliptical Almost circular to rounded rectangle

Narrow and rounded rectangle to narrow lanceolate

Almost

rectangle Rounded

rhombic

Distance (µm) 19.3 (11.7-24.4)

(n = 14) 10.9 (6.7-16.2)

(n = 12) 10.5 (3.8-15.8)

(n = 113) 17.1 (7.9-24.3)

(n = 13) 16.8 (8.6-22.6) (n = 22) Areolae Valve in 10 μm 24.1 (20-28)

(n = 11) 22.3 (20-24)

(n = 7) 20.3 (16-25)

(n = 52) 23.4 (20-30)

(n = 19) 25.6 (20-30) (n = 17) Girdle puncta in

10 μm 47.8 (44-52)

(n = 9) 43.2 (40-48)

(n = 5) 38.7 (34-50)

(n = 39) 44.6 (36-54)

(n = 14) 46.2 (42-50) (n = 6) AA, apical axis; PA, pervalvar axis; DM, diameter.

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Basionym. Möelleria cornuta Cleve (1873).

Synonym. Möelleria cornuta Cleve (1873).

Original description. Van Heurck 1882, Pls 104-132, 22bis, 82bis, 83bis, 83ter, 95bis.

Morphology. Cells curved in the broad girdle view.

Valve face concave. Apical axis 11.5-27.1 µm long and pervalvar axis 15.3-44.4 µm long. The ratio of apical to Eucampia zodiacus f. cylindrocornis Syvertsen

in Syvertsen and Hasle 1983

Eucampia zodiacus var. cornigera Grunow in Van Heurck 1882

Eucampia cornuta (Cleve) Grunow in Van Heurck, 1882 (Fig. 1)

A

C D

B

E F

Fig. 1.

Eucampia cornuta. (A) Colony form with several small plastids, light microscopy (LM). (B) Two-celled colony, large elliptical aperture shape, LM. (C) Long and narrow cylindrical elevations, scanning electron microscopy (SEM). (D) Intercalary bands with rows of puncta, SEM. (E) Ocellus with linear ribs, SEM. (F) Labiate process on valve face in the internal view, SEM. Scale bars represent: A & B, 10 µm; C & F, 1 µm; D & E, 2 µm.

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distance between cells 6.7-16.2 µm. Intercalary band collar-shaped with 40-48 horizontal puncta per 10 µm.

Distribution. Eucampia groenlandica was first report- ed from Baffins Bay in Davis Strait (Cleve 1896). Since then, this species was recorded from North Atlantic fjords of Scandinavia in western Scotland (Halem 1903), the coasts of Norway and Denmark (Hendey 1964) and the northern cold water regions (Hasle and Syvertsen 1996).

In Korea, Eucampia groenlandica was recorded from Kyonggi Bay (Choi 1982), Jeju Island (Lee and Choa 1990).

In the present study, this species was found on Jul 26, 2008 in Incheon, May 3, 2009 in Daecheon Coast, Jul 25, 2009 on Oido Is., Aug 29, 2009 in Geum River estuary, Jan 28, 2010 in Deokheung Coast, Jan 29, 2010 in Yeoja Bay, Jan 30, 2010 in Jinhae Bay and Jun 9, 2011 in Hoejin estuary (Table 1).

Remarks. Hustedt (1930) regarded E. groenlandica as a synonym of E. zodiacus f. zodiacus, because of its size variations. Hendey (1964) disputed about this view, be- cause E. groenlandica has less robust elevations and a long pervalvar axis length unlike E. zodiacus f. zodiacus.

Hasle and Syvertsen (1996) mentioned that these two taxa could be distinguished based on their elevations characteristics and aperture shapes. The colony form of E. groenlandica rarely showed a helical chain (Hasle and Syvertsen 1996).

Eucampia zodiacus f. zodiacus Ehrenberg, 1839 (Fig. 3)

Synonym. E. britannica Smith (1856), E. virginica Grunow in Van Heurck (1882), E. nodosa Schmidt (1888).

Original description. Ehrenberg 1839, pp. 1-94.

Morphology. Rectangular cells formed by helical- coiled chains. Chains curved in the broad girdle view.

Valve face slightly concave. Apical axis 21.8-67.9 µm long and pervalvar axis 3.9-31.2 µm long. The ratio of apical to pervalvar axis about 1 : 0.4. Elevations broad and short with risen, blunt tips. Ocellus with radial ribs and large central area, 3.1-10.6 µm in diameter. Rib of ocellus 0.8- 2.4 µm in length. Number of ribs 36-80 on each ocellus. A single labiate process located on the depressed central inner valve face. Number of areolae 16-25 per 10 µm in the valve face. Apertures narrow, round rectangular to narrow lanceolate aligning with apical axis. Aperture distance between cells 3.8-15.8 µm. Intercalary band collar-shaped with 34-50 horizontal puncta per 10 µm.

Distribution. Eucampia zodiacus f. zodiacus was origi- nally described from Cuxhaven in the North Sea of Ger- many (Ehrenberg 1839). This species was recorded from pervalvar axis about 1 : 1.9. Elevations narrow and long

cylindrical. Ocellus with linear ribs. Ocellus 0.8-3.3 µm in diameter. Rib of ocellus 0.6-1.1 µm in length. Number of ribs 20-29 on each ocellus. A single labiate process located on the depressed central inner valve face. Number of areolae 20-28 per 10 µm in the valve face. Aperture large and elliptical, and aperture distance between cells 11.7- 22.4 µm. Intercalary bands collar-shaped with 44-52 horizontal puncta per 10 µm.

Distribution. Eucampia cornuta was first described from the Sea of Java in Indonesia (Cleve 1873). This species was also found in Red Sea and Malay Archipelago (Ostenfeld 1902), the European regions of Atlantic Ocean (Hustedt 1930, Subrahmanyan 1946), the coast of Africa (Hendey 1937), and Sandy Cape to Montague Is. and St.

Vincent Gulf (Crosby and Wood 1958).

In Korea, Eucampia cornuta was recorded from South Sea (Park 1956), Soo-Young Bay (Choe 1969), Kyonggi Bay (Chung et al. 1969), Nakdong River (Lee 1973) and Korea Strait (Shim and Lee 1983). In the present study, this species was found on Jan 31, 2010 at Pusan Harbor, Jul 22, 2010 on Oido Is., and Oct 11, 2010 in Jinhae Bay (Table 1).

Remarks. E. cornuta was originally described as Möel- leria cornuta Cleve (1873), but Grunow (Van Heurck 1882) transferred this species to the genus Eucampia with re- combined nomenclature of Eucampia cornuta. Many authors agreed with Grunow’s view based on narrow elevations and long pervalvar axis with distinct intercalary bands (Hustedt 1930, Hendey 1937, Cupp 1943). Crosby and Wood (1958) mentioned that aperture of E. cornuta was oval, and Hasle and Syvertsen (1996) added ocellus illustration in their description of E. cornuta.

Both E. cornuta and E. zodiacus f. cylindrocornis have cylindrical elevations (Table 2), but the former differs from latter with respect to a large and elliptical aperture, and a long pervalvar axis length, respectively.

Eucampia groenlandica Cleve, 1896 (Fig. 2)

Original description. Cleve 1896, pp. 1-22.

Morphology. Cells slightly curved in the broad girdle view. Valve face concave or almost flat. Apical axis 15.5- 31.0 µm long and pervalvar axis 27.5-42.2 µm long. The ratio of apical to pervalvar axis about 1 : 1.5. Elevations broad and short with risen tips. Ocellus with linear ribs, 1.8-5.2 µm in diameter. Rib of ocellus 1.0-1.3 µm in length. Number of ribs 27-38 on each ocellus. A single labiate process located on the central inner valve face.

Number of areolae 20-24 per 10 µm in the valve face. Ap- erture almost circular to rounded rectangular. Aperture

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in polar waters (Hasle and Syvertsen 1996).

Eucampia zodiacus f. zodiacus was recorded from all parts of Korean coastal waters (Lee 1995). In this study, this species was recorded frequently in Korean coastal waters; Jul 26, 2008 in Incheon coasts, Jan 21, 2009 in Yeongil Bay, Feb 16, 2009 in Pusan Harbor, May 3, 2009 the North Atlantic Ocean (Hustedt 1930, Crosby and

Wood 1958), the east coast of Africa (Hendey 1937), Alas- ka coasts (Cupp 1943), and all parts of North Sea (Smith 1856, Halem 1903, Brandt and Apstein 1908, Hendey 1964). Hendey (1964) reported that it is widely distributed all around the world, but this species is probably absent

Fig. 2.

Eucampia groenlandica. (A) Two-celled colony form, cells slightly curved chain with several plastids, light microscopy (LM). (B) Almost circular to rounded rectangular aperture shape, LM. (C) Short and broad elevations with form of risen tips, labiate process (arrow) on the internal valve center, scanning electron microscopy (SEM). (D) Intercalary bands with rows of puncta, SEM. (E) Ocellus with linear ribs, SEM. (F) Labiate process, SEM. Scale bars represent: A, 20 µm; B, 10 µm; C, 5 µm; D-F, 1 µm.

A

C D

B

E F

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in Jinhae Bay, Oct 14, 2010 in Wolgot estuary, and Oct 15, 2010 in Mangyeong River estuary (Table 1).

Remarks. Hustedt (1930) mentioned that E. britannica (Smith 1856) and E. nodosa (Schmidt 1888) were synonyms of E. zodiacus f. zodiacus because these two taxa were rep- resent the initial cell state as E. zodiacus f. zodiacus.

in Daecheon coast, Jul 25, 2009 on Oido Is., Aug 29, 2009 in Geum River estuary, Jan 12, 2010 in Mokpo Bay, Jan 28, 2010 in Sumun coast, Jan 28, 2010 in Deokheung coast, Jan 29, 2010 in Yeoja Bay, Jan 29, 2010 in Yeosu coast, Jan 30, 2010 in Jinhae Bay, Jan 31, 2010 in Pusan Harbor, Apr 23, 2010 on the periphery of Yeongnang Lake, Oct 11, 2010

Fig. 3.

Eucampia zodiacus. (A) Colony formation, light microscopy (LM). (B) Partial colony, narrow and rounded rectangular aperture shape, LM.

(C) Short and broad elevations with risen blunt tips, labiate process (arrow) on the internal valve center, scanning electron microscopy (SEM). (D) Intercalary bands with rows of puncta, SEM. (E) Ocellus with radial ribs and large central area, SEM. (F) Labiate process, SEM. Scale bars represent: A, 20 µm; B, 10 µm; C, 5 µm; D-F, 1 µm.

A

C D

B

E F

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species differ with respect to the length and shape of their elevations (Table 2).

Eucampia zodiacus f. cylindrocornis Syvertsen in Syvertsen and Hasle, 1983 (Fig. 4)

E. zodiacus f. zodiacus has no resting stage in life cy- cle, or resting period is much shorter than that of other diatom species possessing resting stage (Nishikawa et al. 2007). E. zodiacus f. zodiacus has radial ribs and large central area in ocellus characteristics. E. zodiacus var. cor- nigera has similar ocellus characteristics, but, these two

Fig. 4.

Eucampia zodiacus f. cylindrocornis. (A) Solitary cell with rectangular form in broad girdle view, light microscopy (LM). (B) Two-celled chain, almost rectangular aperture shape, LM. (C) Long and narrow cylindrical elevations, labiate process on the valve center, scanning electron microscopy (SEM). (D) Intercalary bands with rows of puncta, SEM. (E) Ocellus with linear ribs, SEM. (F) Labiate process, SEM. Scale bars represent:

A & B, 10 µm; C, 5 µm; D, 2 µm; E & F, 1 µm.

A

C D

B

E F

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tween cells 8.6-22.6 µm. Intercalary band collar-shaped with 42-50 horizontal puncta per 10 µm.

Distribution. Eucampia zodiacus var. cornigera was first reported from Japan (Van Heurck 1882) and Tempère and Peragallo (1915) reported this species from Bohuslav- ice in Czechoslovakia.

Eucampia zodiacus var. cornigera was found in the coastal and the brackish water ecosystems such as coasts, bays and estuaries. This species was recorded on Jul 26, 2008 in Incheon coast, May 3, 2009 in Daecheon coast, Aug 29, 2009 in Geum River estuary, Apr 23, 2010 on the periphery of Yeongnang Lake, Jul 22, 2010 in Asan Bay, Jul 24, 2010 at Saemangeum Seawall, Oct 11, 2010 in Jinhae Bay, Oct 14, 2010 in Wolgot estuary and Oct 15, 2010 in Man-gyeong River estuary (Table 1). This study reports the first record for E. zodiacus var. cornigera in Korean coastal waters.

Remarks. Grunow (Van Heurck 1882) distinguished E.

zodiacus f. zodiacus from E. zodiacus var. cornigera based on the shape of elevations. E. zodiacus var. cornigera was described, however, only with the aid of LM observations (Van Heurck 1882). In this study, these two taxa were separated based on the shape and length of their elevations, and the fine structure of ocellus (Table 2). This study is the first to report the fine structure of ocellus in this species.

DISCUSSION

The major key characteristics of the genus Eucampia are cell size, ocellus, elevations, colony, areolae and ap- erture shape (Table 2). E. cornuta and E. zodiacus f. cyl- indrocornis have narrow, long, and cylindrical elevations, however, they differ with respect to their aperture and cell shapes. E. cornuta has large elliptical aperture and long pervalvar axis length. E. zodiacus f. cylindrocornis has al- most rectangular aperture and cell with long apical axis length. E. groenlandica and E. zodiacus f. zodiacus have broad, short, and risen tip elevations. E. zodiacus f. zodia- cus has radial ribs and large central area in ocellus charac- teristics, unlike linear ribs of E. groenlandica. E. zodiacus var. cornigera has broad, long, and truncated conical ele- vations that include radial ribs and small central area. Es- pecially, this characteristic of conical elevations is distinct from cylindrical elevations. The cylindrical elevations are straightly extended from each pole. However, conical elevations are extended from the central valve face and each pole. Aperture shape existed in various forms. E. cornuta has large elliptical form. E. groenlandica has almost cir- Original description. Syvertsen and Hasle 1983, pp.

169-210.

Morphology. Colony comparatively curved in the broad girdle view. Valve face almost flat. Apical axis 20.0- 42.9 µm long and pervalvar axis 7.1-27.7 µm long. The ratio of apical to pervalvar axis about 1 : 0.5. Elevations narrow and long cylindrical, and separated from conical elevations. Ocellus with linear ribs, 0.7-3.8 µm in diameter. Rib of ocellus 0.8-1.3 µm in length. Number of ribs 20- 36 on each ocellus. A single labiate process located on the central inner valve face. Number of areolae 20-30 per 10 µm in the valve face. Aperture almost rectangle and paral- lel to apical axis. Aperture distance between cells 7.9-24.3 µm. Intercalary band collar-shaped with 36-54 horizontal puncta per 10 µm.

Distribution. Eucampia zodiacus f. cylindrocronis was originally reported from tropical and subtropical areas of Ubatuba in Brazil (Syvertsen and Hasle 1983).

Eucampia zodiacus f. cylindrocronis was widely dis- tributed in Korean coastal waters; Jul 26, 2008 in Incheon coast, Jan 23, 2009 in Jeongdongjin coast, May 3, 2009 in Daecheon coast, Jul 25, 2009 on Oido Is., Aug 17, 2009 in Incheon coast, Aug 29, 2009 in Geum River estuary, Sep 12, 2009 on Jeju Is., Jan 31, 2010 at Pusan Harbor, Jul 22, 2010 on Oido Is., Jul 22, 2010 in Asan Bay, Jul 24, 2010 at Saemangeum Seawall, Oct 11, 2010 in Jinhae Bay and Oct 15, 2010 in Mangyeong River estuary (Table 1).

Remarks. E. zodiacus f. cylindrocornis was nominated as forma of E. zodiacus f. zodiacus based in the differences of its long and narrow cylindrical elevations (Syvertsen and Hasle 1983). This species is incorrectly marked as E. zodiacus f. cylindricornis (Hasle and Syvertsen 1996, Crosbie and Furnas 2001).

Eucampia zodiacus var. cornigera Grunow in Van Heurck, 1882 (Fig. 5)

Original description. Van Heurck 1882, Pls 104-132, 22bis, 82bis, 83bis, 83ter, 95bis.

Morphology. Colony curved in the broad girdle view.

Valve face concave. Apical axis 10.7-32.2 µm long and pervalvar axis 4.3-23.2 µm long. The ratio of apical to pervalvar axis about 1 : 0.6. Elevations broad and long with a truncated conical form, and it separated from cylindrical elevations. Ocellus with radial ribs and small central area. Ocellus 2.2-6.2 µm in diameter. Rib of ocellus 0.8- 1.0 µm in length. Number of rib 26-34 on each ocellus.

Single labiate process located on the central inner valve face. Number of areolae 20-30 per 10 µm in the valve face.

Aperture shape rounded rhombic. Aperture distance be-

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this, aperture form of sufficiently developed cells rather than initial developing cells should be considered. These five species have a single labiate process that is centrally located on the inter-valve face. As for the other species of the genus Eucampia from polar regions also have a sin- gle labiate process, however on the marginal valve face cular to rounded rectangular form. E. zodiacus has nar-

row and elliptical to rounded rectangular and lanceolate form. E. zodiacus f. cylindrocornis has almost rectangu- lar form. E. zodiacus var. cornigera has elliptical rhombic form (Table 2). Furthermore, aperture form is subject to considerable variability with respect to cell cycle. To avoid

Fig. 5.

Eucampia zodiacus var. cornigera. (A) Solitary cell, labiate process on the valve center, light microscopy (LM). (B) Three-celled colony, rounded rhombic aperture shape, LM. (C) Long and broad conical elevations, scanning electron microscopy (SEM). (D) Intercalary bands with rows of puncta, SEM. (E) Ocellus with radial ribs, SEM. (F) Labiate process, SEM. Scale bars represent: A & B, 10 µm; C, 5 µm; D & E, 2 µm; F, 1 µm.

A

C D

B

E F

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ing E. cornuta, E. groenlandica, E. zodiacus f. zodiacus, and E. zodiacus f. cylindrocornis were previously recorded (Lee 1995). E. zodiacus var. cornigera is a newly recorded species in Korean coastal waters. E. zodiacus var. cornig- era was identified based on its long conical shape eleva- tions and ocellus characteristics with radial ribs.

As a result of this research, major key characteristics of the genus Eucampia are shape of aperture and elevations, and ocellus characteristics. If ocellus characteristics are not recognizable, characteristics of elevations are very important for identification. In addition, ratio of cell size- range and other characteristics are noticeable features.

ACKNOWLEDGEMENTS

This research was supported by Sangmyung University in 2011. The quthors convey their gratitude to all those helped with sample collections and technical assistanc- es during this study, Dr. S. W. Jung in Library of Marine Samples of Korea Institute of Ocean Science & Technol- ogy (KIOST) and Mrs. J. S. Park, and S. D. Lee, Department of Life Science, Sangmyung University, Korea.

REFERENCES

Anonymous. 1975. Proposals for a standardization of diatom terminology and diagnoses. Nova Hedwigia Beih.

53:323-354.

Brandt, K. A. H. & Apstein, C. H. 1908. Nordisches plankton.

Lipsius and Tischer, Botanischer Teil, Kiel and Leipzig, pp. 98-99.

Choe, J. S. 1969. Seasonal changes in abundance and composition of diatoms in the Suyung Bay, Pusan. Bull. Korean Fish. Soc. 2:16-24.

Choi, J. K. 1982. On the phytoplanktonic community structure of the Kyunggi Bay, Yellow Sea, in autumn season.

Bull. Inst. Basic Sci. Inha Univ. 3:169-176.

Chung, Y. H., Shim, J. H. & Lee, M. J. 1969. Studies on the water pollution and productivity in Kyunggi-Bay in summer season (3): classification of the phytoplankton (I).

Rep. IBP Korean Natl. Comm. 3:3-16.

Cleve, P. T. 1873. Examination of diatoms found on the sur- face of the Sea of Java. Bihang K. Svenska Vet.-Akad.

Handlingar 1:1-13.

Cleve, P. T. 1896. Diatoms from Baffin Bay and Davis Strait.

Bihang K. Svenska Vet.-Akad. Handlingar 22:1-22.

Crosbie, N. D. & Furnas, M. J. 2001. Net growth rates of pico- cyanobacteria and nano-/microphytoplankton inhabit- (Hasle and Syvertsen 1996).

Five taxa of the genus Eucampia could be divided into three types (Fig. 6). “Narrow H type” including E. cornuta and E. groenlandica has about 1.5-2 times longer perval- var axis length than apcial axis length. “Regular H type”

including E. zodiacus f. cylindrocornis and E. zodiacus var.

cornigera appear almost square with respect to size ratio of the cell, because this type has long elevations although pervalvar axis length is shorter than apical axis length.

“Wide H type” including E. zodiacus f. zodiacus has short elevations and pervalvar axis length. These three types support the previous vague description of E. groenland- ica as having a long pervalvar axis (Hendey 1937). With regard to the “regular H type” and “wide H type” groups, elevations characteristics are considered species distin- guishing characteristic as opposed to their cell size ratio.

In this study, E. cornuta was recorded during most sea- sons except spring. This species is frequently found in the Kuroshio Current water that is known to strongly influence Korean coastal waters both in summer and winter.

E. groenlandica was previously reported from the Yellow Sea and South Sea (Lee 1995). E. zodiacus f. zodiacus, E.

zodiacus f. cylindrocornis, and E. zodiacus var. cornigera were widely distributed in all the sampled location of the Korean coastal waters. However, E. zodiacus var. cornigera was reported only from brackish waters ecosystems such as bays and estuaries.

This research provides a list of five Eucampia species in Korean coastal waters. Among them, four species includ-

Apical axis Length (µm)

0 10 20 30 40 50 60 70 80

Pervalvar axis Length (µm)

0 10 20 30 40 50

1 1

1 1 1 1

2 2 2 2

2

3 3

3 3 3

3

33

4

4 4 4

4 4

4 5 5

5

5 5

5

1 2

4 3 5

Narrow H type

Regular H type

Wide H type

Fig. 6.

Size variations of apical axis and pervalvar axis of Eucampia species. 1, E. cornuta, “narrow H type”; 2, E. groenlandica, “narrow H type”; 3, E. zodiacus f. zodiacus, almost “wide H type” or some “regular H type”; 4, E. zodiacus f. cylindrocornis, “regular H type”; 5, E. zodiacus var. cornigera, “regular H type” (Underlined numbers show an average of cell size).

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biete. In Rabenhorst, L. (Ed.) Kryptogamen-Flora von Deutschlands, Österreich und der Schweiz. Akademische Verlagsgesellschaft m. b. h., Leipzig, pp. 1-920.

Jousé, A. P. 1949. Algae Diatomaceae Aetatis Supernecreta- ceae Ex Arenis Argillaceis Systematis Fluminis Bolscoy Aktay in Declivitate Orientali Ural Borealis. Bot. Mater.

Otd. Sporov. Rast. Bot. Inst. Komarova Akad. Nauk SSSR 6:65-78.

Kokubo, S. 1955. Plankton diatoms. Nihon Kakujutsu, Tokyo, 330 pp (in Japanese).

Kützing, F. T. 1844. Die kieselschaligen Bacillarien oder Diato- meen. W. Ktihne, Nordhausen, 152 pp.

Lee, J. B. & Choa, J. H. 1990. The dynamics of phytoplankton communities at Hanrim and Songsan harbor of Cheju Island, Korea. Bull. Mar. Res. Inst. Cheju Nat. Univ. 14:9- 24.

Lee, J. C. 1973. Studies on the influence of water quality of sa- line sensitive estuaries of Nak-dong River to microflora.

Korean J. Limnol. 6:1-12.

Lee, J. H. 1995. Additional check-list of marine planktonic algae in the coastal waters of Korea. I. Bacillariophyceae. J.

Nat. Sci. Sangmyung Women’s Univ. 2:71-198.

Nishikawa, T., Hori, Y., Tanida, K. & Imai, I. 2007. Population dynamics of the harmful diatom Eucampia zodiacus Eh- renberg causing bleaching of Porphyra thalli in aquacul- ture in Harima-Nada, the Seto Inland Sea, Japan. Harm- ful Algae 6:763-773.

Ostenfeld, C. H. 1902. Marine plankton diatoms. Bot. Tidsskr.

25:219-245.

Park, T. S. 1956. A study on the quantity and composition of microplankton at the southern sea of Korea in Summer, 1956. Bull. Pusan Fish. Coll. 1:13-32.

Rivera, P., Avaria, S. & Cruces, F. 2003. The family Hemiau- laceae (Bacillariophyceae) from marine Chilean waters.

Rev. Chil. Hist. Nat. 76:651-664.

Round, F. E., Crawford, R. M. & Mann, D. G. 1990. The dia- toms: biology and morpholgy of the genera. Cambridge University Press, Cambridge, 747 pp.

Schmidt, A. 1888. Atlas der Diatomaceen-kunde. Series III (Heft 35-36). Fues’s Verlag (R. Reisland), Leipzig, 480 pp.

Shim, J. H. & Lee, W. H. 1983. Plankton study in the south- eastern sea of Korea (I). Phytoplankton distribution in September, 1981. J. Oceanol. Soc. Korea 18:91-103.

Simonsen, R. 1979. The diatom system: ideas on phylogeny.

Bacillaria 2:9-71.

Smith, W. 1856. A synopsis of the British Diatomaceae: with remarks on their structure, functions and distribution, and instructions for collecting and preserving specimens.

Vol. 2. John Van Voorst, London, 107 pp.

Subrahmanyan, R. 1946. A systematic account of the marine ing shelf waters of the central (17°S) and southern (20°S)

Great Barrier Reef. Aquat. Microb. Ecol. 24:209-224.

Crosby, L. H. & Wood, E. J. F. 1958. Studies on Australian and New Zealand Diatoms. I. Planktonic and allied species.

Trans. R. Soc. N. Z. 85:483-530.

Cupp, E. E. 1943. Marine plankton diatoms of the west coast of North America. Bull. Scripps Inst. Oceanogr. Univ. Ca- lif. 5:1-238.

Ehrenberg, C. G. 1839. Über nach jetzt zahlreiche lebende Thierarten der Kreidebildung und den Organismus der Polythalamien. Abhandlungen der königlichen Akad- emie der Wissenschaften zu, Berlin, 94 pp.

Fryxell, G. A. 1991. Comparison of winter and summer growth stages of the diatom Eucampia antarctica from the kerguelen plateau and south of the Antarctic conver- gence zone. In Barron, J., Larsen, B., et al. (Eds.) Proc.

Ocean Drilling Program, Sci. Results, Vol. 119, Ocean Drilling Program, College Station, TX, pp. 675-685.

Fryxell, G. A. & Prasad, A. K. S. K. 1990. Eucampia antarctica var. recta (Mangin) stat. nov. (Biddulphiaceae, Bacillari- ophyceae): life stages at the Weddell Sea ice edge. Phy- cologia 29:27-38.

Gómez, F. & Souissi, S. 2007. Unusual diatoms linked to cli- matic events in the northeastern English Channel. J. Sea Res. 58:283-290.

Haeckel, E. 1878. Das protistenreich. Eine populäre uebersi- cht über das formengebiet der niedersten lebewesen. Mit einem wissenschaftlichen anhange: system der protisten.

Ernst Günther’s Verlag, Leipzig, 104 pp.

Halem, G. A. v. 1903. Abhandlungen Naturwissenschaftlichen Verein zu Bremen. Vol. 17. Nabu Press, Verlag, 402 pp.

Hasle, G. R. & Fryxell, G. A. 1970. Diatoms: cleaning and mounting for light and electron microscopy. Trans. Am.

Microsc. Soc. 89:469-474.

Hasle, G. R. & Syvertsen, E. E. 1996. Marine diatoms. In To- mas C. R. (Ed.) Identifying Marine Phytoplankton. Aca- demic Press, San Diego, CA, pp. 5-385.

Hendey, N. I. 1937. The Plankton diatoms of the southern seas. Discovery reports. Vol. 16. Institute of Oceanograph- ic Sciences (Great Britain), Cambridge University Press, London, pp. 151-364.

Hendey, N. I. 1964. An introductory accout of the smaller al- gae of British coastal waters. Part V. Bacillariopyhyceae (Diatoms). Her Majesty’s Stationary Office, London, 317 pp.

Hendey, N. I. & Sims, P. A. 1984. Some new or unusual eco- cene Biddulphioid diatoms, I. Bacillaria 7:59-90.

Hustedt, F. 1930. Die Kieselalgen Deutschlands, Österreichs und der Schweiz unter Berücksichtigung der übrigen Länder Europas sowie der angrenzenden Meeresge-

(13)

83bis, 83ter, 95bis.

Van Landingham, S. L. 1969. Catalogue of the fossil and recent genera and species of diatoms and their synonyms, Part III. Coscinophaena through Fibula. 3301. Verlag von J.

Cramer, Lehre, pp. 1087-1756.

Willis, L., Page, K. M., Broomhead, D. S. & Cox, E. J. 2010. Dis- crete free-boundary reaction-diffusion model of diatom pore occlusions. Plant Ecol. Evol. 143:297-306.

plankton diatoms of the Madras Coast. Proc. Indian Acad. Sci. B 24:85-197.

Syvertsen, E. E. & Hasle, G. R. 1983. The diatom genus Eu- campia: morphology and taxonomy. Bacillaria 6:169- 210.

Tempère, J. & Peragallo, H. 1915. Diatomées du Monde Entier, Edition 2. Tables. Chez J. Tempère, Arcachon, pp. 1-68.

Van Heurck, H. 1882. Synopsis des diatomées de Belgique.

Atlas. Ducaju & Cie, Anvers, Pls. 104-132, 22bis, 82bis,