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 delimitation of species when cells extend after an initial cell division (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 Syvertsen 1996, Rivera et al. 2003). These are arranged into ligule-closed and linear-half bands with horizontal punctate striae. Only species from the polar regions have resting 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 (Gomez and Souissi 2007). In Korea, previous studies have reported only the illustrations or species checklist without light micrographs, illustrations and descriptions 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.
Samples were collected at 24 sites with 20 μm meshsized 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, Japan) 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 Diatoms, Kiel (Anonymous 1975), and recent terminology follows Hasle and Syvertsen (1996).
This research described the characteristics of the genus 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
Suborder Biddulphiineae Simonsen 1979
Family Biddulphiaceae Kutzing 1844
Subfamily Hemiauloideae Jouse (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
Eucampia zodiacus f. cylindrocornis Syvertsen in Syvertsen and Hasle 1983
Eucampia zodiacus var. cornigera Grunow in Van Heurck 1882
[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.
Basionym. Moelleria cornuta Cleve (1873).
Synonym. Moelleria 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 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 Moelleria cornuta Cleve (1873), but Grunow (Van Heurck 1882) transferred this species to the genus Eucampia with recombined 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.
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. Aperture almost circular to rounded rectangular. Aperture 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 reported 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, because 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).
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 helicalcoiled 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 originally described from Cuxhaven in the North Sea of Germany (Ehrenberg 1839). This species was recorded from the North Atlantic Ocean (Hustedt 1930, Crosby and Wood 1958), the east coast of Africa (Hendey 1937), Alaska 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.
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 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.
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 represent the initial cell state as E. zodiacus f. zodiacus.
E. zodiacus f. zodiacus has no resting stage in life cycle, 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. cornigera 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.
species differ with respect to the length and shape of their elevations (Table 2).
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 parallel 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 distributed 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).
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 between 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 Tempere and Peragallo (1915) reported this species from Bohuslavice 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.
The major key characteristics of the genus Eucampia are cell size, ocellus, elevations, colony, areolae and aperture shape (Table 2). E. cornuta and E. zodiacus f. cylindrocornis 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 almost 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. zodiacus has radial ribs and large central area in ocellus characteristics, unlike linear ribs of E. groenlandica. E. zodiacus var. cornigera has broad, long, and truncated conical elevations that include radial ribs and small central area. Especially, 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 circular to rounded rectangular form. E. zodiacus has narrow and elliptical to rounded rectangular and lanceolate form. E. zodiacus f. cylindrocornis has almost rectangular 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.
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 single labiate process, however on the marginal valve face
[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).
(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 pervalvar 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. groenlandica 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 distinguishing characteristic as opposed to their cell size ratio.
In this study, E. cornuta was recorded during most seasons 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 including 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. cornigera was identified based on its long conical shape elevations 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 sizerange and other characteristics are noticeable features.
