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Morphology and taxonomy of the Aphanizomenon spp. (Cyanophyceae) and related species in the Nakdong River, South Korea
© The Author(s) 2017
Received: 22 September 2016
Accepted: 6 December 2016
Published: 24 December 2016
The purpose of this study is to describe the morphological characteristics of the Aphanizomenon spp. and related species from the natural samples collected in the Nakdong River of South Korea.
Morphological characteristics in the four species classified into the genera Aphanizomenon Morren ex Bornet et Flahault 1888 and Cuspidothrix Rajaniemi et al. 2005 were observed by light microscopy. The following four taxa were identified: Aphanizomenon flos-aquae Ralfs ex Bornet et Flahault, Aphanizomenon klebahnii Elenkin ex Pechar, Aphanizomenon skujae Komárková-Legnerová et Cronberg, and Cuspidothrix issatschenkoi (Usačev) Rajaniemi et al. Aph. flos-aquae and Aph. klebahnii always formed in fascicles; the others only occurred in solitary. Aph. flos-aquae was similar to Aph. klebahnii, whereas these species differed from each other by the size and shape of fascicles, which was macroscopic in Aph. flos-aquae and microscopic in the Aph. klebahnii. One of their characteristics was that trichomes are easily disintegrating during microscopic examination. C. issatschenkoi could be clearly distinguished from other species by hair-shaped terminal cell. Its terminal cell was almost hyaline and markedly pointed. Young populations of the species without heterocytes run a risk of a misidentification. Aph. skujae was characterized by akinete. Morphological variability of akinetes from natural samples collected in the Nakdong River was rather smaller than those reported by previous study.
C. issatschenkoi are described for the first time in the Nakdong River. In addition, Aph. klebahnii and Aph. skujae are new to South Korea.
The genus Aphanizomenon Morren ex Bornet et Flahault 1888 (type species: Aph. flos-aquae) belongs to order Nostocales and family Nostocaceae, which has a worldwide distribution (Rajaniemi et al. 2005a). The species of genus Aphanizomenon and several of its members have been described as the cause for harmful bloom (Mcdonald and Lehman 2013; Ma et al. 2015). Some species can produce hepatotoxic and neurotoxic, such as aphantoxin, anatoxin-a, cylindrospermopsin, and saxitoxin, cyanobacterial secondary metabolites which can cause critical problems (Paerl and Huisman 2009; Ballot et al. 2010; Zhang et al. 2015). Therefore, it is very important for the accurate species identification of Aphanizomenon because of water bloom with several toxin-producing species (Guzmán-Guillén et al. 2015).
In the Nakdong River, Microcystis and Anabaena have been considered as the representative bloom-forming cyanobacteria genera (Yu et al. 2014). After the construction of eight weirs, the number of its bloom has been recently growing in mid-upperstream (Ryu et al. 2016). Nevertheless, two Aphanizomenon floras (Aph. flos-aquae and Aph. issatschenkoi) have been described until a recent date (Park 2004) in South Korea; only one Aphanizomenon species has been reported in the ecological study of Nakdong River: Aph. flos-aquae (Choi et al. 2007; Yu et al. 2014). Recent studies using polyphasic approach, e.g., involving morphology but also ecology and phylogenetics, have revealed that the genus Apohanizomenon is in reality very heterogeneous (Cirés and Ballot 2016). According to newly defined approach, 22 taxa identified and described throughout the world have been assigned to the new genera Aphanizomenon (e.g., Aph. flos-aquae Ralfs ex Bornet et Flahault), Cuspidothrix (e.g., former Aph. issatschenkoi (Usačev) Proshkina-Lavrenko), Sphaerospermopsis (e.g., former Aphanizomenon aphanizomenoides (Forti) Hortobágyi and Komárek), Chrysosporum (e.g., former Aphanizomenon ovalisporum Forti), Anabaena/Aphanizomenon like (e.g., Aphanizomenon gracile (Lemmermann) Lemmermann), and Anabaena-like group (e.g., Aphanizomenon volzii (Lemmermann) Komárek) (Lyra et al. 2001; Gugger et al. 2002; Rajaniemi et al. 2005b; Komárek and Komárková 2006; Zapomĕlová et al. 2012; Komárek 2013).
The classification of genus Aphanizomenon which frequently form blooms is in some cases difficult that is due to lack of the study for morphology and taxonomy in South Korea. The purpose of this study is to describe the morphological characteristics of the Aphanizomenon spp. and related species from the natural samples collected in the Nakdong River, South Korea.
Results and discussion
Within the genus Aphanizomenon, three clusters were distinguished by Komárek and Komárková (2006) and Komárek (2013) for classification. The first cluster (i) included the type species Aph. flos-aquae Ralfs ex Bornet et Flahault 1888 and Aphanizomenon klebahnii Elenkin ex Pechar 2008, together with Aph. yezoense, Aph. paraflexuosum, Aph. flexuosum, Aph. solvenicum, Aph. platense, and Aph. hungaricum. Trichomes of Aph. flos-aquae and Aph. klebahnii taxa always formed macroscopic and microscopic fascicles, and those were able to cause intensive water blooms in eutrophic stagnant water (Hindák 2000). Aph. flos-aquae was common species with Microcystis spp. and Anabeana spp. and the major component of the water bloom in the Nakdong River (Park et al. 2015; Yu et al. 2014). Whereas Aph. klebahnii was described for the first time in the South Korea. Cluster (ii) included species with slightly curved or flexuous trichomes. The terminal cells were narrowed, elongated, and hyaline with sharply pointed. Akinetes were distant to heterocytes. This cluster included Cuspidothrix issatschenkoi (Usačev) Rajaniemi et al. 2005, together with C. elenkinii, Aph. tropicalis, Aph. capricorni, and Aph. ussatchevii. C. issatschenkoi was described for the first time in the Nakdong River. Cluster (iii) was comprised of species described as morphotype of Aphanizomenon gracile with straight, solitary trichomes and with narrowed ends, which belong into the vicinity of Dolichospermum according to molecular sequences. Aph. skujae Komárková-Legnerová et Cronberg 1992 belonged to this cluster, together with Aph. gracile, Aph. Schindleri, Aph. manguinii, Aph. chinense, and Aph. sphaericum. Identification of the species is the first report in South Korea.
Diacritical morphological characteristics of four Aphanizomenon taxa reviewed from natural samples collected in the Nakdong River
Band-like, up to 2 cm long, straight or bent, often grouped in fascicles
Elongated cylindrical, not narrowed, without aerotopes, almost hyaline
Cylindrical to slightly barrel-shaped, 4.0–12.1 × 3.6–5.6 μma (n = 45)
Intercalary, solitary, cylindrical, 6.6–8.5 × 3.3–3.9 μma (n = 19)
Intercalary, long cylindrical, distant from heterocytes, 30–62 × 5.2–7.5 μma (n = 22)
Spindle-like, up to 3 mm long, straight or slightly arcuated, often grouped in fascicles
Elongated cylindrical, without aerotopes, and with remaining cytoplasm in the form of fine granulation
Cylindrical or slightly barrel-shaped, 3.9–8.3 × 3.6–4.9 μma (n = 31)
Solitary, intercalary, oval to cylindrical, 5.5–6.7 × 3.2–4.0 μma (n = 6)
Intercalary, solitary, elongated cylindrical, 26–39 × 4.5–5.9 μma (n = 17)
Solitary, straight, bent or irregularly curved
Narrowed and elongated, bluntly pointed, containing a smaller amount of pigment and sporadic aerotopes
4.8–8.4 × 1.2–2.5 μma (n = 19)
Solitary, intercalary, oval to cylindrical, 6–15 × 2–3 μmb
Solitary or up to 3 in a row, cylindrical with rounded ends, wider than trichomes, 7.6–11.8 × 3.8–4.6 μma (n = 13)
Solitary, straight, bent, or slightly coiled
Tapered like hair-shaped, almost hyaline, continually pointed
Cylindrical to long-cylindrical, usually with scarce aerotopes, 4.4–7.0 × 2.5–3.3 μma (n = 36)
Solitary, intercalary, 6.6–8.7 × 3.4–3.7 μma (n = 5)
Solitary or 2–3 in a row, distant from heterocytes, long cylindrical with rounded ends, 8.5–12.5 × 4–4.6 μmc
Systematics of genus Aphanizomenon and genus Cuspidothrix
Class Cyanophyceae Sachs 1874
Order Nostocales Borzi 1914
Family Nostocaceae C.A. Agardh 1824 ex Korchner 1898
Genus Aphanizomenon Morren ex Bornet et Flahault 1888
Aphanizomenon flos-aquae Ralfs ex Bornet et Flahault 1888
Aphanizomenon klebahnii Elenkin ex Pechar 2008
Aphanizomenon skujae Komárková-Legnerová et Cronberg 1992
Genus Cuspidothrix Rajaniemi et al. 2005
Cuspidothrix issatschenkoi (Usačev) Rajaniemi et al. 2005
Morphology and taxonomy of individual species
(Smith 1950, p. 585, fig. 503; Hirose et al. 1977, p. 85, pl. 36 3a-3d; Komárek and Kováčik 1989, fig. 8; John et al. 2002, p. 96, pl. 18g-j; Rajanieimi et al. 2005b, Fig. 7. a; Komárek and Komárková 2006, Fig. 6; Komárek 2013, p. 688, Fig. 853)
Synonyms: Aphanizomenon incurvum Morren 1835; Aphnizomenon cyaneum Ralfs 1850; Aphanizomenon holsaticum Richter 1896; Aphanizomenon americanum Reinhard 1941
Ecology: This species is planktonic in eutrophic reservoir (Komárek 2013). It has shown positive growth within a wide range of temperatures (16–25 °C) (Preussel et al. 2009) and can grow below 10 °C (Üveges et al. 2012). It has a competitive advantage under situations of low light intensities (Mehnert et al. 2010). We collected this specimen in waterbodies of mesotrophic or eutrophic status (range of total phosphorus 0.017–0.040 mg L−1).
Material examined: Sangju (Jun. 2015, Oct. 2015, Dec. 2015, Nov. 2015, Jan. 2015, May. 2016), Daegu (Jun. 2015, Oct. 2015, Dec. 2015, Nov. 2015, Jan. 2016, Feb. 2016, Mar. 2016, Apr. 2016, May 2016), Haman (Jun. 2015, Oct. 2015, Dec. 2015, Nov. 2015, Jan. 2016, Feb. 2016, Mar. 2016, Apr. 2016, May 2016)
Synonyms: Aphanizomenon flos-aquae var. klebahnii Elenkin 1909; Aphnizomenon klebahnii Elenkin 1909 (Nomen alternat.)
Ecology: This species is planktonic in eutrophic up to hypertrophic reservoir (Komárek 2013). It is adapted to high water temperatures (Yamamoto and Nakahara 2006). We collected this specimen in waterbodies of mesotrophic or eutrophic status (range of total phosphorus 0.028–0.036 mg L −1).
Material examined: Daegu (Oct. 2015, Nov. 2015), Haman (Oct. 2015, Feb. 2016)
(Komárek and Komárková 2006, Fig. 17)
Synonyms: Aphanizomenon cf. flos-aquae var. klebahnii sensu Skuja 1956
Identification of this species is the first report in South Korea. Trichomes of the species were solitary, fine, straight, bent or irregularly curved, and without mucilage (Fig. 2c). Cells usually were with aerotopes, particularly in the central part, towards the ends sometimes more hyaline, 4.8–8.4 × 1.2–2.5 μm; terminal cells were narrow and elongated, containing a smaller amount of pigment and sporadic aerotopes. Terminal cells were bluntly pointed (Fig. 3A-3). Heterocytes were not found from natural samples collected in the Nakdong River. Akinetes were oval to cylindrical with rounded ends, conspicuously wider than vegetative cells, and with an akinete/trichome width ratio often greater than twofold. Morphological variability of akinetes from natural samples collected in the Nakdong River was rather small. It was reported by Komárek (2013) as 20–34 × 2.7–4.7 μm but mostly 7.6–11.8 × 3.8–4.6 μm. Akinetes range from 1 to 2 in number (rarely up to 3) in a row, with smooth and colorless exospore; the content was greenish and granular (Table 1).
Ecology: This species is planktonic in lakes. It is distributed in northern and colder parts of temperate zone in Eurasia (Komárek 2013). We collected this specimen in waterbodies of oligotrophic status (total phosphorus 0.009 mg L−1).
Material examined: Sangju (Jun. 2015)
(John et al. 2002, p. 96, pl. 18k; Rajanieimi et al. 2005b, Fig. 7. c; Komárek and Komárková 2006, Fig. 31; Figueiredo et al. 2011, Fig. 1. a-c; Ballot et al. 2010. Fig. 1; Komárek 2013, p. 668, Figs. 822-823)
Synonyms: Aphanizomenon issatschenkoi Usačev 1938
The presence of this species has been reported in freshwaters from many European countries (Kastovsky et al. 2010) and in Asia including China (Wu et al. 2010; Ballot et al. 2010), Japan (Watanabe 1985), and Singapore (Pham et al. 2011). In South Korea, this species has been described only one time until a recent date in the Han River (Park 2004) and it is described for the first time in the Nakdong River. The species was characterized by solitary, bent, or slightly coiled trichomes. The trichomes were isopolar, cylindrical in central part, and continually narrowed or pointed towards ends (developed trichomes). Other morphological features include a not or slightly constricted at the cross-walls and subsymmetric (Fig. 2d). Cells were cylindrical to long cylindrical, usually with scarce aerotopes, 4.4–7.0 × 2.5–3.3 μm; terminal cell was almost hyaline and markedly pointed. The hair-shaped terminal cell was in general narrower than the vegetative cells and continually elongated (Fig. 3A-4). Heterocytes were solitary, intercalary, 1–2 (rarely 3) on a trichome, cylindrical, and 6.6–8.7 × 3.4–3.7 μm. Akinetes were not found from natural samples collected in the Nakdong River. This species was easily recognized by trichomes with hair-shaped terminal cells. However, young field populations of this species without heterocytes can be easily misidentified as the very similar Rapidiopsis mediterranea Skuja or as the non-heterocystous life stages of Cylindrospermopsis raciborskii (Woloszynska) Seenayya and Subba Raju (Moustaka-Gouni et al. 2010).
Ecology: This species is sporadically planktonic in mesotrophic and eutrophic reservoirs (Komárek 2013). It has shown positive growth within a moderate range of temperatures (22–28 °C) (Dias et al. 2002). It has also been observed thriving in freshwater, as well as in oligohaline and brackish waters (Marshall et al. 2005). We collected this specimen in waterbodies of eutrophic status (range of total phosphorus 0.032–0.043 mg L−1).
Material examined: Haman (Oct. 2015, Nov. 2015, Apr. 2016)
The four investigated species in the Nakdong River were classified in the genus Aphanizomenon (Aph. flos-aquae, Aph. klebahnii, Aph. skujae) and in the genus Cuspidothrix (C. issatschenkoi). C. issatschenkoi are described for the first time in the Nakdong River. In addition, Aph. klebahnii and Aph. skujae are new to South Korea.
This research was supported by the Daegu University Research Grant 2013.
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Please contact author for data requests.
RHS carried out the design of the study, performed the fieldwork, and drafted the manuscript. SRY participated in the microscopic analysis. LJH participated in the design and coordination of manuscript and helped draft the manuscript. All authors read and approved the final manuscript.
The authors declare that they have no competing interests.
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