Algal Flora of Korea

Volume 3, Number 1 Chrysophyta: Bacillariophyceae: Centrales Freshwater Diatoms I o.3 No. 1 Vol. 3, Freshwater Diatoms

I Flora and Fauna of Korea

National Institute of Biological Resources Ministry of Environment National Institute of Biological Resources NIBR Ministry of Environment Russia

CB Chungcheongbuk-do CN Chungcheongnam-do HB GB Gyeongsangbuk-do China GG Gyeonggi-do YG GN Gyeongsangnam-do GW Gangwon-do HB Hamgyeongbuk-do JG HN Hamgyeongnam-do HWB Hwanghaebuk-do HN HWN Hwanghaenam-do PB JB Jeollabuk-do JG Jagang-do JJ Jeju-do JN Jeollanam-do PN PB Pyeonganbuk-do PN Pyeongannam-do YG Yanggang-do HWB HWN GW East Sea GG GB (Ulleung-do) Yellow Sea CB CN GB

JB GN JN

JJ South Sea Algal Flora of Korea

Volume 3, Number 1 Chrysophyta: Bacillariophyceae: Centrales Freshwater Diatoms I Acknowledgement

This work was derived from the “Flora and Fauna of Korea” project supported by the National Institute of Biological Resources, the Ministry of Environment, Korea. Algal Flora of Korea

Volume 3, Number 1 Chrysophyta: Bacillariophyceae: Centrales Freshwater Diatoms I

Gyeongje Joh School of Environmental Science and Engineering, Inje University Gimhae, Gyeongsangnam-do

Flora and Fauna of Korea

Published by the National Institute of Biological Resources Environmental Research Complex, Gyeongseo-dong, Seo-gu Incheon 404-708, Republic of Korea www.nibr.go.kr

All rights reserved. No part of this book may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, electronic, mechanical, photocopying, recording, or otherwise, without the prior permission of the National Institute of Biological Resources.

ISBN : 978-89-94555-15-7-96470 Government Publications Registration Number 11-1480592-000069-01

Printed by Junghaengsa, Inc. in Korea on acid-free paper

Publisher : Chong-chun Kim Editor : Sook Shin Reviewer : Hans U. Dahms, John Christopher Priesing Project Staff : Youn-Bong Ku, Chang-Hwan Bae, Moon-Soo Lim

Published on April 23, 2010

The Flora and Fauna of Korea logo was designed to represent six major target groups of the project including vertebrates, invertebrates, insects, algae, fungi, and bacteria. The book cover and the logo were designed by Jee-Yeon Koo. Preface

In the wake of the Convention on Biological Diversity (CBD), which recognized national sover- eignty over indigenous biological and genetic resources when adopted in 1992, countries around the world have been putting their best foot forward in unearthing raw biological materials reckoned as one of the crucial resources upon which national competitiveness depends to a great extent in the 21st century. Being well aware of the priority of securing and managing biological resources, the National Institute of Biological Resources (NIBR) under the Korean Ministry of Environment decided to issue the Flora and Fauna of Korea in an attempt to attain systematic management and comprehensive conservation of biological resources at the national level. Endowed with diverse landscapes involving a wide range of topographic conditions, Korea is acclaimed as one of the nations with high levels of biological diversity. Purporting to establish a thorough record on national indigenous species, the NIBR embarked on the publication of the Flora and Fauna of Korea in Korean and English detailing those species inhabiting the Korean peninsula in 2006. Our dedication to research during the past three years led by a group of professionals in the field of systematics finally came to fruition with issuance of the first of a kind monograph for Korean animals, fungi and algae encompassing approximately 1,037 species in 158 families belonging to 9 phyla. It is my firm belief that this very first national the Flora and Fauna of Korea is indeed the culmination of our persevering scientific research efforts aimed at deepening our understanding on native species and acutely identifying Korean biota. It will not only serve as an important initiative for sustainable biodiversity conservation but also a catalyst for rational and far-sighted use of biological resources. I would like to extend my utmost gratitude to the team of over 29 professors and associated experts headed by Prof. Sook Shin of Sahmyook University for their unsparing efforts in producing this groundbreaking work. I earnestly hope that on-going publication of the Flora and Fauna of Korea initiated by the Ministry of Environment will significantly contribute to unveiling all Korean native species estimated up to 100,000 and expanding wise utilization of beneficial indigenous resources.

Chong-chun Kim, Ph. D. President NIBR

Contents

List of Taxa 3 Introduction 5 Materials and Methods 11 Taxonomic Notes 13 1. Aulacoseira alpigena (Grunow) Krammer 19 2. Aulacoseira ambigua (Grunow) Simonsen 22 3. Aulacoseira ambigua f. japonica Tuji and Williams 27 4. Aulacoseira crenulata (Ehrenberg) Thwaites 30 5. Aulacoseira granulata (Ehrenberg) Simonsen 32 6. Aulacoseira granulata f. spiralis (Hustedt) Czarnecki and Reinke 37 7. Aulacoseira granulata var. angustissima (O. Müller) Simonsen 39 8. Aulacoseira laevissima (Grunow) Krammer 41 9. Aulacoseira muzzanensis (Meister) Krammer 43 10. Aulacoseira nygaardii (Camburn) Camburn and Charles 45 11. Aulacoseira subarctica (O. Müller) Harworth 48 12. Aulacoseira tethera Haworth 51 13. Cyclotella asterocostata Lin, Xie and Cai 57 14. Cyclotella atomus Hustedt 59 15. Cyclotella fottii Hustedt 62 16. Cyclotella glomerata Bachmann 63 17. Cyclotella meneghiniana Kützing 64 18. Cyclotella pseudostelligera Hustedt 68 19. Cyclotella radiosa (Grunow) Lemmermann 70 20. Cyclotella stelligera (Cleve and Grunow) Van Heurck 71 21. Cyclotella woltereckii Hustedt 73 22. Cyclostephanos dubius (Fricke) Round 76 23. Cyclostephanos invisitatus (Hohn and Hellerman) Theriot, Stoermer and Håkansson 79 24. Stephanodiscus hantzschii Grunow 83 25. Stephanodiscus hantzschii f. tenuis (Hustedt) Håkansson and Stoermer 85 26. Stephanodiscus parvus Stoermer and Håkansson 92 27. Thalassiosira bramaputrae (Ehrenberg) Håkansson and Locker 95 28. Thalassiosira faurii (Gasse) Hasle 97 29. Thalassiosira weissflogii (Grunow) Fryxell and Hasle 98 30. Skeletonema potamos (Weber) Hasle 101 31. Skeletonema subsalsum (A. Cleve) Bethge 104 32. Melosira moniliformis (O. F. Müller) Agardh 109 33. Melosira nummuloides (Dillwyn) Agardh 111 34. Melosira varians Agardh 113 35. Orthoseira roeseana (Rabenhorst) O’Meara 117 36. Actinocyclus normanii (Gregory) Hustedt 120 2 Algal Flora of Korea·Freshwater Diatoms I

37. Rhizosolenia longiseta Zacharias 123 38. Hydrosera whampoensis (Schwartz) Deby 127 39. Acanthoceras zachariasii (Brun) Simonsen 131 40. Chaetoceros muelleri Lemmermann 134 41. Pleurosira laevis (Ehrenberg) Compère 136 Literature Cited 140 Index to Korean Names 158 Index to Korean Names as Pronounced 159 Index to Scientific Names 160 3

List of Taxa

Class Bacillariophyceae Order Centrales Suborder Coscinodiscineae Family Thalassiosiraceae Lebour 1930, emend. Hasle 1973 Genus Aulacoseira Thwaites 1848 Aulacoseira alpigena (Grunow) Krammer 1991 Aulacoseira ambigua (Grunow) Simonsen 1979 Aulacoseira ambigua f. japonica Tuji and Williams 2007 Aulacoseira crenulata (Ehrenberg) Thwaites 1848 Aulacoseira granulata (Ehrenberg) Simonsen 1979 Aulacoseira granulata f. spiralis (Hustedt) Czarnecki and Reinke 1982 Aulacoseira granulata var. angustissima (O. Müller) Simonsen 1979 Aulacoseira laevissima (Grunow) Krammer 1991 Aulacoseira muzzanensis (Meister) Krammer 1991 Aulacoseira nygaardii (Camburn) Camburn and Charles 2000 Aulacoseira subarctica (O. Müller) Harworth 1990 Aulacoseira tethera Haworth 1988 Genus Cyclotella Kützing ex de Brébisson 1838 Cyclotella asterocostata Lin, Xie and Cai 1985 Cyclotella atomus Hustedt 1937 Cyclotella fottii Hustedt 1933 Cyclotella glomerata Bachmann 1911 Cyclotella meneghiniana Kützing 1844 Cyclotella pseudostelligera Hustedt 1939 Cyclotella radiosa (Grunow) Lemmermann 1892 Cyclotella stelligera (Cleve and Grunow) Van Heurck 1882 Cyclotella woltereckii Hustedt 1942 Genus Cyclostephanos Round 1987, description in Round 1982 Cyclostephanos dubius (Fricke) Round 1982 Cyclostephanos invisitatus (Hohn and Hellerman) Theriot, Stoermer and Håkansson 1987 Genus Stephanodiscus Ehrenberg 1845 Stephanodiscus hantzschii Grunow 1880 Stephanodiscus hantzschii f. tenuis (Hustedt) Håkansson and Stoermer 1984 Stephanodiscus parvus Stoermer and Håkansson 1984 Genus Thalassiosira Cleve 1873 Thalassiosira bramaputrae (Ehrenberg) Håkansson and Locker 1981 Thalassiosira faurii (Gasse) Hasle 1978 Thalassiosira weissflogii (Grunow) Fryxell and Hasle 1977 Genus Skeletonema Greville 1865 Skeletonema potamos (Weber) Hasle 1976 Skeletonema subsalsum (A. Cleve) Bethge 1928 4 Algal Flora of Korea·Freshwater Diatoms I

Family Melosiraceae Kützing 1824 Genus Melosira Agardh 1824 Melosira moniliformis (O. F. Müller) Agardh 1824 Melosira nummuloides (Dillwyn) Agardh 1824 Melosira varians Agardh 1827 Genus Orthoseira Thwaites 1848 Orthoseira roeseana (Rabenhorst) O’Meara 1875 Family Hemidiscaceae Hendey 1937 emend. Simonsen 1975 Genus Actinocyclus Ehrenberg 1837 Actinocyclus normanii (Gregory) Hustedt 1957 Suborder Rhizosoleniineae Family Rhizosoleniaceae Petit 1888 Genus Rhizosolenia Ehrenberg 1843: 402; emend. Brightwell 1858 Rhizosolenia longiseta Zacharias 1893 Family Biddulphiaceae Kützing 1844 Genus Hydrosera Wallich 1858 Hydrosera whampoensis (Schwartz) Deby 1891 Family Chaetoceraceae Smith 1872 Genus Acanthoceras Honigmann 1910 Acanthoceras zachariasii (Brun) Simonsen 1979 Genus Chaetoceros Ehrenberg 1844 Chaetoceros muelleri Lemmermann 1898 Family Eupodiscaceae Kützing 1849 Genus Pleurosira (Meneghini) Trevisan di San Leon 1848 Pleurosira laevis (Ehrenberg) Compère 1982 5

Introduction

1. Diatoms and their research history Belonging to the phylum Chrysophyta, diatoms are unicellular or colonial algae which have microscopic dimensions from 3 μm to 200 μm length. Different to other algal groups, the cell walls (named frustules) of diatoms are peculiarly composed of pectin impregnated with silica, and the morphology of the frustules and the markings on the valve faces are key characteristics to identify or classify the diatoms. Those having only raphe systems are capable of movement instead of the flagellate movement. They can move by the streaming of their cytoplasm in direct contact with the external medium through the raphe canals. Freshwaters and marine waters are inhabited by a variety of planktonic or periphytic diatoms which can exist anywhere, in which there is water and exposed habitats to light. They show a ubiquitous distribution throughout the world. As a result, they show a broad range of adaptations and remarkable variations in response to the environmental conditions. The numbers of diatom species is estimated to be about the order of 104 worldwide (Werner 1977). These diatom species are assigned to around 450 genera. Diatoms are separated into two orders by morphology - centric and pennate forms. The primary differences between the two groups: the morphology of the valves and the arrangement of striae on the face. The striae of the centrics are radially arranged from a point on the valve and those of the pennates are fashioned bilaterally symmetrical. Various ornaments are sculptured on the valve as punctae, areolae, processes, spines and other appendages, and they serve as keys to classify the diatoms and resolve their affinity. In the course of the history of diatom study, earlier classification systems were established by Pascher (1914), Hustedt (1930), Hendey (1964) and other diatom researchers. The classification proposed by Simonsen (1979) and further developed by Round et al. (1990) has been evaluated as a more natural system and currently is the most commonly accepted one. The floristic study of diatoms already started in the late eighteenth century and taxonomic research was remarkably enhanced in the early nineteenth century with the improvements of the microscopic magnification and resolution. In the late nineteenth century, many hand-illustrated monographs of diatom taxonomy were published by several authors - P. T. Cleve, C. G. Ehrenberg, A. Grunow, A. Schmidt, H. Van Heurck and others - establishing the foundations for diatom classification. Especially, in the early 1900s, F. Hustedt was prominent in producing a taxonomic and ecological study of diatoms which remains a key reference until nowadays. Since then, the descriptions on diatom taxa have been accomplished and a systematic study was established by the activity supported by many diatomists in Germany, the United Kingdom, Sweden and other countries. Taxonomic documentations of diatom flora are well compiled by Hustedt (1930), Patrick and Rei- mer (1966, 1975) and Krammer and Lange-Bertalot (1986, 1988, 1991a, 1991b). According to our earth’s history, fossil records of diatoms go back to the Cretaceous stage as centric forms. The araphid pennate diatoms have been recorded in the late Creaceous sediments, and the raphid forms from sediments of the middle Eocene stage. The earliest freshwater diatoms were discovered in the Palaeocene Stage. It is assumed that silicified skeletons of diatoms have gradually increased in weight during the course of evolution. 6 Algal Flora of Korea·Freshwater Diatoms I

2. Diatom research in South Korea In Korea, B. W. Skvortzow was the first to describe 58 and 87 taxa of freshwater diatoms from Lake Seoho around Suwon and a lake located in Seoul in 1929, respectively. Diatom studies before the 1945 Liberation in Korea were mainly conducted by the Japanese limnologists (Lee 1984). The diatom flora published before the 1960s were already tabulated with 221 diatom taxa by a Korean scholar (Chung 1962). Diatom studies were accelerated after those times and the representative research was titled, ‘A Study on Microflora in the Han River’. The first study was published in 1965 by Chung et al. (1965) and the serial publications continued up until the tenth edition by Chung and Lee (1984). In the first edition, the 98 diatom taxa collected from the downstream of the Han River were recorded in Korea (Chung et al. 1965). Additionally, a floristic study on diatoms was conducted in wetlands and recorded the 77 and 166 diatom species from swamps in Haman District and Yongneup Swamp in the Mountain Daeam, respectively (Chung and Kim 1987; Chung and Noh 1987). From the 1960s to 1980s, Y. H. Chung made the first substantial contribution to the knowledge of the diatom flora in Korea. In the early 1980s, the pennate diatoms collected in the Han River were comprehensively described with the photographic illustrations (Lee 1983). Through the gradual eutrophication and the deterioration of freshwater quality, limnological studies on plankton distribution were greatly expanding. Especially, the largest rivers in Korea such as the Yeongsan River, Nakdong River and Geum River were reclaimed to build the estuarine barrages at river mouths, and planktonic algae subsequently began to bloom in those waters. During those times, the algal research was centered on the lower parts of large rivers or estuarine lakes (Kim and Lee 1991; Cho et al. 1993; Lee 1994; Lee et al. 1995a; Kim et al. 1998c). Stream bed systems in Korea are prevailingly covered with stones or gravel. Therefore, diatoms are the most important component in the stone-attached (epilithic) biofilm and the leading groups in the periphytic algal assemblages. Periphytic diatoms were first described and illustrated from small streams in the vicinity of Gyeongju City (Chung and Watanabe 1984). The 393 diatom taxa attached to the sandy bottoms were reported from the estuarine brackish waters of the Nakdong River (Cho 1988). The 182 taxa of stone-attached diatoms were described from the Gwangcheon Stream of Uljin-gun (Lee 1992; Lee et al. 1994a; Lee et al. 1994b), and the 271 periphytic diatom taxa from the Namdaecheon Stream of Bukcheong District in North Korea (Cho 2000a, 2000b, 2000c). With the more and less limited activity on diatom study, most limnologists in Korea concentrated on floristic and ecological research of other planktonic algal taxa rather than on diatoms. Consider- ing freshwater diatom researches, taxonomic studies on the species of genera Aulacoseira, Cyclotella and Stephanodiscus collected in the Han River and Nakdong River, were documented in the ‘Korean Journal of Phycology’ (renamed as ‘Algae’ in 1997). In addition, monographic studies for this genus group were conducted in Korea by the following authors: Lee and Lee (1988), Lee and Yoon (1994), Cho (1995, 1996, 1999). Noh (1991) examined the genus Pinnularia and its 44 species comparatively from the whole Korean Peninsula for its taxonomic characteristics. In addition to the monograph of this genus, taxonomic examinations were applied to the diatom species Amphora by Lee and Round (1987, 1988) and Round and Lee (1989a, 1989b), Gomphonema species by Lee et al. (1992a) and Cymbella orientalis by Lee et al. (1993). Diatom researches for specific groups in Korea can be summarized as follows;

•Taxonomic accounts of Amphora ovalis, A. copulata, A. pediculus and epiphytic Amphora on other diatoms by Lee and Round (1987, 1988) and Round and Lee (1989a, 1989b) •Monographic descriptions of the genus Cyclotella collected in the coastal area of the West and South Sea of Korea (Lee and Lee 1988) Introduction 7

•Description of the 44 taxa belonging to the genus Pinnularia in Korea (Noh 1991) •Taxonomic accounts of Cymbella affinis collected in Lake Yeongcheon (Lee and Chung 1991) •Taxonomic accounts of Gomphonema vibrio var. subcapitatum sampled from Gwangcheon Stream in Uljin (Lee et al. 1992a) •Description of new species Cymbella orientalis Lee from epilithon by Lee et al. (1993) and Lee et al. (2006) •Morphological study of Cyclotella pseudostelligera collected in the Nakdong River by Lee et al. (1994c) •Morphological variations of Aulacoseira granulata population observed in the Han River (Lee and Yoon 1994) •Two species of genus Stephanodiscus blooming in the Nakdong River (Cho 1995) •Monographic description of Cyclotella species collected in the Nakdong River (Cho 1996) •Monographic description of Aulacoseira species collected in the Nakdong River (Cho 1999) •Morphological variability and taxonomic accounts of 19 Synedra taxa collected in Korean freshwaters (Lee and Yoon 2001)

As a result, much of the research on diatoms has dealt with diatoms Thalassiosiraceae, reflecting their dominance and potentials as pollution indicators in Korean freshwaters. In fertile and eutrophic water bodies, algal assemblages usually tend to be composed of a few dominant taxa and many rare taxa, whereas, in oligotrophic waters, there are commonly many rare taxa. Centric diatoms of Aulacoseira, Cyclotella and Stephanodiscus are the most widespread and are commonly dominant throughout the Korean rivers and lakes.

3. Diatom flora in Korean freshwaters An illustrated guide to Korean algal flora was already published in 1968, compiling the reported algal taxa into a guide book including the description of 512 diatom taxa (Chung 1968). The second guide for 169 diatom taxa was published with photographic illustrations of other algal groups by Chung (1993). Besides the illustrated books, diatom species recorded from Korean freshwaters were listed up several times - 724 taxa from freshwaters by Lee (1988), 1,457 taxa from freshwaters and marine water by Lee et al. (1995b). In the literature review for the identification of biodiversity in Korea, a total of 1,512 taxa were tabulated with support of Ministry of the Environment (KNCCN 1996). In addition, Lee (1997) reviewed the 992 diatom taxa from Korean freshwaters. According to previous reviews, approximately a thousand diatom taxa are distributed in freshwaters and brackish waters in Korea. In addition to recent diatoms, more 340 fossil diatom species were reported in Korea by palaeontologists (Lee 1990).

4. Classification of Korean diatoms This monograph adopts the proposed classification scheme by Simonsen (1979), where particularly the taxonomic hierachies above the family category are as follows.

Class Bacillariophyceae 돌말강 Order Centrales 중심돌말목 Suborder Coscinodiscineae 체돌말아목 Family Thalassiosiraceae 끈원반돌말과 8 Algal Flora of Korea·Freshwater Diatoms I

Family Melosiraceae 원통돌말과 Family Coscinodiscaceae 체돌말과 Family Hemidiscaceae 반원반돌말과 Suborder Rhizosoleniineae 관돌말아목 Family Rhizosoleniaceae 관돌말과 Family Biddulphiaceae 실패돌말과 Family Chaetoceraceae 센털돌말과 Family Eupodiscaceae 눈돌말과 Order Pennales 깃돌말목 Suborder Araphidineae 헛등줄돌말아목 Family Fragilariaceae 김발돌말과 Suborder Raphidineae 등줄돌말아목 Family Eunotiaceae 눈썹돌말과 Family Achnanthaceae 땅콩돌말과 Family Naviculaceae 쪽배돌말과 Family Ephithemiaceae 피각돌말과 Family Bacillariaceae 윷돌말과 Family Surirellaceae 방패돌말과

5. Centric Diatoms Centric diatoms have radial symmetry, representatively like that of Aulacoseira and Thalassiosira. They lack a slit, called a raphe, on valves and are never motile. The centrics usually have numerous small plastids in cytoplasm, whereas in pennate diatoms, the plastids are fewer and larger. This group is comprised of 12 major subgroups, to be recognized now as family. Their cell forms are discoid, cylindrical, subcylindrical, tubular, solenoid, elongate, box-shaped (biddulphioid) and ruti- larioid. Generic and specific discrimination on centric diatoms mainly have relied on the organiza- tion of valve structures about a point rather than about a line (Stoermer and Julius 2003). The most characteristic morphology for centric diatoms, both freshwater and marine waters, is the strutted process or fultoportular system. The presence of tubular processes are associated with cytoplasm and allow secretion of external organic threads, which reduce sinking velocity in water body (Stoer- mer and Julius 2003). Colony formations are another aspect of centric diatoms and are exhibited in many euplanktonic species. The order Centrales has 12 family, 130 genera and more than a thousand species worldwide in the second hierarchy of diatom classification. Centric diatoms are most common and a major component of freshwaters and marine waters. Especially, the family Thalassiosiraceae has become the most important one in freshwaters, particularly those showing some degree of eutrophication. Thalassiosiraceae has a large and phylogenetically diverse lineage within the centric diatoms, and are nominally diverse. They contain more than a thousand names within the level of species (Alver- son et al. 2007). In freshwaters and marine waters of Korea, the 54 genera and about 400 species of centric diatoms have been recorded according to the flora database by Lee (1995), KNCCN (1996) and Lee (1997) (Table 1). Among them, five genera (Aulacoseira, Cyclotella, Stephanodiscus, Melosira, Thalassiosira) are major groups in Korean freshwaters and other 10 genera occurring in freshwaters or brackish waters contain only one or two species. The other diatoms belonging to family except two family groups, Thalassiosiraceae and Melosiraceae, are mainly restricted to the marine waters in Korea. Introduction 9

Table 1. The summary of taxa of centric diatoms in freshwaters and marine waters in Korea (the numerics indicate the numbers of species) Genus Family Freshwaters Marine waters Detonula (2) Aulacoseira (19) Lauderia (1) Cyclostephanos (2) Planktoniella (1) Cyclotella (17) Thalassiosiraceae 105 51 Porosira (3) 54 Skeletonema (2) Skeletonema (1) Stephanodiscus (8) Thalassiosira (45) Thalassiosira (3) Tryblioptychus (1) Corethron (4) Orthoseira (2) Endictya (1) Melosiraceae 20 8 12 Melosira (6) Hyalodiscus (4) Melosira (3) Coscinodiscus (49) Coscinodiscaceae 51 - Craspedodiscus (1) 51 Gossleriella (1) Actinocyclus (16) Hemidiscaceae 18 Actinocyclus (1) 1 17 Hemidiscus (1) Asterolampra (1) Asterolampraceae 9 - 9 Asteromphalus (8) Actinoptychus (12) Heliopeltaceae 16 - 16 Aulacodiscus (4) Pyxillaceae 1 - Pyxilla (1) 1 Rhizosoleniaceae 37 Rhizosolenia (1) 1 Rhizosolenia (36) 36 Anaulus (3) Arachnoidiscus (5) Biddulphia (7) Campylosira (1) Climacodium (2) Hydrosera (1) Cymatosira (1) Biddulphiaceae 42 2 40 Acanthoceras (1) Eucampia (4) Goniothecium (4) Hemiaulus (7) Isthmia (2) Terpsinoe (1) Stictodiscus (3) Acanthoceras (1) Bacteriastrum (9) Chaetoceraceae 89 2 87 Chaetoceros (1) Chaetoceros (78) 10 Algal Flora of Korea·Freshwater Diatoms I

Table 1. Continued Genus Family Freshwaters Marine waters Bellerochea (1) Lithodesmiaceae 4 - Ditylum (2) 4 Streptotheca (1) Auliscus (3) Cerataulus (1) Eupodiscaceae 16 Pleurosira (1) 1 Odontella (9) 15 Rutilaria (1) Triceratium (1) 11

Materials and Methods

1. Sampling For diatom collections, various materials are gathered from planktons, epiphytons or periphytons, which are attached to the stone, sand, mud, aquatic macrophytes and other substrata. Planktons can be quantitatively collected by water samplers and also qualitatively by plankton net. Firmly attached and associated algae with substrata are scraped from stones through scouring their surface with tooth brushes. As benthic diatoms, surface sediments are taken using small cylinders (3 cm in diameter and 5 cm in length) and benthic suspensions are sampled from the bottom of small pools in mountain wetlands. Epiphytic diatoms are separated from the submerged portions of plants using toothbrush or forceps in laboratory. The sample volumes can be made up to 100 mL, if necessary, and the samples are subsequently preserved with formalin to a concentration of 2-3%. On the other hands, diatoms in the sample materials are concentrated by allowing materials settled in formalin-fixed water samples for two days.

2. Preparation of permanent specimen The diatom materials are oxidized with nitric acid and potassium dichromate on sand bath, a hot plate covered with coarse sands. Beakers, containing 10 mL subsample and equivalent concentrated nitric acid, are transferred to the hot plate and are heated from 400°C to 450°C under a fume hood. The oxidizing chemicals are to be added to the materials whenever the color changes into green. The green color indicates the deficiency of the oxidizer. Boiling is continued until the most of the raw solution in the beaker is evaporated. When the volume declines to low near to bottom, add deionized water (DW) to stop cleaning reactions. Dilution with DW is repeatedly conducted after centrifugation to remove completely the treated chemicals. Instead of centrifugation, dilution can be achieved by allowing diatom cells to settle for 12 hours in long cylinders. Besides of the nitric acids, sulfuric acids or hydrogen peroxide can be used for the oxidation of organic matter or cell materials (Hendey 1964; Patrick and Reimer 1966). Hydrogen peroxide is required for the weak skeleton or frustules among diatoms (Hasle and Fryxell 1970). Oxidized clean cells are mounted on cover glasses with Pleurax or Hyrax medium to make permanent specimens. Pleurax resin can be produced in laboratory using phenol (C6H5OH), sulfur powder (S) and sodium sulfide (Na2S·9H2O).

3. Observation and identification of diatoms Diatoms are observed under light microscopes (Zeiss Axioplan or Olympus Provis AX2), identified and counted for each taxon, where photographs and differential interference contrast (DIC) photos are also taken. The final photographs enlarge diatoms in permanent specimen to 2,000 fold size. All centric diatoms encountered through these diatom collections are described and illustrated for taxonomic and iconographic studies in Korea. Taxonomic literature and illustrations by Hustedt (1930) and Krammer and Lange-Bertalot (1991a) are the main references to identify diatoms. Many other literatures are consulted to expand high diversity of freshwater diatoms in Korean peninsula. The morphological variations in a diatom group or assemblage are also re-evaluated for the autoeco- logical and taxonomic aspects. On the other hand, fresh materials without acid-cleaning are examined in the process of diatom observation for the floristic study. To provide synonyms and basionyms of diatom species, a website is referred, ‘Catalogue of Diatom 12 Algal Flora of Korea·Freshwater Diatoms I

Names’ of academic website, http://www.calacademy.org/ (CAS 2009), which has been held by California Academy of Sciences (CAS) for world life’s diversity. The information about diatom flora over the world comes from the global database (http://www.algaebase.org/, Algaebase 2009). Cata- logues or check-lists authorized by Lee (1995), KNCCN (1996) and Lee (1997) are source documents to sum up the diatom flora reported or described in Korea.

4. Electron microscopy For SEM observations, the oxidized diatom frustules are placed on the fragments of cover glass and dried. The glasses containing diatoms are attached on aluminum stubs and coated with deionized gold. The specimens are scanned under the SEM microscopes (model JEOL CM35, JEOL JSM- 840A). For TEM observation, materials are placed on Formvar-coated copper grids and the water is allowed to evaporate. The dried grids are coated with a carbon film inside a vacuum evaporator and are observed under a TEM microscope (model JEOL JEM-1200 EX II). 13

Taxonomic Notes

Family Thalassiosiraceae Lebour 1930, emend. Hasle 1973: 67. Kkun-won-ban-dol-mal-gwa (끈원반돌말과)

Cells discoid, drum-shaped, cylindrical, and solitary or forming colony. Colonies commonly comprised of a few to a lot of cells. Valves with fultoportulae (strutted process) (reduced in genus Aulacoseira) and at least one rimoportula (labiate process). The location of fultoportulae and rimoportulae on valve important according to species. These characteristics related to the process invariable within a species and usually distinguishable by careful observation. The position and morphology of the rimoportulae key characters in establishing the phylogenetic relationships in freshwater Thalassiosiraceae.

GENERA AND SPECIES: In this family, more than a thousand species have been recorded worldwide in freshwaters and marine waters. There are six genera (Aulacoseira, Cyclotella, Stephanodiscus, Cyclo- stephanos, Skeletonema and Thalassiosira) in freshwaters. The number of species in this family is estimated approximately 450 species in freshwaters worldwide (Algaebase 2009). Four genera, such as Aulacoseira, Cyclotella, Stephanodiscus and Cyclostephanos, are important diatom groups in the freshwaters, and Skeletonema and Thalassiosira group have some freshwater or brackish species. Another nine genera such as Bacterosira, Planktoniella and others are marine or belong to the brackish water flora. The family flora reported in Korean freshwaters are also six genera and approximately 50 species according to literature studies (Lee 1995; KNCCN 1996; Lee 1997). DISTRIBUTION: Thalassiosiraceae as centric diatoms are truly planktonic in diverse water bodies such as rivers and reservoirs, freshwater lakes, brackish and estuarine waters, coastal marine and open ocean habitats. The dominance of centric diatoms in the form of discoid and filamentous diatoms is characteristic of the freshwaters in temperate regions of the northern hemisphere. Cen- trics predominate pennate diatoms in the phytoplankton, whereas pennate diatoms are relatively minor components in terms of numerical abundance. The species of Thalasssiosiraceae constitute the majority of the phytoplankton and provide the most significant part of phytoplankton biomass. Representatives of the family Thalassiosiraceae also provide the largest cellular volumes of centric diatoms in freshwaters. The predominance of centrics in the freshwaters is known from the temperate regions such as the Hungarian section of the Danube River (Kiss 1984), the Meuse River of Belgium (Gosselain et al. 1994), the Thames and Trent River in England (Speller 1990; Skidmore et al. 1998), the Spanish reservoirs (Sabater 1991), in Agrentina (Gómez and Bauer 1998), the Río de la Plata on the east coast of South America (Licursi et al. 2006), the San Joaquin River of Sierra Nevada (Leland et al. 2001), the 49 lakes in the Yangtze River of China (Yang et al. 2005). As for their phenology and seasonality, phytoplankton can be dominated in summer by ‘r-selected’ centric diatoms (Thalassiosiraceae) - Cyclotella, Cyclostephanos, Thalassiosira, Skeletonema etc. In contrast to phytoplanktons, the centric diatoms of the family Thalsssiosiraceae provide minor components of the diatom assemblages attached to gravel (epilithon), sand (epipsammon) and aquatic macrophytes (epiphyton). 14 Algal Flora of Korea·Freshwater Diatoms I

Paleolimnologically, the Thalassiosiraceae genera - Stephanodicsus, Cyclostephanos, Thalassiosira and Aulacoseira - markedly increased in the recent-deposited sediment of lakes, reflecting anthropogenic eutrophication and subsequently greater productivity of freshwaters. A great quantity of species among the previously mentioned taxa are good indicators of highly eutrophied freshwaters (Sayer and Roberts 2001). KEY REFERENCE: Simonsen (1979), Kiss (1984). Theriot and Serieyssol (1994), Hasle and Syvertsen (1996), Alverson et al. (2007).

Key to the genera of family Thalassiosiraceae

1. Cell with long mantles and generally long chains ····································································2 - Cell discor drum shaped, mantle short, solitary or short chain·················································3 2. Very weakly silicified cells and usually deformed with acid oxidation ·····················Skeletonema - Strong silicified cells and areolae on the mantles distinctly visible under LM············Aulacoseira 3. Areolae arranged into some sectors·········································································Thalassiosira - Areolae not divided into sectors·······························································································4 4. Areolae fascicles in valve margin and another structure in the central region ··············Cyclotella - Areolar line or striae from central region to valve margins·······················································5 5. Areolar striae multiseriate in the valve margin ····················································Cyclostephanos - Areolar striae uniseriate·······················································································Stephanodiscus

REMARKS: The family Thalassiosiraceae was originally established by Lebour (1930) and later emended by Hasle (1973) to include all diatoms that possess fultoportulae, a characteristics now recognized as representative for the lineage (Theriot and Serieyssol 1994). The family is composed of marine as well as freshwater planktonic diatoms, partly having fultoportular processes and typical areolar structures as main morphological and taxonomic characters. Fultoportular processes of Thalassiosiraceae diatoms are associated with the presence of chitin fibrils (e.g., seta or thread) which have roles in colony formation or buoyancy (Medlin et al. 1996). The family was further delineated by Simonsen (1979).

Genus Aulacoseira Thwaites 1848: 167. Dae-rong-dol-mal-sok (대롱돌말속)

Cells forming a long cylindrical chain by uniting adjacent sibling valves with spines around valve. Valves circular and their plain with irregularly scattered poroids. Valve mantles deep developed and cells usually seen in girdles when viewed microscopically. Areolae on the mantle arranging in straight, curved or spiraling rows in opposite directions between cell junctions. Collum, as an areolae-free band, developed in the margin of mantle and sulcus occasionally deep between the collum and areolated mantle. A ring of spines at the junction area of valve and mantle, and two types as separation and interlocking spine. Separation cells embedded in filaments and the frequency of separation valve controlling filament length. However, some species no separation valves and only linking valves which easily separated. Rimoportulae, as externally simple pores, located on valve mantle, often close to Ringleiste. Ringleiste, as circular ledge on the inside of cylinder, narrowly or broadly developed. Bacillariophyceae: Centrales: Thalassiosiraceae 15

Separation Valve spine

Mantle Sulcus (S) Girdle Collum (C)

Pseudosulcus (P)

S C

P Interlocking spine

Deep Ringleiste shallow Ringleiste

Fig. 1. Morphological characteristics of diatoms of the genus Aulacoseira.

Useful key characteristics in identifying Aulacoseira species are as follows: shape and arranging patterns of areolae on mantle, presence or absence of separation valves, the spines of separation valves, the ratios of mantle height and valve diameter, a true sulcus between mantle and collum, pseudosulcus between linking sibling valves and thickness of Ringleiste. Furthermore, viewed in the electron microscopy, the shape of interlocking and separation spines, presence or absence of a Ringleiste and the location of rimoportulae inside the collum are important characteristics for identification.

•Sulcus: a constriction in distal ends or outer side of valve mantle, and between collum and areolated mantle. This furrow zone has no areolae. Most sulci of Aulacoseira diatoms are narrow, while a few species such as A. ambigua and A. nygaardii have wide and deep constrictions at the outer side of mantle. •Collum: an areolae-free area at the distal end of mantle. The collum is separated from the areolated mantle by a small furrow, namely suclus. •Ringleiste: A ring-like thickening (‘Ringleiste’ in German) inwards at the border between column and areolated part of mantle. This is also known as the annular ledge, a solid ridge or a hollow thickening. As Ringleiste is an internal septum, sulcus and Ringleiste are different in their structures. However the sulcus is often used to describe the thickness of Ringleiste in light microscopy. Small rimoportulae are occasionally situated inward of the Ringleiste. 16 Algal Flora of Korea·Freshwater Diatoms I

•Girdle: A collective term for all structural elements between two valves. Girdle bands, all open and closed segments of girdles, i.e. valvocopulae, intercalary band. •Pseudosulcus: an opening or V-shape at the junction of two valve faces. Its shape depends on the convexness of valve face. The deep constrictions between two faces are seen as deep V-shapes or circles in unresolved focus of light microscopy. Lectotype: Aulacoseira crenulata (Ehrenberg) Thwaites 1848: 168 (=Gaillonella crenulata Ehrenberg 1843).

SPECIES: There are 79 species names in the database, of which 40 have been flagged as currently accepted taxonomically in the world (Algaebase 2010). In Korea, 11 taxa are listed up until 1988 by Lee (1988), 12 taxa until 1995 (Lee et al. 1995b) and 16 until 1997 (Lee 1997). Finally, 19 species of Aualcoseira are recorded in Korean freshwaters. DISTRIBUTION: The species of Aulacoseira diatoms are cosmopolitan over the temperate regions of the world and abundant in rivers as well as in lakes. The Aulacoseira diatoms are globally distributed as the most dominant algae in European freshwaters, in North America - San Joaquin River of Sierra Nevada (Leland et al. 2001), in other regions, in Australia - the Murray River in northern Victoria. This taxon is seasonally composed of a considerable portion of the phytoplankton in freshwaters. As some species of the genus Aulacoseira have a wide spectrum in their distributions, they remains dominant species both in eutrophic lakes and in strongly oligotrophic waters (Petrova 1986). Aulacoseira diatoms are a major component of the phytoplankton in the freshwaters of South Korea and play an important ecological role as a primary producer in the aquatic system. Aulaco- seira is commonly widespread and regularly produces its bloom in the plankton of most large rivers in South Korea - Han River, Nakdong River, Yeongsan River, Geum River etc, (Chung et al. 1987b; Cho et al. 1993; RDC 1997; Lee and Chang 1997; Kim and Oh 1998; Kim et al. 1998c), and lakes from spring to autumn - Lake Paldang, Soyang, Daecheong, Chungju, Imha, Hapcheon, Jinyang, Juam and Gachang etc (Kim and Chung 1993; Choi et al. 1994; Lee and Yoon 1994; Lee 1995; Lee and Song 1995; Han et al. 1995; Kim et al. 1995; Kim et al. 1998b; Kim et al. 1998c; Kim et al. 1999; Park and Kim 2003). The important species of genus Aulacoseira show bimodal patterns blooming in spring and autumn in their seasonality or algal magnitude, and display more regular variations. The diatoms of this group decline significantly in August and early September when blue-green algae such as Microcystis occur. For example, the seasonal variations of Aulacoseira in two locations - the Nakdong and Seonak- dong River - are shown in figures below. Genera Aulacoseira diatoms show annually the regular variations in their abundance. Many other planktonic algae occur with Aulacoseira bloom. The Aulacoseira populations are accompanied by significant growth of the green-algae and cryptomonads such as Scenedesmus, Cryptomonas and Rhodomonas. Especially, various green algae are coincident with Aulacoseira occurrence. Diatoms Stephanodiscus hantzschii f. tenuis appeared in autumn and succeed the Aulacoseira group. Small Stephanodiscus diatom assemblages bloomed persistently from October to April and discolored the river water to be yellow brown (Cho and Shin 1995). Filamen- tous Aulacoseira would seem to be incompatible with the discoid diatom Stephanodsicus. Diatoms of genus Aulacoseira generally appear from March to December with a slight decline or interruption during August in Korean freshwaters. These diatoms are rich in the flooding periods from late-June to early August and decline with blooms of the blue-green algae in summer. For example, Microcystis scum on the water surface would prevent the growth of other algae. Regard- less of the significant decline in summer, Aulacoseira populations usually appear in spring and per- Bacillariophyceae: Centrales: Thalassiosiraceae 17

Aulacoseira species Nakdong River 106

105

104

103

102

101 Seonakdong River 106

105

4 Algal abundance (cells/mL) 10

103

102

101 91 92 93 94 95 96

Fig. 2. Seasonal variations of genus Aulacoseira (grey area) in the lower reaches of the Nakdong River (upper) and in the Seonakdong River (below). Solid lines indicate total cell abundance of planktonic algae in the freshwaters (cited from Cho and Shin (1999)).

sist until December. Aulacoseira diatoms are not observed or are few in the algal abundance from January to March in the large rivers. In less polluted water, a number of Aulacoseria flora usually appear throughout a year. ECOLOGY: Reynolds (1988) classifies Aulacoseira species as a r-strategist (see also Grime 1979). Silica concentrations which are commonly limiting diatom growth in the water are influenced by two factors - diatom biomass and water discharge - and increase during the flooding periods. Diatom biomass is negatively correlated with the silica concentrations and discharges. Silica is exhausted during the period following blooms of Aulacoseira and Stephanodiscus in the period from October to May of the following year in the rivers. KEY REFERENCE: Hustedt (1930), Crawford (1981), Krammer and Lange-Bertalot (1991), Lee and Yoon (1994), Siver and Kling (1997), Cho (1999).

Key to the species of genus Aulacoseira

1. No areolae on valve mantle or only one cross areolae-line on margins of mantle····················2 - Two or more than two areolae in a pervalvar stria of mantle ··················································3 18 Algal Flora of Korea·Freshwater Diatoms I

2. Valve mantle without areolae ·················································································A. perglabra - One cross areolae-line on the distal and proximal end of mantle···············A. lirata var. biseriata 3. The 2-3 areolae on pervalvar striae of mantle·········································································4 - Always more than three areolae in a pervalvar stria on mantle ··············································9 4. Valve face only with one marginal ring of small areolae·············································A. tethera - Valve face other formed··········································································································5 5. Areolar distribution very variable in valve face, 2-3 areolar lines on the margin of valve or areolae free on middle parts of valve·············································································A. perglabra - Areolae distributed on the whole valve ··················································································6 6. The 2-3 areolae in a pervalvar row on mantle···········································A. distans var. tenella - Most valves with more than three areolae in a pervalvar row·················································7 7. Very large areolae irregularly distributed on valve face ·············································A. distans - Large areolae regularly distributed on valve face ···································································8 8. Collum short in girdle view······································································A. distans var. nivalis - Collum long in girdle view······················································································A. pfaffiana 9. Areolae on mantle very coarse or bead-shaped, mostly less than 10 punctas in 10 μm on a pervalvar stria, or punctas irregular on striae ············································································10 - Areolae of mantle other formed ····························································································11 10. Mantle height shorter than valve diameter···································································A. lirata - Mantle height longer than valve diameter·······················································A. crassipunctata 11. Striae on mantle parallel along pervalvar axis or weakly oblique··········································12 - Striae on mantle distinctly oblique along pervalvar axis, with exception of separation valves ··· ·············································································································································19 12. Punctas in pervalvar striae on mantles, at least, partly elongated ·········································13 - All punctas on mantles rounded or quadrat-shaped ·····························································15 13. Less than 15 punctas in 10 μm on pervalvar striae ··················································A. crenulata - More than 18 punctas in 10 μm on pervalvar striae·······························································14 14. Large areolae on valve margins and middle area hyaline without areolae ···············A. lacustris - Fine areolae on whole valve ························································································A. tenuis 15. Colony with different separation cells and long pointed spines·························A. muzzanensis - Separation cells with no different areolae ·············································································16 16. Areolae on pervalvar striae very fine, more than 20 striae in 10 μm ······································17 - Pervalvar striae less than 16 in 10 μm ···················································································18 17. Valve flat and collum wide in girdle view ·····························································A. laevissima - Valve convex and collum relatively deep and wide················································A. nygaardii 18. Mantle height longer than valve diameter·······························································A. islandica - Valve diameter longer than mantle height ············································································19 19. Collum relatively short ······························································································A. distans - Collum as long as the remaining valve mantle ························································A. pfaffiana 20. Separation cells with parallel striae on mantle, large areolae and long pointed spines··············· ······························································································································A. granulata - No such separation cells ·······································································································21 21. Interlocking spines very large·······························································································22 - Interlocking spines small ······································································································23 22. Cell skeleton relatively thin and Ringleiste shallow·····················································A. italica - Cell wall thick and Ringleiste broad ············································································A. valida Bacillariophyceae: Centrales: Thalassiosiraceae 19

23. Valve face finely areolate, interlocking spines with spathular spines························A. ambigua - Valve face with marginal punctas and interlocking spines other formed·······························24 24. Interlocking spines pointed without anchor, lining up with two costae ·················A. subarctica - Interlocking spines short and broad with anchor at tip, lining up with one costae······················ ································································································································A. alpigena (Krammer and Lange-Bertalot 1991a)

REMARKS: In 1848, S. W. Thwaites separated two groups (genus Aulacoseira and Orthoseira) from the genus Melosira C. A. Agardh and proposed new genera. Thwaites proposal has been largely ignored and disused for a long times. Starting with Crawford (1971), his detailed examinations with electron microscopy revealed considerable heterogeneity in the genus Melosira. Since then, there have been many reassessments of the taxa as well as a proposal for the separation of various sections into different genera: Aulacoseria in Simonsen (1979), Paralia and Ellerbeckia in Crawford (1988). Simonsen (1979) resurrected the long-disused name Aulacoseira and gave the validity of Aulacoseira. Crawford (1981) substantiated the differences between the two genera by light and electron microscopy observations. A distinctive type of tube-process is present in Aulacoseira, while Melosira section shows a rimoportular structure. Aulacoseira species in Korean freshwaters are primarily present in three species - A. ambigua, A. granulata and A. subarctica. These species are distinctly separated by their morphology of mantle areolae, spines of linking and separating valves. In addition, each species among the genus Aula- coseira can be discriminated by the cell size or dimensions. Ranges of valve diameter and mantle height are important and useful data. Regardless of the characteristic informations, it is difficult to identify Aulacoseira diatoms due to similarity in the morphology of mantle or girdle view.

1. Aulacoseira alpigena (Grunow) Krammer 1991: 93 (Figs. 3-5).

Krammer 1991a: 93: f. 1. Krammer and Lange-Bertalot 1991a: 34. pl. 2. f. 3. Siver and Kling 1997: 1828. f. 93.

BASIONYM: Melosira distans var. alpigena Grunow in Van Heurck 1882. pl. 86, f. 28. SYNONYM: Melosira italica var. alpigena (Grunow in Van Heurck) Cleve-Euler 1934: 10. Aulacoseira distans var. alpigena (Grunow) Simonsen 1979: 57. Aulacoseira distans var. alpigena (Grunow) Valeva and Temniskova-Topalova 1993: 69. pl. 1. f. 15. Aulacoseira lirata var. alpigena (Grunow) Haworth 1990: 195. Melosira distans subsp. alpigena (Grunow in Van Heurck) Skabichevskii 1960: 124.

Cells cylindrical and connected with valves to form long filaments. Valves circular, 4-15 μm in diameter and 4-7 μm in mantle height. The ratios of mantle height and valve diameter 0.35 to above 1. Striae on the mantle usually oblique or curved, 15−24 striae in 10 μm and 15-22 areolar punctas in 10 μm on a strial row. The punctas on mantle arranging in regular patterns and appearing to be a little larger than the others near the margin. A peripheral ring of areolae on valve and areolae absent on the majority of the valve. Striae on the mantle mainly alternate with marginal spines, but their arrangement irregular. Collum broad and sulcus deep developed. Marginal spines pointed and long spathulate forms: valves with the former separated easily, but those with the latter 20 Algal Flora of Korea·Freshwater Diatoms I

A B C

H G E F J I

K L M OPQ m

μ 10

R S N

Fig. 3. Aulacoseira alpigena. A-J, O-Q. the valve mantle and oblique arrangements of areolae on mantle; K, L. the Ringleiste on the inside of cylinder; M, N. the hyaline surface in central area and a ring of areolae on valve margin (×2,000, LM); L-Q. DIC images of LM; R, S. interlocking spines between two valves and areolar striae on the mantle (SEM). Bacillariophyceae: Centrales: Thalassiosiraceae 21

A B C

D F

Fig. 4. Aulacoseira alpigena. A. a ring of large arolae on valve margin; B-D. irregular areolae in sizes on the mantle; E, F. interlocking spines between two valves (SEM). 22 Algal Flora of Korea·Freshwater Diatoms I firmly interlocked and rarely separated. Interlocking spines usually spatula-shaped with lateral thorns. However, spines occasionally varied and highly irregular in size and morphology, and their morphology appearing more and less molded around neighboring spines. Ringleiste on the inward side of cylinder shallow developed.

TYPE: Nova Hedwigia 52: 93 (1991). SEASONALITY: A. alpigena occurs in the most abundance in spring, and less in autumn. DISTRIBUTION: This species is widespread in low alkalinity and oligotrophic freshwaters; the Cumbrian waters in England (Haworth 1988), the northern and alpine regions in Europe (Krammer 1991a), Connecti- cut and Canadian Shield waters (Siver and Kling 1997). The species is dominant as acidophilous taxa in sedimentary Holocene algae in the palaeolimnological studies in northwest Spain and Finland (Siver and Fig. 5. Distribution of Aulacoseira alpi- Kling 1997; Leira 2005). It dominated algal assem- gena. blages of Holocene sediments in a high alpine soft water lake in Austria (Koinig et al. 1998). KOREA: The diatoms of the species are reported in Korean freshwaters such as Lake Imha, Lake Yeongcheon and the Nakdong River, however, its actual existence is obscure due to the potential misidentifications (Lee et al. 1992b; Cho et al. 1993; Kim et al. 1995; Lee et al. 1995). In recent times, A. alpigena was observed abundantly in a mountain wetland, the third Mujechineup Bog of Moun- tain Jeongjok in Ulsan, in December 25, 2009. SPECIMEN EXAMINED: (Benthic diatoms collected in the third Mujechineup Bog of the Jeongjok Mountain, Ulsan: 25.xii.2009). ECOLOGY: This species prefers the oligotrophic and the low alkalinity freshwaters in the northern Hemisphere. Additionally, they are acidophilus taxon. REMARKS: Viewed the valve mantle under light microscopy, A. alpigena is somewhat difficult to distinguish from small specimen of A. subarctica, A. distans and A. lirata. They are frequently confused because of overlapping characteristics in the mantle view.

2. Aulacoseira ambigua (Grunow) Simonsen 1979: 56 (Figs. 6-9).

Krammer and Lange-Bertalot 1991a: 25. pl. 21. f. 1. Cohu 1991: 409. f. 1. Kobayasi and Nozawa 1981: 125. f. 1. Cho 1999: 144. f. 1.

BASIONYM: Melosira crenulata var. ambigua Grunow in Van Heurck 1882: 88. SYNONYM: Melosira granulata var. ambigua (Grunow in Van Heurck) Thum 1889. Melosira ambigua (Grunow in Van Heurck) O. Müller 1903: 332. Melosira italica f. ambigua (Grunow in Van Heurck) Balachonzew (Bolochonzew) 1909: 374. Bacillariophyceae: Centrales: Thalassiosiraceae 23

A B D m

μ C F 10 E J G

K I

Fig. 6. Aulacoseira ambigua. A-I. spiral arrangement of striae on mantle, distinct pseudosulcus between linking or sibling valves (B, I) and true sulcus between mantle and collum (B, I) (×2,000) (LM); J. the acute spines of separation valves; K, L. the bifidly spanner-formed spines of two linking valves; J, K. an outward aperture of the rimoportula near Ringleiste (SEM). A-C. DIC images of LM. 24 Algal Flora of Korea·Freshwater Diatoms I

A B

2.5 μm

D C

Fig. 7. Aulacoseira ambigua. A, C. the spanner-shaped spines of two linking valves; B. the outer aperture of a rimoportula; D. the acute spines of separation valve (SEM).

Melosira italica var. ambigua (Grunow in Van Heurck) A. Cleve-Euler in Backmann and Cleve-Euler 1922. t. 9. Melosira italica subsp. ambigua (Grunow) Cleve-Euler 1938: 156. Melosira italica var. ambigua (Grunow) Cleve-Euler 1951: 26.

Cells cylindrical, linked tightly by interlocking spines to form long tubular filaments. Filamentous chains composed of 5 cells in minimum and 30 cells in maximum. Valves circular, flat or a little convex, 4-17 μm in diameter and 5-13 μm in mantle height. The ratios of mantle height and valve diameter 0.75 to more than 2. Pseudosulcus distinct around the edge of valve junction. True sul- Bacillariophyceae: Centrales: Thalassiosiraceae 25

Aulacoseira ambigua Nakdong River 106

105

104

103

102

101 Seonakdong River 106

105

4 Algal abundance (cells/mL) 10

103

102

101 91 92 93 94 95 96

Fig. 8. Seasonal variations of diatom Aulacoseira ambigua (grey area) and total phytoplankton (solid lines) in the Nakdong River (upper graph) and in the Seonakdong River (lower graph) (cited from Cho and Shin (1999)).

cus apparent between the mantle and collum. Areolae on the mantle of separation and linking valve curved to pervalvar axis and two arranging patterns identical. On the mantle, 16-19 areolar striae in 10 μm and, in the case of finer areolae, 20-25 striae in 10 μm, 17-19 areolae in 10 μm on a stria, and 19-22 finer areolae in 10 μm. In electron microscopy, linking valves connected into chains by bifidly spanner-formed spines with a thickening near the base. Spines on separation valve pointed and regularly arranged. The circular ledge or hollow projection named as “Ringleiste” inward from the distal margin of the mantle. One or two rimoportulae into the Ringleiste and open to the outside with large or quadrangular apertures on the edge of mantle. The true sulcus and pseudosulcus clear, and connecting spines relatively short and acute.

TYPE: Mollerod, Bangal (?). Grunow 2224, 2212, 2678, 2678. Bacillaria 2: 56 (1979). SEASONALITY: A. ambigua also blooms from March or April to December with a slight decline in August like other Aulacoseira members. In the Nakdong River, A. ambigua appears in spring earlier than other Aulacoseira and is usually followed by A. subarctica. The seasonal variations of A. ambigua 26 Algal Flora of Korea·Freshwater Diatoms I in the Nakdong River are presented in the below figure. The peak abundance was recorded as 8,500 cells/ mL in the lower reaches of the river. DISTRIBUTION: This species is widespread throughout the world as a dominant or subdominant component of the phytoplankton like other centric filaments. The taxon is reported in many regions - the Rhine and the Meuse River of Europe (Gosselain et al. 1994; Ibe- lings et al. 1998), in the Seine River of France (Garnier et al. 1995), in Sicilian Reservoir in Italy (Naselli-Flores 2000). In South America, the species was reported in Rio de la Plata of the east coast of South America (Licur- si et al. 2006). The species is commonly distributed in 116 low alkalinity lakes in the Adirondack Mountain Park in northern New York (Camburn and Charles 2000). In stratigraphic studies on microfossil diatoms, A. ambigua increased with European settlements around 55 Minesota lakes (Ramstack et al. 2004), and domi- Fig. 9. Distribution of Aulacoseira ambigua. nant in Lake Tule of Northern California in USA (Brad- bury 1992) and in shallow Danish lakes (Anderson and Odgaard 1994). KOREA: A. ambigua is another leading phytoplankton in Korea. In the Nakdong River, this population shows similar variation to A. granulata in the blooming patterns. The magnitude and the maximal abundance of the taxa are a little greater than A. granulata and the most abundant among the genus Aulacoseira. The species appears as a dominant taxon in several Korean rivers - the Han River (Lee and Chang 1997; Kim et al. 1998b; Kim et al. 1998c; Lee and Jung 2004), the Nakdong River (Cho et al. 1993; Lee et al. 1995a; Cho and Shin 1999; Kim 2004), the Yeongsan River (Kim 2003) and the Imjin River (Lee and Yoon 2002). It is subdominant in Lake Paldang (Han et al. 1995; Kim 1998), Lake Imha (Kim et al. 1995; Kim et al. 1997; Park et al. 1999), Lake Juam (Lee and Song 1995), Lake Jinyang (Kim et al. 1995) and dominant in Lake Yeongcheon (Lee et al. 1992b) and Okjeong (unpublished data). The spherical auxospores are occasionally observed in rivers. Maxi- mum diameter of A. ambigua valve is approximately 15 μm in diameter as auxospore size. SPECIMEN EXAMINED: (Planktonic diatoms collected from the Seonakdong River near Gimhae Bridge: 21.xi.1992). ECOLOGY: The diatoms of this taxon are mesotrophic and eutrophic indicators requiring elevated nutrient levels and is known as alkaliphilous algae (Siver and Kling 1997). However, it has wide tolerance from eutrophic state to oligotrophic state (Pertova 1986). REMARKS: Some authors have reported the bloom of Aulacoseia italica in the Nakdong River in the past (Chung et al. 1987b; Kim and Lee 1991; Cho et al. 1993; Seo and Chung 1993; Lee 1994) and other regions in South Korea. The species is abundantly common in the Nakdong River System and concurs with A. granulata in its blooms. However, it is assumed that A. ambigua would probably be misidentified as A. italica or A. granulata, and it is questioned whether the species has been accounted as A. italica in many publications. Therefore, the A. italica described in past literatures can be counted as A. ambigua in the present study. As mantles of Aulacoseira filaments Bacillariophyceae: Centrales: Thalassiosiraceae 27 are most frequently viewed under microscopy, some Aulacoseira species may be mistaken in the observation of unclean diatoms (Cho 1999). A. granulata collected from the Han River in Korea has been observed in four morphological types (Lee and Yoon 1994) and the fourth type is certainly A. ambigua, viewing the morphology of areolar arrangements and the connecting spines between two sibling valves.

3. Aulacoseira ambigua f. japonica (Meister) Tuji and Williams 2007: 69 (Figs. 10-12).

Cho 1999: 145. f. 10. Tuji and Williams 2007: 69. f. 1.

SYNONYM: Melosira japonica Meister 1913: 305. pl. 4. f. 1. Non Synonym: Helosira japonica Pantocsek 1892 (1905: 62) pl. 4. f. 63. non: Melosira japonica Pantocsek 1892. (1905: 62) pl. 4. f. 63.

Aulacoseira ambigua f. japonica Nakdong River 106

105

104

103

102

101 Seonakdong River 106

105

4 Algal abundance (cells/mL) 10

103

102

101 91 92 93 94 95 96

Fig. 10. Seasonal variations of diatom Aulacoseira ambigua f. japonica (grey area) and total phytoplankton (solid lines) in the downstream of the Nakdong River (upper graph) and in the Seonakdong River (lower graph) (cited from Cho and Shin (1999)). 28 Algal Flora of Korea·Freshwater Diatoms I m

μ 10

D 2.5 μm

A C B

E m

G 10 H I

F J

Fig. 11. Aulacoseira ambigua f. japonica. A, B. the spiral filament of a colony (×400, LM); C, E. the spanner-shaped spines of two linking valves; D. pointed spines of a separation valve (SEM); F-J. the view of girdle and mantle in colonial filaments (×2,000, LM). Bacillariophyceae: Centrales: Thalassiosiraceae 29

Regularly spiral arrangements of tubular filaments, one turn of a spiral filament 40-60 μm in breadth, and 40-45 μm in height. Valves 3.5-5.5 μm in diameter and 7-9 μm in mantle height. Areolar striae on mantle 19-22 in 10 μm. The cell dimensions of the taxon relatively narrow ranged. The spines of linking and separation valve as well as the areolar arrangement of the taxon identical with those of the type species.

TYPE: Locality - Lake Suwa, Nagano Prefecture, Japan. Lectotype designated by Tuji and Williams: Slide BRM “A3/57” (Hustedt Collection, Bremerhaven, Germany). Isotype: Slide no. 801 of Tempère and Peragallo (2nd ed.), BM 69153. SEASONALITY: The seasonality of the taxon is similar with the type species (A. ambigua). DISTRIBUTION: A. ambigua f. japonica has been described in Japanese freshwaters such as Lake Suwa, Lake Biwa and other localities (Tuji and Williams 2007). Fig. 12. Distribution of Aulacoseira ambi- It is assumed that A. ambigua f. spiralis recorded in gua f. japonica. subtropical Brazilian reservoirs is A. ambigua f. japonica (Aparecida et al. 2008). The distribution of the species is obscure in other regions. KOREA: Referring to the diatom check-list of Lee (1997), the species was named as Melosira granulata var. angustissima f. spiralis Hustedt and recorded ten times before 1996 in Korean freshwaters. The species was first reported from the Namhan River by Chung (1972). The taxon was a common species before the construction of an estuarine dam in 1987 (Chung et al. 1987b) and has increased in abundance recently in the lower parts of the Nakdong River (Cho 1988; Cho and Shin 1999). In the Nakdong River, this variety has also coincided with A. ambigua and bloomed with 2,000-6,000 cells/mL in September-October, and 2,500 cells/mL in June in the river. After the bloom, its maximum abundance was recorded below 1,000 cells/mL in the lower river. As the spiral form has a concrete and significant difference in morphology with the species. This spiral type was described as a morphotype of A. ambigua (A. ambigua morphotype spiralis) in the Nakdong River as dimorphic species (Cho 1999). It is unclear whether the morphological variations are caused by specific environmental conditions or not. Further examinations are required for its taxonomic and ecological status. SPECIMEN EXAMINED: (Material collected in the Seonakdong River near Gimhae Bridge: 18.ix.1999). ECOLOGY: In the Nakdong River, the spiral morphotypic diatoms occasionally increased with the flooding current caused by heavy rainfall. This suggests that the spiral types have a close relationship to turbid hydrodynamic conditions in river. REMARKS: The spiral form of A. ambigua has been reported as a subspecific taxon of A. granulata in many ecological and floral reports in Korea, and the two taxa are confused. Though Melosira japonica Meister is a synonym of Aulacoseira ambigua f. japonica, it has been sometimes recorded as M. granulata var. tenuissima f. spiralis in Japan(Tuji and Williams 2007). Melosira japonica Pantocsek was additionally described from fossil material in Hokkaido and is clearly different from M. japonica F. Meister (Tuji and Williams 2007). 30 Algal Flora of Korea·Freshwater Diatoms I

4. Aulacoseira crenulata (Ehrenberg) Thwaites 1848: 168 (Figs. 13, 14).

Krammer and Lange-Bertalot 1991a: 30. pl. 26. f. 1. Crawford et al. 2003: 9. f. 15.

BASIONYM: Gaillonella crenulata Ehrenberg 1843. pl. 2/1. f. 41. SYNONYM: Aulacoseira italica f. crenulata (Ehrenberg) R. Ross in Hartley 1986: 606. Lysigonium crenulatum (Ehrenberg) Trevisan 1848: 96. Aulacoseira crenulata (Ehrenberg) Thwaites 1848: 168. Lysigonium crenulatum (Ehrenberg) Kuntze 1891: 902. Melosira crenulata (Ehrenberg) Kützing 1844: 55. pl. 2. f. 8. Melosira italica f. crenulata (Ehrenberg) Otto Müller 1906: 70. Melosira italica var. crenulata (Ehrenberg; Kutzing) Meister 1912: 43. Melosira orichalcea var. crenulata (Ehrenberg; Thwaites) Brun 1880: 137. pl. 1. f. 9h. Melosira polymorpha f. crenulata (Ehrenberg) Bethge 1925: 36. pl. 2. f. 19. Melosira italica var. crenulata (Ehrenberg) Kützing 1844: 55. Orthosira orichalcea var. crenulata (Kützing) Rabenhorst 1863: 14. Melosira crenulata (Ehrenberg) Rabenhorst 1853: 14.

Cells cylindrical and united to form a long tubular filament. Valves circular, 5-32 μm in diameter and 8-20 μm in mantle height. The ratios of mantle height to diameter almost above 1, however, below 1 in larger sizes. Valves covered with randomly arranged areolae or hyaline without areolae. Areolar striae on valve mantle parallel to pervalvar axis and 14-9 striae in 10 μm and 9-13 strial punctas in 10 μm. Areolae elongated or slit-like. Linking spines around the margin of valve strong in light microscopy and cell skeleton strong. In fine morphology viewed with electron microscopy, the spine around the valve margin thinly spatula-shaped or T-shaped in form. Pseudosulcus indistinct with depression between connecting cells. Ringleiste on the inward of cylinder weakly developed.

TYPE: Bacillaria 2: 60 (1979). Locality - Diatomite from Westpoint, New York. SEASONALITY: The seasonality of A. crenulata may be obscure due to the lower frequency in the freshwaters of temperate regions. DISTRIBUTION: A. crenulata is cosmopolitan, but low in frequency and abundance as living diatoms in freshwaters. It has more sporadic distributions (Krammer and Lange-Bertalot 1991a). The diatoms of the species are dominant in the plankton assemblages of Plánicèskˇ pond, in South Sumavaˇ mountains, Czechoslovakia (Sejnohováˇ et al. 2003) and on the surface of sediment samples from some riverine and impounded wetlands of Willamette basin, Oregon (Weilhoefer et al. 2004, 2007). At the same basin, the species has high biovolume in epilithic diatoms on rocks in riffle streams of 28 watersheds in Willamette River basin and surrounding area (Waite et al. 2008). It was occasionally abundant or common in surface sediments in 46 tributaries from four river floodplains in the southeast Murray-Darling Basin, Australia (Reid and Ogden 2009). It is usually found in fossil diatoms, together with essentially benthic species which are different with open-water planktons (Crawford et al. 2003; Hayward et al. 2004). KOREA: The species was only observed in the epilithic algal assemblages of the Daejong Stream in Gyeongju. This is the first description for A. crenulata in South Korea. SPECIMEN EXAMINED: (Epilithic diatoms collected in the downstream of the Daejongcheon Stream Bacillariophyceae: Centrales: Thalassiosiraceae 31

C B

m D μ 10

G E F A

Fig. 13. Aulacoseira crenulata. A-G. the mantle and linear punctuate striae on mantle in view of girdle (×2,000, LM). 32 Algal Flora of Korea·Freshwater Diatoms I in Yangbuk of Gyeongju: 21.xii.1990). ECOLOGY: A. crenulata is benthic or periphytic diatoms, and prefers more and less acidophilic and oligotrophic water bodies. The ecological characteristics of A. crenulata differ considerably with those of A. italica, though both species share jointly their morphology (Sejnohováˇ 2003). A. italica occurs in more or less eutrophic waters, while A. crenulata is typical for the benthos in oligotrophic waters. REMARKS: In 1844, F. T. Kützing presented Melosira crenulata as a form of M. italica, and he recognized the former as living diatoms from flowing waters and the latter from fossil diatoms (Crawford et al. 2003). Based on Melosira crenulata Kützing, the genus name Aula- coseira was first used by G. H. K. Thwaites in 1848. Though the genus name was not used until 1979, R. Simonsen drew attention to the validity of Aulacoseira and made many new combinations. In the study of 47 Aulacoseira species based on morphology observed Fig. 14. Distribution of Aulacoseira cre- by light and electron microscopy, A. crenulata and A. nulata. italica were the most basal types among Aulacoseira species (Edgar and Theriot 2004). The above two species are assigned to one species and its variety in the literature of Krammer and Lange-Bertalot (1991), and some authors. Crawford et al. (2003) concluded that A. crenulata and A. italica are conspecific upon examining the type materials of Ehrenberg’s, and emended the species description of A. italica and clarified the morphological characteristics. As they are sibling species, the most important differences between A. italica and A. crenulata are the degree of curva- tures or spiraling of pervalvar areolar lines: straight rows of A. crenulata and curves of A. italica. The second feature is the difference of areolar shapes: more circular of A. italica and elongated or slit-like of A. crenulata. However, the shapes of areolae appear more and more as slits with the thickness or silicification of valves (Crawford 2003). A. crenulata has the intermediate form of A. islandica and A. italica in the morphology of areolae and linking spines.

5. Aulacoseira granulata (Ehrenberg) Simonsen 1979: 58 (Figs. 15-18).

Davey and Crawford 1986: 145. f. 1. Krammer and Lange-Bertalot 1991a: 22. f. 17. Cho 1999: 145. f. 13.

BASIONYM: Gaillonella granulata Ehrenberg 1843: 415. SYNONYM: Melosira granulata (Ehrenberg) Ralfs in Pritchard 1861: 820. Melosira punctata var. granulata (Ehrenberg) Cleve and Müller 1879: 220. Lysigonium granulatum (Ehrenberg) Kuntze 1891: 902. Orthosira granulata (Ehrenberg) Schonfeldt 1907: 76. pl. 2. f. 10. Melosira polymorpha subsp. granulata (Ehrenberg) Bethge 1925: 30. Bacillariophyceae: Centrales: Thalassiosiraceae 33

A C

B m

D 10

F G

HI JK

Fig. 15. Aulacoseira granulata. A, B. the valve view and faint punctas on face; C, D. the shallow Ringleiste in the inside of cell; E-K. the mantle and linear punctuate striae on mantle in view of girdle, and spines of separation valves (×2,000) (LM); A-E, G-I; DIC images of LM. 34 Algal Flora of Korea·Freshwater Diatoms I

A C B m

μ 10

D E F

Fig. 16. Aulacoseira granulata. A, B. the spines of separation valve; C, D. the more triangular spinpes of linking valves (SEM); E, F. mantles and coarse punctas on mantles in the girdle view, and different areolae on mantle in a cell (F) (×2,000, LM). Bacillariophyceae: Centrales: Thalassiosiraceae 35

Aulacoseira granulata Nakdong River 106

105

104

103

102

101 Seonakdong River 106

105

4 Algal abundance (cells/mL) 10

103

102

101 91 92 93 94 95 96

Fig. 17. Seasonal variations of diatom Aulacoseira granulata (grey area) and total phytoplankton (solid lines) in the downstream of the Nakdong River (upper graph) and in the Seonakdong River (lower graph) (cited from Cho and Shin (1999)).

Cells cylindrical and connected to form long tubular filament. Valves circular, 4-30 μm in diameter and 5-24 μm in mantle height. The ratios of mantle height and valve diameter variable, however, above 0.8. Cells composed of two types of valve, linking and separation valve. Separation valves with long spines, having variable lengths, their irregular spines frequent in the terminal of filament. Linking spines united adjacent cells to form long cylindrical chains. The length of filament determined by the frequency of separation valves. The areolae of separation valve mantle in straight rows, those on linking valve mantle spiralling away from adjacent junction in opposite directions. Areolar striae on mantle variable in sizes: fine striae over 15 in 10 μm, intermediate striae 10-15 in 10 μm, and coarse striae 7-10 in 10 μm. Viewed by electron microscopy, interlocking spines of linking valve conversely triangle-shaped, lining up a rib on mantle. On the other hand, spines of the separation valve with two costal ribs on mantle.

TYPE: Berlin. K 39. 03. 08. Bacillaria 2: 56 (1979). SEASONALITY: A. granulata appears from late March to mid-May and its maximal abundance occurs from June to July and from October to November. Especially, the species accounts for the 36 Algal Flora of Korea·Freshwater Diatoms I majority of the phytoplankton biomass during the overturn period in lakes of some regions. DISTRIBUTION: This species is commonly widespread in large and turbid freshwaters around the world. As this is a representative taxon among the Aulacoseira population, it is linked to well-mixed and eutrophic waters. The taxon is dominant in the phytoplankton of many Spanish reservoirs (Gómez et al. 1995), in the Seine River of France (Garnier et al. 1995) and in the Murray River of Australia (Hötzel and Cromme 1996). The species occasionally exhibits overwhelming dominance in Lake Biwa in Japan (Miyajima et al. 1994), and prevails in the phytoplankton of the River Para in Argentina (O’Farrell et al. 2001), in Río de la Plata on the east coast of South America (Licursi et al. 2006), and in lakes and reservoirs of Brazil (Huszar et al. 1998). As for quantitative studies of phytoplankton for 33 years and for more than 80 years of qualitative studies from Lake Peipsi-Pihkva in Russia, A. granulata Fig. 18. Distribution of Aulacoseira gra- continually prevailed in the phytoplankton of sum- nulata. mer and autumn (Yang et al. 1997). This taxon is commonly widespread in the freshwaters of the South America. In addition, paleological studies revealed that A. granulata was the most abundant taxon in the sediment of lowlands in Central Chile (Jenny et al. 2002). KOREA: The occurrence of the species is mostly common and frequent in Korean freshwaters, and this species, including its relatives, are dominant one in plankton assemblages (Chung et al. 1987b; Cho et al. 1993; Lee and Yoon 2002). Distributional patterns of the species in the Nakdong River and the Seonakdong River are shown in the figures below. Maximal abundance of A. granulata was recorded as 4,900 cells/mL in July in the Nakdong River and 4,100 cells/mL in October in the Seonakdong River. The occurrence is frequently interrupted by heavy rains and the abundance progressively declines in August. Filamentous chains of the species are composed of two cells in minimum and 25 cells in maximum in the lower parts of the Nakdong River. Though A. granulata is a leading diatom species among the genus Aulacoseira, it is sometimes subdominant in freshwaters. The seasonal bloom patterns of A. granulata are generally similar in many lakes - Lake Hapcheon, Lake Jinyang, Lake Andong, and other lakes (Kim et al. 1998a; Kim et al. 1999). This species shows larger autumnal and less vernal blooms in its seasonality. However, it occasionally blooms in summer and its abundance reaches over 3,000 cells/mL in Lake Paldang (Han et al. 1995). SPECIMEN EXAMINED: (Planktonic diatoms collected from the Nakdong River near Gupo Bridge: 25.ix.1998). ECOLOGY: This species is mesotrophic and eutrophic algae. The population dynamics of Aulaco- seira are related to flow conditions, turbidity, silica concentration and alkalinity. Aulacoseira diatoms are less prevalent in the more slowly flowing parts of rivers and will reach high cell density when flowing conditions provide physically sufficient turbulence (Hötzel and Croome 1996). In lakes, turbulent or vertical water movement plays an important role in maintaining Aulacoseira filaments Bacillariophyceae: Centrales: Thalassiosiraceae 37 in suspension (Petrova 1986). Diatoms have a large specific gravity compared with other algae and prefer relatively high turbulence to prevent sinking (Petrova 1986). Wind-driven turbulence helps to sustain A. granulata populations in lake waters and to overwhelm the plankton dominance (Miyajima et al. 1994). Turbulence in rivers is active to keep algal filaments in suspension and algal populations develop substantially. Persistent thermal stratification causes Aulacoseira to sink out of euphotic zone and buoyant blue-green algae, such as Anabaena, replace Aulacoseira diatoms in the euphotic zone (Sher- man et al. 1998). In the context of diatom sinking, cell size, shape and density have been considered as a primary cause. However, the sinking velocity of Aulacoseira is correlated with filament morphology rather than cell density (Davey 1986). Morphological variability and dimensions of the valves are closely related with environmental factors - water discharge and level, transparency and turbidity, nutrient concentration and gradients in the reaches (O’Farrell et al. 2001; Turkia and Lepistö 1999). A. granulata is a typical tychoplankton (facultative plankton) buoyed in water column during growing periods and sinking to the bottom at a other certain periods. REMARKS: This is easily defined under light microscopy by the large spines of separation valves and coarse areolae on the mantle. Aulacoseira filaments are separated by two series of cell divisions: firstly to produce the separation valves and secondly to make consecutive divisions (Davey and Crawford 1986). Occasionally, the cells of filaments are alternately covered by cingulum (girdle). Linking valves may be covered by the cingulum and, at this condition, areolar patterns of the mantle are heteromorphic - coarsely vs finely punctate. The species is the most common among the Aulacoseira populations in Korean freshwaters.

6. Aulacoseira granulata f. spiralis (Hustedt) Czarnecki and Reinke 1982: 174 (Figs. 19, 20).

Cho 1999: 145. f. 30. Tuji 2006: 76. f. 1.

BASIONYM: Melosira granulata f. spiralis Hustedt 1927: 251. f. 80. SYNONYM: Melosira granulata var. angustissima f. spiralis Hustet 1930: 88. f. 46.

The tubular filament of colony concentrically coiled on a large scale and 80-120 μm in diameter. One or two spines of separation valve projecting outwards the terminals of the filaments. Valves about 3 μm in diameter and 12 μm in mantle height. Other characteristics of this taxon similar with those of the type species and A. granulata var. angustissima. Fig. 19. Distribution of Aulacoseira granu- TYPE: Locality - Mitterteich in Süd-Mähren region of lata f. spiralis. 38 Algal Flora of Korea·Freshwater Diatoms I

A D

B m

μ 10

C m μ F

10 E

Fig. 20. Aulacoseira granulata f. spiralis. A-D. the view of spirally coiled filaments (×400, LM); E, F. the terminal spine and girdle view of cell (E. ×2,000, LM; F. SEM).

Germany. Holotype - A1/48 in BRM [figure plate 174/1-3 in Simonsen (1987)]. SEASONALITY: The morphotypic taxon occurs mainly in spring and autumn with other Aulacoseira populations. DISTRIBUTION: A. granulata f. spiralis occurs coincidently with other Aulacoseira, but their abundance is relatively low. The species is recorded in Lake Inba-numa, Chiba Prefecture in Japan (Tuji 2006) and in the Pearl River Estuary in China (Wang et al. 2009). It occurs as planktons in the Great Lakes in North America (Stoermer et al. 1999), in the Southern Coastal Fringe of the Río de la Plata in Argentina (Gómez and Bauer 1998) and in Rincón del Bonete Reservoir in Uruguay (Pérez et al. 1999). KOREA: The abundance and frequency of this species are relatively low or less common in Korean freshwaters. In South Korea, the species was recorded three times before 1996 in rivers as A. granulata var. angustissima f. spiralis (Lee 1997) - the Geum River (Chung et al. 1985), the Nakdong River (Kim et al. 1990; Cho 1999) and the Yeongsan River (Chung et al. 1986a). In the lower reaches of the Bacillariophyceae: Centrales: Thalassiosiraceae 39

Nakdong River, the species was less commonly encountered in planktons. SPECIMEN EXAMINED: (Planktonic diatoms collected from the Nakdong River near Gupo Bridge: 28.xi.1993). ECOLOGY: This species has too small population size to clarify its ecological characteristics. REMARKS: Further research is needed to determine whether the variability of this type is generic or environmental conditions.

7. Aulacoseira granulata var. angustissima (O. Müller) Simonsen 1979: 58 (Figs. 21-23).

Krammer and Lange-Bertalot 1991a: 23. f. 18. Cho 1999: 145. f. 19.

BASIONYM: Melosira granulata var. angustissima O. Müller 1900: 315. pl. 12. f. 28. SYNONYM: Melosira granulata subsp. angustissima (O. Müller) Cleve-Euler 1938: 154. Melosira granulata subsp. angustissima (O. Müller) Skabichevskii 1960: 158. m

μ m

μ 10 10

F A B C D G

Fig. 21. Aulacoseira granulata var. angustissima. A-C. the filament of colony (×400); D-G. the mantle and terminal spines of cell in view of girdle (×2,000, LM). 40 Algal Flora of Korea·Freshwater Diatoms I

Aulacoseira granulata var. angustissima Nakdong River 106

105

104

103

102

101 Seonakdong River 106

105

4 Algal abundance (cells/mL) 10

103

102

101 91 92 93 94 95 96

Fig. 22. Seasonal variations of diatom Aulacoseira granulata var. angustissima (grey area) and total phytoplankton (solid lines) in the downstream of the Nakdong River (upper graph) and in the Seonakdong River (lower graph) (cited from Cho and Shin (1999)).

Cells long cylindrical and connected to form long tubular filaments. The filaments composed of 5 cells in minimum and 14 cells in maximum. Valves 3-5 μm in diameter and 11-20 μm in mantle height. The ratios of mantle height and valve diameter 3-5 (to 10). Areolar striae on mantle relatively weak, 7-16 striae in 10 μm, and 9-12 punctas in 10 μm. This variety is more slender than the type species. It is not only differentiated from the morphology of A. granulata, but also with the size.

TYPE: Bacillaria 2: 58 (1979). SEASONALITY: This taxon also shows the bimodal pattern - spring and autumn occurrence. The species overlapped with A. granulata in seasonal variations. DISTRIBUTION: Its seasonal variation and distribution are similar with the type species. The species has higher frequency and dominance in the phytoplankton in Rio de la Plata of Argentina (Gómez and Bauer 1998; O’Farrell et al. 2001), and small lakes of Southern Sweden (Håkansson and Regnéll 1993). KOREA: The annual variations of A. granulata var. angustissima are more irregular than the type Bacillariophyceae: Centrales: Thalassiosiraceae 41 species and other species of genus Aulacoseira. The species is observed mainly from May to November and overlaps with its type species A. granulata. This variety was more important before the estuarine dam contruction in 1987 in the Nakdong River (Chung et al. 1987b) and markedly increased after the 1990s in the Han River to dominate the phytoplankton assemblages (Lee 2004). The species was recorded in the Imjin River by Lee and Yoon (2002). SPECIMEN EXAMINED: (Planktonic diatoms collected in the Nakdong River, Gupo Bridge: 28.xi.1993). ECOLOGY: This species is mesotrophic to eutrophic. Its abundance in flowing rivers is generally less than in lentic waters. REMARKS: The morphological and taxonomic significance between thin A. granulata and the variety shoud be examined further.

Fig. 23. Distribution of Aulacoseira granulata var.

8. Aulacoseira laevissima (Grunow) Krammer 1991: 98 (Figs. 24, 25).

Krammer 1991b: 488. f. 57. Krammer and Lange-Bertalot 1991a: 35. pl. 31. f. 16. Siver and Kling 1997: 1828. f. 75.

BASIONYM: Melosira laevissima Grunow in Van Heurck 1882. pl. 86. f. 24. SYNONYM: Aulacoseira distans var. laevissima (Grunow) Haworth 1990: 195. Melosira laevissima Grunow in Van Heurck 1882. pl. 86. f. 24. Melosira distans var. laevissima (Grunow) O. Müller 1898: 55.

Cells drum-shaped or cylindrical, forming chain by connecting valves. Valves 6-17 μm in diameter and 5-10 μm in mantle height. The ratios of mantle height and valve diameter 0.4-0.7. Valve surface flat and small areolae more and less regularly distributed on the surface, showing typical areolar patterns on the valve of Aulacoseira distans. The rows of areolae on the mantle straight, 21-28 rows in 10 μm and 24-30 puncta in 10 μm, showing fine structures. Collum relatively wide and sulcus distinct between collum and mantle. Linking spines long and pointed with branched tips and lateral thorns. Sometimes, the spines branched at tips or largely dichotomously branched, showing more variable forms. The base of spine lining up one or two mantle costae. Ringleiste (circular ledge on the inside of cylinder) extending about one third of valve diameter.

TYPE: Loch Canmor, Scotland. Coll. Grunow No. 2851. SEASONALITY: A. laevissima dominates the benthic algal assemblages in June and August in moun- 42 Algal Flora of Korea·Freshwater Diatoms I

A B C D E

F m

μ G 10 I

H JK

Fig. 24. Aulacoseira laevissima. A-F. the valve mantle and delicate striae on the mantle (LM); G, H. the valve mantle and interlocking spines around the valve; I-K. the interlocking spines with tips between two valves (SEM). Bacillariophyceae: Centrales: Thalassiosiraceae 43 tain mire pool of Japan (Watanabe et al. 2000). DISTRIBUTION: The diatoms of the species have been found less frequently in Europe except the the type locality and the Cumbrian waters in UK (Krammer and Lange-Bertalot 1991a). It occurred in freshwaters of Connecticut in USA (Siver and Kling 1997) and predominated 40% of the biomass of epipelic algae in a mire pool covered with Sphagnum in Japan (Watanabe et al. 2000). KOREA: So far, this species was collected only in a mountain bog, Daeseongdwitneup, near Mountain Jeongjok at Ulsan. This is the first description in South Korea. SPECIMEN EXAMINED: (Benthic diatoms collected in Daeseongdwineup Bog around Mountain Jeongjok in Ulsan: 26.xii.2009). ECOLOGY: This species inhabit preferably the waters of low alkalinity and conductivity. REMARKS: The numbers of mantle costae per a spine Fig. 25. Distribution of Aulacoseira laevis- are variable from one to even four (Siver and Kling, sima. 1997). The bases of the spines of our specimens were from one or two mantle costae. The diameter of our specimens are wider than mantle height. A. laevissima has some similarities to the A. lacustris (Gru- now) Krammer and A. nygaardii (Camburn) Camburn and Charles, however, the former has completely areolated valves (Krammer 1991b).

9. Aulacoseira muzzanensis (Meister) Krammer 1991: 98 (Figs. 26, 27).

Krammer 1991: 478. f. 1. Krammer and Lange-Bertalot 1991a: 24. f. 20. Cho 1999: 151. f. 32.

BASIONYM: Melosira muzzanensis Meister 1912: 41. 232. pl. 1. f. 10. SYNONYM: Melosira polymorpha var. muzzanensis (Meister) Bethge 1925: 32. pl. 1. f. 5. Melosira granulata var. muzzanensis (Meister) Hustedt 1930: 88. f. 47. Aulacoseira granulata var. muzzanensis (Meister) Simonsen 1979: 59.

Cells drum-shaped or short cylindrical, connected to form tubular filaments. The filament relatively short and two-cell filaments frequent. Valves circular and flat, 8-25 μm in diameter and 4-8 μm in mantle height. The ratios of mantles and valve diameter 0.3-0.6. The areolar striae on the mantle of separation valve strong, straight or nearly parallel to pervalvar axis. However, striae on the other mantle weakly curved or oblique to pervalvar axis. Pervalvar striae 10-13 in 10 μm and punctas 9-19 in 10 μm. In electron microscopic view, areolae covered by irregular lips and lying between pervalvar and transapical ribs ornamented by dots. Interlocking spines of linking valve, arranged as conversely equilateral triangle. The spines intermediate forms between A. granulata 44 Algal Flora of Korea·Freshwater Diatoms I m

μ 10

C D

Fig. 26. Aulacoseira muzzanensis. A, D. the linear punctuate striae on mantle and terminal spines (×2,000, LM); B. the spines in the margin of separation valve (SEM); C. locking spines between two linking valves (SEM).

and A. ambigua. The spines of separation valve long pointed and lining up two pervalvar costae.

TYPE: Nova Hedwigia 52: 98 (1991). SEASONALITY: A. muzzanensis occurs in more warmer periods or summer than other Aulacoseira species. In the Nakdong River, A. muzzanenesis is observed with high frequency in July and August, while its abundance is low. DISTRIBUTION: This taxon is reported in many more humid regions in the Northern Hemisphere. KOREA: The abundance of this species is relatively low in Korean freshwaetrs. In the past, it may be first recorded as A. granulata var. muzzanensis in the North Han River (Chung and Kim 1970). This species is less commonly observed in the lower parts of the Nakdong River (Cho 1999; Bacillariophyceae: Centrales: Thalassiosiraceae 45

Cho and Shin 1999). SPECIMEN EXAMINED: (Planktonic diatoms collected from the Nakdong River near Gupo Bridge: 25.ix.1998). ECOLOGY: The diatoms of this species would have low competitive potential due to large size. REMARKS: The morphological outline is similar to A. granulata. However, the valve diameter is longer than the mantle height. Spines of separation valves are more numerous than in A. granulata. This species has been included as a member of A. granulata in Korean freshwaters until recently. It was first reported as A. muzzanensis in the Nakdong River by Cho (1999).

10. Aulacoseira nygaardii (Camburn) Camburn and Charles 2000: 14 (Figs. 28-30). Fig. 27. Distribution of Aulacoseira muz- Camburn and Charles 2000: 14. pl. 3. f. 9. Siver and zanensis. Hamilton 2005: 258. f. 1.

BASIONYM: Melosira nygaardii Camburn in Camburn and Kingston 1986: 26. pl. 3. f. 16.

Cells drum-shaped or cylinder in outlines, rectangular in girdle view with rounded junction of valve face and mantle. A step-like demarcation below the junction of valve and mantle. Valves 5- 11 μm in diameter and 4-19 μm in mantle height. The ratios of mantle and valve diameter 0.6-1.1. Striae on the mantle usually parallel to pervalvar axis, 20-30 striae in 10 μm and 25-30 punctas in 10 μm. The collum broadly developed and unornamented. Valve faces hyaline except for a peripheral ring of areolae. These areolae continuous on the mantle. Marginal spines at the junction of valve and mantle, broadly flattened or isosceles triangle with lateral papillae. However, the spines highly irregular in length and shape, and appeared to be molded around neighboring spines. A spine lining up a costal rib and firmly interlocked to make long filaments. Ringleiste very shallow, simple swellings on the inside of girdle. The presence of rimoportulae on mantle not yet convinced, though constant characteristics in many Aulacoseira species.

TYPE: Locality, sediments in Lake Sand, Alger County, Michigan, USA. SEASONALITY: As this species prefer cold waters in alpine area, it may well adapt to cold season throughout the year, different with other Aulacoseira diatoms. DISTRIBUTION: A. nygaardii is commonly distributed in 116 low-alkalinity lakes in the Adirondack mountain park in northern New York (Camburn and Charles 2000). The species reported to be widespread in the midwest, the northeast and the southeast regions in USA, the northern regions in Quebec, and less frequently reported in northern Europe (Siver and Hamilton 2005). This is dominant species in sedimentary and palaeoecological records of a high alpine soft-water lake, in Austria (Koinig et al. 1998), a permafrost profile from a lake in central Siberia (Kienel et al. 1999), 46 Algal Flora of Korea·Freshwater Diatoms I

A E

B G

C D H F m

μ 10

LK P I

MN O

Fig. 28. Aulacoseira nygaardii. A-L. the mantle and areolar striae on mantle; M. Ringlesite on the inside of cellular cylinder; N-P. a ring of striae on valve margin. J-O. DIC images of LM. Bacillariophyceae: Centrales: Thalassiosiraceae 47

C A B

D F

E G

Fig. 29. Aulacoseira nygaardii. A. the valve mantle, convex valve in girdle view, and a step-like demarcation below the junction of valve and mantle; B. a ring of areolae on valve margin; C. the inside of valve; D, E. interlocking spines and areolar striae on mantle; F, G. the irregular forms of interlocking spines (SEM). 48 Algal Flora of Korea·Freshwater Diatoms I and of a small lake in northwest Spain (Leira 2005). KOREA: A. nygaardii occurred dominantly in Wang- deungjaeneup Bog of Mountain Jiri in Sancheong, in January and April, 2010. It is the first report of this species in Korea. SPECIMEN EXAMINED: (Benthic diatoms collected in Wangdeungjaeneup Bog of Jiri Mountain, Sancheong: 17.iv.2010). ECOLOGY: The species diatoms are more common in acidic, nutrient-poor waters of alpine environments. REMARKS: Though our specimens are significantly different with the description of Siva and Hamilton (2005) in shapes of interlinking spines, the local taxon is certainly A. nygaardii. A. nygaardii shares some similarities with neighboring species - A. lacustris (Grunow) Krammer, A. perglabra (Østrup) Haworth and A. laevissima (Siver and Hamilton 1997). Melosira nygaardii Camburn reported from the Okefenokee swamp in Georgia by Scherer (1988) is similar to A. nygaardii, Fig. 30. Distribution of Aulacoseira nyga- however, is quite different in important characteristics ardii. to be required the further studies (Siver and Hamilton 2005).

11. Aulacoseira subarctica (O. Müller) Harworth 1990: 195 (Figs. 31-33).

Haworth 1988: 143. f. 43. Krammer and Lange-Bertalot 1991a: 28. f. 23. Cho 1999: 151. f. 24. Gibson et al. 2003: 84. f. 1.

BASIONYM: Melosira italica subsp. subarctica O. Müller 1906: 78. pl. 2. f. 10. SYNONYM: Aulacoseira italica subsp. subarctica (O. Müller) Simonsen 1979: 60. Aulacoseira italica var. subarctica (O. Müller) Davydova in Gleser, Makarova, Moisseeva and Nikolaev 1992: 82. pl. 61. f. 19.

Cells drum-shaped or cylindrical, and connected to form long tubular filament. Valves circular, 3-15 μm in diameter and 2.5-18 μm in mantle height. The ratios of mantles and valve diameter 0.8-3. Valves slightly convex and pseudosulcus definite around the margin of two valve junction. Areolar striae on mantle curved in rows to pervalvar axis, 18-20 striae in 10 μm and 18-21 punctas in 10 μm. Collum short, and sulcus clear between the mantle and intercalary band in the unresolved focus of light microscopy. Sulci V-shaped, however, not as clear as in A. ambigua. In electron microscopy, spines long pointed and arranged regularly around valve margin. Spines lining up two pervalvar ribs on mantle. Ringleiste relatively broad on the inside near mantle margin. Siliceous walls of cells very thick, and separation and linking valves not differentiated.

TYPE: Diatom Research 5: 195 (1990). Bacillariophyceae: Centrales: Thalassiosiraceae 49

B E C m A μ F 10 D

G I J

Fig. 31. Aulacoseira subarctica. A-E. the girdle view of diatom cell (×2,000); F. two linking valves covered by cingulum (girdle band); G, J. spines of separation valve; H. the Ringleiste (circular edge) in the inside of a cylinder; I. the valve face and areolae in valve margin (SEM).

SEASONALITY: A. subarctica blooms in spring and autumn, and represents a typically bimodal annual phenology. DISTRIBUTION: This species is widely reported from many parts of the world and its distribution 50 Algal Flora of Korea·Freshwater Diatoms I

Aulacoseira subarctica Nakdong River 106

105

104

103

102

101 Seonakdong River 106

105

4 Algal abundance (cells/mL) 10

103

102

101 91 92 93 94 95 96

Fig. 32. Seasonal variations of the diatom Aulacoseira subarctica (grey area) and total phytoplankton (solid lines) in the downstream of the Nakdong River (upper graph) and in the Seonakdong River (lower graph) (cited from Cho and Shin (1999)).

overlaps with other Aulacoseira populations. In the early times, the species is dominantly recorded in many lakes of the English Lake District and Scotland, and in Lake Lough Neagh of Ireland (Gib- son et al. 2003). It is also widely distributed in inland waters of Northern Europe, Scandinavia and North America (Siver and Kling 1997). In paleologcal distribution, it is abundant from early-Holo- cene to mid-Holocene throughout northwest Europe (Gibson et al. 2003). KOREA: The population appears early in spring and peaks in May-June, and November. The maximal abundance range was 600-1,550 cells/mL in May-June and 800-6,780 cells/mL in Novem- ber (Cho 1999). In 1995, A. subarctica abnormally bloomed in September with 1,250 cells/mL; the abundance of A. subarctica was higher in autumn than in spring. The species was a dominant phytoplankton in Suer Stream, a mountain stream of Gwangyang (Lee and Yoon 2000). The species have also bloomed as a dominant species in Lake Daecheong, Lake Jinyang, Lake Imha and Lake Paldang; it prefers lake habitats to streams. SPECIMEN EXAMINED: (Planktonic diatoms collected in the Joman River near Joman Bridge: 11.xi. 1998). ECOLOGY: A. subarctica is more competitive in the warmer season than other Aulacoseira species. Bacillariophyceae: Centrales: Thalassiosiraceae 51

The species is considered to be diatoms of mesotrophic waters. It is all abundant at lower total phosphorus concentrations than common planktonic Aulacoseira species, A. granulata, A. ambigua and other eutrophic diatoms (Gibson et al. 2003). REMARKS: It is doubtful that A. subarctica may be widely mistaken as A. distans or A. distans var. alpigena by some authors in Korea, because of the difficulty in distinguishing the two group by light microscopy. Concerning its cellular size and outlines viewed by light microscopy, this taxon resembles A. distans and its relatives. However, the species is identified as A. subarctica considering features of its spines of interlocking valves with electron microscopy (Cho 1999). A. subarctica observed in the Nakdong River has two forms with different cell size. Typically, cells are markedly wider than long and, therefore, the ratios of mantle and valve diameter low. Valves 4-7 μm in diameter, mantles 2.5-3.5 μm in height and mantle/ Fig. 33. Distribution of Aulacoseira suba- diameter ratios 0.4-0.7. In some populations, valve rctica. diameter 3.5-4.5 μm, mantle height 3.5-4.5 μm and their ratios approximately 1. These diatoms are less abundant.

12. Aulacoseira tethera Haworth 1988: 142 (Figs. 34, 35).

Haworth 1988: 142. f. 28. Krammer 1991a: 96. f. 73. Krammer and Lange-Bertalot 1991a: 36. pl. 33. f. 1.

Cells drum-shaped or short cylinder, connected with valves to form filaments. Valves flat or plain, 6.5-14 μm in diameter and 2.5-4 μm in mantle height, generally wider than long. The valve face hyaline except for a peripheral ring of coarse areolae or large pores. These areolae continuous on the mantle. Areolar striae on mantle parallel or slightly curved along pervalvar axis, 11-16 striae in 10 μm. Striae distinctly areolate and the areolae varied in size. Collum very small and sulcus narrow, poor developed. Marginal spines on valve spathulate-shaped with anchor-tips. Ringleiste quite shallow and two or three rimpoportulae near mantle margins.

TYPE: Locality, three tarns, at Langdale, in Cumbria of England and also present in other upland tarns. SEASONALITY: It is assumed that the seasonality of the species is spring or summer in arctic regions, and spring and autumn in north temperate regions. DISTRIBUTION: A. tethera is important in acidic and no alkaline tarns of Cumbrian waters in England (Haworth 1988). Furthermore, it is observed abundantly in seven arctic lakes of an island 52 Algal Flora of Korea·Freshwater Diatoms I

E F G H CD I AB

JKLM

ON m

P 10

T SR

Fig. 34. Aulacoseira tethera. A-O. the mantle view and areolar striae on the mantle (×2,000) (LM); P. valve mantle and large areola on mantle; Q, R. valve face and a ring of areolae on valve margin; S, T. shallow Ringleiste in the inside of a cylinder. (SEM); E-O. DIC images of LM.

off northeast Greenland (Cremer and Wagner 2004; Cremer et al. 2005). The species is abundant in the low-alkalinity waters of Adirondack mountain lakes, New York of North America (Camburn and Chalres 2000). Bacillariophyceae: Centrales: Thalassiosiraceae 53

KOREA: The diatoms of the species occurred abundantly in the third Mujechineup Bog in Mountain Jeongjok of Ulsan, in December 25, 2009. This is the first report in South Korea. SPECIMEN EXAMINED: (Peat deposits collected in the third Mujechineup Bog in Mountain Jeongjok of Ulsan: 25.xii.2009). ECOLOGY: This species is acidophilous and oligotrophic, and abundantly occurs in low-alkalinity waters. It is reported from freshwaters, between pH 4.4 to 5.3 in upland lakes of Cumbria in England (Haworth et al. 1988). These diatoms of the species prefer shallow waters, but with enough open water habitats. REMARKS: Diatoms belonging to A. tethera are occasionally confused with the neighboring species, especially, A. distans and its relatives, A. alpigena and other small Aulacoseira. However, it well delimited from A. distans groups with the morphology of valve faces. Fig. 35. Distribution of Aulacoseira tethera.

Genus Cyclotella Kützing ex de Brébisson 1838: 19. Dan-chu-dol-mal-sok (단추돌말속)

Cells short drum-shaped with circular valves. Primarily solitary and occasionally in short chains. Central and marginal regions distinctly separated and often either tangentially or concentrically undulated in central parts. Various ornamented structures or hyaline spaces in central area. Areolar rows grouping as fascicles from valve center toward outer region of the valve. Valve margin without a distinct ring of spines. Fultoportulae near the valve margin and often scattered on the valve center. A single rimoportula on folds or the edge of valve. The interior of the valve margin chambered as loculi along costal ribs. Valve mantle very shallow. Additional characteristics taken into consideration are the structure of areolar fascicles, the presence of fultoportulae and spines on the valve face, the undulation of central area, the location and numbers of fultoportulae and rimoportulae (Loginova 1988). The genus Cyclotella is differentiated from other cyclostephanoid diatoms by a number of morphological characteristics such as the separation of central and marginal valve region, the undulation and often granular ornamentation in the valve center, locular chambers in the valve margin, a shallow valve mantle, etc. In addition to the above-mentioned characteristics, Cyclotella differs from Stephanodiscus in the absence of a marginal spine circumstance and external portular tubes. Lectotype: Cyclotella operculata (C. A. Agardh) Brébisson.

SPECIES: There are approximately 228 species and infraspecific names of this genus in the database, of which 106 species are accepted taxonomically (Algaebase 2010). According to the check-list 54 Algal Flora of Korea·Freshwater Diatoms I data compiled by Lee (1995), KNCCN (1996) and Lee (1997), 17 Cyclotella taxa were recorded in Korea. DISTRIBUTION: Cyclotella diatoms are primarily planktonic and most of them are restricted to freshwater habitats. Cyclotella taxa are widely distributed in oligotrophic to eutrophic waters, deep alpine and subalpine lakes in significant abundances. But, some live in brackish waters and only a few taxa in marine waters. Some taxa are tolerant to the brackish or marine water environment. Approximately more than 100 Cyclotella taxa were identified and described throughout the global scales (Round et al. 1990; Krammer and Lange-Bertalot 1991a). Approximately 20 Cyclotella species have been recorded until now in freshwaters, brackish and marine waters of Korea. Cyclotella species in freshwaters are more rich and diverse than any other centric group. In the Han and Nakdong River, twelve Cyclotella species are described or reported in floral studies: C. atomus, C. comta (=C. radiosa), C. glomerata, C. kützingiana, C. meneghiniana, C. ocellata, C. orientalis (=C. asterocostata), C. pseudostelligera, C. stelligera (Chung et al. 1987b; Kim and Lee 1991; Cho et al. 1993; Seo and Chung 1993; Lee 1994, Moon and Lee 1995). C. fottii Hustedt, C. rossii Håkansson and C. wolterekii Hustedt were added to the species pool of Cyclotella by Lee (1995) and Cho (1996). After the construction of estuarine barrages in the large rivers of Korea, eutrophication of estuarine waters was accelerated. All Cyclotella species prefer eutrophic or hypereutrophic water, particularly with nitrogen and phosphorus fertilization. Small planktonic Cyclotella species are abundant in many nutrient-rich waters. KEY REFERENCE: Round (1970), Harworth and Hurley (1986), Kling and Håkansson (1988), Logi- nova (1988), Lee and Lee (1988), Krammer and Lange-Bertalot (1991), Lee (1994), Cho (1996)

Key to the species of genus Cyclotella

1. No shadow lines in the margin of valve ·················································································2 - Shadow lines present in the margin of valve·········································································26 2. Indistinct ornaments or no ornaments in the central zone of valve ·········································3 - Distinct ornaments in central zone························································································12 3. Tangentially undulation in the central zone of valve ······························································4 - Different with the tangential undulation ················································································9 4. The central zone of valve elliptical-shaped ·············································································5 - Other formed ·························································································································6 5. Without fultoportulae in central zone··············································································C. iris - Many fultoportulae in central zone···································································C. michiganiana 6. Irregular pits and elevation in central zone·············································································7 - Other structures in central zone ·······································································C. meneghiniana 7. Valve diameter more than 20 μm ················································································C. striata - Valve diameter less than 20 μm ······························································································8 8. Delocate ornaments in the margin of valve··································································C. caspia - Strong ornaments in the margin of valve ···························································C. hakanssoniae 9. Relatively large form, more than 25 μm in diameter·············································C. plitvicensis - Relatively short form, less than 20 μm in diameter ·······························································10 10. Colony form···········································································································C. delicatula - Unicell form··························································································································11 11. Many sectors by radial structures in the central zone···············································C. comensis - Central zone hyaline without ornaments··························································C. cyclopunctata 12. Star-shaped structures in central zone ··················································································13 Bacillariophyceae: Centrales: Thalassiosiraceae 55

- Other forms in central zone ··································································································16 13. Valves less than 10 μm in diameter ·······················································································14 - Valves more than 10 μm in diameter·····················································································15 14. Cells forming a colony ···························································································C. glomerata - Cells solitary without joining ········································································C. pseudostelligera 15. Star-shaped ornaments, not composed of areolae, in central zone ···························C. stelligera - Star-shaped ornaments composed of areoale ································································C. rossii 16. Small forms between 3-10 μm in diameter ···········································································17 - Large forms, more than 25 μm in diameter ···········································································19 17. The papillar projections in central zone rounded ··································································18 - The papillar projections in central zone seldom rounded ·····································C. trichonidae 18. The central zone of valve flat without undulation ·····················································C. ocellata - The central zone of valve undulated ········································································C. tripartia 19. Radial ornaments in central zone··························································································20 - Other forms in central zone ··································································································22 20. Cells solitary ················································································································C. elgeri - Cells forming colony ············································································································21 21. Colony cylindrical-shaped···················································································C. planctonica - Colony other formed ·································································································C. socialis 22. Rarely ornamented in central area ························································································23 - Distinctly ornamented in central area ···················································································24 23. The central zone of valve elliptical ······································································C. schumannii - The central zone of valve rounded·····································································C. distinguenda 24. No crater-shaped structures in central zone··········································································25 - Apparently areolar structures or areolae in central zone·········································C. krammeri 25. Central zone large, with regular areolation ·······························································C. areolata - Central zone small, with irregular areolation ································································C. fottii 26. Radial structures in central zone···························································································27 - Other formed in central zone································································································32 27. Faint or weak structures in the marginal zone of valve ·························································28 - More distinct structures in marginal zone·············································································30 28. Valve with strongly radial structures ···················································C. bodanica var. lemanica - Valve without radial undulation···························································································29 29. Radial areolar lines in central zone, relatively weak·····························C. bodanica var. bodanica - Radial areolar lines in central zone, loosely, not densely arranged···········C. bodanica var. affinis 30. Cells forming long chain colony ·················································C. praetermissa, C. quatrijuncta - Cells solitary·························································································································31 31. Valves weakly silicified ······················································································C. glabriuscula - Valves thickly silicified ······························································································C. radiosa 32. Valves less than 7 μm in diameter·························································································33 - Valves more than 7 μm in diameter·······················································································34 33. The margin of valve shallow and central area large ···················································C. atomus - The central area relatively small ······································································C. wuethrichiana 34. Star-shaped ornaments composed of large areolae in central zone·····························C. antique - Other forms in central zone ··································································································35 56 Algal Flora of Korea·Freshwater Diatoms I

35. Valves elliptical ·······································································································C. austriaca - Valves rounded·····················································································································36 36. Radial areolation in central zone···············································································C. styriaca - Tangential undulation in central zone···················································································37 37. The structure of marginal zone relatively weak·······················································C. stylorum - The structure of marginal zone strong ··································································C. baikalensis (Krammer and Large-Bertalot 1991a)

REMARKS: Since F. T. Kützing first described the genus Cyclotella in 1833, microstructures of diatoms have been revealed by electron microscopy. Recently, many new taxa have been reported by the revision of the earlier described discoid diatoms such as Cyclotella and Stephanodiscus, especially small centric diatoms. Some small centrics can not be resolved in sufficient detail under light microscopy and their morphologies can now be exclusively differentiated on the basis of electron microscopy. Except for large diatoms such as C. meneghiniana, there has been some taxonomic confusion in describing Cyclotella taxa in the local studies of phytoplankton. Important Cyclotella floras encountered in the Nakdong River were not in accordance among the authors. It is assumed that there has been a lot of inaccuracy in taxonomic identification in floral study. Taxonomic confusion is due to small size and the lack of local informations regarding light or electron microscopic morphology. Floral studies for the ecological distribution have been more usual than the morphological studies for taxonomy until now. The first electron micrographes of Cyclotella were made by Lee and Lee (1988) in the study of phytoplankton in the southern and western coastal zone of Korea. Five Cyclo- tella species were illustrated by Lee et al. (1994b) and Lee et al. (1995a), and eight species were described by Cho (1996) in the lower reaches of the Nakdong River, repectively. During a phytoplankton monitoring course in the Nakdong River in the last 5 years, many Cyclo- tella species were encountered with high abundance and importance, including small-size (⁄5 μm) diatoms that could not be easily resolved with light microscopy. Small centric diatoms such as

Table 2. Summary of morphological characteristics of eight Cyclotella species observed in Korean freshwater. RP: rimoportular number, mFP: marginal fultoportulae, cFP: central fultoportulae, CA: central area, mSP: marginal spine, a: i-th costae per each FP, b, e: satellite pores of marginal and central FP, respectively, c: presence of FP external tube on valve face, d: numbers of cFP, f: tangential undulation in the central zone, g: ornaments of the central zone. +: presence, -: absence. Characteristics included in parenthesis are cited from other reference. mFP cFP CA Species RP mSP abc d ef g C. meneghiniana 112- 0-4 3 + hyaline + C. atomus 13-42- 13- hyaline +/- C. stelligera 13-42+ ---striated - C. pseudostelligera 13-52+ ---striated - C. woltereckii 13-62+ ---striated/absent - C. glomerata 13-42+ ---striated - C. asterocostata 13-52+ ---striated - C. radiosa 112- (30-90) 2-4 - striated - Bacillariophyceae: Centrales: Thalassiosiraceae 57

Cyclotella and Stephanodiscus are the most common and important in Korean freshwaters. In addi- tions, C. meneghiniana and stelligeroid Cyclotella group are abundant in the lakes and rivers. They simultaneously occur in their bloom or growths, however, their ecological niches are unique. Ste- phanodiscus persistently blooms in the cold season from November to April of the following year (Cho and Shin 1995). On the other hand, Cyclotella species generally bloom from spring to autumn or early winter. Some Cyclotella species are overlapped in their seasonality or the local distributions and make algal assemblges with polyspecific populations. The morphology and ultrastructure of Cyclotella species are summarized in Table 2. Eight species are classified into three groups. These are C. meneghiniana, C. stelligera and C. radiosa form. Krammer and Lange-Bertalot (1991) also classified this genus into three groups. The important characteristics are the structure of the central zone (except undulation and fultoportulae) and the presence of coarse costal ribs. The numerical characteristics of 3 stelligeroid species are identical with each other, but their morphological characteristics are variable.

13. Cyclotella asterocostata Lin, Xie and Cai in Xie, Lin and Cai 1985: 473 (Figs. 36, 37).

Lin, Xie and Cai. 1985: 473. f. 1. Lee et al. 1995b: 37. f. 9. Cho 1996: 12. f. 12.

SYNONYM: Cyclotella orientalis Lee et al. 1995: 145. Discostella asterocostata (Lin, Xie and Cai) Houk and Klee 2004: 220.

Cells large disc-shaped and solitary. Valves circular and 15-27 μm in diameter. Central and marginal zones divided by hyaline area on valve. The central zone concave in one valve and convex in the opposite valve. Striae 13-15 in 10 μm and composed of two areolar rows. Striae arranged radially in the central and marginal zone of the valve. Fultoportulae with long external tube on valve margin and situated at intervals of 3-5 interfascicular costal ribs.

TYPE: China (type locality not specified). JNU HOP 760358 (16). Acta Phytotax. Sin. 23: 473. pl. 1 (1985). SEASONALITY: Considering the bloom in a reservoir in Korea, its seasonality is likely to be autumn. Its abundance is relatively high in autumn (Spetember and October) in the Nakdong River. DISTRIBUTION: The taxonomic description for the species was reported at three countries - China, Lake Biwa in Japan and some freshwaters in Korea (Xie et al. 1985; Lee et al. 1995a; Cho 1996; Tuji and Houki Fig. 36. Distribution of Cyclotela astero- 2001). It is suggested that the species is confined to costata. 58 Algal Flora of Korea·Freshwater Diatoms I

B CD A m

10 G E F

HIJ

Fig. 37. Cyclotella asterocostata. A-G. the valve view of cell (×2,000, LM); H. the radiating striae on valve and a ring of fultoportulae on valve margin (SEM); I, J, L. a rimoportular tube and many fultoportulae in the inside of valve margin (SEM); K. the valve view of a cell (TEM). Bacillariophyceae: Centrales: Thalassiosiraceae 59 the Northeast Asia regions. KOREA: The diatoms of this species are observed less commonly in the lower reaches of the Naktong River. However, it was reported as the dominant plankton in Nammae Reservoir of Gyeongsan in October, 2000 (Kim et al. 2003). SPECIMEN EXAMINED: (Planktonic diatoms collected from the Nakdong River near Gupo Bridge: 28.xi.1993). ECOLOGY: Dependent upon insufficient information of population dynamics, the ecological characteristics of the taxon are not clear. REMARKS: This species is the largest among Cyclotella diatoms observed in Korean freshwaters. It was described as a new species, C. orientalis, in South Korea by Lee et al. (1993, 1995), however, had already been established in 1985 as a specimen type in China.

14. Cyclotella atomus Hustedt 1937: 143 (Figs. 38-40).

Lowe 1975: 415. f. 1; Krammer and Lange-Bertalot 1991a: 53. pl. 51. f. 19. Genkal and Kiss 1993: 40. f. 1. Cho 1996: 11. f. 7.

A B

EFGH D m μ 10 C I J K L M

Fig. 38. Cyclotella atomus. A. the valve view of a diatom cell (TEM); B, C. a fultoportula in central area and a ring of fultoportuae on marginal area in inside view of valve (a white arrow indicates the outer opening of the fultoportula) (SEM); D-J. the marginal striae and a central punct on valve (×2,000); K-M. the girdle view of the cell (×2,000) (LM). 60 Algal Flora of Korea·Freshwater Diatoms I

Cyclotella atomus Nakdong River 106

105

104

103

102

101

Seonakdong River 106

105

Algal abundance (cells/mL) 10

103

102

101

91 92 93 94 95 96

Fig. 39. The seasonal variations of Cyclotella atomus population (grey area) and total phytoplankton (solid lines) in the Nakdong and Seonakdong River (cited from Cho and Shin (1999)).

Cells small drum-shaped and solitary. Valves 3.5-7 μm in diameter, weakly undulated or flat. The central and marginal zone of the valve not differentiated. Costae stronger and thickened, slightly depressed on the marginal zone of valve. Fultoportulae situated per 3-4 costal interval, having no external tubes on valve or valve mantle. One fultoportula near the central zone of valve. From the view of valve inside, the central fultoportula with three satellite pores and the marginal fultoportula with two pores. In TEM view, areolar structures similar with those of C. meneghiniana.

TYPE: Java, Sindanglaja Stausee, pl. Coll. Hustedt, Ac 1/48. Arch. Hydrobiol. Suppl. 15: 143. pl. IX: f. 1 (1937). SEASONALITY: The data illustrate the seasonal variations of the C. atomus population during last 5 years in the Nakdong River in Korea. The fittest season for the C. atomus growth is from April to June, and September to October. Its maximal abundance ranges from 103 cells/mL to 105 cells/mL. Its decrease in summer and winter is related with the monospecific bloom of other planktonic algae such as Stephanodiscus and Microcystis population, respectively. Its maximum has been recorded in spring and summer in the drainages of the Great Lakes (Klarer and Millie 1994). DISTRIBUTION: Phytoplankton was completely dominated by C. atomus in the Tamar River estuary Bacillariophyceae: Centrales: Thalassiosiraceae 61 of England (Jackson et al. 1987) or concurrently col- onized with both C. atomus and C. meneghiniana in many regions - the Meuse River in Belgium, the Ebro River of Spain, the Sandusky River in Ohio, Lake On- tario and adjacent Rivers, Lake Erie, the lower reach of the Nagara River in Japan and the 49 lakes along the Yangtze River in China (Lowe and Kline 1976; Makarewicz 1987; Sabater and Munoz 1990; Mura- kami et al. 1992; Gosselain et al. 1994; Klarer and Millie 1994; Yang et al. 2005). The diatom was recorded for the first time in Lake Michigan in 1964 and is widespread over the adjacent lakes and rivers. C. atomus is abundant in freshwater and even brackish environments in North America, Europe and Asia, and has also been recorded in Argentina and South Africa. KOREA: C. atomus was first reported in the epipsammic diatoms in the estuary of the Nakdong River by Cho (1989) and recorded in the Donghwa Stream by Hong and Chung (1990). Since then, the species have Fig. 40. Distribution of Cyclotela atomus. mainly been reported in the Nakdong River system (Lee and Chung 1992; Cho et al. 1993; Lee et al. 1995a). Particularly, the major plankton in the algal bloom in Lake Shihwa was C. atomus and C. meneghiniana before the input of seawater into the lake to improve water quality (Choi et al. 1997). In many localities, this is also a sub-dominant plankton in freshwaters and its abundance may rank as the second among Cyclotella species. SPECIMEN EXAMINED: (Planktonic diatoms collected from the Nakdong River near Gupo Bridge: 13.ix.1993). ECOLOGY: As a halophilic species, the abundance of C. atomus is correlated with high conductivity and chloride levels, and C. atomus and C. meneghiniana are dominant in the lower reaches of rivers (Makarewicz 1987). Also, the two species are good indicators of highly elevated eutrophication in water bodies. In the Great lakes, it is often associated with polluted, eutrophic, warm harbors and nearshore areas (Yang et al. 2005). C. atomus grows well at 15-20°C water temperature and occurs at maximum abundance at the upper end of this range, although it can also tolerate higher temperature. The species can tolerate turbulence as well as frequent osmotic stress. It has been recorded with common frequency in freshwaters, brackish water and saltwater. In Lake Michigan, it occurs in littoral areas that have abnormally high chloride levels. It has made up large component of diatoms in Lake Ontario and the Oswego River regions during periods of high chloride concentration. REMARKS: The species is ranked as second next to C. meneghiniana in its abundance and frequency among Cyclotella groups in Korean freshwaters. 62 Algal Flora of Korea·Freshwater Diatoms I

15. Cyclotella fottii Hustedt in Huber-Pestalozzi 1942 (Figs. 41, 42).

Huber-Pestalozzi 1942: 400. f. 492. Krammer and Lange-Bertalot 1991a: 49. pl. 47. f. 3a.

SYNONYM: Cyclotella fottii Hustedt in Fott 1933: 162. Cells disc-shaped and solitary. Valves flat and (13)40-90 μm in diameter. The central and marginal area of the valve clearly divided, central area hyaline and marginal area with costae. Hyaline central area small and their boundary more and less regular. Costal ribs strong and dichotomously branched from center towards valve margin. The costae regularly arranged, 8-10 in 10 μm.

TYPE: Fott, Bull. Inst. Et Jard. Bot. Univ. Beograd 2: 162(1933). SEASONALITY: Its seasonality is obscure due to rare frequency and low abundance in freshwaters. DISTRIBUTION: C. fottii is an important endemic phytoplankton of Lake Ohrid of Macedonian - Albanian border, which is oligotrophic and the oldest lake in Europe (Roelofs and Kilham 1983; Matzinger et al. 2006). In addition to the current flora, Cyclotella diatoms such as C. fottii are abun-

B A

C m

μ 10

E F

Fig. 41. Cyclotella fottii. A-F. the valve view and radial costae from the center towards the margin of valve (×2,000, LM). Bacillariophyceae: Centrales: Thalassiosiraceae 63 dant in the sediment stratigraphy of the lake. KOREA: This species occurs in the lower reaches of the Nakdong River, however, its abundance and frequency are low. It is found in the epilithic diatom assemblages in the Namhan River. SPECIMEN EXAMINED: (Epilithic diatoms collected in the lower parts of the Namhan River in 1993). ECOLOGY: This species is classified as typically pelagic and oligotrophic species. C. fottii shows major growth between 20-50 m depth and is clearly dominant between 40-150 m depth in Lake Ohrid (Matzin- ger et al. 2006). REMARKS: It is typically euplankton and is frequently observed as fossil diatoms in stratigraphic studies of Lake Ohrid of Yugoslavia (Roelofs and Kilham 1983).

Fig. 42. Distribution of Cyclotella fottii.

16. Cyclotella glomerata Bachmann 1911: 131 (Figs. 43, 44).

Lowe 1975: 421. f. 21. Kling and Håkansson 1988: 78. f. 101. Krammer and Lange-Bertalot 1991a: 51. pl. 49. f. 11. Cho 1996: 12. f. 76. Tuji and Williams 2006b: 2. pl. 1. f. 1.

SYNONYM: Discostella glomerata (Bachmann) Houk and Klee 2004: 220

Cells small drum-shaped and connected to form short chains with a few cells or balls of long thread. Valves circular and 3-8 μm in diameter. Valves divided into central and marginal zone. Th central area hyaline or radially striated, and convex or concave. Marginal fultoportulae radially situated on mantle to every 3-4 striae. Fultoportulae with cone-shaped tubes in ouside and two strut pores in inside. A rimoportula on valve mantle, close to the junction of valve and mantle. Radial striae, 15-17 in 10 μm, with two punctate rows.

TYPE: Switzerland: Lake Zugersee. Phytoplankton Vierwaldstättersee 131, f. 106-108. 191 (G). SEASONALITY: This species prefer warmer season in its occurrence in the northern regions. DISTRIBUTION: C. glomerata has been recorded frequently in North America. This species has reached great abundances in lakes or rivers of arctic and subarctic regions. In a phytoplankton survey in 153 lakes and rivers above a latitude of 55 degrees in the Canadian Northwest district, C. glomerata was the most dominant (Moore 1978). In additon, this speices peaked in the epilimnion of Lake Tahoe in Sierra Nevada mountains. Though C. glomerata was not recorded before liming, this species, responding to the liming, increased to a dominant group in abundance of phytoplankton in Lake Njupfatet of Central Switzerland (Anderson et al. 1997). The species also occurred in other lakes of Switzerlannd before a period to acidification in diatom stratigraphic study. 64 Algal Flora of Korea·Freshwater Diatoms I m

A B C D 10

E F

Fig. 43. Cyclotella glomerata. A-D. the valve view of cell (×2,000, LM); E, F. the areolar striae on valve and fultoportulae in valve margin (SEM).

KOREA: It was first recorded in Korea as a plankton from the Namhan River by Chung (1972) and was observed in seven localities of the Han River and the Mangyeong River before 1996 (Lee 1997). The species was observed as very rare in the Nakdong River. SPECIMEN EXAMINED: (Planktonic diatoms collected from the Nakdong River near Gupo Bridge: 23.ix.1993). ECOLOGY: This species is well-adapted to the nutrient-poor conditions of freshwaters and likely to prefer the alkaline waters. REMARKS: This is a representative of the small diatom Cyclotella group.

17. Cyclotella meneghiniana Kützing 1844: 50 (Figs. 45-47).

Lowe 1975: 416. f. 3. Lee and Lee 1988: 136. f. 7. Kram- Fig. 44. Distribution of Cyclotela glome- mer and Lange-Bertalot 1991a: 44. pl. 44. f. 1. Cho rata. 1996: 10. f. 1.

Cells drum-shaped and solitary. Valves tangentially undulated and prominently undulated in the view of girdle. Valves circular, 5-43 μm in diameter. The central area of the valve well-defined Bacillariophyceae: Centrales: Thalassiosiraceae 65

AB C DE

F G

L m

J 10

M I O

Fig. 45. Cyclotella meneghiniana. A-H. the valve view of cell (×2,000); I, J. the girdle view of cell (× 2,000); K. an auxospore of the species; L. fultoportulae in the inside of valve (SEM); M, N. small spines (a white triangular symbol) and the external tubes of fultoportulae (a white arrow) on valve margin (SEM); O, P. the areolar structure on valve (TEM). 66 Algal Flora of Korea·Freshwater Diatoms I

Cyclotella meneghiniana Nakdong River 106

105

104

103

102

101

Seonakdong River 106

105

Algal abundance (cells/mL) 10

103

102

101

91 92 93 94 95 96

Fig. 46. The seasonal variation of Cyclotella meneghiniana (grey area) and total phytoplankton (solid lines) in the Nakdong and Seonakdong River (cited from Cho and Shin (1999)).

and broad striae radially arranged towards the marginal zone of the valve. The costae between the striae, 6-10 in 10 μm and depressed on the face. Small fultoportulae located at each costa without external tube and with two satellite pores. In small cells below 10 μm in diameter, costae occasionally without fultoportulae. Small spines above the external opening of each marginal fultoportula. Fultoportulae 1-4 in the central area, with 3 satellite pores. Some small specimens no central fultoportular tubes. Besides the fultoportulae, other ornaments or structures not in central region. A rimoportula present in valve margin.

TYPE: Ferrara Italy. BM17988 from the package 133 sent by Mr. Meneghini. Bacillarien p. 50. pl. 30. f. 68 (1844). SEASONALITY: C. meneghiniana is leading species in the Cyclotella diatom group and shows typically the bimodal patterns of spring and autumn blooms. The species occurs frequently in the warm periods, except during winter or the cold season in Korea. The species reach their maximum in summer or autumn in cold regions. DISTRIBUTION: This species is one of the most commonly and intensively studied algae in the freshwaters over the world. The taxon is dominant in the water bodies of cold regions - in Central Fin- Bacillariophyceae: Centrales: Thalassiosiraceae 67 land, in the mouth area of the Rupert River in Canada (Eloranta 1980; de Séve 1993), and co-dominant or subdominant in the Meuse River, and major rivers and waterways in the United States (Williams and Scott 1962; Descy and Gosselain 1994). KOREA: It is a common and widespread species in inland and estuarine waters. The species was already recorded in 1929 by B. W. Skvortzow who was the first author to record diatom flora in Korea. It has the highest frequency in floristic recordings of planktonic and periphytic algae. The species was reported as dominant or subdominant in Lake Paldang, six dam lakes in the Nakdong River, mesotrophic Lake Juam, along the middle to lower reaches of the Han River and the Nak- dong River, the lower reaches of the Yeongsan River, the Seomjin River and other freshwaters (Kim 1996; Kim 1998; Lee et al. 2000; Ha et al. 2002; Kim 2003; Lee and Jung 2004; Kim and Hwang 2004). In the Nak- dong River, it was a major dominant in phytoplankton Fig. 47. Distribution of Cyclotela mene- before the estuarine dam construction in the mouth of ghiniana. the river (Chung et al. 1987b). This species colonizes the benthic algal assemblages in the river in significant abundance (Cho 1988; Cho 1994). They would either sink into the sediment or be trapped in the substrates rather than in endemic periphyton or benthos. In addition to its widespread distribution in inland waters, it was observed in the coastal zone of South Sea, the West Sea and Jeju Island in Korea (Shim 1994). SPECIMEN EXAMINED: (Planktonic diatoms collected from the Seonakdong River near Gimhae Bridge: 21.xi.1992). ECOLOGY: This is classified as a representative tychoplankton (facultative plankton) in the water column and sediment of inland waters. The taxon is eutrophic indicator for highly fertilized waters and usually observed in waters of high conductivity. Auxospores of C. meneghiniana were frequently observed and occasionally had more than 50% frequency in this specific population of the Nakdong River. Auxospores are spherical and about 27 μm in diameter. Larger cells are hardly encountered in this regions and this would be maximum size of this species. Auxospore formations are reported to relate to the Na concentraton in water (Schultz and Trainor 1968). REMARKS: This species was reported to be highly abundant as a sub-dominant in the Nakdong River (Kim and Lee 1991; Cho et al. 1993; Seo and Chung 1993; Lee 1994; Lee et al. 1995b). The graphs below illustrate the variation of C. meneghiniana populations at two stations located in the Nakdong River mouth during the last 5 years. A series of one bloom annually occurs from June- August to December, with maximum abundance usually occurring in October - November. During the blooms, its maximal density ranged from 103 cells/mL to 104 cells/mL. The algal blooms terminate with the outburst of Stephanodiscus hantzschii group diatoms (Cho and Shin 1995). 68 Algal Flora of Korea·Freshwater Diatoms I

18. Cyclotella pseudostelligera Hustedt 1939: 581 (Figs. 48, 49).

Lowe 1975: 421. f. 22. Krammer and Lange-Bertalot 1991a: 51. pl. 49. f. 5. Lee 1994: 112. f. 1. Cho 1996: 11. f. 25.

SYNONYM: Discostella pseudostelligera (Hustedt) Houk and Klee 2004: 223.

Cells small disc-shaped and solitary. Valves circular and 4-10 μm in diameter. The central zone of the valve concave, convex or flat, having stellate ornamentations with radial areolar fascicles. A single large puncta in the center of stellate ornaments. Radial fascicles uniform or irregularly arranged and the costal ribs between fascicles 17-20 in 10 μm. The branches of costal ribs on valve margin and their delicate structures apparently different with C. stelligera. Marginal fultoportulae with long tubes per each 3-5 costae. Viewed in valve inside, fultoportular tubes positioned between the costae rather than on the costae. Some specimens having externally simple or long bifur- cate tubes or no external tubes. One rimoportula on valve mantle. Morphological variations frequently observed in patterns of costal branches, the stellate fascicles of the central zone, fultoportular external tubes and valve thickness.

TYPE: Germany: the Ems River, near Papenburg. BRM 51/1 (LT fide R. Simonsen, Atlas and Cat. Diatom Types Hustedt: 250. pl. 371. f. 26 (1987)). Diatom Research 19: 223 (2004). SEASONALITY: This species has wide seasonality from spring (March) to late autumn (November) showing the typical seasonality of genus Cyclotella. DISTRIBUTION: C. pseudostelligera is commonly widespread. It is well known from Europe, Russia, the United States, Africa, and South America (Mills et al. 1993). C. pseudostelligera has appeared in some alpine lakes in the Canadian Cordillera, where its presence is thought to indicate longer ice-free conditions and more stability in thermal stratification in recent years (Karst-Riddoch et al. 2005). KOREA: This species is reported as the dominant plankton in Lake Paldang of the Han River system (Kim 1998). Further, the relative abundance of the species ranged from 20% to 74% in five dam lakes (Lake Andong, Imha, Yeongcheon, Hapcheon, Jinyang) of the Nakdong River basin (Kim and Lee 1996). C. pseudostelligera ordinarily occurred with 100-200 cells/mL density and occasionally 5,000 cells/mL during the fittest periods in the Nakdong River. In Korea, it was first recorded as benthic diatoms of the estuary of the Nakdong River by Cho (1988) and was fully described with morphological study by Lee et al. (1994c). SPECIMEN EXAMINED: (Planktonic diatoms collected from the Nakdong River near Gupo Bridge: 28.xi.1993). ECOLOGY: This species is small, grows quickly, and Fig. 48. Distribution of Cyclotela pseudo- is typical of shallow, nutrient-enriched and often tur- stelligera. Bacillariophyceae: Centrales: Thalassiosiraceae 69 m

A B C D E 10

H F G

I J K

L MN

Fig. 49. Cyclotella pseudostelligera. A-E. the valve view of cell (×2,000, LM); F-K. the radiating areolae on valve and the varied structures of fultoportulae on valve margin (SEM); the areolar ornaments on valve margin (TEM).

bid aquatic habitats (Reynolds et al. 2002). It is a mesotrophic and eutrophic planktonic diatom. REMARKS: Although it has a small-sized dimension, the morphological variability regarding the valve flatness and central area are quite remarkable. The morphology and ultrastructure of C. 70 Algal Flora of Korea·Freshwater Diatoms I pseudostelligera valve resemble C. stelligera described later in the nature of the central area and areolar fascicle. It is difficult to make a definite separation of C. stelligera and C. pseudostelligera on the basis of morphological characteristics or costal branches under light microscopic examination. Occasionally, the characteristics of the two species show an appreciable overlap or continuum. In the light microscopy field, the density and the strength of interfascicular costae are useful to discriminate between the two species. Costal ribs are spaced above 17 in 10 μm in C. pseudostelligera and below 14 in 10 μm in C. stelligera.

19. Cyclotella radiosa (Grunow in Van Heurck) Lemmermann 1892: 30 (Figs. 50, 51).

Lowe 1975: 416. f. 7. Håkansson 1986. f. 42. Krammer and Lange-Bertalot 1991a: 57. pl. 62. f. 1. Lee and Lee 1988: 135. f. 1. Cho 1996: 19. f. 30.

BASIONYM: Cyclotella comta var. radiosa Grunow in Van Heurck 1882. pl. 92. f. 23. SYNONYM: Cyslotella comta (Ehrenberg) Kützing 1849: 20 pro parte. Lindavia radiosa (Grunow) De Toni and Forti 1900: 553.

Cells disc-shaped, solitary or in short chains with a few cells. Valves circular, concentrically undulated, 8-50 μm in diameter. Radial punctate rows in central zone and, in marginal zone, more and less broad striae 13-16 in 10 μm. Sometimes, irregular punctas distributed in central region. In electron microscopy, the central punctas as fultoportular pores.

TYPE: W: Grunow slide 913. Austria: Mondsee (fide Håkansson, Diatom Research 17: 114. 2002).

D E C B A m

10 F G H I

Fig. 50. Cyclotella radiosa. A-H. the punctas on the central zone and the radial striae on the marginal zone of valve (×2,000, LM); I. the valve view (TEM). Bacillariophyceae: Centrales: Thalassiosiraceae 71

Naturw. Beitr. Kenntn. Kaukasusländer: 126 (1878) (G). SEASONALITY: C. radiosa primarily appears from spring to autumn, often at its maximum in summer. DISTRIBUTION: This species is rare or less common planktons in freshwaters. It is frequently known to be codominant in paleolimnological diatom flora. Diatom stratigraphy showed dominance of the centric C. radiosa at some localities such as the Windermere South Basin in England, subalpine Crowfoot Lake in Alberta and other regions reflecting the warmer climate and a longer ice-free season of the early Holocene (Hickman and Reasoner 1998; Sabater and Haworth 1995). KOREA: This species have been rather reported as C. comta (Ehrenberg) Kützing in South Korea. The abundance of the species is relatively low in Korean freshwaters, while it is the Cyclotella having high frequency in phytoplankton survey and exhibiting wide distribution along with C. meneghiniana. SPECIMEN EXAMINED: (Planktonic diatoms collected Fig. 51. Distribution of Cyclotela radiosa. from the lower reaches of the Nakdong River at Mul- geum: 13.ii.1993). ECOLOGY: It is confined to the rather freshwaters and classified as an alkaliphilous taxon by some authors. This is a pelagic and eutrophic species. REMARKS: As net plankton, it coincides with other large Cyclotella diatoms in Korea.

20. Cyclotella stelligera (Cleve and Grunow in Cleve) Van Heurck 1882 (Figs. 52, 53).

Lowe 1975: 421. f. 26. Harworth and Hurley 1984: 44. f. 1. Krammer and Lange-Bertalot 1991a: 50. pl. 49. f. 1a. Cho 1996: 11. f. 16.

BASIONYM: Cyclotella meneghiniana var. stelligera Cleve and Grunow in Cleve 1881: 22. pl. 5. f. 63c. SYNONYM: Discostella stelligera (Cleve and Grunow) Houk and Klee 2004: 208.

Cells disc-shaped. Valves circular and 5-40 μm in diameter. The central and marginal zone of valve separated with a broadly hyaline zone. The central area concave or convex, with stellate areolar fascicles and a large puncta in center. Areolar fascicles consistently with two rows from the center to the margin. Interfascicular costae well-developed under light microscopy. Areolar fascicles and interfascicles 10-14 in 10 μm. Fultoportuae developed per 3-4 costae, with external tubular structures. A rimoportula with labiate aperture in valve margin.

TYPE: France: Vosges: Lac de Gerardmer. In Van Heurck, Syn. Diat. Belgique: pl. XCIV: f. 22 (1882) (no description). 72 Algal Flora of Korea·Freshwater Diatoms I

ABCDEFG

HI JKLMN

P m μ 10 R Q

S T

Fig. 52. Cyclotella stelligera. A-P. the ornaments in the central and marginal area of valve (×2,000, LM); Q, R. the radiating areolae on the surface and marginal fultoportulae in the inside of valve (SEM); S, T. the structure of areolar striae (TEM).

SEASONALITY: C. stelligera is observed from spring to autumn and is particularly abundant in summer at many lakes of North America. DISTRIBUTION: This species is abundant in some oligotrophic lakes and Lake Tahoe of North Bacillariophyceae: Centrales: Thalassiosiraceae 73

America, forest-tundra lakes of Northern Russia, Span- ish reservoirs and Tasmanian lakes of Australia (Saba- ter 1991; Laing and Smol 2000). The species has been more occasionally recorded in surface-sediment or stratigraphic studies of many regions - the 16 New Brunswick lakes and the subarctic treeline lakes in Canada, the Southern Ontario Lakes, Lake Titicaca in Peru and Bolivia and Western Tasmania of Australia (Laing et al. 2002; Rühland et al. 2003; Harris et al. 2006). KOREA: The species diatoms occur in most lakes and rivers in Korea showing an apparent high frequency, however, its abundance is relatively low in comparison with other Cyclotella populations. The species was recorded as a codominant in the Suer Stream of Gwangyang by Lee and Yoon (2000). The species was encountered in low frequency in comparison with C. pseudostelligera and its maximum density was below 100 cells/mL in the Nakdong River. Fig. 53. Distribution of Cyclotela stelligera. SPECIMEN EXAMINED: (Planktonic diatoms collected from the Nakdong River near Gupo Bridge: 28.xi.1993). ECOLOGY: This species widely spreads in lentic waters like lakes. The species is a pelagic freshwater diatom (Holland and Beeton 1972) and prefers oligotrophic to somewhat mesotrophic water (Whitmore 1989). The grazing pressure in lakes decreases the nannoplankton such as C. stelligera and C. pseudostelligera. REMARKS: This taxon has a wide variability in valve morphology and it is a hard task to clearly differentiate the small Cyclotella species in mixed assemblages. C. stelligera group diatoms have a wide range of morphological variations and a continuum. Especially, C. stelligera, C. pseudostelligera and C. woltereckii are obscure in the boundaries differentiating their specific identities. In these specimens, some cells have no central zone with stellate or radial areolar fascicles, and externally no fultoportular tubular protrusion in the valve margin. Haworth and Hurley (1986) suggest that new taxa combinations should be made for C. glomerata Bachmann, C. stelligeroides Hustedt, C. pseudostelligera Hustedt, C. woltereckii Hustedt as varieties belonging to C. stelligera.

21. Cyclotella woltereckii Hustedt 1942: 16 (Figs. 54, 55).

Haworth and Hurly 1986: f. 19. Cho 1996: 12. f. 24. Klee and Houk 1996: 20. f. 1. Tuji and Williams 2006a: 15. f. 1.

SYNONYM: C. stelligera var. pseudostelligera f. woltereckii (Hustedt) Haworth and Hurley 1986: 52. f. 19.

Cells drum-shaped and usually single. Valves circular, flat or somewhat undulate and 4.5-13 μm in diameter. Central and marginal zone poorly developed compared with C. stelligera and C. pseu- 74 Algal Flora of Korea·Freshwater Diatoms I

CD D E

A m

μ 10

F B G

Fig. 54. Cyclotella woltereckii. A, B. the valve view of cell (×2,000, LM); C-F. the radial striae on valve and fultoportuar tubes on valve margin (SEM); G. the radial arrangement of areolae on valve (TEM).

dostelligera. Central areas concave, however, not often developed. Marginal striae extending to the center of valve. The costal ribs dense and their bifurcations deeper than those of C. pseudostelligera. Marginal fultoportular tubes variable in forms: simple, horn-shaped or more grotesque than those previously described in C. pseudostelligera. A rimoportula on the junction of valve and mantle.

TYPE: Material of the Wallacea-Expedition from a pond in the botanical garden in Buitenzorg, Java. SEASONALITY: Its seasonality is obscure, however, it may be same with the other stelligeroid Cyclotella. DISTRIBUTION: C. woltereckii is widespread. It was originally described in Java but has been also known from such countries as Germany (Huebener 1999), Hungary (Szabo et al. 2005), Iraq (Al-Kaisi 1974), Argentina (Echenique and Guerrero 2003), and Poland (Wojtal et al. 2005). C. woltereckii was recorded in Lake Michigan in 1964 (Stoermer and Yang 1969; Mills et al. 1993). KOREA: In the Nakdong River, the species is rarely encountered, and further examination of this floral taxonomy is required. The species is first reported by Cho (1996) in the plankton of the Nak- dong River. SPECIMEN EXAMINED: (Planktonic diatoms collected in the Nakdong River near Gupo Bridge: 25.ix.1998). ECOLOGY: This species occurs in mesotrophic to eutrophic conditions. It has been recorded in Bacillariophyceae: Centrales: Thalassiosiraceae 75 relatively alkaline water with pH of 7.8-8.1, and is also known in inland and brackish waters. In addition to occurrence as plankton, it is known to occur epiphytically. REMARKS: These specimens are identical with the C. pseudostelligera suggested those by Lowe (1975) (cf. Figs. 19, 20) and Germain (1981) (cf. Pl. 8, Figs. 20, 21). However, morphology of these specimens would be different with C. pseudostelligera in the dense costal ribs and their deep bifurcation patterns. Lowe (1975) and Germain (1981) classified these specimens as C. pseudostelligera. However, these valves seem to be closely related to the C. woltereckii Hustedt, which holotype is shown in Krammer and Lange-Bertalot (1991). Haworth and Hurley (1986) assigned these forms to the C. woltereckii and C. pseudostelligera f. woltereckii.

Fig. 55. Distribution of Cyclotella woltereckii.

Genus Cyclostephanos Round ex Theriot et al. 1987: 346, description in Round 1982: 326. Wang-gwan-dol-mal-sok (왕관돌말속)

Cells small disc-shaped with circular valves. Cells solitary or a few cells linked to short chains. Valves concentrically or tangentially undulated with a ring of spines on the submargin or margin of valve. Single row stria of areolae at valve center and increasing to 3-4 rows at valve margin. Costae from valve mantle edge to a point on valve center. Each spine lining up raised interfascicular costae between striae. The areolae on mantle continuous with those on valve face, but smaller in size and simpler in form. Areolae internally simple, with domed cribra. Marginal fultoportulae, which open internally on one of the struts between fascicles, situated below some spines to form a ring at the margin of valve. Spines scarcely discernible in light microscopy. Scattered fultoportulae with two satellite pores also occurring on valve face. Lectotype: Cyclostephanos novaezeelandiae (Cleve in Cleve and Moller) Round in Theriot et al. 1987 (=Stephanodiscus novaezeelandiae Cleve in Cleve and Moller 1881) validated by Theriot 1987, 346.

SPECIES: There are 28 species names in the database, of which ten species are accepted taxonomically (Algaebase 2010). In South Korea, two species, C. dubius and C. invisitatus (alternately Stephano- discus invisitatus), were reported in 1995 (Lee 1995). DISTRIBUTION: In the temperate freshwaters of the world, Cyclostephanos is an important component of phytoplankton assemblages with other diatom groups, Aulacoseria and Stephanodiscus. The 76 Algal Flora of Korea·Freshwater Diatoms I most common species of Cyclostephanos found in Korean freshwaters are C. dubius and C. invisitatus. They are typically found in the plankton from late summer to autumn. In South Korea, the genus Cyclostephanos was firstly recorded by Lee (1992), describing C. dubius collected in the Gwangcheon Stream of Uljin and subsequently in the downstream of the Nakdong River (Lee et al. 1995a). KEY REFERENCE: Lowe and Crang (1972), Round (1982), Kobayasi and Inoue (1985), Håkansson and Kling (1990), Krammer and Lange-Bertalot (1991).

Key to the species of genus Cyclostephanos

1. Valve surface is flat·································································································C. invisitatus - Valve surface is divided into the central and marginal area due to the concentrical valve undulating····························································································································C. dubius

REMARKS: Cyclostephanos was established from genus Stephanodiscus by Round (1982) to be situated in an intermediate position between Stephanodiscus and Cyclotella. Cyclostephanos has been reported for a long time as Stephanodiscus species with marginally locular chamber and has characteristics shared with both Stephanodiscus and Cyclotella. The genus has characteristics intermediate to Stephanodiscus and Cyclotella. Stephanodiscus, Cyclotella and Cyclostephanos are closely related in their morphology and even share geographical and stratigraphic distribution. The three genera have a spectrum of morphological characteristics: similar areola structure, fultoportulae on the valve and mantle, the location of single rimoportula in the submarginal zone of the valve face. Regardless of their similarity, it has been suggested that three criteria may be useful for species differentiation: the topography of the flat or undulating valve face, the presence or absence of a fultoportula on the valve, and the depth of the mantle. Cyclostephanos differs from Stephanodiscus species in having the fascicles of areolae continued down the valve mantle and internal ribbing in the mantle region. For the rimorportulae, all Stephanodiscus species have tubes with external openings, whereas Cyclostephanos species possesses rimoportulae that open beneath the spines. The presence of a rimoportula that opens beneath the spine and has a tubular external extension, is sufficient evidence for classification of the two genus groups - Stephanodiscus and Cyclostephanos. In the observation of small centric diatoms under light microscopy, discrimination of Cyclotella, Cyclostephanos and Stephanodiscus is very difficult. Especially, it seems nearly impossible to discern the morphological differences between small diatoms of the genera Stephanodiscus and Cyclostephanos without more detailed descriptions including EM observation.

22. Cyclostephanos dubius (Fricke) Round 1982: 326 (Figs. 56, 57).

Hickel and Håkansson 1987: 36. f. 9. Piennar and Pieterse 1990: 202. f. 1. Krammer and Lange-Ber- talot 1991a: 64. pl. 67. f. 8a.

BASIONYM: Stephanodiscus dubius (Fricke in Schmidt ) Hustedt 1928: 367. f. 192. SYNONYM: Cyclotella dubia Fricke in Schmidt 1900: pl. 222. f. 23. Stephanodiscus dubius Hustedt 1930: 109.

Cells drum-shaped and solitary or short chain by being connected with a few cells. Valves circu- Bacillariophyceae: Centrales: Thalassiosiraceae 77

EF C D A B m

μ 10 GH

J L

Fig. 56. Cyclostephanos dubius. A-H. the valve view of cell (×2,000, LM); I. the internal view of the valve, a fultopotula in central area and many ones in marginal area, and a rimoportula in the marginal area (SEM); J. the concentrical undulation of valve, a fultoportula in central area and a ring of fultoportulae (white triangle marks) in marginal area (SEM); K, L. the more simpler pattern of areolae on valve and two futoportulae in central area (TEM). 78 Algal Flora of Korea·Freshwater Diatoms I lar and 4.5-35 μm in diameter, stong undulated in con- centric fashion and concave or convex in central zone. Areolar fascicules on valve separated by distinct interfascicular costae. Uniseriate areolae or large punctas in the center, but 2-4 rows towards the margin. Areolae continuously arranged from the center to the margin, but central and marginal zone distinctly separated due to deep undulation. A ring of fultoportulae with two strut pores on valve mantle with intervals of 3-4 fascicles and, additionally, a few fultoportulae in central area. A rimoportula on the ring of tubes of marginal area. Some morphological variations in density and strength of areolae and costae on the valve.

TYPE: Arch. Protistenk 125: 326 (1982). SEASONALITY: C. dubius shows diverse seasonality in the occurrence as planktons. The species is dominant in the phytoplankton of shallow Lake Doïrani in Macedonia in spring, March and April (Temponeras et Fig. 57. Distribution of Cyclostephanos al. 2000), while it is the most important in summer dubius. plankton in Lake Müggelsee of Germany (Köher and Hoeg 2000). The species is more abundant from late summer to autumn (from August to October) than in any other season in some lakes of Korea. How- ever, its seasonality is from September to November in the Nakdong River (Ha et al. 1998). DISTRIBUTION: In the 127 localities in Norfolk England, C. dubius is widespread and mainly confined to lakes (Clarke 1989). This taxon is halophilic as observed in some brackish inland waters (Hickel and Håkansson 1987). The species is dominant over the local phytoplankton assemblages in season, at least in temperate and cold regions in the world - the River Danube and Vils of Bavaria, Lake Müggelsee of Germany, the Norfolk district and a shallow pond of England, the Thames River of England, Lake Llangorse of Wales, the Danube River of Servia, many Danish lakes, eutrophic Swedish lakes, Vistula Lagoon of Poland, Lake Verevi of Estonia, shallow lakes of the Czech Repub- lic, Curonian Lagoon of Lithuania, lakes near the Baltic coast, Lake Doïrani of Greece, and Lake Hir- fonli of Turkey (Clarke 1989; Håkansson and Regnéll 1993; Temponeras et al. 2000; Bradshaw and Anderson 2003). It is also observed in the Yangzte River of China, Lake Biwa and Yamanaka of Japan, etc. This is the most important flora in the Lake Utah, however, it has been less commonly reported in North America. In addition to the current distribution, a high percentage of C. dubius accompanying Stephanodiscus species occurred in the stratigraphic sediment of three shallow Danish lakes (Anderson and Odgaard 1994; Bradshaw and Anderson 2003) and in a small lake (Groby Pool) of England (Sayer and Roberts 2001). From Lake Bussjösjön of southern Sweden, C. dubius suddenly appeared with deforestation of the catchment (2,700 BP) and Stephanodiscus species increased with the enormous soil erosion and cultural eutrophication from predominant pasture to arable land (1,300 BP) (Håkansson and Regnéll 1993). KOREA: The species was first described by Lee (1992) in the country. This taxon was reported as a dominant in Lake Jinyang and Deokdong (Kim et al. 1995; Kim 1999). While less abundant as the subdominant in the Nakdong River (Ha et al. 1998), some authors reported the importance of this Bacillariophyceae: Centrales: Thalassiosiraceae 79 species (Lee 1995). Earlier than the previous studies, Lee (1992) described the morphological characteristics of this taxon collected in the Gwangcheon Stream in Uljin in the course of epilithic diatom examinations. SPECIMEN EXAMINED: (Planktonic diatoms collected from the Nakdong River near Gupo Bridge: 28.xi.1993). ECOLOGY: This species is frequently recorded in freshwaters having a eutrophic state, high conductivity or chloride content. It is classified as an important eutrophic indicator, especially in palaeolimnological studies in lakes. In the stratigraphic and microfossil study, this is also a taxon abruptly appearing in the eutrophication layer. In other aspects, C. dubius is inhibited by waters of high alkalinity. The diatoms prefer the autumn or spring blooms associated with other Stephano- discus diatoms. The species is usually accompanied by a number of Stephanodiscus diatoms (S. hantzschii or S. neoastraea) and other species such as Aulacoseira. REMARKS: C. dubius may be easily confused with Stephanodiscus alpinus Hustedt due to their valve morphology, silicified thickness and concentrical undulation. They are different from the presence of loculi in the margin of valve inside.

23. Cyclostephanos invisitatus (Hohn and Hellerman) Theriot, Stoermer and Håkansson 1987: 256 (Figs. 58, 59).

Hohn and Hellerman 1963: 325. pl. 1, f. 7. Lowe and Crang 1972: 258. f. 1. Krammer and Lange- Bertalot 1991a: 63. pl. 67. f. 3.

BASIONYM: Stephanodiscus invisitatus Hohn and Hellerman 1963: 325. pl. 1. f. 7.

Cells drum-shaped and solitary or in short chains. Cell skeleton weakly silicified, compared with other stphanodiscoid diatoms. Valves circular and flat, 6.4-14 μm in diameter. Fascicular striae radiating from center to margin of valve and nearly 15-20 in 10 μm. The striae poorly defined toward the center, in smaller valves. In the view of TEM, areolae having two rows in marginal zone and tapering to a single row near the center. Interfascicular costae more conspicuous and, in electron microscopy, a circular costa distinct in the central zone. A circle of spines, situated at the end of interstitial costae, on the margin of valve. Fultoportular opening beneath the spine with interval of 4-5 spines. A rimoportuar pore near the center, however, not to be distinct in light microscopy.

TYPE: The Potomac River, Md. and Ridley Creek, Pa. USA. Diatom Res. 2: 256 (1987). SEASONALITY: The optimum seasonality of the species is in the period from spring to early autumn. The species is reported to bloom in spring (March-May) or early summer (June-July) in the temperate regions of the north hemisphere. In Korean freshwaters, the species is observed abundantly in spring (March and April) more than any other season throughout the year (Cho and Shin 1995). DISTRIBUTION: The dominance or importance of this taxon has been frequently reported in many European countries - three ponds of Attenborough in the UK (Sayer and Roberts 2001), the Thames River of England, Lake Lough Augher of North Ireland (Anderson 1990), Lake Vela in central Portugal, Lake Balaton Hungary, the Southern Hungarian section of the Danube River, etc. This 80 Algal Flora of Korea·Freshwater Diatoms I m

μ 10 D A B C

G H

Fig. 58. Cyclostephanos invisitatus. A-D. the valve view of cell (×2,000, LM); E, F. the valve view, a ring of spines and fultoportulae below the spine on marginal area (SEM); G, H. the structure of areolae on valve and a circular costa in central area (TEM).

taxon is among the common flora in the eutrophic waters throughtout North America (Lowe and Crang 1972). Its dominance was reported in North America as follows: the Sesquehanna River of Pennsylvania, the Sandusky River of Ohio, the San Joaquin River of California and the Lake Barkey of Tennessee. Centric diatoms such as Cyclostephanos invisitatus, C. dubius and Stephanodiscus parvus paleolimnologically dominated the diatom assemblages of the sediment throughout the northern hemisphere (Finsinger et al. 2007). Bacillariophyceae: Centrales: Thalassiosiraceae 81

KOREA: The presence and taxonomic characteristics of this species in South Korea were first described in the Gwangcheon Stream of Uljin (Lee 1992) and subsequently in the Nakdong River (Cho and Shin 1995; Lee 1995). In the Nakdong River, the species was counted as a member of the Stephanodiscus hantzschii f. tenuis, which persistently blooms in the lower parts of the river from autumn to spring of the following year. Accompanying S. hantzschii f. tenuis, this taxon is distributed widely in rivers and lakes of Korea and has been reported as a dominant in the Han River (Kim 1998). SPECIMEN EXAMINED: (Planktonic diatoms collected in the Nakdong River near Gupo Bridge: 29.i.1997). ECOLOGY: This species is a typical indicator occuring in the eutrophic freshwaters and accompanies other stephanodiscoid or small discoid centric diatoms. Its ecological characteristics are similar with S. hantzschii f. teuis and its relatives. Fig. 59. Distribution of Cyclostephanos REMARKS: It is difficult to discriminate this taxon invisitatus. from S. hantzschii f. tenuis under light microscopy due to the morphological homology.

Genus Stephanodiscus Ehrenberg 1845: 72. Go-ri-dol-gi-dol-mal-sok (고리돌기돌말속)

Cells small drum-shaped or discoid, solitary or united to form short chains. Valves circular and almost flat. A ring of spines and fultoportulae situated around valve margin and one to several rimoportulae near valve center. Areolae on valve radiating from the center to the margin, grouping into fascicles. Fasciculous striae uniseriate in the middle and multiseriate towards the margin. The useful characteristics for identification: the number of radial rows in a fascicle, the width of interfasciculous costae, the size and number of the areolae on valve and mantle, the position of fultoportulae and rimoportulae, and the distance between spines and fultoportulae. Lectotype: Stephanodiscus niagarae Ehrenberg 1845: 80.

SPECIES: There are approximately 163 species reported in the genus worldwide, however, approximately 40 species are taxonomically recognized (Algaebase 2010). Through the literature review and species-list filing, seven taxa are reported until 1995 in South Korea (Lee et al. 1995b) and 4 species around the Nakdong River Estuary (Moon and Lee 1995). The species of genus Stephanodis- cus were eleven - Stephanodiscus astraea var. minutula (Kützing) Grunow, S. carconensis (Eulenstein) Grunow, S. carconensis var. pusilla Grunow, S. hantzschii Grunow, S. hantzschii f. tenuis (Hustet) Håkansson and Stoermer, S. parvus Stoermer and Håkansson, S. niagarae Ehrenberg, S. rotula (Kützing) Hendey, S. invisitatus Hohn and Hellerman, S. dubius (Fricke in Schmidt et al.) Hustedt, 82 Algal Flora of Korea·Freshwater Diatoms I

S. kanitzii Pantocsek and Grunow (Lee 1988; Lee et al. 1995; KNCCN 1996; Lee 1997). The three latter species were transferred to other groups, Cyclostephanos invisitatus, C. dubius (Fricke) Round, Actinocyclus kanitzii (Pantocsek and Grunow) Schauderna, respectively. S. carconensis is known to be fossil diatoms in sediments and the presence of S. astraea, S. rotula in the Han River is actually obscure. It is assumed that the genus Stephanodiscus has four or five species in Korean freshwaters. Regardless of the reports in the floral list of phytoplankton, it is doubtful the presence of some taxa except four or five species of Stephanodiscus in Korean freshwaters. DISTRIBUTION: The Stephanodiscus diatoms are distributed in lakes and rivers worldwide as the most common and leading phytoplankton in temperate regions. Furthermore, the algal members of Stephanodiscus are the typical indicators representing the eutrophic status and the tolerant taxa to severe eutrophication or high nutrient level in freshwaters. Members of the genus Stephanodiscus (S. parvus, S. hantzschii f. tenuis and S. binderanus) were among the ten most dominant species in all lakes of the Laurentian Great Lakes in North America (Barbiero and Tuchman 2001). In South Korea, genus Stephanodiscus was first described in the study of the benthic diatoms living on the sand bottom of the Nakdong River Estuary (Cho 1988). At that time, small unidentified Stephanodiscus diatoms (exclusively S. hantzschii f. tenuis) were dominant from the freshwaters to brackish waters (river mouth) in the saline gradient, and having 2-20‰ abundance on the bottom. The other dominants of the bottom diatom assemblages were Navicula gregaria, Cyclotella pseudostelligera, C. meneghiniana etc. Small centric Stephanodiscus hantzschii diatoms suddenly appeared as plankton after estuarine dam construction in 1987. Considering Stephanodiscus is inherently planktonic algae, these stephanodiscoids seem to be present in the water column in the Nakdong River Estuary far before the construction of estuarine barrages. In the stratigraphic and sedimentary study, centric Stephanodiscus and Cyclostephanos diatoms dominated the phytoplankton assemblages with anthropogenic pollution in freshwaters in the world. The stephanodiscoid predominances over sedimentary diatoms have been frequently reported from many localities of European and North American countries. KEY REFERENCE: Kobayasi et al. (1985a, 1985b), Krammer and Lange-Bertlaot (1991a), Kling (1992), Håkansson and Bailey-Watts (1993), Cho (1995).

Key to the species of genus Stephanodiscus

1. Valve is flat and a rimoportula is present in center ·······················································S. parvus - Valve is flat, without rimoportula on valve ··············································································2 2. Valve diameter is around 11 μm, and an areolar rosette developing in the center of valve··········· ···················································································································S. hantzschii f. tenuis - Valve diameter is around 20 μm, and more wide areolar fascicles are present on the valve ········· ·······························································································································S. hantzschii

REMARKS: In the past, microstructures of Stephanodiscus diatoms have been examined by many authors with light and electron microscopy, however, great confusion remains in spite of the morphological information. Bacillariophyceae: Centrales: Thalassiosiraceae 83

24. Stephanodiscus hantzschii Grunow in Cleve and Grunow 1880: 115 (Figs. 60-62).

Casper et al. 1987: 18. f. 1. Krammer and Lange-Bertalot 1991a: 73. pl. 75. f. 4. Kling 1992: 243. f. 1.

Cells disc-shaped, solitary or short chains by being connected with a few valves. Valves flat or slightly convex. Valves circular and 18-30 μm in diameter. Radial rows of areolae on valve, usually grouping in fascicles of 2-3, separated by distinct interfasciculous costae. The strial fascicles straight, 8-10 lines in 10 μm and 16-20 areolar punctas in 10 μm. Other morphological characteristics similar with S. hantzschii f. tenuis.

TYPE: The Ems River. Perpenberg, Germany. 51/1 Ems bei Perpenberg 197, Hustedt collection, Bremerhaven. SEASONALITY: S. hantzschii occurs in the winter or spring, and is observed less commonly in Korean freshwaters than small tenuis-type Stephanodiscus. DISTRIBUTION: It coincides with the tenuis-type in its population distribution. In many cases of floral studies of phytoplankton, S. hantzschii and S. hatzschii f. tenuis have not been distinguished from each other into separate taxa. KOREA: In the past, forma tenuis was persistent for long times in monospecific blooms in the Nakdong River, while large Stephanodiscus (S. hantzschii) has appeared only since 2000 in the river.

A BC m

μ 10

D E

Fig. 60. Stephanodiscus hantzschii. A-E. the valve view of cell, the radiating and the fasciculous arrangement of areolae in valve (×2,000, LM). 84 Algal Flora of Korea·Freshwater Diatoms I

90 S. parvus 80 S. hantzschii f. tenuis 70 S. hantzschii

30 Frequency (%) 20

45678910111213141516171819202122232425 Diameter of valve (μm)

Fig. 61. Size distributions of three diatom species - Stephanodiscus parvus (N=100), S. hantzschii f. tenuis (N=200) and S. hantzschii (N=100) - observed in the lower parts of the Nakdong River.

In the spring, large hantzschii-types are not observed or occasionally observed with low abundance usually below 100 cells/mL. The abundance of this taxon is very low in comparison with those of forma tenuis- type. SPECIMEN EXAMINED: (Planktonic diatoms collected from the Nakdong River near Gupo Bridge: 29.i.1997). ECOLOGY: This species is a typical eutrophilous indicator, which can adapt to lower nutrient levels than forma tenuis diatoms. REMARKS: In limnological and ecological studies, many authors usually do not establish a distinction between both hantzschii and tenuis type in the S. hantzschii diatom population. S. hantzschii diatoms are somewhat variable in their morphology and display a degree of polymorphism (Håkansson and Bailey-Watts 1993). The type material of S. hantzschii Grunow reveals several morphotypes and some morphological types can be extracted from Fig. 62. Distribution of Stephanodiscus ha- the polymorphic populations (Håkansson and Stoer- ntzschii. mer 1984). This species can be differentiated into two types - ‘hantzschii’ type of S. hantzschii and ‘tenuis’ of S. hantzschii f. tenuis (Casper et al. 1987). In the Nakdong River, tenuis-type (around 11 μm in diameter) Stephanodiscus exclusively blooms after the construction of an estuarine dam in 1987. After 2000, Bacillariophyceae: Centrales: Thalassiosiraceae 85 hantzschii-type large (around 20 μm) Stephanodiscus appears and their dominances are irregularly below 0.2% abundance. As the two types of stephanodiscus are not overlapped in their size distributions, they are considered to be different forms of the same species. In observation of the type materials of S. hantzschii, this is a polymorphic species with at least three morphotypes (Håkansson and Stoermer 1984). On the other hand, clonal cultures in a controlled laboratory distinctly exhibited heteromorphic patterns (Kling 1992). An amended description of the species should include all the morphological variability in life cycle.

25. Stephanodiscus hantzschii f. tenuis (Hustedt) Håkansson and Stoermer 1984: 486 (Figs. 63-67).

Håkansson and Stoermer 1984: 480. f. 1. Kobayasi et al. 1985: 234. f. 1. Kling 1992: 243. f. 1. Håkans- son and Bailey-Watts 1993: 318. f. 2. Cho 1995: 70. f. 1.

SYNONYM: Stephanodiscus tenuis Hustedt 1939: 583.

Cells drum-shaped and solitary or in short chains, not obligate colony. Valves circular, almost flat and 8-15 μm in diameter. Fascicles composed of several areolar striae, showing the radial arrangement from the center toward the margin of valve. Fascicles uniseriate near the center, becoming biseriate or triseriate towards the margin. Areolae almost identical in size from the center to the margin, and 10-13 lines in 10 μm. Between the areolar fascicles, interfascicular costae arranged 10-13 in 10 μm. Sometimes, fascicles sinuous rather than straight in light microscopy. In most specimens found in the Nakdong River, a few areolae near the center of valve, distinctly surrounded by circular costae (rosette annulus). The radial costae on valve from the central costae to the valve margin. Spines on the terminal of the every interfascicular costa forming a ring around valve margin. External tubular fultoportulae beneath every second to third, rarely fourth spine. Tubes of fultoportulae well developed internally and externally, and the internal tube with three satellite pores. But, no fultoportulae on valve. In the fultoportular ring on valve margin, one tubular spine (rimoportula) different from the others; an externally short tube and internally two labial structures. The boundary of the valve and mantle clearly defined, and mantle shallow. Many delicate setae, radiating from the edge of cell to support the diatom buoyancy in water column (Fig. 61).

TYPE: The Ems River. Perpenberg, Germany. 51/1 Ems bei Perpenberg 197, Hustedt collection, Bremerhaven. SEASONALITY: Blooming in the spring in the northern hemisphere, it is commonly distributed in freshwaters and brackish waters in the world. There are small Stephanodiscus blooms from the middle of October or November until disappearing in mid-April in the next year in rivers of Korea. The maximum density was recorded 124,000 cells/mL in the downstream of the Nakdong River in 1998. With monospecific blooms, other algae scarcely coincide with Stephanodiscus. In these periods, the river is discolored to deeply brown. Stephanodiscus diatom populations increase below 12°C water temperature in an algal bloom onset in October, and decreased above 15°C in an algal dieback in April. From the field observations, it is assumed that the optimum temperatures for Stephano- discus hantzschii population growth range from 0°C to 15°C. Occasionally, the taxon has high num- 86 Algal Flora of Korea·Freshwater Diatoms I m

μ 10

Fig. 63. Stephanodiscus hantzschii f. tenuis. Solitary cells and a short chain loosely joining valve to valve with many thread-like setae on valve margin.

bers in plankton in summer season (Spaink et al. 1998) and also in the Nakdong River.

DISTRIBUTION: S. hantzschii f. tenuis diatoms are the most common and ecologically important in freshwater of the northern hemisphere. They are the most populous algae in spring. The stephanodiscoid centric populations are distributed dominantly in the shallow lakes, rivers and lagoons in Europe - Lake Loch Leven of Scotland, the Thames River and the Trent River of England, thirty one lakes of South East England, Lake Lough Augher of North Ireland (Anderson 1990), the Humber River of UK, the Meuse River of Belgium (Gosselain et al. 1994), the Elbe River Estuary of Germany, Southern Hungarian section of the Danube River, many Danish lakes, fifteen shallow lakes of Czech Bacillariophyceae: Centrales: Thalassiosiraceae 87 m

μ 10 A B CDE

J K

Fig. 64. Stephanodiscus hantzschii f. tenuis. A-D. the valve view and radiating striae on valve (× 2,000), E. the girdle view of cell (×2,000); F. assemblages of cleaned cells (×2,000) (LM); G-I. the ring of spines and fultoportulae below spines at the junction of valve and mantle; J, K. a rimoportula and a ring of fultoportulae in valve margin, and a fultoportula in central area on the inside of valve (SEM). 88 Algal Flora of Korea·Freshwater Diatoms I

C D

E F m μ G 10

Fig. 65. Stephanodiscus hantzschii f. tenuis. A, B. the radial arrangement and fascicles of areolae, and a circular ring of costae in central area (TEM); C, D. the valve with teratological and heavy silicification; E. the inside view of valve (SEM); F, G. the collapsed auxospores during life cycles (F, SEM; G, LM). Bacillariophyceae: Centrales: Thalassiosiraceae 89

Stephanodiscus hantzschii f. tenuis group diatoms Nakdong River

106

105

104

103

102 91 92 93 94 95 96 97 98 Seonakdong River

106

105

Algal abundance (cells/mL) 104

103

102

101 96 97 98 99 00 01

Fig. 66. Seasonal variations of diatoms Stephanodiscus hantzschii f. tenuis group diatoms (S. hantzschii f. tenuis, S. parvus and Cyclostephanos invisitatus) in the downstream of the Nakdong River (upper) and in the Seonakdong River (below) (cited from Cho and Shin (1999)).

Republic, the Baltic Lake District and in Argentina (Gómez and Bauer 1998). In North America, stephanodiscoid blooms were more or less weak, whereas the population was reported in Sandu- skey River of Ohio and in Lake Michigan as causing clogging problems in the drinking water systems (Holland and Beeton 1972). These diatoms had reported blooms in freshwaters of Northeastern Asia: the Yangtze River in China, and some rivers and lakes in Japan. This diatom group has been found abundantly in the stratigraphic sediment in the northern hemisphere - Lake Big of British Columbia in Canada and other regions (Cumming et al. 2002). KOREA: In Korea, this taxon occurs in autumn and persistently blooms in winter and spring through the dry season. Small tenuis-type stephanodiscoids usually bloom in the large rivers in South Korea - the Han River, the Geum River, the Yeongsan River, the Nakdong River and the Imjin River (Lee et al. 1995a; Cho and Shin 1995; Lee and Chang 1997; Ha et al. 2002; Lee and Yoon 2002; Kim 2003) and some lakes - Lake Paldang, Lake Deokdong and others (Kim et al. 1998c; Kim 1999). Planktonic algae have bloomed throughout the year in the rivers and lakes, and the explosive and persistent blooms of stephanodiscoid diatoms are not unusual in the downstream of large rivers in Korea. Their numerical abundances are more than 40,000 cells/mL in the lower parts of rivers. The small centric diatoms predominate over the phytoplankton from autumn to spring next year in the river and discolor the waters to yellow-brown. The algal blooms, though seemingly monospecific populations are actually comprised of a few leading species: primarily S. hantzschii f. 90 Algal Flora of Korea·Freshwater Diatoms I

Fig. 67. The geographical distribution of stephanodiscoid diatoms (Stephanodiscus hantzschii f. tenuis group) in the important rivers and lakes in South Korea on February and March in 1996 (cited from Cho et al. (1998)). Bacillariophyceae: Centrales: Thalassiosiraceae 91 tenuis, S. parvus and Cyclostephanos invisitatus. Throughout the season and sampling stations, S. hantzschii f. tenuis is a major component, S. parvus is a sub-dominant and Cyclostephanos invisitatus diatoms have low abundance or less frequency as co-occurring flora. In addition to the dominant taxa, the dimension and morphology of S. hantzschii f. tenuis group (stephanodiscoid) diatoms are similar or nearly identical. Valve diameter of these taxa were indiscriminately 9-13 μm, girdle bands as below 9 μm in length. When the centric diatoms are observed with light microscopy, it is impossible to identify these taxa by morphological features. Furthermore, with the cleaned diatom cells, it is difficult to differentiate diatoms from each other when they are mixed. These small stephandiscoid diatoms are grouped as S. hantzschii f. tenuis complexe or its polymorphic populations. In the prevailing of the small stephanoiscoid diatom group, larger ones (S. hantzschii) have been appearing since 2000 in the river and recently these diatoms have gradually increased in abundance and frequency. SPECIMEN EXAMINED: (Planktonic diatoms collected from the Nakdong River near Gupo Bridge: 29.i.1997).

ECOLOGY: S. hantzschii f. tenuis has the lowest ks (half coefficient) value for silica and phosphate in the nutrient kinetics of the phytoplanktonic diatoms. These are the best competitors in low concentrations of the two nutrients and in low Si/P conditions (Van Donk and Kilham 1990). Inorganic nutrient concentrations in the downstream of the river are correlated with the algal biomass or growth, and silica and phosphate would limit further algal growth in the downstream of the river. These group diatoms are well adapted to low light conditions. Small diatom Stephanodiscus populations would be the best competitors for the prevailing water conditions in the cold season. During the monospecific blooms in cold season, algal compositions change temporarily after nutrient gaps or disturbances, for example, after rainfall (Cho and Shin 1998). It is observed that other competitive diatoms succeed to stephanodiscoid diatom group. REMARKS: In Korea, S. hantzschii f. tenuis group diatoms have been unfortunately recorded as Cyclotella unidentified species for a long time due to their close morphological resemblance. It was identified as S. hantzschii f. tenuis upon careful examination of the following literature: Håkansson and Stoermer (1984), Kobayasi et al. (1985a), Håkansson and Kling (1989), Kling (1992). However, Casper et al. (1987) denied differentiating S. hantzschii and S. hantzschii f. tenuis (=S. tenuis Hustedt) as different taxonomic units in the sense of Håkansson and Stoermer (1984). They demonstrated the different epivalve and hypovalve in the same cell. Stephanodiscus hantzschii and S. hantzschii f. tenuis are considered to be different forms of the same species and show very little overlap in their distribution in the Great Lakes of North America (Barbiero and Tuchman 2001). Areola-occluded valves with thick spines are occasionally observed in SEM microscopy. The degree of occlusion varies from incompletely circular to slit-like areolae and sometimes the external opening of the areolas is entirely closed. It is reported that the degree of occlusion of the areolae is related to that of silicification of the valve (Genkal and Håkansson 1980; Håkansson and Stoermer 1984). The morphological teratology depends on the growth satges of the population. Especially during the exponential growth phase, Stephanodiscus hantzschii cells often have a heterovalve, one with occluded areolae and one with open well developed areolae (Kling 1992). In addition, auxospores of the species is occasionally collapsed having organics rather than silicious walls (Kling 1992) (Figs. 65F, G). Many weakened auxospores was observed in the lower reaches of the Seonakdong River. 92 Algal Flora of Korea·Freshwater Diatoms I

26. Stephanodiscus parvus Stoermer and Håkansson 1984: 505 (Figs. 68, 69).

Stoermer and Håkansson 1984: 500. f. 1. Krammer and Lange-Bertalot 1991a: 71. pl. 74. f. 1. Cho 1995: 73. f. 16.

SYNONYM: Stephanodiscus hantzschii f. parva Grunow ex Cleve and Müller 1879: 266. Stephanodiscus hantzschii sensu Haworth 1981 (non Grunow in Cleve and Grunow 1880: 115).

Cells discoid or small drum-shaped. Valves circular and 5-11 μm in diameter, almost flat or a little concave in center, but, never a well-defined central area. Interfascicular costae especially broad, radially arranged, 13-15 lines in 10 μm and 30-39 areolae in 10 μm. Areola sizes large towards valve margin. Circular costae in the center absent or inconspicuous. A fultoportula beside the center diagonally opposite the rimoportula. The central fultoportula with two internal satellite pores (struts), located diagonally across from the marginal rimoportula. The marginal fultoportula with three strut pores. Occasionally, fultoportular tubes poorly developed on valve.

TYPE: Kieselguhr von Ceyssal, Puy-de-Dôme, France. Slide 9036 Grunow, in Grunow Collection, Wien. SEASONALITY: As the leading species in spring algal blooming, S. parvus exclusively constitutes the important component in many regions of Europe and North America (Gosselain et al. 1994) and occasionally occurs in summer in the Southern Hemisphere. DISTRIBUTION: Since the 1950s, S. hantzschii f. tenuis group including S. parvus predominated over phytoplankton assemblages especially in spring - in Lake Lough Augher of North Ireland and the River Meuse of Belgium in the 1990s (Anderson 1990; Gosselain et al. 1994). Phytoplankton assemblages are dominated by S. parvus in Lake Bouchie of British Columbia in Canada (Heinrichs et al. 2005). The species is subdominant in summer phytoplankton of Lake Laguna Azul in Argentina (Messyasz et al. 2007). Besides the currently important phytoplankton, this taxon has been reported more frequently as the dominant species in the stratigraphic study of the recent sedimentology of inland lakes. S. parvus increased paleolimnologically in records of lake sediments progressing towards eutrophication in European localities: a subalpine hard-water lake of Bavaria (Steinberg and Trumpp 1993), three shallow Danish lakes (Anderson and Odgaard 1994), Lake Pavin of France (Stebicha et al. 2005). It shows dominance since the 1920s in Lake Rotsee and in the 1950s in Lake Baldeggersee of central Switzerland (Lotter 1998), Lake Lago Grande di Avigliana of North Italy (Finsinger et al. 2007), Lake Windermere and a small lake in England (Groby Pool) (Sergi and Haworth 1995; Sayer and Roberts 2001), stephanodiscoid centrics including S. parvus were recorded in Lake Lough Augher of North Ireland (Anderson 1990), and showed its stratigraphic expansion in Lake Peipsi of Estonia/Russia (Heinsalu et al. 2007). The taxon is also reported in the paleolimnological study in North America regions: Lake Big of British Columbia and Lake Ontario in Canada (Yang and Duthie 1993; Cumming et al. 2002). KOREA: This species blooms concurrently with S. hantzschii f. tenuis in Korean freshwaters. S. parvus is recorded at three localities - Nakdong River (Cho 1995; Lee et al. 1995b; Cho and Shin 1995), the Gwangcheon Stream in Uljin (Lee 1992a) and Lake Paldang (Kim 1998). S. parvus was first described by Cho (1995) in the plankton of the Nakdong River. Bacillariophyceae: Centrales: Thalassiosiraceae 93

AB C m

DEF 10

L KJ

Fig. 68. Stephanodiscus parvus. A-F. the valve view and the radiating striae on valve (×2,000, LM); G, H. a ring of fultoportulae in the margin and a fultoportula in the center of valve; I. a fultoportula in the central area, and a ring of spines in the marginal area of valve inside; J. a ring of spines and the fultoportulae below the spine at the junction of valve and mantle; K. a fultoportular tube and adjacent two strutted pores in the inside of valve (SEM); L. the radiation and fasciculation of areolae on valve and a circular costae in central area (TEM). 94 Algal Flora of Korea·Freshwater Diatoms I

SPECIMEN EXAMINED: (Planktonic diatoms collected in the Nakdong River near Gupo Bridge: 21.xi.1992). ECOLOGY: The species has similar ecological characteristics with its variety, S. hantzschii f. tenuis. REMARKS: S. parvus can be easily confused with S. minutulus (Kützing) Grunow in Cleve. The only differentiating characteristics are the shape and position of the valve facing the fultoportula. It should be concentrically corrugated in S. minutulus and plane in S. parvus. Some authors hold that S. minutulus is a synonym of S. parvus (Kobayasi et al. 1985b). Other Stephanodiscus species, except S. hantzschii f. tenuis, are commonly observed in the phytoplankton of Korean freshwaters. Morphological characteristics of S. parvus are similar with the previously described S. hantzschii f. tenuis; it is clearly differentiated from the previous taxon under SEM observations. However, in light microscopy, subtle differences in valve morphology discriminate this species from S. hantzschii f. tenuis. Fig. 69. Distribution of Stephanodiscus The central region of S. parvus valves, neglecting the parvus. presence of the central fultoportular tube, may be grossly similar in appearance to the central region of S. hantzschii f. tenuis (Stoermer and Håkansson 1984). It can be identified as another taxon S. parvus Stoermer and Håkansson upon careful examination of taxonomic literatures such as Theriot and Stoermer (1982).

Genus Thalassiosira Cleve 1873: 6. Kkun-won-ban-dol-mal-sok (끈원반돌말속)

Cells coin, drum or shallow cylinder shaped, and often very small and thin. Cells connected by chitin threads or valve to valve to make a variety of chains. Valves circular and girdle view rectangular, with a highly variable ratio of diameter to pervalvar axis. Areolae arranged in linear, radial, fasciculate or eccentric patterns on valve. Very few features visible in light microscopy; often only marginal spines, and central and marginal fultofortulae. Patterns of processes on valve, useful in the differentiation at species level. Radial striae on valve, straight or sinous, but probably indistinct or invisible in light microscopy. Lectotype: Thalassiosira nordenskiöldii Cleve 1873, emend Berg 1952: 31, f. 59. The lectotype was collected from the Davis Strait in the Arctic Sea.

SPECIES: There are 202 species names in the database, of which about 100 species are currently accepted (Algaebase 2010). The majority of this group diatoms occurs from the Arctic and Antarctic and 12 species inhabit freshwaters or brackish waters (Silva and Hasle 1994). In South Korea, about 48 species are recorded until 1995 and are proven to be mostly marine or coastal. Thalassiosira bra- Bacillariophyceae: Centrales: Thalassiosiraceae 95 maputrae is unique species in Korean freshwaters. DISTRIBUTION: Most species are marine and coastal, among the 12 freshwater or brackish species, T. weissflogii is probably the best known. Three taxa described in this monograph are usually confined to brackish waters. KEY REFERENCE: Hasle (1978), Krammer and Lange-Bertalot (1991).

Key to the species of genus Thalssiosira

1. Highly silicified cells and strong valve structure ··················································T. bramaputrae - Normal silicification of the cell and typical centric thalssiosiroids ············································2 2. Areolar structures on the valve and valves are arranged into several sections ················T. faurii - Delicate and invisible structures of areolae and distinct fultoportuar tubes on the central area ··· ································································································································T. weissflogii

REMARKS: The present circumscription of the genus and many of the species is the result of electron microscopic studies, primarily by G. Hasle, G. Fryxell and their coworkers. The genus Thalas- siosira has finer sculpturings than the genus Coscinodiscus, and submarginal spines on the valve.

27. Thalassiosira bramaputrae (Ehrenberg) Håkansson and Locker 1981: 125 (Figs. 70, 71).

Håkansson and Locker 1981: 123. f. 5. Hu and Wei 2006: 1. pl. 4. f. 16.

BASIONYM: Stephanodiscus bramaputrae Ehrenberg 1854: pl. 35A/9. f. 9. SYNONYM: Thalassiosira lacustris (Grunow) Hasle in Hasle and Fryxell 1977: 40. Coscinodiscus lacustris Grunow in Cleve and Grunow.

Cells drum-shaped and thickly silicified. Valves circular, tangentially undulated and arched in central area and 10-75 μm in diameter. Polygonal areolae in central regions and in irregular rows towards the margin of valve, with siliceous raised costae between areolar lines in central area. A ring of more or less regularly spaced spines around the margin of valve. The presence of spines barely visible under light microscopy. Fultoportulae around the central area and a single rimoportular process on valve.

TYPE: Birket Garag, EI Faiyum, Egypt. Ehrenberg Collection, Box 10, book 5, slides “Fajurm, See Garag”. SEASONALITY: This species is known to occur during Fig. 70. Distribution of Thalassiosira bra- the cold season. mapturae. 96 Algal Flora of Korea·Freshwater Diatoms I

C m B μ A 10

D E F

Fig. 71. Thalassiosira bramaputrae. A-F. the undulation in central area and the arrangement of areoale on valve (×2,000, LM).

DISTRIBUTION: T. bramaputrae is primarily planktonic in the coastal waters, or occasionally in freshwater and as such less common in its abundance. This taxon is widespread in the coastal regions and large rivers around the world: Europe, North America, Baltic and Caspian Sea, Japan and Australian waters (Hasle 1978; Mills et al. 1993). In inland waters, its distribution is confined to Lake Erie where it maybe introducted from Europe or Asia in the 1970s probably by ship ballast water (Smucker et al. 2006). In biostratigraphic studies of Lake Bradley in Oregon, the presence of T. bramaputrae was supported by the short-lived periods of slightly elevated salinities in the lake (Hemphill-Haley and Lewis 2003). KOREA: The species diatoms are distributed in the estuarine waters as common or rare ones. This speceis was fully described in the epilithic diatom examination of the Gwangcheon Stream in Uljin (Lee 1992). Furthermore, it is reported in the lower parts of the Nakdong River (Lee et al. 1995a). It is already then named Coscinodiscus lacustris Grunow from lakes (Lake Yeongrang and Juam) and rivers (the Hyeongsan River, the Nakdong River, the Mangyeong River) (Lee 1997). In addition to the freshwater distribution, It is commonly observed in the coastal area around Gang- hwa Island, Gyeonggi Bay and the West Sea of Korea (Shim 1994). SPECIMEN EXAMINED: (Planktonic diatoms collected in the Seonakdong River: 27.viii.2007). ECOLOGY: This is common in brackish waters and also tolerates freshwaters. It is clear from data Bacillariophyceae: Centrales: Thalassiosiraceae 97

A BC m

μ 10

D E F

Fig. 72. Thalassiosira faurii. A-F. the radial arrangement and sectors of areolae on valve (×2,000, LM).

that a wide range of salinities from 2‰ to 15‰ are possible for the species to be accomodated (Hemphill- Haley and Lewis 2003). REMARKS: In this text, Thalassiosira lacustris is syn- onymous with Coscinodiscus lacustris.

28. Thalassiosira faurii (Gasse) Hasle 1978: 282 (Figs. 72, 73).

Hasle 1978: 282. f. 61.

BASIONYM: Coscinodiscus faurii Gasse 1975: 24 (v. 2). pl. 32. f. 1

Cells disc-shaped. Valves circular, 18-43 μm in diameter. The areolae on valve radiating from center to margin, arranged into sectors being parallel to the Fig. 73. Distribution of Thalassiosira faurii. middle row of a sector. Areolar striae 13-18 lines in 10 μm, decreasing towards margin. In the margin of valve, a ring of spines on marginal zone, 6-9 spines in 10 μm. Three or four rimoportulae, situated bewteen two marginal futoportulae closer to valve margin. 98 Algal Flora of Korea·Freshwater Diatoms I

TYPE: Lakes of Central Afar, Ethiopia, Upper Pleistocene, Holocene. SEASONALITY: The diatoms of this species prefer the spring in spite of otherwise low relative abundance. DISTRIBUTION: This species have been recorded from lakes in Central and East Africa. KOREA: T. faurii is rare or occasionally occurring in plankton assemblages. However, it was recorded in exceptionally high abundances with 1,016 cells/mL in the freshwater zone of the lower parts of the Nakdong River in October of 1991. SPECIMEN EXAMINED: (Planktonic diatoms collected in the Seonakdong River near Gimhae Bridge: 21.xi.1992). ECOLOGY: It occurs in brackish waters and seems to be halophilic. REMARKS: T. faurii (Gasse) Hasle and T. rudolfi Hasle are similar in their valve morphology.

29. Thalassiosira weissflogii (Grunow) Fryxell and Hasle 1977: 68 (Figs. 74, 75).

Krammer and Lange-Bertalot 1991a: 79. f. 77. Kang et al. 1996: 25. f. 1.

BASIONYM: Micropodicus wessflogii Grunow in Van Heurck 1882-85: 210. SYNONYM: Micropodiscus weissflogii Grunow in Van Heurck 1882-1885: 3. 10. Eupodiscus weissflogii Grunow in Van Heurck 1882-1885: 3. 100. Eupodiscus weissflogii (Grunow in Van Heurck) De Toni 1894: 1087. Thalassiosira fluviatilis Hustedt 1926: 565. f. 1.

Cells drum-shaped, singly or in short colony connected by a central mucilage thread. Furthermore, sometimes enveloped in a gelatinous matrix. Valves circular and flat, 4-32 μm in diameter, weakly concave or convex in central area. Areolae on valve irregularly shaped or polygonal, however, invisible in light microscopy. Areolar striae radiating from the center of valve towards the margin. A marginal ring of fultoportulae at valve margin with 10-13 processes in 10 μm, and 2-15 processes in central area forming irregular ring.

TYPE: Saumatre-Blankenberghe, Belgium. Types du Synopsis No 11 and 416. SEASONALITY: Its seasonality is similar with other Thalassiosira species. DISTRIBUTION: T. weissflogii is considered to be widespread. It is known in European and Asian coastal waters, and some inland rivers and reservoirs: rivers in North America, inland waters of South America, and Hawaii and the Solomon Islands. This species Fig. 74. Distribution of Thalassiosira weis- has been found to be a halophilous freshwater form, sflogii. Bacillariophyceae: Centrales: Thalassiosiraceae 99

A B

C m

μ 10

D E

Fig. 75. Thalassiosira weissflogii. A. the valve view (×2,000, LM); B-D. the radiating areolae, and a few fultoportuae on the central and a ring of fultoportulae in the marginal area of valve; E. the tubular projection at valve margin (SEM).

widely distributed. T. weissflogii was probably introduced in ballast water to the Great Lakes basin in North America: Lake Michigan, Lake Erie, Lake Ontario, the Portage River and the Detroit River (Stoermer and Yang 1969; Millie and Lowe 1981; Mills et al. 1993). KOREA: This speices is less common in the brackish water in Korea. It is more commonly reported in the coastal zone of the South Sea, southern parts of the West Sea and Jeju Island (Shim 1994). T. weissflogii explosively bloomed in July 1998 in Yeoja Bay of Southern Sea (Lee and Yoon 2000). SPECIMEN EXAMINED: (Planktonic diatoms collected from the Seonakdong River near Noksan: 12.ix.1993). ECOLOGY: As a species of brackish diatoms, T. weissflogii occurs commonly in brackish waters and also tolerates freshwaters. The species is well adapted to marine conditions, showing a wide range in various salinities (Vrieling et al. 1999). For example, this species have exhibited abundant growth in freshwater conditions in the Great Lakes. It had 74% abundance by biovolume in Lake Michigan during sampling in 1972-1973, although it only reached 11% abundance by biovolume in 100 Algal Flora of Korea·Freshwater Diatoms I this lake during the 1973-1974 sampling period (Lauer 1976; Lauer and Mccomish 1976). REMARKS: This is the best known taxon among the Thalassiosira species observed in freshwaters. The number of central processes on the valve, as well as the degree of silicification are believed to vary with salinity.

Genus Skeletonema Greville 1865: 43. Gol-pyon-dol-mal-sok (골편돌말속)

Cells cylindrical to disc-shaped with relatively high mantle and well developed girdle. Cells joining with long marginal processes to form filamentous colonies. Especially marine colonies giving the appearance of beads connected with fine threads in light microscopy. Cellular skeleton weakly silicified and easily deformed during the sample preparation or treatment. Valves circular with convex to flat faces. A ring of fultoportular processes around the top of mantle. The most important characteristics of long this family: the morphological feature of chains, the structure of fultoportulae, and the number of rimoportulae. Lectotype: Skeletonema costatum Cleve 1873, type cons.

SPECIES: Approximately 21 species in this genus were reported worldwide and, amomg them, 20 species are taxonomically recognized as valid taxa (Algaebase 2010). Marine or coastal species have been reported in Korean water and, additionally, two species, S. potamos and S. subsalsum, are observed in freshwaters or brackish waters. DISTRIBUTION: The genus diatoms live in the estuarine, brackish and coastal area as saline diatoms. The two species are distributed in brackish waters and even inland waters. Skeletonema diatoms in freshwaters are important plankton in eutrophic estuaries and lagoons in Eurasian regions. KEY REFERENCE: Weber (1970), Hasle and Evensen (1976), Chang and Steinberg (1988), Krammer and Lange-Bertalot (1991).

Key to the species of genus Skeletonema

1. Distinct pseudosulcus occurs between two joining valves ··········································S. potamos - Pseudosulcus is absent····························································································S. subsalsum

REMARKS: The type specimen of the species was originally Skeletonema barbadense Greville. However, the S. barbadense was transferred to a new genus Skeletonemopsis P. A. Sims and S. costatum was conserved as the new type species of Skeletonema by replacing S. barbadense. The genus diatoms are inherently marine except two freshwater species - S. potamos and S. subsalsum. The former can be distinguished from the latter by its usually longer spines so that valves are separated. Also S. potamos usually has domed valves while S. subsalsum has flat valves. The pseudosulcus is more distinct in S. potamos than in S. subsalsum. Bacillariophyceae: Centrales: Thalassiosiraceae 101

30. Skeletonema potamos (Weber) Hasle in Hasle and Evensen 1976: 73 (Figs. 76-79).

Weber 1970: 151. f. 2. Hasle and Evensen 1976: 75. f. 1. Chang and Steinberg 1988: 199. f. 5. Kram- mer and Lange-Bertalot 1991a: 82. pl. 85. f. 4.

BASIONYM: Microsiphonia potamos Weber 1870: 151. SYNONYM: Stephanodiscus subsalsus (A. Cleve) Hustedt sensu Hustedt 1928: 372 (non Melosira subsalsa A. Cleve 1912: 509). Stephanodiscus subsalsus (A. Cleve) Hustedt 1928: 372. Skeletonema subsalsum (A. Cleve) Bethge 1928: 343.

Cells short cylindrical forms with deep mantle. Cells connected to short or long chains. Valves circular, flat to slightly rounded, 3-6 μm in diameter and 4-10 μm in pervalvar length. Silicified, granulated and knobby costae in radial arrangements on valve and mantle. Typically 5-8 fultoportular processes on a valve and 5-8 rows of areolae between them.

TYPE: Little Miami River, Cincinnati, Ohio USA. Smithonian Institution USA. SEASONALITY: This species reaches maximum in abundance in spring, summer or early autumn worldwide. Its maximum abundance frequently occurs in summer. The species usually blooms during summer and autumn in the Seonakdong River in Korea. DISTRIBUTION: S. potamos was first described from the Jensensee in Germany under the name S. subsalsus in 1928 but then redescribed as S. potamos in the Little Miami River at Cincinnati (Kiss et al. 1994). It is one of the most important species in the plankton in Europe and North America. It is now known in North American rivers (the tributary of Lake Erie, the Sandusky River of Ohio) on both sides of the continent, and parts of Europe including France, Netherlands (the Waal River), England and North Ire- land (Attenborough pond and shallow lakes), Ger- many (the Weser River), Austria, Hungary (the Danube River), the Ukraine, Russia, and Spain (Hasle and Evensen 1975; Chang and Steinberg 1988; Schmidt 1994; Spaink et al. 1998; Sayer and Roberts 2001). S. potamos is also known in Japanese coastal waters (Ueno 1992) and in the La Trobe River in Australia (Chess- man 1985). S. potamos first occurred in Lake Erie in 1963 at Tole- do, Ohio and subsequently has been reported in other parts of Lake Erie and its drainage, Lake Ontario, and Lake Huron (Mills et al. 1993). S. potamos was very likely introduced by ship ballast water via entering the Great Lakes from North American river drainages outside the basin or to European ports. Fig. 76. Distribution of Skeletonema pota- KOREA: It occurs abundantly in the freshwater zones mos. 102 Algal Flora of Korea·Freshwater Diatoms I

H K G

C I

B E F A m

μ m

μ 10 L 10 m

D 10 M N

Fig. 77. Skeletonema potamos. A-F. the cell and colonial chain (A-C. ×1,000; D-F. ×400); G-N. the girdle view of cell (G-K. ×1,000; L-N. ×2,000) (LM); O, P. a ring of interlocking tubes at the junction of valve and mantle and the mantle view (SEM). Bacillariophyceae: Centrales: Thalassiosiraceae 103

Fig. 78. Skeletonema potamos. A, B. the arrangement of weak punctas on valve and fultoportular tubes on marginal area of the valve (SEM).

Skeletonema potamos Nakdong River 106

105

104

103

102

101

Seonakdong River 106

105

Algal abundance (cells/mL) 10

103

102

101

91 92 93 94 95 96

Fig. 79. Seasonal variations of diatom Skeletonema potamos (grey area) and total phytoplankton (solid lines) in the downstream of the Nakdong River (upper) and in the Seonakdong River (below). 104 Algal Flora of Korea·Freshwater Diatoms I of the Nakdong River estuary, the Seonakdong River, the Joman River and the Nakdong River, after 1995. However, it is probable that this species have usually bloomed around the downstream reaches of the Seonakdong River in the past. This species have not previously been described from Korean freshwaters. SPECIMEN EXAMINED: (Planktonic diatoms collected in the lower parts of the Seonakdong River: 31.xii.1992). ECOLOGY: This species prefers water of 2-34‰ salinity (Hasle and Evensen 1976). At the Grand River mouth of Lake Erie, the occurrence of S. potamos has been associated with relatively elevated concentrations of phosphorus, nitrogen and chloride (Nicholls et al. 1983). It is generally considered a warm stenothermic and photophilic species with a broad salinity tolerance, typically found in inland rivers and lakes, tidal estuaries and coastal waters. S. potamos is restricted to the down- streams of river or river mouths and particularly abundant in eutrophic waters. REMARKS: With very delicate and weak silicified skeletons, carefulness is required for the specimen preparations and handling. The colonial lengths of this species depend on salinity concentration.

31. Skeletonema subsalsum (A. Cleve) Bethge 1928: 343 (Figs. 80-82).

Hasle and Evensen 1975: 285. f. 1. Krammer and Lange-Bertalot 1991a: 82. pl. 84. f. 5. Gibson et al. 1993: 69. f. 4.

BASIONYM: Melosira subsalsa A. Cleve-Euler 1912: 509. f. 1.

Cells short cylindrical and connected to chains with a maximum of 10 cells. Valves circular, flat

Fig. 80. Skeletonema subsalsum. A. the areolar and costal ornaments on valve; B. the connection of linking spines between two valves. Bacillariophyceae: Centrales: Thalassiosiraceae 105 m

E μ 10

D I G H B C F m

A 10

JKLM

Fig. 81. Skeletonema subsalsum. A-F. the girdle and valve view of cell (×2,000); G-I. the cells and their colonial chains (×400); J. the valve view (×2,000); K-M. the girdle view of cell (×2,000) (LM); N. the inside of the valve; O. a ring of fultoportulae at the junction of valve and mantle, the radiating areolae on valve (SEM). 106 Algal Flora of Korea·Freshwater Diatoms I to somewhat rounded, 3-8 μm in diameter and 5-18 μm in pervalvar length. Areolae on valves and mantles usually rectangular, and arranged in radial patterns on valve. Typically 3-4 areolar striae between each process on the margin. Fultoportulae lining around the edge of valve as a ring, from which hollow processes emerging, perpendicular to the valve. Mar- ginal tubular processes connected to the next cell’s processes. The basic morphology of cell similar to that of S. potamos.

TYPE: None. SEASONALITY: S. subsalsum has been recorded in temperate regions in spring, summer, and fall. It is recorded with highest abundances in spring in the Great Lakes and with a summer maximum in the St. Lawrence inlet of the Great Lakes, and in Lake Lough Erne in North Ireland (Gibson et al. 1993). DISTRIBUTION: S. subsalsum is native to Eurasian Fig. 82. Distribution of Skeletonema sub- waters including the Baltic Sea and the Caspian Sea. salsum. S. This species is dominant in the lower Rhine River on German/Dutch border (Admiraal et al. 1994; Ibelings et al. 1998), and was a summer maximum in Lake Lough Erne of Northern Ireland (Gibson et al. 1993) and in the Waal River of the Netherlands (Spaink et al. 1998). In North America, it is dominant in the rainy season in a lagoon in the Gulf of Mexico (Castillo et al. 1995), in the Joaquin River Delta of California (Muller-Solger et al. 2002) and in the St. Lawrence River mouth in Canada (Winkler et al. 2003). S. subsalsum was first recorded in 1973 in Lake Erie and subsequently reported in Lake Ontario, Lake Michigan, and Lake Huron (Hasle and Evensen 1976; Stoermer 1978; Mills et al. 1993). This taxon was likely introduced to the Great Lakes drainage by ship’s ballast water (Mills et al. 1993). The species was also recorded in South American waters in Argentina and Brazil. KOREA: This species has not been entirely described in South Korea, whereas it was reported as planktons in the Seonakdong River, and as epiphytic diatoms to reed plants in Lake Gocheonam located in Haenam (Cho 2004). SPECIMEN EXAMINED: (Planktonic diatoms collected in the Seonakdong River at Gimhae Bridge: 14.vi.1997). ECOLOGY: S. subsalsum is a freshwater to brackish water species, usually occurring in salinity of up to 15‰ in rivers, lakes, inland seas, coastal waters, and marshes, and often associated with eutrophic conditions. The number of processes and their lengths of this species is positively related to salinity like S. potamos. It is particularly known to occur during periods of elevated water temperature, rainy seasons or summer. REMARKS: This species is known to be a stenohaline species and to represent the equivalently spatial distribution. Bacillariphyceae: Centrales: Melosiraceae 107

Family Melosiraceae Kützing 1824: XIV. 8. Won-tong-dol-mal-gwa (원통돌말과)

Cells cylindrical, spherical or capsule-shaped with rounded valve corners and strongly developed mantle towards the pervalvar axis. Cells in long chain. Pseudosulcus between two joining valves and the sulcus in girdle. Valves primarily circular. A ring of rimoportulae on valve margin or mantle, but sometimes reduced. Specific structures such as pseudoloculus, carina and corona to some species of family Melosiraceae. Pseudoloculi, chambers on the outer side of valve by the expansion of distal parts of anastomosing costae. Carina, a circular collum on the face of valve. Corona, a ring of large irregular spines at the inner parts of carina. Resting spores frequent in life cycles.

GENERA AND SPECIES: There are names of 14 genera and 1,151 species, of ehich 146 species are accepted or flagged as valid taxa (Algaebase 2010). They are almost marine species except 20 species of three genera Melosira, Orthoseira and Ellerbeckia. In Korea, taxa belonging to the family are 8 speices in freshwaters or brackish waters and 12 species in marine waters (Lee 1995; KNCCN 1996; Lee 1997). DISTRIBUTION: Melosira varians is apparently a freshwater species, while other Melosira and taxa belonging to the family are brackish or marine endemics, and primarily benthic or periphytic. KEY REFERENCE: Simonsen (1979), Hasle and Syvertsen (1996).

Key to the genera of family Melosiraceae

1. Valve faces show irregular structures in light microscopy ·············································Melosira - Valve faces show radial structures or fasciculation in light microscopy ····································2 2. Radial or fasciculous lines occur with invisible puncta ···············································Ellerbeckia - Radial or fasciculous lines composed of distinctly punctate striae ······························Orthoseira

REMARKS: Simonsen (1979), who established the family characteristics, regarded the family circumscription as unsatisfactory and suggested that Melosiraceae should be split into more families without doing so himself. Melosira and its two derivatives (Orthoseira and Ellerbeckia) are the freshwater genera of the family. Later, Round et al. (1990) subdivided the family Melosiraceae into other familial lines - Melosiraceae, Orthoseiraceae, Paraliaceae and other family groups.

Genus Melosira C. A. Agardh 1824: XIV. 8. Won-tong-dol-mal-sok (원통돌말속)

Cells cylindrical, often subspherical and capsule-shaped with high mantle and well developed girdle. Mantle not usually differentiated from the valve in most species. Cells united to form long chains by mucilage pads, lacking the spines of Aulacoseira. Valves circular, flat or domed and covered with small spines or granules. Valves rarely seen due to the exposed girdle view. Pseudoloculi, chambers on the face of valve by expansion of the distal parts of anastomosing costae. Loculi randomly arranged in rows radiating from the centre of valve. Spine-like projections, called ‘corona’, 108 Algal Flora of Korea·Freshwater Diatoms I occasionally developed in the inner parts of the carina. The corona surrounded by another collar- like structure, ‘carina’, as in M. nummuloides. Areolae on mantles barely discernible in light microscopy. The surface of the valve mantle hyaline without ornamentation or granules. Specific structures such as pseudoloculus, carina and corona to some species of the genus Melosira. Using electron microscopy, rimoportulae usually seen in a ring near the mantle margin and sometimes scattered on valve. Numerous plastids and small plates lying in peripheral cytoplasm. Lectotype: Melosira nummuloides Agardh 1824: 8.

SPECIES: There are 734 species named the diatom database (Algaebase 2010), and the majority of species are being transferred to Aulacoseira and other taxonomic groups. The 57 Melosira species are currently taxonomically recognized. In Korea, freshwater and brakish taxa of the genus Melosir are 11 species - M. lineata (Dillwyn) Agardh (=M. juergensii Agardh), M. moniliformis (O. F. Müller) Agardh (=M. borreri Greville), M. nummuloides Agardh, M. octogona Schmidt, M. varians Agardh, M. undulata (Ehrenberg) Kützing, M. roeseana Rabenhorst, M. roeseana var. epidendron Grunow, M. solida Eulenstein. The latter three species are transferred to Orthoseira roeseana (Rabenhorst) O’Meara, O. epidendron (Ehrenberg) H. Kobayasi and Aulacoseira solida (Eulenstein) Krammer, respectively. With exception of two synony- mous species, there are about six species of genus Melosira in Korean freshwaters and three species in marine waters. DISTRIBUTION: Diatoms belonging to this genus appear as cosmopolitan in inland waters and are uncommon in coastal waters. Many Melosira species belong to the tychoplankton living in both benthic and planktonic algal assemblages. Algal buoyancy can no longer be achieved if once filamentous colonies reach a certain length and settle on benthic environments. Some Melosira blooms caused by flooding events have been observed in freshwater from near shore coastal environments or after heavy storms (Julius 2007). ECOLOGY: Diatoms of the genus Melosira commonly occur in freshwater and coastal water as periphytons or planktons. This group of diatoms is more epibenthic or aerial in natural waters rather than planktonic. KEY REFERENCE: Crawford (1973, 1979), Round et al. (1990), Krammer and Lange-Bertalot (1991).

Key to the species of genus Melosira

1. Ring of collar is present in the margin of valve face ···········································M. nummuloides - Collar is absent in the valve margin ·························································································2 2. One large puncta occur around the central zone of valve. Mother cells with many inner layers occur as a result of multiplications···············································································M. dickiei - Variable valve structure············································································································3 3. No ornaments occur on valve mantle or girdle in light microscopy··········································4 - Distinct ornaments are on the mantle and girdle ······································································5 4. Rectangular outline in the girdle view········································································M. varians - Long octagon outline in the girdle view··········································M. moniliformis var. octagona 5. Relatively gross structures occur on valve, mantle and girdle·····························M. moniliformis - Regularly fine puncta occur on valve ··········································································M. lineata (Krammer and Lange-Bertlaot 1991a)

REMARKS: The genus Melosira was established in 1824 by C. A. Agardh to include five species: M. nummuloides, M. moniliformis, M. lineata, M. discigera and M. jurgensii. The genus contained many Bacillariphyceae: Centrales: Melosiraceae 109 other important floras in freshwaters as designated by Hustedt (1930) and Cleve-Euler (1951). Using electron microscopy, Crawford (1971) and other authors revealed considerable heterogeneity in the genus Melosira, after that, many species of the genus were transferred to other genera. Many common species were removed to Aulacoseira (Simonsen 1979) and some Melosira were transferred to the genus Orthoseira. Melosira arenaria and the related diatoms were assigned to Ellerbeckia (Crawford 1988).

32. Melosira moniliformis (O. F. Müller) Agardh 1824: 8 (Figs. 83, 84).

Krammer and Lange-Bertalot 1991a: 8. pl. 5. f. 1. Crawford 1977: 299. f. 1.

SYNONYM: Conferva moniliformis O. F. Müller 1783: 80. pl. 3. f. 1. Lysigonium moniliforme (O. F. Müller) Link 1820: 4. Gaillonella moniliformis Bory 1825: 102. Lysigonium moniliforme (O. F. Müller) Trevisan 1848: 1848. Melosira borreri (borrerii) var. moniliformis (O. F. Müller) Grunow 1878: 128. Melosira borreri Greville 1833: 401.

Cells cylindrical with convex valve surface and round corner, or short disc forms. Cells united into chains or filaments, forming a pair of cells regularly enveloped in mother girdle. Two cells often bound by sharing the girdle of a mother cell. Valves circular, 25-70 μm in diameter and 14-30 μm in mantle height. The ratios of mantle height and valve diameter 0.4-0.6 and below 1.0. Valves with fine punctas and seemingly differentiated into central and marginal region due to valve topography. A ring of spines situated at the boundary of valve and the connector of adjacent cells. Sulci, pseudosulci in girdle view, and Ringleiste structures inwards of valve absent. Areolae on valve mantle arranged in parallel along pervalvar axis in 10-12 rows in 10 μm. Rimo- portulae near the central area of valve.

TYPE: Syst. 8. 1824 (L). SEASONALITY: As a cold-water species, this species prefers the winter season and northern areas, even the subarctic sea in the northern hemisphere. DISTRIBUTION: M. moniliformis is widely distributed throughout the entire southern Pacific and Atlantic coastal regions (Julius 2007). These diatoms show strong dominance along the the Tagus estuary, Portu- gal (Brogueira et al. 2007). Stones and vascular plants are covered by M. moniliformis and M. lineata, both of which are dominnat in the discharge channel outside the Olkiluoto nuclear power station in Finnish coast Fig. 83. Distribution of Melosira monili- of the Bothnian Sea in 1985-1986 (Keskitalo and Heitto formis. 110 Algal Flora of Korea·Freshwater Diatoms I

A B C

D G

F m

μ 10 m

E 10 H

Fig. 84. Melosira moniliformis. A-F. the valve view and punctas in the marginal area of the valve (×2,000); G. the mantle view and connection of two joining valves (×2,000); H. a pair of cells in colony and many plastids in a cell (×400) (LM). Bacillariphyceae: Centrales: Melosiraceae 111

1987). M. moniliformis was observed to be dominant in eutrophic waters of the western Baltic Coast (Hillebrand and Sommer 1997). It comprised the majority of the total algae in fish (Mugil cephalus) stomachs (Julius 2007). Though this diatom species is not a major component of the algal community in Hawaiian estuaries, it is reported to be selectively fed upon by Mugil cephalus during foraging activities. The species diatoms are abundantly found in the Holocene sediments through palaeological studies in the coastal harbors of New Zealand and Australia (Hayward et al. 2003; McMinn et al. 2003). KOREA: This species is found in the coastal zone of the Cheonsu Bay, a southern region of the West Sea of Korea (Shim 1994). The species diatoms are also observed in streams and the river mouths of some rivers. The frequency and dominance of the species is usually low in Korean coastal regions. SPECIMEN EXAMINED: (Epilithic diatoms collected in the estuary of the Osipcheon Stream at Ganggu of Yeongdeok: 5.i.2009). ECOLOGY: Like other Melosira, M. moniliformis is tychoplankton and exists both in benthic and planktonic habitats, but prefers the benthic environments in saline environments. Through micropalaeological studies in New Zealand, habitats that are favoured by the species is shallow, turbulent and brackish waterbodies such as a narrow tidal arms of a harbor lined by salt marsh plants (Hayward et al. 2003). REMARKS: Sexual reproduction in the centric diatoms is known to a few this group’s diatoms. M. moniliformis diatoms seem to possess patterns of gamete production (Mizuno 2006).

33. Melosira nummuloides (Dillwyn) Agardh 1824: 8 (Figs. 85, 86).

Crawford 1973: 132. f. 1. Crawford 1975: 324. f. 1. Krammer and Lange-Bertalot 1991a: 11. pl. 8. f. 1.

BASIONYM: Conferva nummuloides Dillwyn 1809: 43. pl. B. SYNONYM: Fragilaria nummuloides (Dillwyn) Lyngbye 1819: 184. pl. 63. f. C. Gaillonella nummuloides (Dillwyn) Bory 1831: 102. Melosira salina Kützing 1844. Lysigonium nummuloides (Dillwyn) Trevisan 1848: 96.

Cells rather elliptical to globose or orbicular in girdle view, however, more and less elongated along pervalvar axis. Cells connected to form moniliform filaments and two cells bound by sharing the girdle of a mother cell, such as M. moniliformis. Valves circular and convex, 9-42 μm in diameter and 10-14 μm in mantle height. A collar-like projection, ‘carina’, between the valve center and the margin to form a circle. In the inner parts of the carina, other projections or pieces, Fig. 85. Distribution of Melosira nummu- collectively called ‘corona’, surrounding the central loides. 112 Algal Flora of Korea·Freshwater Diatoms I

B A C D m

E 10

JK L M

Fig. 86. Melosira nummuloides. A-E. the view of valve and mantle; F, G. the girdle view of a cell; H. the membraneous collum around the mantle; I. the connection of two valves (×2,000); J-M. a pair of cells enveloped by girdle in a colony (×400) (LM). Bacillariphyceae: Centrales: Melosiraceae 113 area, linking two adjacent valves. Formation of resting spores not known.

TYPE: Syst. Alg. XIV. 8. 1824(L). SEASONALITY: M. nummuloides is most abundant during cold seasons, even in the Arctic Sea, and least abundant during August or summer. In spring, the species provides one of the dominants in the Kiel Fjord, of the western Baltic Sea (Hillebrand and Sommer 1997). DISTRIBUTION: This species is cosmopolitan as epibenthic diatoms in brackish and coastal waters, and also occurs in saline waters of inlands. M. nummuloides is often observed in plankton with detachment from substratum. These diatoms are most abundant in the Yaquina Estuary, Oregon (McIntire and Overton 1971) and dominates the polluted sites in the Clyde Estuary, Scotland (Rendall and Wilkinson 1983). KOREA: The species is observed in the brackish and coastal waters in general, near the Ganghwa Island (Chung 1969), the estuary of the Nakdong River and the Geum River (Lee 1973; Shim and Yang 1982), and the coastal area of Yeosu (Yang 1977). The species was observed in low abundances in the lower reaches of the Nakdong River before the estuarine dam construction (Chung et al. 1987b). SPECIMEN EXAMINED: (Epilithic diatoms collected in the estuary of the Osipcheon Stream, Ganggu in Yeongdeok: 5.i.2009). ECOLOGY: This species is common in brackish and organically polluted waters. M. nummuloides is favored by nutrient enrichment, as along the western Baltic Coast (Hillebrand and Sommer 1997). REMARKS: When C. Agardh included five species into the genus Melosira, the first of these species was M. nummuloides.

34. Melosira varians Agardh 1827: 628 (Figs. 87-89).

Crawford 1971: 176. f. 1. Crawford 1978: 241. f. 33. Krammer and Lange-Bertalot 1991a: 7. pl. 4. f. 1.

SYNONYM: Gallionella varians Ehrenberg 1836. Lysigonium varians (Agardh) De Toni 1892: 902.

Cells cylindrical and united by valves to form long chains. On valve, a number of irregular granules and small irregular spines as linking device. Valves circular, 8-35 μm in diameter, 4-17 μm in mantle height, and the ratios of mantle height and valve diameter usually less than 1. Collars absent on valve. Mantle uniformly thin throughout cells compared to that of other Melosira species. In the microstructures of cell, closed pseudo-loculae with poroid areolae being open to the outside through a number of small pores and to the inner surface by somewhat larger pores which may be partially or completely bridged by silica struts. Rimoportulae as simple pores randomly arranged on mantle. Fig. 87. Distribution of Melosira varians. 114 Algal Flora of Korea·Freshwater Diatoms I

C D

B A m

μ 10

E FGHIJ

Fig. 88. Melosira varians. A. connected portion by thread between valves; B-D. the valve face; E-I. the view of girdle and mantle; J. the consecutively developed auxospores in a colonial filament (×400) (LM). Bacillariphyceae: Centrales: Melosiraceae 115

Fig. 89. Melosira varians. A-C. the view of valve, micro-structures in the central and marginal zone of valve; D. mantle without any distinct ornaments on surface; E. rimoportular pores on mantle; F. the view of valve and mantle (SEM). 116 Algal Flora of Korea·Freshwater Diatoms I

TYPE: Flora 10 (40): 628 (1827) (L). The Tepl river at Carlsbad influvio, Czechoslovakia. SEASONALITY: As benthic, periphytic or planktonic algae, M. varians is common during high waters from spring to autumn, however, occasionally it occurs abundantly in winter. DISTRIBUTION: This is truly an obligatory freshwater diatom that is distributed worldwide. The species is also found in brackish waters. The species was dominant in eutrophic lakes of Finland (Karjalainen et al. 1996). At the beginning of colonization on reed plants, M. varians was found being dominant in algal groups of epiphytes in a Turkish lake (Albay and Akcaalan 2003). KOREA: M. varians is one of the most common species in Korean freshwaters. It is observed as plankton with high frequency in the lower and middle reaches of the Han River (Chung et al. 1965; Chung 1972). The species was very abundant at Mulgeum in the estuary of the Nakdong River before the dam construction in 1987 (Chung et al. 1987b). However, after the dam construction in the estuary, the species is less common in frequency and abundance in the plankton (Lee et al. 1995a). The species is also observed in the Imjin River (Lee and Yoon 2002). It is also observed in lakes, Lake Yeongcheon and Lake Hapcheon (Kim and Lee 1996), and Lake Imha (Kim et al. 1997). This species is observed in the epilithic assemblages of streams: the Sincheon and the Donghwa Stream of the Geumho River system (Hong and Chung 1990; Lee and Chung 1992; Choi et al. 1993), in the Seomjin River (Lee et al. 2000) and in the Hyeongsan River (Chung 1987). Besides of rivers and streams, they are observed in oligotrophic mountainous streams of Mountain Jiri, Baekun and Unjang in Korea (Chung and Lee 1983; Chung et al. 1986b; Kim et al. 1998a). They are also found in the Yongneup Alpine Swamp (Chung and Kim 1987). Their frequency and abundance are relatively low in the Haman lowland wetland (Chung and Noh 1987). SPECIMEN EXAMINED: (Epilithic diatoms collected in the estuary of the Daejongcheon Stream, Yangbuk in Gyeongju: 7.x.1995). ECOLOGY: M. varians has a wide ecological tolerance from oligotrophic to eutrophic status and from freshwater to brackish water. It is one of the most eutrophilous algae in freshwaters, and occurs in dystrophic waters of moor lands and even oligotrophic waters (Karjalainen et al. 1996). REMARKS: It is possible to confuse M. lineata and its morphotypes with M. varians. Apart from their different ecology, the thinner and straighter valve of M. varians is perhaps the most reliable features to distinguish them by light microscopy, and the larger rimoportulae, more robust girdle- band and plain valves are other characteristics seen in electron microscopy (Crawford 1978).

Genus Orthoseira G. H. K. Thwaites 1848: 167.

Cells cylindrical and united to form short filaments by connecting adjacent valves. Valves circular with areolate punctas radiating from the center to the valve margin even down to the valve mantle. Short spines forming a ring at the margin of valve to interlock with the adjacent valves in colonies. Spines not needle-shaped, but triangularly well-defined plate types. Some simple granules or openings on the central parts of valve, called ‘carinoportulae’. Their microstructures simple internal openings and well-defined collars to outside. All these taxa characterized by the presence of carinoportulae. The cingulum composed of numerous intercalary bands. Numerous small and discoid plastids in the peripheral area around the central nucleus in cell. Lectotype: Melosira americana Kützing 1844: 55. pl. 30. f. 69 (=Orthoseira americana (Kützing) Spaulding and Kociolek 1998: 143). Bacillariphyceae: Centrales: Melosiraceae 117

SPECIES: There are 16 species in the database, of which six species are recognized as taxonomically valid (Algaebase 2010). Four species - O. roeseana, O. dentroteres, O. dendrophila and O. circularis - are known to be freshwaters. Two species, O. roeseana (Rabenhorst) O’Meara, O. roeseana var. epidendron Grunow, occur in Korean freshwaters. DISTRIBUTION: The group’s diatoms are usually aerial or subaerial, and are less frequently observed in planktons. They are abundant in caves, even ice caves, being epiphytic or aerophytic ones in mosses, lichens and bryophytes. Lichen thalli in tropical rain forests are inhabited by some epiphytic diatoms, among them prevails the genus Orthoseira (Lakatos et al. 2004). The diatoms are also observed in epilithic assemblages on rock surfaces. ECOLOGY: The species is aerial or subaerial diatoms commonly found in bryophytes and caves in alkaline environments. KEY REFERENCE: Crawford (1981), Round et al. (1990), Krammer and Lange-Bertalot (1991). REMARKS: The diatoms of this group can be differentiated from neighboring centric diatoms by the radially areolation characteristics on the valve face. Genus Orthoseira resembles the Cyclotella diatom in its valve structure.

35. Orthoseira roeseana (Rabenhorst) O’Meara 1875: 255 (Figs. 90, 91).

Krammer and Lange-Bertalot 1991a: 13. pl. 3. f. 5. Houk 1993: 395. f. 74.

BASIONYM: Melosira roeseana Rabenhorst 1848-1860: 383. SYNONYM: Gaillonella (Gallionella) roeseana (Rabenhorst) Petit 1880: 21. Melosira dendroteres var. roeseana (Rabenhorst; Rabenhorst) Ross 1947: 181.

A C

D m

B 10 E

Fig. 90. Orthoseira roeseana (×2,000). A-C. the large carinoportular punctas in central area and the radial arrangement of areolae in marginal area of valve; D, E. the broad collum and sulcus in girdle (LM); B-E. Chung 1993: 104. f. 181, 181a. 118 Algal Flora of Korea·Freshwater Diatoms I

Cells cylindrical with flat valves and rounded corners, the junction of valve and mantle. Cells connected by short spines around the valve margins to form short filaments. Valves circular, 8-70 μm in diameter and 6-13 μm in mantle height. The ratios of mantle height and valve diameter, 0.5-0.7, less than 1. Areo- late punctas on valve arranged in radiating pattern and fainter from the margin to the central parts. The radial striae on valve 14-20 in 10 μm and the longitudinal striae on the mantle 19-28 in 10 μm. The 2-4 large openings (carinoportulae) and spines on the central parts of valve. Valve mantle deep developed. Valve and mantle areolate, even in intercalary bands. Several thin rings of large circles, attenuations of the silica wall, in the interior of valve margin. These circular patches visible with unresolved focus in light microscopic observation.

TYPE: Diatoms: 174 (1982). Fig. 91. Distribution of Orthoseira roeseana. SEASONALITY: This species is a cold-water species and is frequently observed in arctic regions. DISTRIBUTION: O. roeseana is commonly an aerophytic diatom on wet rock faces, bryophytes and trees, especially in alkaline areas all over the world (Krammer and Lange-Bertalot 1991a). The species was observed less commonly in the bryophytes of the subarctic regions of South Georgia (Van de Vijver and Beyens 1997). It was recorded abundantly in the caves in Hungary, North Ame- rica and the Czech Republic (Poulíckováˇ and Haslerˇ 2007). Cryogenic cave calcite powders, ice plugs and others were collected from ice caves in the northern Yukon Territory of Canada, and were dominated by O. roeseana and O. dendroteres (Lauriol et al. 2006). The diatom was dominant in the symbiotic algal assemblages within the thalli of a common filamentous lichen (Coenogonium linkii) growing in the understory of neotropical lowland rain forest in Panama and French Guiana (Lakatos et al. 2004). This species was also less frequently observed as periphytic diatoms in lakes and other freshwaters. It was observed on rocks in Dunedin of New Zealand (Wood 1961) and in only one lake among the epilithic diatoms of 34 high mountain lakes in Slovakia (Stefkovaˇ 2006). KOREA: These diatoms were reported in mountain streams (Chung 1979), Wolak Mountain in Jecheon, Juheul Mountain in Mungyeong and Daeam Mountain in Inje and the Yongneup subalpine wetland of Daeam Mountain (Chung 1974). They were observed in the periphytic assemblages collected in Lake Paldang (Chung and Lee 1978), in streams of Gyeongju (Chung and Watanabe 1984). Its frequency and abundance are very low in Korean freshwaters. SPECIMEN EXAMINED: (Periphytic diatoms collected from a spring in Jeolmul Recreation Forest in Halla Mountain, Jeju Island: 22.xi.2009). ECOLOGY: This species is abundant in natural caves, even ice caves and common as aerophytic diatoms of rocks, bryophytes and trees especially in alkaline areas. REMARKS: The ratios of mantle/diameter are influenced by the auxospore stage within the life cycle. The diameters of pre-auxospore valves vary more than those of the height, as the decrease in cell size is due to a much more rapid reduction in diameter than in mantle height. F. T. Kützing, in Bacillariphyceae: Centrales: Hemidiscaceae 119

1844, described and depicted the new species Melosira americana from tropical America and, after that, G. H. K. Thwaites removed this species from Melosira and transferred it to the new genus Orthoseira (Houk 1993). L. Rabenhorst, in 1852, collected and illustrated a new species, Melosira roeseana. From early times, there was much confusion in the taxonomy and nomenclature of O. roeseana. The specimens collected by L. Rabenhorst become to be the type meanwhile.

Family Hemidiscaceae Hendey 1937 emend. Simonsen 1975. Ban-won-ban-dol-mal-gwa (반원반돌말과)

Cells short cylindrical to discoid. Valves with radial and often fasciculate areolation. Few bands seen in girdle view. A marginal ring of large rimoportular processes, similar in shape and generally also in size. Pseudonodulus, an open hole or an area covered by densely packed smaller areolae, a marginal to submarginal structure, always only one per valve. The principal diagnostic feature of this family and barely observed by light microscopy.

GENERA AND SPECIES: There are four genera - Actinocyclus, Hemidiscus, Roperia and Azpeitia - in the world. There are 396 listed species in the database, of which 40 species are accepted taxonomically as valid ones (Algaebase 2010). The three genera and 18 species are reported in Korea and are also marine diatoms except Actinocyclus normanii. DISTRIBUTION: The diatoms of this family are primarily observed in marine waters, with a few species in coastal or brackish waters. KEY REFERENCE: Simonsen (1979), Hasle and Syvertsen (1996). REMARKS: Simonsen (1979) considered the pseudonodulus structure as the principal diagnostic feature of the Hemidiscaceae, whereas Round et al. (1990) and some diatomists questioned the taxonomic eminence of the pseudonodulus.

Genus Actinocyclus Ehrenberg 1837: 61. Ba-kui-dol-mal-sok (바퀴돌말속)

Cells disc-shaped or barrel-shaped with circular valve and shallow valve mantle. Valves flat or domed. Areolar patterns on valve, usually fasciculate with radial rows of variable length. Foam- like or bubbly (known as bullulate) areolae on valve. Areolae often denser in marginal zone. Usual- ly seen in valve view with central and marginal areas composed of the same pattern. A marginal ring of fultoportulae and a pseudonodulus at valve margin in light microscopy with careful focus. Rimoportulae absent in valve center and a ring of simple rimoportula arranged in mantle. A wide valvocopula, narrow second and third band in girdle view. As a result, valve mantle deep with simple rimoportular openings. Plastids discoid-shaped and numerous in cytoplasm. Lectotype: Actinocyclus octonarius Ehrenberg 1837: 61. 120 Algal Flora of Korea·Freshwater Diatoms I

SPECIES: Total 378 Actinocyclus species have been reported worldwide and 30 species are validly described. However, only four or five species have been common among brackish or marine planktons. DISTRIBUTION: The group belongs to the primarily estuarine planktons, but occurs in the planktons of some saline or eutrophic inland waters as well. ECOLOGY: The freshwater diatoms of this genus occur mainly in slow flowing waters and lakes that are shallow enough to be wind-mixed, as well as in turbulent rivers and streams. This genus is probably epiphytic on seaweeds, but is often encountered in nearshore plankton. KEY REFERENCE: Hasle (1977), Round et al. (1990), Krammer and Lange-Bertalot (1991). REMARKS: The pseudonodulus is a structural feature of many marine genera, as Actinocyclus, and is hardly ever apparent in freshwater diatoms. These diatoms have relatively heavily silicification and can be easily distinguished from other centric diatoms by the lack of processes and the absence of ribs. Characteristics used to differentiate the species: type of fasciculation, position of rimoportulae, the presence of an annulus (a ring of costae around the valve center) and the pseudonodulus, and their positions.

36. Actinocyclus normanii (Gregory ex Greville) Hustedt 1957: 218 (Figs. 92, 93).

Krammer and Lange-Bertalot 1991a: 88. pl. 81. f. 1.

BASIONYM: Coscinodiscus normanii (‘normanni’) Gregory ex Greville 1859: 80. pl. 6. f. 3. SYNONYM: Coscinodiscus curvatulus var. normanii (Gregory manuscript in Greville) Cleve 1883: 488. Coscinodiscus normannicus Gregory ex Greville in Van Heurck 1883. pl. 131. f. 1. Coscinodiscus rothii var. normani (normanii) (Gregory) Van Heurck 1885: 218. Coscinodiscus subtilis var. normanii (-manii, -manni) (Gregory) Van Heurck 1885: 218.

Cells drum-shaped with concentrically undulating valves. Valves circular, 25-100 μm in diameter and the ratios of mantle height and diameter 0.4 to more than 1. Valves composed of polygonal or large areolae forming radial lines with variable lengths. Areolar striae 10-13 lines in 10 μm and 8-12 areolae in 10 μm. Finer areolation in valve mantle. A circular rimoportulae in marginal area of valve. Other features referred to the description of the genus.

TYPE: Abh. Naturw. Ver. Bremen 34: 218 (1957). SEASONALITY: Spring phytoplankton is succeeded by centric diatoms and A. normanii in some regions (Köhler et al. 2002). Furthermore, the species is record- Fig. 92. Distribution of Actinocyclus nor- ed as summer plankton with high abundance in manii. Bacillariphyceae: Centrales: Hemidiscaceae 121 m

μ 10

A B

C DEF

Fig. 93. Actinocyclus normanii. A-F. the radiation and fascicles of areolae on valve, and seven black spots, rimoportulae, on the marginal zone of valve (×2,000, LM).

Lithuania (Kasperovicieneˇ 2001), the German North Sea (Köhler and Hoeg 2000) and North America (Stoermer et al. 1993). DISTRIBUTION: A. normanii is one of the dominant phytoplankton species in some freshwaters and brackish waters of Europe and North America - in Lake Erie in the 1960s and polluted nearshore regions of the other Great Lakes (Stoermer et al. 1993), the tidal Elbe River between Cuxhaven and Hamburg (Carstens et al. 2004), the lowland rivers Spree and Warnow in northeastern Germany (Köhler et al. 2002), and Lake Kaloté in a Lithuanian protected area (Kasperovicieneˇ 2001). The species has high frequency in the southern coastal fringe of the Rio de la Plata in Argentina (Gómez and Bauer 1998) and abruptly increases with the eutrophication of the North End Lake in South Africa (García-Rodríguez et al. 2007). This is one of the prevailing species in bottom sediments of the Curonian Lagoon, a semi-enclosed water body which is separated from the Baltic Sea (Vaikutiene 2002). In the late glacial records, the species was predominantly observed in the sediment cores from a lagoon of the south western Baltic Sea (Witkowski et al. 2004). KOREA: This species is relatively rare in Korea. The species is observed in the Bay of Gwanyang on the south coast of Korea (Shim 1994), and in the lower reaches of the Gwangcheon Stream in Uljin (Lee 1992) and the Nakdong River. SPECIMEN EXAMINED: (Periphytic diatoms collected in the estuary of the Nakdong River: 25.vii.1997). ECOLOGY: A. normanii is a salt-tolerant taxon and its presence indicates the influence of brackish waters (Sabater 2000). The residence time in tidal freshwater reaches is a key factor controlling the 122 Algal Flora of Korea·Freshwater Diatoms I seasonal and spatial occurence in an estuary. The species is well adapted to strongly changing light conditions and thus, is adapted to estuaries with high vertical turbulent mixing (Rehbehn et al. 1993). Furthermore, the downstream limit of the A. normanii habitat is primarily determined by light limitation rather than by saline stress. In addition, the species is tolerant to pollutant and eutrophication (García-Rodríguez et al. 2007). As a cosmopolitan species, it is often observed in waters where water quality has been severely degraded. REMARKS: The species has been recorded under various names during recent times. This is often confused with Thalassiosira bramaputrae (Ehrenberg) Håkansson and Locker in the valve morphology. However, it is distinguished by the absence of a pseudonodulus, the tangential undulation of the valve and a finer areolation on flat valve.

Family Rhizosoleniaceae Petit 1888. Gwan-dol-mal-gwa (관돌말과)

Cells elongated cylinder-forms with long spines at apices, connected by the spines to make chains. Single spine more tubular form. The girdle with imbricate scale-like segements. Valves cone-like (calyptra) with unilateral symmetry and being isopolar. Pseudoloculi unknown and single rimoportula on valve apex rarely reduced. Numerous small rounded plastids in cytoplasm. Resting spores rarely developed. Weakly siliceous cells, easily destroyed by acid oxidation treatment during the preparation of specimens.

GENERA AND SPECIES: There are six genera and 285 species reported in the world, wholly marine. However, among them, 64 species are accepted or flagged (Algaebase 2010). In South Korea, there are three genera and 41 species recorded. Among them, 26 species are Rhizosolenia diatoms. DISTRIBUTION: Rhizosoleniaceae and Chaetoceraceae are poorly represented in freshwater phytoplankton, and a few species are only observed in freshwaters. KEY REFERENCE: Simonsen (1979), Hasle and Syvertsen (1996). REMARKS: Dactyliosolen, Guinardia and Rhizosolenia belong to this family as described by Simonsen (1979). Round et al. (1990) included the more recently described genera - Proboscia, Pseudosolenia and Urosolenia - in this family. On the other hand, Sundström (1986) suggested to split Rhizosole- niaceae into two groups, the genus Rhizosolenia and other genera.

Genus Rhizosolenia Ehrenberg 1843: 402; emend. Brightwell 1858: 94. Kwan-dol-mal-sok (관돌말속)

Cells having particularly long tubular or solenoid structures with long or short, asymmetric spines at each pole. An eccentric apex with a spine in girdle view. Girdle with numerous transverse bands crossed by zigzag girdles and copulae like scales. Valves (calyptrae) asymmetrically cone-like, Bacillariphyceae: Centrales: Rhizosoleniaceae 123 converging into spines. Some platelet plastids in the cytoplasm and generally the plastids sparcely distributed in cytoplasm. Rhizosolenia diatoms forming resting spores in life cycles. Lectotype: Rhizosolenia americana Ehrenberg 1843: 422 (134).

SPECIES: Though the genus has approximately 230 species, some 35 species are accepted or flagged (Algaebase 2010). The remaining ones, except two species - R. longiseta Zacharias and R. erienis Smith - are wholly marine. DISTRIBUTION: Rhizosolenia diatoms are widespread and common in marine plankton. Two species (R. eriensis, R. muelleri) have been recorded in freshwater. These taxa from inland waters are solitary with long hair-like spines at the apex instead of strong ones. The cells of Rhizosolenia diatoms in freshwaters, however, are very delicate and easily overlooked under observation of light microscopy. Freshwater Rhizosolenia is generally planktonic in larger lakes. The diatoms of this group usually do not have high dominance in planktonic assemblages. However, Rhizosolenia diatoms were reported in remarkable numbers in some freshwaters of Finland and north European regions (Nõges and Vijrret 2001). ECOLOGY: It is among the common plankton in marine waters. KEY REFERENCE: Round et al. (1990), Krammer and Lange-Bertalot (1991).

Key to the species of genus Rhizosolenia

1. Spine is on the center of the pole ···············································································R. longiseta - Spine is on the side of the pole ····················································································R. eriensis

REMARKS: Nomenclatural changes were proposed in the marine and freshwater taxa of Rhizoso- lenia. The freshwater Rhizosolenia was transferred to a new genus Urosolenia by F. E. Round and R. M. Crawford in 1990. This genus diatoms are characterized by long fine hair-like spines. Con- cerning its fine morphology, the freshwater species does not have the grooves on the valves for valve connection, rimoportulae associated with the bases of the process, and the characteristic vela of the genus Rhizosolenia. The resting spores in freshwaters are limited to a few centric like Rhizoso- lenia and pennate diatoms (von Stosch and Fecher 1979; Edlund and Stoermer 1993).

37. Rhizosolenia longiseta Zacharias 1893: 38 (Figs. 94, 95).

Krammer and Lange-Bertalot 1991a: 85: pl. 86. f. 1. Edlund and Stoermer 1993: 59. f. 16.

SYNONYM: Urosolenia longiseta (Zacharias) Edlund and Stoermer 1993: 59. pl. 1. f. 5. Urosolenia longiseta (Zacharias) Bukhtiyarova 1995: 417.

Cells long cylinder forms elongated in pervalvar directions with numerous intercalary bands, 2- 3 per 10 μm, in girdle view. Valves 4-10 μm in diameter and pervalvar cells 40-200 μm in length. A long spine from the terminal of elongated cell. Girdle view almost hyaline, except a few small lobes of plastids in girdle bands. Plastids concentrated in the central parts of cell and most of the cell volume occupied by vacuoles. A single endogeneous resting spore in a mother cell. 124 Algal Flora of Korea·Freshwater Diatoms I

F B

G m

μ m C μ 10 10

D E

Fig. 94. Rhizosolenia longiseta. A-G. the girdle view as live cells before oxidation cleaning (A-D. × 400, F, G. ×800) (LM).

TYPE: ForschBer. Biol. Stat. Plön 1: 38. f. 7 (1893) (G). Gr. Plöner See. SEASONALITY: The species occurs with highest numbers in October in a mountainous stream (Lee and Yoon 2000), it is assumed that its seasonality is autumn. The species was also observed in July in other streams (Lee 1989). R. longiseta is common in cold regions and reached the highest numbers in June and October in Bacillariphyceae: Centrales: Rhizosoleniaceae 125

Finnish lakes (Ilmavirta 1982; Karjalainen et al. 1996; Horppila et al. 2000), and was very abundant in Octo- ber in Belgian lakes (Symoens et al. 1978). It occurred abundantly in summer and early autumn in a lake of Estonia (Kangro et al. 2005). DISTRIBUTION: This species is frequently reported in North European freshwaters as important plankton. It is observed during eutrophication periods and important in naturally eutrophic and humic lakes in the Tuusulaujarvi coastal lowland of southern Finland (Lepistö et al. 2006). These diatoms are observed abundantly in oligotrophic lakes (Lepistö and Rosenström 1998) and during the eutrophicaton periods of the 1960s and 1970s in Finland lakes (Lepistö et al. 2006). This species is dominant in eutrophic lakes of Pääjä- rvi, Saimaa and Hiidenvesi in Finland (Ilmavirta 1982; Karjalainen et al. 1996; Horppila et al. 2000), Etang du Gland Lake of Belgium (Symoens et al. 1978), Lake Verevi in Southeast Estonia (Kangro et al. 2005), Lake Fig. 95. Distribution of Rhizosolenia long- Upper Kuito, a forest lake in Northwest Russia (Holo- seta. painen et al. 2008) and a lake-river system in the Kos- tomnksha region of Russia (Holopainen et al. 2003). KOREA: These diatoms are planktonic, however, their abundances are low in Korean freshwaters. The species is reported in mountain streams in Korea such as the Suer Stream near Gwangyang, and the streams of Wolchul Mountain in Yeongam and Juwang Mountain in Cheongsong (Chung et al. 1985; Lee 1989; Lee and Yoon 2000). Especially in the Suer Stream, its relative dominance is recorded as being above 70% and its abundance ranges from 300 cells/mL to 1,240 cells/mL (Lee and Yoon 2000). Besides mountainous streams, the species is observed in many reservoirs for agricultural waters in the southern regions of Korea and the lower reaches of the Seonakdong River (unpublished data). SPECIMEN EXAMINED: (Ths species bloomed in Sirye Reservoir, Gimhae in autumn and was collected: 6.x.2008). ECOLOGY: The abundance of these diatoms indicates the water body to be eutrophic state, since it is one of the dominant plankton taxa during the first period, when fertilizers are added to Norwegian lakes (Reinertsen and Langeland 2006). The species showed adaptation to naturally eutrophic or slightly humic lakes in northern countries (eg. Finland). In other areas, the species was important in the oligotrophic lakes of Finland (Lepistö and Rosenström 1998) and was classified as an oligosaprobic algae (Andreev et al. 2003; Lepistö et al. 2006). In an enclosure experiment to assess the effect of zooplankton in Swedish lakes, exclusion of zooplankton especially favoured R. longiseta diatoms and dinoflagellates (Svensson and Stenson 1991). REMARKS: This was formally transferred to genus Urosolenia by Edlund and Stoermer (1993). 126 Algal Flora of Korea·Freshwater Diatoms I

Family Biddulphiaceae Kützing 1844: 15. Sil-pae-dol-mal-gwa (실패돌말과)

Valves primarily bipolar, secondarily tri- to multi- polar to circular. Valves often having elevations and some having linking spines. Pseudocellus very common though not always present. Rimopor- tulae in distinct patterns (if not reduced) on valves and never marginal. Some species with its own heterovalves in subfamily Hemiauloideae.

GENERA AND SPECIES: There are 3 subfamilies, 35 genera and 1,168 species reported in the world, however, 95 species are accepted and flagged (Algaebase 2010). The 14 genera and 42 species occur in South Korea as marine diatoms. Two species of genus Hydrosera and Acanthoceras are only freshwater diatoms. DISTRIBUTION: The diatoms of this group are entirely marine or coastal. Only genus Hydrosera and Acanthoceras are inland or brackish waters. KEY REFERENCE: Simonsen (1979), Hasle and Syvertsen (1996). REMARKS: In the family, three subfamilies - Hemiauloideae, Biddulphioideae and Stictodiscoideae - are suggested by Simonsen (1979).

Genus Hydrosera Wallich 1858: 251.

Valves with basically a triangular shape and a pole protruding from each of the three sides in valve face, totally six poles. Short or long chains formed by connection of three pseudoocellar poles of adjacent valve. Valves flat with deep mantle. Girdle view rectangular and cell forming a hexa- gonal cylinder with undulating sides across pervalvar axis. Pseudoocelli developed at three poles of valve and pseudosepta extending across the bases of three poles. Both valves and mantles coarsely areolate. In internal valve, loculate chambers separated by pseudosepta. A stalked rimoportula with an S-shaped slit seen in internal valve. Numerous plastids like elliptical platelets. Lectotype: Hydrosera triquetra Wallich 1858: 251. pl. 13. f. 1.

SPECIES: Only two species - Hydrosera triquetra Wallich, H. whampoensis (Schwarz) Deby - are known worldwide and H. whampoensis is found in Korean freshwaters. DISTRIBUTION: As large periphytic diatoms, the two species have different habitats. H. triquetra may be restricted to brackish-marine waters in tropical and subtropical areas, while H. whampoensis occurs more in freshwaters and brackish waters of temperature regions (Qi et al. 1984). As epiphytic or epilithic diatoms, these diatoms are usually distributed in estuarine and coastal regions. The diatoms of this genus progress upstream and frequently inhabit inland waters. It was found growing all year round in rice fields, irrigation ditches and small mountain streams in Taiwan (Li and Chiang 1977). Concerning their geographical distribution, they are generally regarded as tropical but also occur in some European and North America waters of the temperate regions. They have been recorded as the new diatoms in France, from European waters since 1990 (Coste and Ector 2000). The genus was reported in southern Brazil, California and South Dakota of North America, in the streams of Hawaiian Islands, the Portuguese west coast, France and England, and in Japanese Bacillariphyceae: Centrales: Biddulphiaceae 127 streams. These diatoms have been newly observed in the streams of Korea. ECOLOGY: Hydrosera diatoms are periphytic and warm-water species, occurring in estuary of tropical or subtropical regions. However, it may penetrate upstream in rivers and even into other freshwaters (Li and Chiang 1977). KEY REFERENCE: Li and Chiang (1977), Qi (1984), Sherwood (2004). REMARKS: Between H. whampoensis (Schwartz) Deby and H. triquetra Wallich, significant confusion is present in their identities since the genus was originally described by C. G. Wallich in 1858. Some diatomists identify two kinds as a single taxon, like Li and Chiang (1977). In 1939, M. Voigt argued that two taxa could be separated in view of morphological and ecological characteristics. H. triquetra has a rather undulate or sub-circular shape in valve view, and a different distribution with H. whampoensis.

38. Hydrosera whampoensis (Schwartz) Deby 1891: 209 (Figs. 96-98).

Qi et al. 1984: 216. f. 2. Sherwood 2006: 43. f. A.

BASIONYM: Triceratium whampoense Schwarz 1874: 163.

Cells connected with pseudoocelli on valve to form long filaments. Cells, barrel-shaped cylinder with flat ends, but with an undulated surface by longitudinal foldings. Valves basically trianular with six poles. Valves flat, however, having partition in surface elevation in light microscopy. Valves 110-140 μm in diameter and valve mantle 15-25 μm in height. Pervalvar cells 130-150 μm in length. Punctas on valve 3-4 in 10 μm. An internal partition or pseudoseptum at the base of three projected poles. Three pseudosepta clearly visible by light microscopy. Areolar punctas more irregularly distributed on valve and finely punctuate areas (pseudoocelli) at the three projected poles.

TYPE: Quart. J. Micr. Sc. 6: 251. pl. XIII. f. 1 (1858). SEASONALITY: The species is frequently observed in the warm season from July to September. DISTRIBUTION: H. whampoensis is extremely abundant, forming a long filament having a few hundred cells in a stream of the oldest Kaua’i island in Hawai’i (Julius 2007). The diatoms are reported as epiphytic or epilithic assemblages in the Savannah River in Gerogia, the San Joaquin River in southern California, and the other inland waters of the United States (Qi et al. 1984; Tiffany and Lange 2002) and in Hawaiian stream surveys from 2001 to 2003 (Sherwood 2006). The species is abundant at the lotic stream or river segments of South America - Atlantic rainforest regions Fig. 96. Distribution of Hydrosera wham- (Landucci and Ludwig 2005; Borges and Júnior 2006), poensis. 128 Algal Flora of Korea·Freshwater Diatoms I

A m μ B 10 F

D C

Fig. 97. Hydrosera whampoensis. A-C. the valve view and gross ornaments on valve (×1,000); D, E. the girdle view and longitudinal undulations (×200); F. a long filamentous chain (×100) (LM). Bacillariphyceae: Centrales: Biddulphiaceae 129

C D

Fig. 98. Hydrosera whampoensis. A. the valve view and flat surface of a valve; B. the girdle view and mantle; C. the triangular cylinder of a cell; D. areolar punctas on the valve; E. a pseudoocellus at the apex of valve (SEM). 130 Algal Flora of Korea·Freshwater Diatoms I at the most disturbed sites in a southern regions of Brazil (Burliga et al. 2008), and in the Yacyretá reservoir in Argentina and Paraguay. The species is reported in Lake Biwa of Japan (Tuji and Houki 2001), and is dominant or subdominant as bottom algae of a Japanese stream, in the downstream of the Hitokura dam in the Ina River (Yanagawa et al. 2006). The species was originally collected from the mouth regions of ‘Whampoa’ River in China. Although described as euryhaline diatoms in early times, H. whampoensis was found mostly in freshwaters in China and in the United States. KOREA: This species was first collected in Sincheon Stream, a tributary of the Geumho River, in 2005 (Kim et al. 2008). It occurs as epiphyton in the Seonakdong River in September 2008 and in freshwaters of Jeju Island in November 2009. SPECIMEN EXAMINED: (Epiphytic diatoms collected in the upper regions of the Seonakdong River: 29.ix.2008). ECOLOGY: This is one of the large periphytic algal groups or macroalgae having long filaments attached to substrates in streams (Sherwood, 2004). The species is of characteristically dark brown color in its growth. The species is usually associated with Biddulphia laevis Ehrenberg, Terpsinoe musica Ehrenberg and Melosira varians when they are predominant in freshwaters. Flooding frequency in Hawaiian streams appears to be important in regulating the filamentous length of larger diatoms such as Hydrosera (Julius 2007). The filaments of the species have some hundred cells in undisturbed streams, whereas it occurs as a cell or in short 2-5 cell groups being easily divided in high periodicity of flood events. This species has the cell geometry as host diatoms and acts as a attachment substratum for smaller diatoms (Tiffany and Lange 2002). It is rather confined to well-shaded or low light conditions in streams (Qi et al. 1984). REMARKS: This species is a macroalgae in tropical lotic ecosystems.

Family Chaetoceraceae H. L. Smith 1872. Sen-teol-dol-mal-gwa (센털돌말과)

Cells rarely solitary, and in most cases inseparable being united by fused silica between setae of adjacent cells. Valves elliptical, with two long setae emerging from apices. Resting spores common, always endogenous and distinctly different from vegetative cells. Cellular skeletons weakly siliceous and being carefully handled in the pretreatment of specimen preparation.

GENERA AND SPECIES: There are three genera - Acanthoceras, Bacteriastrum and Chaetoceros - and 573 species listed up in the world database (Algaebase 2009). Among them, 219 species were regarded validly (Algaebase 2010). In the family, the genus Chaetoceros has the largest 212 species. In South Korea, three genera and 89 species have been recorded. Two species occur in Korean freshwaters. DISTRIBUTION: The diatoms of this group are exclusively planktonic in marine water. Two species, Acanthoceras zachariasii, and muelleri, occur only in freshwaters among the family. KEY REFERENCE: Simonsen (1979), Hasle and Syvertsen (1996). REMARKS: In the diatom system of Round et al. (1990), Chaetoceraceae Simonsen is assigned two families - Chaetocerataceae Ralfs and Acanthocerataceae Crawford. Bacillariphyceae: Centrales: Chaetoceraceae 131

Genus Acanthoceras Honigmann 1910: 76. Ga-si-dol-mal-sok (가시돌말속)

Cells solitary and usually seen in girdle view. Cells are broadly cylindrical, girdle view rectangular having two parallel spines at each apex and forming H-shaped forms. With the weak silicification and the hyaline structures of cells, being easily overlooked in light microscopy. Normally four small plate-like plastids in cytoplasm and large hyaline areas around the plastids in girdle view. Resting spores characteristically formed in harsh environments. Lectotype: Acanthoceras magdeburgense Honigmann 1910: 77. pl. 2. f. a.

SPECIES: Ten species and subspecies were described, however, two species, Acanthoceras madebur- gensis Hongimann and A. zachariasii (Brun) Simonsen, are accepted (Algaebase 2010). A. zachariasii has been reported in Korean freshwaters. DISTRIBUTION: This genus is freshwater form of very delicate structure. ECOLOGY: Diatoms of this taxon are planktonic in shallow and eutrophic lakes and ponds. KEY REFERENCE: Simonsen (1979), Round et al. (1990), Krammer and Lange-Bertalot (1991). REMARKS: Attheya species in Biddulphiaceae was transferred to the genus Acanthoceras Honigman in 1910. Acanthoceras was classified as a member of the family Chaetoceraceae by Simonsen (1979). However, Round et al. (1990) proposed a new family Acanthocerataceae for this monotypic genus by reviewing its micro-structures with electron microscopy. A number of morphological features - the valve shape, the multiple girdle bands, the areolar type and the absence of portulae - are sup- posed to be different with the Chaetoceros series.

39. Acanthoceras zachariasii (Brun) Simonsen 1979: 55 (Figs. 99, 100).

Krammer and Lange-Bertalot 1991a: 83. pl. 79. f. 1. Edlund and Stoermer 1993: 59. f. 1.

BASIONYM: Attheya zachariasi Brun 1894: 53. pl. 1. f. 11. SYNONYM: Acanthoceros magdeburgense Honigmann 1910: 77. pl. 2. f. a. Rhizosolenia eriensis var. zachariasi (Brun) Playfair 1913: 538. pl. 56. f. 33.

Cells obligately solitary. Cells more and less squar- ish to rectangular in girdle view, with long projected spines at four corners. Silicified skeleton very delicate. Cells 5-15.5 μm in diameter, 13-40 μm in pervalvar length, and having spines up to 40-80 μm in length, less than 3 times of pervalvar length. In girdle view, Fig. 99. Distribution of Acanthoceras the pervalvar plane somewhat longer than valvar zachariasii. 132 Algal Flora of Korea·Freshwater Diatoms I

A B C m

μ 10 D

Fig. 100. Acanthoceras zachariasii. A-D. the numerous intercalary bands in girdle and long spines at apices (×2,000) (LM).

plane, having numerous intercalary bands in girdle. Girdle bands having hyaline appearance des- pite of the presence of four small plate-like plastids. A single, heavily silicified and endogeneous resting spore centrally located within a mother cell.

TYPE: Bacillaria 2: 55 (1979). SEASONALITY: A. zachariasii occurs only in summer and early autumn in Estonian freshwaters and accompanied by Rhizosolenia longiseta (Kangro et al. 2005), and occurs in Europe and North America (Stoermer et al. 1993). DISTRIBUTION: This species is generally rare in freshwaters where it prefers lakes or reservoirs. It is distributed and occasionally abundant but ephemeral, in alkaline and eutrophic waters, lakes, ponds and rivers in North America and northern Europe (Edlund and Stoermer 1993). In the Lake Bacillariphyceae: Centrales: Chaetoceraceae 133

Karhijärvi in Southwest Finland, diatoms with delicate skeletons such as A. zachariasii and Rhizo- solenia species reach remarkable numbers in some periods (Nõges and Vijrret 2001). However, in the River Meuse in Germany, the species is considered to be decreasing in its relative abundance since 1955 (Ibelings et al. 1998). KOREA: These diatoms were first collected from Lake Paldang and described in 1978 by Chung and Lee (1978). The species was recorded four times in South Korea - in the Han River and the Nakdong River (Lee 1985; Cho et al. 1993). SPECIMEN EXAMINED: (Planktons collected in the Seonakdong River at Gimhae Bridge: 25.viii.1997). ECOLOGY: The species produces resting spores; the occurrence of diatom resting spores in freshwaters is limited to a few centrics. A. zachariasii is widely distributed and occasionally abundant but ephemeral, in alkaline and eutrophic lakes, ponds and rivers. REMARKS: Diatoms belonging to Rhizosolenia and Attheya have been separated into marine and freshwater taxa, respectively. Freshwater Rhizosolenia was reallocated to the genus Urosolenia Round and Crawford and Attheya zachariasii to the genus Acanthoceras Hoigmann.

Genus Chaetoceros Ehrenberg 1844: 198. Sen-teol-dol-mal-sok (센털돌말속)

Cells more and less rectangular in girdle view, with extremely long setae projecting from valve corners. Cells connected by interlocking setae produced from valve margin, leaving openings or foraminae between the valves of neighboring cells. Cells rarely solitary and colonial filaments straight, curved, or coiled. Valves almost elliptical and rarely circular. However, valves hardly visible due to the long filamentous chains and their setae. A rimoportula in the central area of valve and sometimes reduced. One or more small plate-shaped plastids in cytoplasm. Resting spores frequently observed in life cycles. This group of diatoms, one of the most typical marine plankton species and only one species in freshwaters. Lectotype: Chaetoceros tetrachaeta Ehrenberg 1844: 200.

SPECIES: Chaetoceros is one of the largest genera of marine planktonic diatoms with 531 species worldwide. Among them, 212 species and infraspecies are valid as taxonomic groups (Algaebase 2010). C. muelleri is a unique species observed in freshwaters. DISTRIBUTION: They are exclusively oceanic or neritic and only one species has been observed in brackish waters, even in freshwaters. ECOLOGY: Diatoms of this group are typical planktons in marine waters and oceans. Their char- acterisitic colonial growth habits minimize sinking rates in the water column. They are important primary produces in marine waters. KEY REFERENCE: Rushforth and Johansen (1986), Round et al. (1990), Hasle and Syvertsen (1996). REMARKS: With their delicate structures, diatoms of the genus Chaetoceros may be observed or more easily identified in water mounts rather than as permanently fixed specimens by light microscopy. 134 Algal Flora of Korea·Freshwater Diatoms I

B A

D E C

Fig. 101. Chaetoceros muelleri. A-C. the girdle view of cell (A, B. ×500; C. ×2,000); D, E. auxospores of the cell (×1,200).

40. Chaetoceros muelleri Lemmermann 1898: 195 (Figs. 101, 102).

Krammer and Lange-Bertalot 1991a: 84. pl. 80. f. 1. Rushforth and Johanson 1986: 443.

SYNONYM: Chaetoceros subsalsus Lemmermann 1904: 141. pl. 1. f. 16. Chaetoceros zachariasi Honigmann 1909: 72. pl. 1. f. a. Chaetoceros thienemanni Hustedt 1925: 104. f. 16.

Cells more and less rectangular to square in girdle views with projecting spines from the four corners. Cells solitary lacking spines or short chains by joining adjacent valves. Valves rounded or elliptical, however, hardly visible, 5-30 μm in diameter and mantle height 1/3 of pervalvar length. Spines projecting approximately 45°from the corners of a cell. One or two cup- shaped plastids in a cell. Silicified resting spores Fig. 102. Distribution of of Chaetoceros present. muelleri.

TYPE: Forsch Ber. Biol. Stat. Plön 6: 195. text-figs. 1. 2 (1898). SEASONALITY: C. muelleri dominates the summer assemblages of plankton. DISTRIBUTION: It is usually a rare species in its habitat, however, in some regions it is important and quite typical for brackish conditions. The species is abundant in the summer and dominated the Bacillariphyceae: Centrales: Eupodiscaceae 135 plankton of the East Devils Lake, a hyposaline lake in North Dakota of USA (Leland and Berkas 1998). The species is common in the early Holocene sediment of a saline lake in the Canadian Subarctic (Pienitz et al. 1992). KOREA: The species usually is distributed in the coastal zones, near the Ganghwa Island (Chung 1969), the coast of Yeosu (Yang 1977) and Gwangyang (Yang and Kim 1981). SPECIMEN EXAMINED: (Planktons collected in the estuary of the Nakdong River). ECOLOGY: The diatoms grow well over a wide range of salinity and required concentrations of NaCl above 10 mM for their growth (Fujii et al. 1995). REMARKS: The taxonomy of inland Chaetoceros group is somewhat questionable (Rushforth and Johansen 1986).

Family Eupodiscaceae Kützing 1849: 440. Nun-dol-mal-gwa (눈돌말과)

Valves primarily bipolar, secondarily tri- or multi- polar to circular. Cells united to form short or long filaments. Valves with ocelli and rimoportulae. Without bilabiate processes, like the family Lithodesmiaceae, and setae on valve. In addition, no linking spines and pseudoocelli on valve.

GENERA AND SPECIES: There are two subfamily (Rutilarioideae, Eupodiscoideae), 19 genera and 1,365 species in the world, of which 64 species are accepted and flagged as valid taxa. The majority of this family is fossil diatoms. Six genera (Auliscus, Cerataulus, Odontella, Pleurosira, Rutilaria, Triceratium) and 16 species are recorded in Korea as 15 marine species and one freshwater species (Pleurosira laevis). DISTRIBUTION: This diatom group is mostly benthic, attached and epiphytic to a variety of substrata in coastal and marine waters. This family contains many fossil diatom genera. KEY REFERENCE: Simonsen (1979), Round et al. (1990). REMARKS: The majority of taxa in this family are fossil diatoms.

Genus Pleurosira (G. Meneghini) V. B. A. Trevisan di San Leon 1848: 96.

Cells cylindrical, united into zigzag filaments by mucilage excreted from an ocellus protrusion. Valves circular or slightly elliptical and flat. Valve mantle deep. Areolate punctas arranged along the striae on valve. Striae on valve arranged radially from the center to the margin. Two large ocelli slightly raised above valve face. A rimoportular position on the mid-area between the center and margin of the valve across an ocellar axis. Lectotype: Melosira (Pleurosira) thermalis Meneghini 1853: 95.

SPECIES: Four species - Pleurosira laevis (Ehrenberg) Compère, P. laevis f. polymorpha (Kützing) Compère, P. minor Metzeltin et al. and P. socotrensis (F. Kitton) Compère - are recorded worldwide. 136 Algal Flora of Korea·Freshwater Diatoms I

Pleurosira laevis has been only reported in Korean freshwaters. DISTRIBUTION: Their typical habitats are brackish waters in tropical or subtropical regions. They extend into inland waters with high conductivity. In Korea, the genus diatoms are usually found in truly freshwater habitats. ECOLOGY: This is a typical macroalgae in eutrophic freshwaters like Hydrosera whampoensis, Melosira varians and others. KEY REFERENCE: Compère (1982), Johnson and Rosowski (2004). REMARKS: Pleurosira was suggested by G. Meneghini in 1846 as a subgenus of Melosira and the subgenus was assigned to this genus name by V. B. A. Trevisan in 1848. However, Diatoms of the genus Pleurosira were described under different other names (Ceratalulus laevis or Biddulphia laevis) and the name was never used after 1848 until, in 1981, P. Compère suggested and validated the genus Pleurosira as the correct generic name instead of Ceratalulus which had long been used.

41. Pleurosira laevis (Ehrenberg) Compère 1982: 177 (Figs. 103-105).

Krammer and Lange-Bertalot 1991a: 86. pl. 83. f. 1. Johnson and Rosowski 1992: 248. f. 1. Sherwood 2006: 45. f. A.

BASIONYM: Biddulphia laevis Ehrenberg 1843: 339. SYNONYM: Cerataulus laevis (Ehrenberg) Ralfs in Pritchard 1861: 847.

Cells cylindrical and united together in zigzag filaments by means of mucilage excreted through ocellus. Valves rounded to elliptical and flat, and valve mantle very deep. Valves 20-90 μm in diameter, mantle 20-30 μm in height and cells 45-210 μm in length along the pervalvar axis. Valve with two marginal ocelli, which situated on terminal regions of the long axis of valve and only one involved in mak- ing the filamentous chains. Ocelli projecting a little from valve. Ocelli largely oval, 4-5 μm in width and 8-15 μm in length. Cells rectangular in girdle view and having three to eight intercalary bands. The first girdle band (valvocopula) under the mantle, the second and subsequent copulae with ligulae. Two rimoportulae located in central parts, at intermediate positions between the center and the margin. Areolar striae radiating towards the margin, 13-15 striae in 10 μm. Spines on the margin of valve. The structures of the mantle similar to the valve. Many discoid type plastids in a cell. As polymorphisms, four different morphological valve types, the normal vegetative type, the vegetative type of a long and narrow width, the resting spore and the intermediate valve type.

TYPE: Bacillaria 5: 177 (1982). Bailey in Ehrenberg Fig. 103. Distribution of Pleurosira laevis. Bacillariphyceae: Centrales: Eupodiscaceae 137

AB m

μ 10

Fig. 104. Pleurosira laevis. A, B. the alternate connections of cell corners in colonial forms (×200 and ×400); C. two rimoportulae at intermediate location between center and margin, two large ocelli at the marginal area and radiating areolae on valve (×1,000) (LM). 138 Algal Flora of Korea·Freshwater Diatoms I m

10 B

D E

Fig. 105. Pleurosira laevis. A. the valve view (×800, LM); B. the valve face; C. the detailed morphology of the ocellus projection; D. the inside view of the valve; E. a rimoportular opening in the inside of valve (SEM). Bacillariphyceae: Centrales: Eupodiscaceae 139

No. 1755a. Hudson River, West Point, New York in USA. SEASONALITY: P. laevis is relatively abundant in the warm season from July to October in freshwaters. DISTRIBUTION: This species is a typical brackish water diatom that is commonly observed in estuaries of large rivers. It also survives in inland waters with higher conductivity. These diatoms prefer warm or tropical waters, though they are more or less cosmopolitan in distribution. It was reported as the greatest component in the epilithic assemblages from the Missouri River and the Jackson River downstream of Virginia (Johnson and Rosowski 2004, Thomas et al. 2007) and in the periphytics from Hawaiian streams (Sherwood, 2004). The species is collected in the Itajai Mirim River in the neotropical region of southern Brazil and is dominant in pristine sites of Brazilian rivers (Burliga et al. 2008). The species is reported in Lake Biwa of Japan (Tuji and Houki 2001), and in the canals and many natural freshwaters in Egypt (El-Awamri 2008). KOREA: This taxon was first collected from the Sincheon Stream in 2005 (Kim et al. 2008) and was observed in the epiphytic diatom assemblages in the Seonakdong River, in September 2008. SPECIMEN EXAMINED: (Epiphytic diatoms collected from the upper regions of the Seonakdong River: 29.ix.2009). ECOLOGY: The diatoms of this species were recorded in different aquatic habitats, freshwaters, brackish waters, hard waters with high conductivity (El-Awamri 2008). Further, they are eutrophic diatoms occurring in the fertilized waters. In the Hawaiian streams, the algal filaments can grow up to several centimeters in the length (Sherwood 2006). REMARKS: When the distribution of the following two species is reviewed around the world, P. laevis is always accompanied by Hydrosera whampoensis in periphytic algal assemblages in freshwater. 140

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Index to Korean Names

ㄱ ㅂ

가시돌말속 131 바퀴돌말속 119 고리돌기돌말속 81 반원반돌말과 119 골편돌말속 100 관돌말과 122 관돌말속 122 ㅅ

센털돌말과 130 ㄴ 센털돌말속 133 실패돌말과 126 끈원반돌말과 13 끈원반돌말속 94 눈돌말과 135 ㅇ

왕관돌말속 75 ㄷ 원통돌말과 107 원통돌말속 107 단추돌말속 53 대롱돌말속 14 159

Index to Korean Names as Pronounced

B Kkun-won-ban-dol-mal-sok 94 Kwan-dol-mal-sok 122 Ba-kui-dol-mal-sok 119 Ban-won-ban-dol-mal-gwa 119 N

D Nun-dol-mal-gwa 135

Dae-rong-dol-mal-sok 14 Dan-chu-dol-mal-sok 153 S

Sen-teol-dol-mal-gwa 130 G Sen-teol-dol-mal-sok 133 Sil-pae-dol-mal-gwa 126 Ga-si-dol-mal-sok 131 Go-ri-dol-gi-dol-mal-sok 81 Gol-pyon-dol-mal-sok 100 W Gwan-dol-mal-gwa 122 Wang-gwan-dol-mal-sok 75 Won-tong-dol-mal-gwa 107 K Won-tong-dol-mal-sok 107

Kkun-won-ban-dol-mal-gwa 13 160

Index to Scientific Names

A stelligera 71 woltereckii 73 Acanthoceras 131 zachariasii 131 Actinocyclus 119 E normanii 120 Aulacoseira 14 Eupodiscaceae 135 alpigena 19 ambigua 22 ambigua f. japonica 27 H crenulata 30 granulata 32 Hemidiscaceae 119 granulata f. spiralis 37 Hydrosera 126 granulata var. angustissima 39 whampoensis 127 laevissima 41 muzzanensis 43 nygaardii 45 M subarctica 48 tethera 51 Melosira 107 moniliformis 109 nummuloides 111 B varians 113 Melosiraceae 107 Biddulphiaceae 126

O C Orthoseira 116 Chaetoceraceae 130 roeseana 117 Chaetoceros 133 muelleri 134 Cyclostephanos 75 P dubius 76 invisitatus 79 Pleurosira 135 Cyclotella 53 laevis 136 asterocostata 57 atomus 59 fottii 62 R glomerata 63 meneghiniana 64 Rhizosolenia 122 pseudostelligera 68 longiseta 123 radiosa 70 Rhizosoleniaceae 122 Index to Scientific Names 161

S T

Skeletonema 100 Thalassiosira 94 potamos 101 bramaputrae 95 subsalsum 104 faurii 97 Stephanodiscus 81 weissflogii 98 hantzschii 83 Thalassiosiraceae 13 hantzschii f. tenuis 85 parvus 92

Russia

JB GN JN

JJ South Sea Algal Flora of Korea

Algal Flora of Korea

Volume 3, Number 1 Chrysophyta: Bacillariophyceae: Centrales Freshwater Diatoms I o.3 No. 1 Vol. 3, Freshwater Diatoms

I Flora and Fauna of Korea

National Institute of Biological Resources Ministry of Environment National Institute of Biological Resources NIBR Ministry of Environment