Invertebrate Fauna of Korea

Inver tebrate Fauna of Korea

Volume 1, Number 3 Ciliates

Ciliophora: Intramacronucleata

Flora and Fauna of Korea NIBR National Institute of Biological Resources Ministry of Environment

Invertebrate Fauna of Korea

Volume 1, Number 3

Ciliates

Ciliophora: Intramacronucleata

2018

National Institute of Biological Resources Ministry of Environment Invertebrate Fauna of Korea Volume 1, Number 3 Ciliates Ciliophora: Intramacronucleata

Copyright © 2018 by the National Institute of Biological Resources Published by the National Institute of Biological Resources Environmental Research Complex, 42, Hwangyeong-ro, Seo-gu Incheon 22689, 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: 978-89-6811-346-8(96470), 978-89-94555-00-3(Set) Government Publications Registration Number: 11-1480592-001385-01 Printed by Junghaengsa, Inc. in Korea on acid-free paper Publisher: National Institute of Biological Resources Authors: Gi-Sik Min (Inha University), Jae-Ho Jung (Gangneung-Wonju National University) Project Staff: Jung Sun Yoo, Hyun Jong Kil, Eun Jung Nam, Hyeonggeun Kim, Kwang Soo Kim Published on August 31, 2018 Invertebrate Fauna of Korea

Volume 1, Number 3

Ciliates

Ciliophora: Intramacronucleata

Gi-Sik Min and Jae-Ho Jung1 Inha University 1Gangneung-Wonju National University 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. PREFACE

Biological resources include all organisms and their genetic characteristics. Utilization and conserva tion of these resources have the capacity to improve human life and to enhance the world we live in. It is therefore imperative that the practical and potential value of these organisms is conserved and used wisely. The first step towards this goal is to document our diversity and to study it in detail. Biological resources increase the competitiveness of a nation through their use as fundamental resources for making highly valu ed products, such as new lines of medicines, new materials, and new drugs. Since the Nagoya Protocol was adopted in 2010 and entered into force during the 12th Conference of the Parties of the Convention on Bio logical Diversity (CBD) in 2014, it has been expected that competition for biological resources will become more intensive under the rapidly changing circumstance on access to and sharing of genetic resources (ABS). To cope with a new international paradigm on issues related to biological resources, the Ministry of the Environment of Korea enacted a law entitled ‘An act on access and benefit sharing of genetic resources’ on August 17, 2017. Each nation in the world is investigating and clearing information of native species within its territory in order to secure its sovereignty rights over biological resources. The National Institute of Biological Reso urces (NIBR) of the Ministry of Environment has published the ‘Flora and Fauna of Korea’ since 2009 to manage biological resources in comprehensive ways and to enhance national competitiveness by building up the foundation for the sovereignty over biological resources. Professional research groups, consisting of professors and other taxonomic experts, have systematically examined 15,154 species of vascular plants, animals and other organisms over the past 10 years and have published their findings in 184 volumes in Korean and 189 volumes in English, and two volumes of worldwide monographs covering 216 species of invertebrates. This year, 14 volumes of the Flora and Fauna of Korea in both Korean and English versions including 391 species of invertebrates and insects are additionally published. Flora and Fauna of Korea are the first professional records to describe all the species of the nation in a comprehensive way, and they would contribute to level up the taxonomic capacity. The NIBR will continue to publish flora and fauna of Korea that will contribute conservation and appli cation of biological resources for successful implementation of the ABS protocol. Finally, I would like to express my sincere appreciation to authors who spared no effort to publish the Flora and Fauna of Korea.

President National Institute of Biological Resources

CONTENTS

List of Taxa 3 Introduction 6 Materials and Methods 7 Taxonomic Notes 8 1. Euplotes cristatus Kahl 10 2. Euplotes minuta Yocom 12 3. Uronychia binucleata Young 15 4. Uronychia multicirrus Song 17 5. Uronychia setigera Calkins 19

6. Ponturostyla enigmatica (Dragesco and Dragesco-Kernéis) Jankowski 22 7. Pseudocyrtohymena koreana Jung, Park and Min 25 8. Apokeronopsis bergeri Li, Song, Warren, Al-Rasheid, Roberts, Yi, Al-Farraj and Hu 28 9. Apokeronopsis ovalis (Kahl) Shao, Miao, Li, Song, Al-Rasheid, Al-Quraishy and Al-Farray 31 10. Pseudokeronopsis carnea (Cohn) Wirnsberger, Larsen and Uhlig 34 11. Uroleptopsis citrina Kahl 37 12. Pseudourostyla cristatoides Jung, Park and Min 40 13. Anteholosticha multicirrata Park, Jung and Min 44 14. Anteholosticha pulchra (Kahl) Berger 48 15. Bakuella (Bakuella) incheonensis Jo, Jung and Min 51 16. Bakuella (Pseudobakuella) litoralis Jo, Jung and Min 55 17. Birojimia soyaensis Kim, Jung and Min 59 18. Metaurostylopsis cheni Chen, Huang and Song 63 19. Metaurostylopsis struederkypkeae Shao, Song, Al-Rasheid, Yi, Chen, Al-Farraj and Al-Quraishy 66 20. Pseudoamphisiella alveolata (Kahl) Song and Warren 69 21. Pseudouroleptus jejuensis Jung, Park and Min 72 22. Arcuseries petzi (Shao, Gao, Hu, Al-Rasheid and Warren) Huang, Chen, Song and Berger 77 23. Litonotus paracygnus Song 81 24. Litonotus pictus Gruber 84 25. Loxophyllum perihoplophorum Buddenbrock 88 26. Loxophyllum rostratum Cohn 91 27. Dysteria brasiliensis Faria, Cunha and Pinto 95

1 INVERTEBRATE FAUNA OF KOREA Ciliates

28. Dysteria lanceolata Claparède and Lachmann 96 29. Dysteria nabia Park and Min 99 30. Dysteria ovalis (Gourret and Roeser) Kahl 104 Literatures Cited 106 Index to Korean Names 114 Index to Scientific Names 116

2 LIST OF TAXA

LIST OF TAXA

Phylum Ciliophora Doflein, 1901 Subphylum Intramacronucleata Lynn, 1996 Class Spirotrichea Bütschli, 1889 Subclass Hypotrichia Stein, 1859 Order Euplotida Small and Lynn, 1985 Suborder Euplotina Jankowski, 1979 Family Euplotidae Ehrenberg, 1838 Genus Euplotes Ehrenberg in Hemprich and Ehrenberg, 1831 Euplotes cristatus Kahl, 1932 Euplotes minuta Yocom, 1930 Family Uronychiidae Jankowski, 1975 Genus Uronychia Stein, 1859 Uronychia binucleata Young, 1922 Uronychia multicirrus Song, 1997 Uronychia setigera Calkins, 1902 Subclass Stichotrichia Small and Lynn, 1985 Order Sporadotrichida Fauré-Fremiet, 1961 Family Oxytrichidae Ehrenberg, 1830 Genus Ponturostyla Jankowski, 1989 Ponturostyla enigmatica (Dragesco and Dragesco-Kernéis, 1986) Jankowski, 1989 Genus Pseudocyrtohymena Jung, Park and Min, 2015 Pseudocyrtohymena koreana Jung, Park and Min, 2015 Order Urostylida Jankowski, 1979 Family Pseudokeronopsidae Borror and Wicklow, 1983 Genus Apokeronopsis Shao, Hu, Warren, Al-Rasheid, Al-Quraishy and Song, 2007 Apokeronopsis bergeri Li, Song, Warren, Al-Rasheid, Roberts, Yi, Al-Farraj and Hu, 2008 Apokeronopsis ovalis (Kahl, 1932) Shao, Miao, Li, Song, Al-Rasheid, Al-Quraishy and Al-Farray, 2008 Genus Pseudokeronopsis Borror and Wicklow, 1983 Pseudokeronopsis carnea (Cohn, 1866) Wirnsberger, Larsen and Uhlig, 1987 Genus Uroleptopsis Ehrenberg, 1831

3 INVERTEBRATE FAUNA OF KOREA Ciliates

Uroleptopsis citrina Kahl, 1932 Family Pseudourostylidae Jankowski, 1979 Genus Pseudourostyla Borror, 1972 Pseudourostyla cristatoides Jung, Park and Min, 2012 Family Urostylidae Bütschli, 1889 Genus Anteholosticha Berger, 2003 Anteholosticha multicirrata Park, Jung and Min, 2013 Anteholosticha pulchra (Kahl, 1932) Berger, 2003 Genus Bakuella Agamaliev and Alekperov, 1976 Subgenus Bakuella (Bakuella) Agamaliev and Alekperov, 1976 Bakuella (Bakuella) incheonensis Jo, Jung and Min, 2015 Subgenus Bakuella (Pseudobakuella) Alekperov, 1992 Bakuella (Pseudobakuella) litoralis Jo, Jung and Min, 2015 Genus Birojimia Berger and Foissner, 1989 Birojimia soyaensis Kim, Jung and Min, 2016 Genus Metaurostylopsis Song, Petz, and Warren, 2001 Metaurostylopsis cheni Chen, Huang and Song, 2010 Metaurostylopsis struederkypkeae Shao, Song, Al-Rasheid, Yi, Chen, Al-Farraj and Al-Quraishy, 2008 Genus Pseudoamphisiella Song, 1996 Pseudoamphisiella alveolata (Kahl, 1932) Song and Warren, 2000 Family Kahliellidae Tuffrau, 1979 Genus Pseudouroleptus Hemberger, 1985 Pseudouroleptus jejuensis Jung, Park and Min, 2014 Incertae sedis in order Urostylida Genus Arcuseries Huang, Chen, Song and Berger, 2014 Arcuseries petzi (Shao, Gao, Hu, Al-Rasheid and Warren, 2011) Huang, Chen, Song and Berger, 2014 Class Litostomatea Small and Lynn, 1981 Subclass Haptoria Corliss, 1974 Order Pleurostomatida Schewiakoff, 1896 Family Litonotidae Kent, 1882 Genus Litonotus Wresniowski, 1870 Litonotus paracygnus Song, 1994 Litonotus pictus Gruber, 1884

4 LIST OF TAXA

Genus Loxophyllum Dujardin, 1841 Loxophyllum perihoplophorum Buddenbrock, 1920 Loxophyllum rostratum Cohn, 1866 Class Phyllopharyngea de Puytorac, Batisse, Bohatier, Corliss, Deroux, Didier, Dragesco, Fryd-Versavel, Grain, Grolière, Hovasse, Iftode, Laval, Rogue, Savoie and Tuffrau, 1974 Subclass Cyrtophoria Fauré-Fremiet in Corliss, 1956 Order Dysteriida Deroux, 1976 Family Dysteriidae Claparède and Lachmann, 1858 Genus Dysteria Huxley, 1857 Dysteria brasiliensis Faria, Cunha and Pinto, 1922 Dysteria lanceolata Claparède and Lachmann, 1859 Dysteria nabia Park and Min, 2014 Dysteria ovalis (Gourret and Roeser, 1886) Kahl, 1931

5 INVERTEBRATE FAUNA OF KOREA Ciliates

INTRODUCTION

Ciliates are a distinct group of protists, globally distributed in a wide variety of habitats (freshwater, marine, and terrestrial) where they are important trophic links in food webs (Lynn, 2008). They are mostly free-living, but also live as commensals or parasites in or on other animals. The diversity of ciliates was estimated by Foissner et al., 2008 to about 40,000 biological species after applying the detailed habitat studies, species with same morphology but with different resting cysts (cyst species), and the genetic or molecular species. For instance, in the diversity, the most recent monograph by Foissner (2016) reported a total of 459 ciliates from Venezuela and Galápagos, and 128 species (285) were new to science. To date, fourteen classes were identified in this group (Gao et al., 2016). This monograph is the third of a series of publications on Korean ciliates. Fourty ciliate species were described in the first monograph (Shin, 2012), thirty-seven in the second (Choi, 2015), and thirty species are described in the present study. The thirty species are classified to three classes and collected from various habitats since 2007. By the end of 2016, 331 species have been reported in Korean habitats, of which 34 were new to science (Jung et al., 2017). Considering the diversity of species and habitats, many species are probably waiting for our discovery.

6 MATERIALS AND METHODS

MATERIALS AND METHODS

The species studied in this monograph were collected from different freshwater, marine, and terrestrial habitats of South Korea. Water samples were collected using plankton nets with different mesh size, framed slides traps, and PFU pieces for planktonic, sessile, and periphytic ciliates, respectively. Ciliates were then transferred to the laboratory where different kinds of cultures were established at room temperatuse using rice or squashed wheat grains. Soil samples were collected on the field from the surface soil layer, then transferred to the labaratory, and air-dried for at least two weeks before rewetting. The soil samples were rewetted to reactivate the ciliates from the resting cysts using the non-flooded Petri dish method (Foissner et al., 2002). Cells were studied in vivo using a stereomicroscope and a light microscope with high-power oil immersion objectives and differential interference contrast optics. The infraciliature and various cytologi- cal structures were revealed by protargol impregnation using the commercial or the labaratory-synthesized protargol powder (Pan et al., 2013). In addition, the silverline patterns were revealed using the silver nitrate technic (Foissner, 2014). The number of higer taxonomic group of recorded ciliates in Korea did not record specific numbers as the classification could change according to the criteria, while we can check the number of species from a list recored by Jung et al. (2017). Terminology mainly follows Berger (1999, 2006, 2008) and Lynn (2008). Most of morphological descriptions for higher taxonomic groups were borrowed directly from the contents of Lynn (2008).

7 INVERTEBRATE FAUNA OF KOREA Ciliates

TAXONOMIC NOTES

Subphylum Intramacronucleata Lynn, 1996 Nae-haeg-a-mun (내핵아문)

Size small to large; shape, variable, from globular to ellipsoid to elongate; free-swimming or sessile; cortical alveolar system typically well-developed; somatic ciliation, holotrichous, but forms with girdles and strips, and even non-ciliated taxa are known; parasomal sacs, present; extrusomes as somatic mucocysts and trichocysts and oral and somatic toxicysts; oral structures, variable, minimally with oral dikinetids, either encircling cytostome or on right side as a paroral, but some forms also with several to many oral polykinetids in an adoral zone and other forms astomatous or with oralized somatic kinetids; stomatogenesis, variable from telokinetal to buccokinetal; fission, typically isotomic, rarely anisotomic and multiple; macronuclear genome typically differentiated by fragmentation of micronuclear chromosomes during anlage development; polyploid macronucleus dividing by intramacronuclear microtubules; micronucleus, present; conjugation, typically temporary and isogamontic, but some forms showing complete conjugation with an- isogamonty; feeding habits, diverse, including several major classes and subclasses as obligate symbionts, sometimes parasitic; widely distributed in marine, freshwater, and terrestrial habitats.

Class Spirotrichea Bütschli, 1889 Seon-mo-chung-gang (선모충강)

Size small to large; shape, variable, from spheroid to cone-shape to dorso-ventrally flattened; free-swimming or sessile, with some loricate forms that may be attached to substrates and/or sedentary attached within lorica; somatic ciliation, holotrichous in some groups, but nearly devoid of cilia in others; somatic dikinetids usually with anterior or both kinetosomes ciliated or somatic polykinetids, called cirri; extrusomes as mucocysts or trichocyst-like trichites; oral ciliature conspicuous, with adoral zone of oral polykinetids, typically as paramembranelles, especially prominent and often encircling oral region clockwise before entering oral cavity; one or more “parorals” on right, and if two, as paroral (=outer) and endoral (=inner) membranes; stomatogenesis, typically parakinetal or apokinetal, but mixokinetal in Protocruzia; conjugation, typically temporary and isogamontic, but at least one case of total conjugation; feeding habits, diverse, ranging from microphagous bacterivores to predators on other ciliates and even small metazoans; widely distributed in marine, freshwater, and terrestrial habitats.

8 EUPLOTIDA

Subclass Hypotrichia Stein, 1859 Ha-mo-chung-a-gang (하모충아강)

Size small to medium; shape, dorso-ventrally flattened, typically rigid, oval to rectangular; free-swimming; alveoli well-developed and, at least in euplotids, filled with a protein, called platein; somatic ciliature commonly represented by rows or localized groups of polykinetids, called cirri, conspicuous on ventral surface; dorsally, files of widely spaced dikinetids with short cilia (“bristles”) and retention of a laterally directed kinetodesmal fibril; files of marginal cirri, somatic infraciliature typically retained during encystment; prominent adoral zone of generally numerous oral polykinetids, as paramembranelles, on left-anterior portion of ventral surface, bordering a broad, non-ciliated peristomial field and sometimes continuing over apical end of body onto dorsal surface; stomatogenesis, generally apokinetal, beginning in a cortical pocket in some forms, but sometimes parakinetal; macronucleus, ellipsoid to band-shaped or in fragments, with replication bands moving from ends to middle when nucleus elongated; micronucleus, one to several; conjugation, temporary; contractile vacuole, at least present in freshwater forms; cytoproct, present; microphagous and macrophagous; in marine, freshwater, and terrestrial habitats, widely distributed as free-living forms, but a few species as ectocommensals on various invertebrates and one inquilinic in an echinoid.

Order Euplotida Small and Lynn, 1985 Ja-ra-ha-mo-chung-mok (자라하모충목)

Size, small to medium; shape, ovoid to rectangular; free-swimming; frontoventral cirri, sporadically scattered over ventral surface, but never forming more than one conspicuous file on ventral surface, except in Gastrocirrhidae; oral structures, as forsubclass; during cell division, only the ventral somatic infraciliature is replaced while replication of the dorsal ciliature typically occurs within an equatorial band and within the parental kineties (i.e., intrakinetally); caudal cirri, when present, derived from dorsal kinety anlagen; two suborders.

Suborder Euplotina Jankowski, 1979 Ja-ra-ha-mo-chung-a-mok (자라하모충아목)

Size, small to medium; shape, ovoid to ovorectangular; free-swimming; right marginal cirri, absent; left marginal cirri, when present, not as two distinct groups; oral structures, as for subclass; contractile vacuole, typically in right posterior of body; in marine, freshwater, and terrestrial habitats; five families.

9 INVERTEBRATE FAUNA OF KOREA Ciliates

Family Euplotidae Ehrenberg, 1838 Ja-ra-ha-mo-chung-gwa (자라하모충과)

Size, small to medium; shape, ovoid, ventrallyflattened; body, rigid; free-swimming; extrusomes as small vesicles (i.e., ampules) associated with dorsal bristle dikinetids; frontoventral and transverse cirri, dispersed in conspicuous groups; left marginal cirri, reduced typically to fewer than three; caudal cirri, ventral; ventrally-oriented oral cavity with distinct, contiguous, adoral zone of oral polykinetids forming a “collar” and “lapel”; paroral as polykinetid on right of oral area accompanied by single endoral file of kinetosomes; macronucleus, more or less C-shaped; micronucleus, present; contractile vacuole, present; cytoproct (?); feeding on bacteria, microalgae, and smaller protists; in marine, freshwater, and terrestrial habitats, widely distributed but predominantly marine, with one Euplotes species found in the intestines of sea urchins; four genera. Boundary between prosome and urosome well defined.

Genus Euplotes Ehrenberg in Hemprich and Ehrenberg, 1831 Ja-ra-ha-mo-chung-sok (자라하모충속)

Key to the species of genus Euplotes

1. Eight dorsal kineties...... E. cristatus - Nine dorsal kineties...... E. minuta

1. Euplotes cristatus Kahl, 1932 (Fig. 1) Byeo-seul-meo-ri-ja-ra-ha-mo-chung (벼슬머리자라하모충)

Euplotes cristatus Kahl, 1932, p. 633. Euplotes cristatus Park, Kim and Min, 2010, p. 22, fig. 1.

Size in vivo 60-84×38-68 μm. Body elongate oval (Fig. 1A, E, F); anterior end narrowly rounded while posterior end widely rounded; dorso-ventrally flattened (Fig. 1H-I). Dorsal surface sculptured with ridges (Fig. 1K, arrowheads). Buccal field narrow, extending about 67% of body length (Fig. 1A-C, G, M-O). Cytoplasm hyaline, central part opaque due to numerous yellow to green-colored and different-sized lipid droplets, few food vacuoles and granules (Fig. 1A, E-K). Contractile vacuole (CV) adjacent to rightmost transverse cirri (TC), about 7 μm across (Fig. 1J, arrowhead). Macronucleus (Ma) C-shaped, containing numerous large nucleoli; one spherical micronucleus (Mi) on upper left border of Ma (Fig. 1B, M, N).

10 EUPLOTIDAE: Euplotes

FVC

AZM

TC MC CC A B C D

I J G

E F H K L

M N O P

Fig. 1. Morphology and infraciliature of Euplotes cristatus from life (A, E-L), after protargol (B, M, N), and silver nitrate impregnation (C, D, O, P). A, E-F, ventral view of live, arrowheads to show caudal cirri and marginal cirri (F); B, infraciliature of ventral side; C, D, O-P, silverline system on ventral (C, O) and dorsal (D, P) sides; G, adoral zone of membranelles of live; H-I, lateral view of live; J, ventral view of live, note contractile vacuole (arrowhead) and paroral membrane (arrow); K, dorsal view, to show the dorsal ridges (arrowheads); L, detailed view to show the dorsolateral cilia (arrowheads); M-N, ventral (M) and dorsal (N) sides of protargol impregnation. Scale bars=30 μm (cited from Park et al., 2010).

11 INVERTEBRATE FAUNA OF KOREA Ciliates

Infraciliature as shown in Fig. 1A-C, E, F, and M-O. Consistently 10 frontoventral cirri (FVC) arranged in ordinary euplotid pattern on anterior ventral surface (Fig. 1A-C, M, O); five strong TC at posterior region (Fig. 1A-C, E); 2 or 3 caudal cirri (CC) at posterior end and 2 marginal cirri (MC) left of transverse cirri (Fig. 1A-C, F, M; 1F, arrowheads). Adoral zone of membranelles (AZM) prominent, curved and composed of 35-50 membranelles, each ca. 15 μm long (Fig. 1A-C, F, G, M-O). Paroral membrane (PM) small, beneath buccal lip (Fig. 1B, C, J; 1J, arrow). Eight dorsal kineties (DK); of which six extend on dorsal side and two on both margins of ventral surface (Fig. 1B, D, L-N, P; 1L, arrowheads); mid-DK row composed of 10-16 dikinetids (Fig. 1D). Silverline system typical vannus type, single-type dorsal argyrome, irregular pattern on ventral side (Fig. 1C, D, O, P).

Distribution: Korea, France, Germany, USA.

Korea: GG.

Specimen examined: GG: (the public waterfront, Incheon (37°26ʹN and 126°35ʹE) on the Yellow Sea of

Korea (18°C, ca. 29‰, and pH ca. 7.8): 21-29.v.2007). Habitat: Marine.

Remarks: Euplotes cristatus was originally described by Kahl (1932) based on living observation. Eu- plotes cristatus is similar to E. vannus and E. minuta in having a dorsal silverline system of single-vannus type. However, E. vannus has a larger body size (94-111 ×53-75 vs. 60-84×38-68 μm); a higher number of AZM (57-74 vs. 35- 50), CC (4-7 vs. 4-5), DK (9-10 vs. 8), and dikinetids of mid-DK (15-22 vs. 10- 16) than the present population of E. cristatus (Kwon et al., 2007). Euplotes minuta has a smaller body size (44-53×26-35 μm); a higher number of DK (9); and a lower number of AZM (31-41) than E. cristatus of the present population (Park et al., 2010).

2. Euplotes minuta Yocom, 1930 (Fig. 2) Jag-eun-ja-ra-ha-mo-chung (작은자라하모충)

Euplotes minuta Yocom, 1930, p. 242, figs. 1, 2; Borror, 1962, p. 271, figs. 1-4; Curds, 1975, p. 13, fig. 6; Carey, 1992, p. 207, fig. 828; Song and Wilbert, 1997, p. 431, fig. 1; Park, Kim and Min, 2010, p. 24, fig. 2. Moneuplotes minuta Borror and Hill, 1995, p. 461.

Size in vivo 44-53×26-35 μm. Body outline generally oval as shown in Fig. 2A-C, E, F; right margin slightly convex to nearly straight, left margin more convex (Fig. 2A, E, F); both ends rounded; dorso-ventrally highly flattened with dorsal side slightly arched while ventral side concave. Buccal field approximately 3/4 of body length (Fig. 2A, E, F). Cytoplasm hyaline, containing some shiny globules and food particles (Fig. 2E, F). Contractile vacuole posterior to rightmost TC, approximately 6 μm across (Fig. 2H, contractile

12 EUPLOTIDAE: Euplotes

AZM FVC

PM TC

CC MC

A B C D

E F H J

K L M N

Fig. 2. Morphology and infraciliature of Euplotes minuta in vivo (A, E-J), protargol impregnation (B, K, L), and silver nitrate impregnation (C, D, M, N). A, E-F, ventral view of live; B, infraciliature of ventral side; C-D, M-N, silverline system on ventral (C, M) and dorsalv (D, N) sides; G-H, detailed view to show the dorsolateral cilia (H, arrowheads); I, macronucleus of live (Ma, arrow); J, dorsal view, to show the dorsal ridges (arrowheads); K-L, ventral (K) and dorsal (L) sides of protargol impregnation. Scale bars=20 μm (cited from Park et al., 2010).

13 INVERTEBRATE FAUNA OF KOREA Ciliates

vacuole). Macronucleus C-shaped, containing numerous large nucleoli (Fig. 2A, B, I, K, L; I, arrow); one Mi spherical. Adoral zone of membranelles prominent, composed of 31-41 membranelles, each about 10 μm long (Fig. 2B, C, K, M). Paroral membrane small, beneath cytoplasmic lip (Fig. 2B). Cirral pattern rather stable, FVC 10 in number, enlarged, at anterior ventral surface; 5 TC, 2-3 CC at posterior end, and 2MC (Fig. 2A-C, K, M). On dorsal surface, ellipsoid granules packed together around dorsal cilia beneath pellicle in a flower pattern (Fig. 2G, H; 2H, arrowheads). Nine bipolar DK (Fig. 2J, arrowheads), seven DK on dorsal side and two on both margins of ventral surface (Fig. 2B, D, K, L, N); middle DK with about 10-12 dikinetids; leftmost kinety containing only about five dikinetids in posterior portion of body (Fig. 2B). Silverline system typical vannus type, single-type dorsal argyrome, irregular pattern on ventral side (Fig. 2C, D, M, N).

Distribution: Korea, Brasil, China, Italy, USA.

Korea: GG.

Specimen examined: GG: (Songjeong Beach, Busan (35°10ʹN and 129°12ʹE) on the Strait of Korea (18.5 °C, ca. 28.8‰, and pH ca. 8.7): 17.xii.2007). Habitat: Marine.

Remarks: Euplotes vannus is the most closely related species to E. minuta. However E. minuta has some remarkable differences from E. vannus as described by Kwon et al. (2007), such as the body size (44- 53×26-35 vs. 94-111 ×53-75 μm); number of AZM (31-41 vs. 57-74), CC (4 vs. 4-7), DK (9 vs. 9-10), and dikinetids of mid-DK (10-16 vs. 15-22).

Family Uronychiidae Jankowski, 1975 Mal-chong-chung-gwa (말총충과)

Size, small to medium; shape, blunt ovoid, nearlycircular in cross-section; free-swimming; cirri, generally conspicuous with frontoventral cirri reduced to groupings on right side; transverse cirri, well-developed; right caudal cirri, dorsal, well-developed; left marginal cirri, may be conspicuous; oral region, expansive, with oral polykinetids of “lapel” and “collar” separated, the latter anteriodorsal; paroral, prominent, as polystichomonad, encircling right border of the oral region from its right rear to its anterior left; macronucleus, ellipsoid, as two or more separated nodules or moniliform; micronucleus, present; contractile vacuole, may be present; cytoproct (?); feeding on bacteria, microalgae, and smaller protists; in marine habitats, freeliving and in the mantle cavity of molluscs; five genera.

14 URONYCHIIDAE: Uronychia

Genus Uronychia Stein, 1859 Mal-chong-chung-sok (말총충속)

Key to the species of genus Uronychia

1. Two ventral cirri...... 2 - More than two ventral cirri...... U. multicirrus 2. Cell size >70 μm and always two macronuclear nodules...... U. binucleata - Cell size <70 μm and one or two macronuclear nodules...... U. setigera

3. Uronychia binucleata Young, 1922 (Fig. 3) Ssang-haeg-mal-chong-chung (쌍핵말총충)

Uronychia binucleata Young, 1922, p. 360. Uronychia binucleata Kim and Min, 2011, p. 27, fig. 2.

Size in vivo 70-110 ×55-75 μm. Body oval to slightly rectangular; both right and left margins slightly convex. Dorso-ventrally flattened, ratio of about 2:3; buccal area deeply caved, extends about 70% of body length (Fig. 3A, B, D). Two conspicuous spurs appears on posterior region, visible after protargol staining (Fig. 3B, G); lateral spurs inconspicuous. On posterior portion, two depressions on ventral side where TC and LMC emerge; 1 depression on dorsal side where CC emerge (Fig. 3A-C). Cytoplasm grayish to dark gray, with numerous granules and large particles. Two Ma connected by funiculus, left to midline; each nodule irregular sausage-shaped, with spherical nucleoli; Mi between Ma nodules, globular (Fig. 3C). Con- tractile vacuole right of TC; several food vacuoles (FV) recognized after protargol impregnation (Fig. 3D). Movement usually genus typical, like U. setigera. Adoral membranelles pattern stable in this genus; i.e., consists of two areas: AZM1 apical and extends to dorsal surface, composed of 11 membranelles, each consists of three kineties. AZM2 left to mid-body and composed of four membranelles, each consists of 6-8 kineties. Single small cirrus-like membranelle (buccal cirrus; BC), underneath and slightly right to AZM2, 2-3 μm long (Fig. 3A-C, F). Oral region surrounded by horseshoe-shaped PM (Fig. 3B, D). Four frontal cirri (FC) on ventral surface, right to anterior portion of oral region; two small ventral cirri (VC) on right margin, posterior to mid-body; five TC, rightmost cirrus rather small; three enlarged left marginal cirri (LMC), on left side of ventral region, posterior to mid-body; three strong CC emerge on right margin of dorsal side (Fig. 3A-C). Six DK composed of dikinetids on cell surface, genus-typical; two DK on left margin of ventral surface, leftmost of which contains 37 dikinetids (Fig. 3B, C, E, F). Silverline system of dorsal surface net-type (Fig. 3H).

15 INVERTEBRATE FAUNA OF KOREA Ciliates

FC AZM1

PM Ma AZM2 DK1 BC VC Mi

LMC DK

TC CC A B C

D F H

Fig. 3. Morphological characteristics of Uronychia binucleata from life (A), after protargol impregnation (B-G) and silver nitrate impregnation (H). A, D, Ventral view of a typical individual; B, The cirri pattern of the ventral region; C, E, H, Dorsal side, views DK (C, E) and silverline system (H); F, Anterior portion, shows AZM1; G, Posterior region, arrows indicate posterior spurs. AZM, adoral zone of membranelles; BC, buccal cirrus; CC, caudal cirri; DK, dorsol kineties; FC, frontal cirri; LMC, left marginal cirri; Ma, macronuclear nodules; Mi, micronucleus; PM, paroral membrane; TC, transverse cirri; VC, ventral cirri. Scale bars=70 μm (cited from Kim and Min, 2011).

Distribution: Korea, China.

Korea: GG.

Specimen examined: GG: (the public waterfront (37°26ʹN, 126°35ʹE), Incheon in the Yellow Sea of Korea: 19-26.vi.2006).

Habitat: Marine.

Remarks: Uronychia binucleata was originally described by Young (1922) and is commonly found in the

16 URONYCHIIDAE: Uronychia

Yellow Sea of Korea. This species was characterized through comparison with its congeners with respect to body shape and size, number of dikinetids in dorsal kineties and nuclei, and the existence of spur (s) on the posterior region (Song and Wilbert, 1997; Song, 1999). Uronychia binucleata is most similar to U. setigera, and can be distinguished by the following features: body size (ca. 100 vs. 60 μm), the number of dikinetids in the leftmost kinety (ca. 37 vs. 23), and spurs on the posterior region (present vs. absent).

4. Uronychia multicirrus Song, 1997 (Fig. 4) Da-geug-mo-mal-chong-chung (다극모말총충)

Uronychia multicirrus Song, 1997, p. 279, figs. 1-5; Shen, Shao, Gao, Lin, Li, Hu and Song, 2009, p. 296, figs. 1-3; Kim and Min, 2011, p. 30, fig. 3.

Size in vivo 140-200×70-120 μm. Body rectangular; slightly convex in left margin. Dorsoventrally flattened, ratio of about 1:2; buccal area deeply caved, extends about 80% of body length (Fig. 4A, B, F). Usually, single, terminal inconspicuous spur. Two depressions on ventral side of posterior portion where TC and LMC emerge; CC emerge from a posterior dorsal depression (Fig. 4A-E, H, I). Cytoplasm grayish to dark gray, with numerous granules and large crystal-like particles. Usually moniliform Ma composed of 6-9 ellipsoidal to elongate nodules connected by funiculus, C-shaped with spherical nucleoli; Mi at lower left corner of Ma, spherical (Fig. 4C, G). Contractile vacuole right to TC; several food vacuoles recognized after protargol impregnation (Fig. 4G). Movement usually genus typical, as U. setigera. Adoral zone of membranelles pattern genus-typical; AZM1 apical, extends to dorsal surface, composed of 11 membranelles, each consists of three kineties; AZM2 on left side of middle region, composed of four membranelles. Buccal cirrus small, separated from AZM2, base about 4-5 μm long (Fig. 4A, B, H). A buccal field surrounded by enormous horseshoe-shaped PM (Fig. 4A, G). Four FC on ventral surface, right to anterior portion of oral region; 6-9 VC on right margin; five TC, rightmost cirrus rather small; three enlarged LMC, on left margin of ventral surface (Fig. 4B, C, J). Six DK, genus-typical, composed of dikinetids, of which two located dorsolaterally. Silverline system of dorsal side net-type (Fig. 4K). Three strong CC emerge on right margin of dorsal side (Fig. 4A-C, G-I).

Distribution: Korea, China.

Korea: GG.

Specimen examined: GG: (the public waterfront (37°26ʹN, 126°35ʹE), Incheon in the Yellow Sea of Korea: 6-13.viii.2007).

Habitat: Marine.

Remarks: Uronychia multicirrus was originally reported by Song (1997) and then redescribed by Shen

17 INVERTEBRATE FAUNA OF KOREA Ciliates

AZM1 FC

PM Ma

DK1

VC AZM2 BC

Mi LMC DK

A B TC C CC

D F G

H I J K

Fig. 4. Morphological characteristics of Uronychia multicirrus from life (A, D-F), after protargol (B, C, G-J) and silver nitrate impregnation (K). A, Ventral view of a typical individual. B, C, The cirri pattern on the ventral and dorsal side. D-F, Dorsal, ventral and lateral views of different specimens, showing the body shape, the cirral pattern, and the dark area in the middle of the cell and the CV (arrow). G, Ventral view showing the Ma, several VC (arrowheads) and PM. H, I, Posterior region of the cell showing the AZM2, BC (arrowhead), CC, DK, and TC. J, K, Dorsal views showing the DK and silverline system. Scale bars=100 μm (cited from Kim and Min, 2011). et al. (2009). Uronychia multicirrus is most similar to U. transfuga (Song, 1997, 1999; Song and Wilbert, 1997). These species can be clearly distinguished by the following features: the number of ventral cirri (ca. 8 vs. 2) and macronuclear nodules (ca. 7 vs. ca. 11).

18 URONYCHIIDAE: Uronychia

5. Uronychia setigera Calkins, 1902 (Fig. 5) Gang-mo-mal-chong-chung (강모말총충)

Uronychia uncinata Kahl, 1932, p. 627, fig. S. 622, 28. Uronychia setigera Song and Wilbert, 1997, p. 424, fig. 7; Song, Wilbert, Chen and Shi, 2004, p. 315, figs. 1-3; Kim and Min, 2011, p. 26, fig. 1.

Size in vivo 50-80×35-55 μm. Body shape oval, right margin slightly convex. Dorso-ventrally flattened, ratio of about 2:3; buccal area deeply caved, extends about 70% of body length (Fig. 5A, B, D-F). Two conspicuous apical spurs, each on left and right of anterior portion; one very conspicuous lateral spur on left margin (Fig. 5B, E, F). Two depressions on posterior portion of ventral side, from which TC and LMC emerge; three CC emerge from a depression on dorsal side (Fig. 5A-D). Cytoplasm colorless to grayish, with numerous granules. Two ellipsoidal Ma nodules on left side of body connected by funiculus, with numerous, spherical nucleoli; Mi not recognizable (Fig. 5C, D). Contractile vacuole right of TC; several FV recognized after protargol impregnation. Movement typically rapid jumping aside or backwards, swimming with very fast rotation against the longitudinal axis. Adoral zone of membranelles consists of two areas: AZM1 apical and extends to dorsal surface, composed of 11 membranelles, each consists of three kineties; AZM2 left to mid-body and composed of four membranelles, each consists of 6-8 kineties. Only one small inconspicuous BC right to AZM2, about 2-3 μm long (Fig. 5A-C, G-I). Buccal field surrounded by a horseshoe-shaped robust PM (Fig. 5B, E, F). Four FC on ventral surface, right to anterior portion of oral region; two small VC on right margin, posterior to mid-body; five TC, rightmost cirrus rather small; three enlarged LMC, on left margin of ventral surface, beneath AZM2; three enormous CC emerged from dorsal surface (Fig. 5A-D, G, H). Six DK composed of dikinetids, two of which located on left margin of ventral surface, dikinetids densely packed on posterior region, leftmost kinety contains about 23 dikinetids; DK3 extends to posterior end of body, DK4- 6 on dorsal surface, end anterior to CC (Fig. 5B-D).

Distribution: Korea, China, Germany.

Korea: GB.

Specimen examined: GB: (the coastal water of Gumjin-ri (36°22ʹN, 129°23ʹE), Gyeongsangbukdo in the East Sea of Korea: 6.x.2006).

Habitat: Marine.

Remarks: Uronychia setigera can be clearly distinguished from other congeners by the diagnostic characteristics proposed by Song and Wilbert (1997) and Song (1999); i.e. the number of dikinetids in DK and the number of spurs. Uronychia binucleata is the most similar species to U. setigera. However, U. setigera can be distinguished from U. binucleata by the following features: body size (ca. 60 vs. 100 μm), the number of dikinetids in the leftmost DK (ca. 23 vs. 37), and the presence (vs. absence) of a lateral spur on the left margin.

19 INVERTEBRATE FAUNA OF KOREA Ciliates

AZM1 FC

PM Ma

AZM2 DK1 BC DK2 VC

LMC DK

TC CC A B C

D E F

G H I

Fig. 5. Morphological characteristics of Uronychia setigera from life (A) and after protargol impregnation (B-I). A, Ventral view of a typical individual; B, E, F, The cirri pattern of the ventral region, arrows indicate a lateral spur on the left margin; C, D, Dorsal side, views CC, DK, and nuclei; G, Anterior portion, shows AZM1 and FC; H, I, The rightmost TC (arrow) and BC (arrowhead) in the posterior region. AZM, adoral zone of membranelles; BC, buccal cirrus; CC, caudal cirri; DK, dorsol kineties; FC, frontal cirri; LMC, left marginal cirri; Ma, macronuclear nodules; PM, paroral membrane; TC, transverse cirri; VC, ventral cirri. Scale bars=40 μm (cited from Kim and Min, 2011).

20 SPORADOTRICHIDA

Subclass Stichotrichia Small and Lynn, 1985 Yeol-ha-mo-chung-a-gang (열하모충아강)

Size small to large; shape, often elongate, sometimes very drawn out posteriorly, in cross section round to dorso-ventrally compressed; free swimming with a few loricate forms; perilemma in some groups; pellicu- lar alveoli weakly developed; somatic ventral ciliature as ventral cirri ranging from small and quite inconspicuous, occasionally as few as 2-3 cilia per cirrus, arranged in longitudinal, sometimes spiraled, files to a few, larger cirri in scattered groups, with in latter case marginal files of cirri differentiated; transverse cirri, may or may not be present; caudal cirri, may or may not be present; dorsal somatic ciliature as one to many kineties - typically three - of dikinetids without kinetodesmal fibril, but with short, bristle cilium on anterior kinetosome; adoral zone of oral polykinetids as paramembranelles in “collar” and “lapel”, each typically of four rows of kinetosomes, with first two rows equally long and fourth row quite short; right oral cilia variable, but usually as a paroral and endoral; stomatogenesis, parakinetal in those with conspicuous kineties to apokinetal in those with scattered cirri; division morphogenesis may involve replacement of all somatic ciliature of both proter and opisthe; macronucleus, typically two nodules, but often multiple, each component typically with one replication band; micronucleus, one to many; conjugation, typically temporary, but sometimes total; contractile vacuole, at least present in freshwater and terrestrial forms, and typically on middle left of body; cytoproct, very likely present; feeding strategies ranging from bacterivorous to cannibalistic; encysted forms typically dedifferentiate all kinetosomes; in marine, freshwater, and terrestrial habitats, free-living with soe symbiotic forms as endo- and ectocommensals.

Order Sporadotrichida Fauré-Fremiet, 1961 San-po-ha-mo-mok (산포하모목)

Size small to large; shape, sometimes elongate, even tailed, but often oval to elliptical in outline; free-swimming; somatic ventral ciliature as fronto-ventral cirri, typically heavy and conspicuous, arranged in specific, localized frontal and ventral groups, except in a few taxa (e.g., Family Halteriidae, Laurentiella, Onychodromus, and Styxophrya); marginal cirri, typically present; transverse cirri, may or may not be present; caudal cirri, may or may not be present; dorsal somatic ciliature, typically as files of dikinetids with a single bristle cilium; oral ciliature as for subclass; stomatogenesis, apokinetal, usually with five or six anlagen streaks in two groups for differentiation of ventral somatic ciliature; in marine, freshwater, and terrestrial habitats, widely distributed, primarily benthic with some forms planktonic, others interstitial, and a few species symbiotic, either as ectocommensals on integument or in branchial cavity of several invertebrates or as intestinal inquilines of echinoids.

21 INVERTEBRATE FAUNA OF KOREA Ciliates

Family Oxytrichidae Ehrenberg, 1830 Cheom-mo-ha-mo-chung-gwa (첨모하모충과)

Size, small to large; shape, relatively elongate; free-swimming; somatic ventral ciliature as frontoventral and transverse cirri, typically 18 in number, large and distinctive, scattered over mid-area of ventral surface, between right and left marginal cirral files, usually with three frontoventral cirri posterior to posterior vertex of the oral region, but several genera with conspicuous files of cirri (e.g., Laurentiella, Onychodromus); 360 17. The Ciliate Taxa Including Families and Genera right and left marginal files of cirri, obvious; caudal cirri, may or may not be present; somatic dorsal ciliature as several files of bristle dikinetids, often showing fragmentation; adoral zone, typical of order, generally restricted to anterior half or quarter of body; division morphogenesis with six frontoventral anlagen streaks in two streaks in two groups that make a longitudinal fan-like pattern; macronuclei, typically as two ellipsoid nodules; micronucleus, present; contractile vacuole, at least in freshwater and terrestrial forms; cytoproct, dorsolateral left; feeding on bacteria, microalgae, and smaller protists, but several of the included genera are macrophagous carnivores on other ciliates and even smaller metazoa; in a variety of marine, freshwater, and terrestrial habitats, widely distributed (Lynn, 2008).

Genus Ponturostyla Jankowski, 1989 Ba-da-mi-ju-ha-mo-chung-sok (바다미주하모충속)

6. ‌Ponturostyla enigmatica (Dragesco and Dragesco-Kernéis, 1986) Jankowski, 1989 (Fig. 6) Sin-bi-ba-da-mi-ju-ha-mo-chung (신비바다미주하모충)

Paraurostyla enigmatica Dragesco and Dragesco-Kernéis, 1986, p. 437.

Fig. 6. Morphology of Ponturostyla enigmatica from life (A-D, I-L, O, P) and after protargol impregnation (E-H, M, N). A, C, I, J, Ventral views showing the greenish cortical granules arranged in lines between cirri (arrows) and the contractile vacuole (arrowhead). B, F, N, L, Do rsal views showing the shortened dorsal kineties (F; arrows and N, arrowheads). D, Irregular distribution of greenish cortical granules on the dorsal side. E, Infraciliature of the ventral side. G, H, K, M, Ventral views showing the ventral cirri, pretransverse cirri (arrowheads), the transverse cirri (double arrowhead), and the frontal and buccal cirri (arrowheads). O, P, Arrangement of cirri and cortical granules of the ventral and dorsal side. AZM, adoral zone of membranelles; DK, dorsal kineties; EM, endoral membrane; FC, frontal cirri; LMR, left marginal row; Ma, macronuclei; Mi, micronuclei; PM, paroral membrane; RMR, right marginal row; TC, transverse cirri; VC, ventral cirri. Scale bars: A, B, E, F, J, L, N=100 μm (cited from Kim et al., 2013).

22 OXYTRICHIDAE: Ponturostyla

A B C D

E F G I

AZM DK FC EM

RMR LMR

K VC

TC Mi

Ma M N

J L

O P

23 INVERTEBRATE FAUNA OF KOREA Ciliates

Ponturostyla enigmatica Jankowski, 1989, p. 86; Song, 2001, p. 194; Kim, Jung and Min, 2013, p. 147.

Size in vivo 102-156×50-75 μm. Body generally ellipsoidal with a tendency to slightly narrow towards ends, highly flexible, and slightly contractile. Both ends rounded (Fig. 6A, B). Contractile vacuole left to mid-body (Fig. 6I, J, arrowhead). Usually four (rarely up to eight) spherical Ma nodules, 5-7×8-10 μm in size (Fig. 6E, F, N) and two to eight Mi, approximately 2 μm across (Fig. 6F, N). Circular cortical granules tinged with green, about 0.6 μm in diameter, regularly arranged in rows between marginal rows on ventral side, and irregularly distributed on dorsal side (Fig. 6A-D, 6C, arrows, O). Adoral zone of membranelles about 40% of body length, continuous, and proximal portion covered with buccal lip (Fig. 6A, B, J). Both PM and EM long and strongly curved (Fig. 6M). Three FC, a single BC near anterior portion of PM and four other smaller cirri arranged in two pairs right to BC (Fig. 6H, arrowheads). Three VC posterior to proximal end of AZM and two pretransverse cirri (PTC) anterior to TC (Fig. 6G, arrowheads). Five to seven TC near posterior end of cell (Fig. 6G, J, M). Six to eight marginal rows of cirri (LMR and RMR) on each side (Fig. 6J, M), between the two groups of marginal rows, a blank area containing VC, PTC, and TC. Six to eight DK on dorsal side, four of which are bipolar, two shortened anteriorly and one or two dorsomarginal kineties on anterior right margin (Fig. 6F, arrows, N, arrowhead).

Distribution: Korea, Bénin, China.

Korea: GN.

Specimen examined: GN: (Dongbaek Island: 2.vi.2011).

Habitat: Marine.

Remarks: Ponturostyla enigmatica was first identified in Cotonou, Bénin, by Dragesco and Drages- co-Kernéis (1986) as type species by monotypy. The Korean population of P. enigmatica conforms to the description of the Chinese population provided by Song (2001). However, the Korean population differs from the Chinese population in having a smaller body size (131×70 μm vs. 172×73 μm, on average), a lower maximum number of MR (7 vs. 9), and a higher maximum number of TC (7 vs. 5).

Genus Pseudocyrtohymena Jung, Park and Min, 2015 Han-gug-yu-sa-gwan-mak-ha-mo-chung-sok (유사관막하모충속)

Oxytrichidae with Australocirrus-Cyrtohymena undulating membrane; body flexible, cytoplasm colorless; cortical granules present; caudal cirri, when present, at end of dorsal kinety 3; dorsal kinety 3 nonfragment- ed during morphogenesis (Urosomoida pattern) (Jung et al., 2015).

24 OXYTRICHIDAE: Pseudocyrtohymena

7. Pseudocyrtohymena koreana Jung, Park and Min, 2015 (Figs. 7, 8) Han-gug-yu-sa-gwan-mak-ha-mo-chung (한국유사관막하모충)

Pseudocyrtohymena koreana Jung, Park and Min, 2015, p. 283.

Size in vivo 100-145×30-60 μm; on average 112 μm×47 μm in protargol preparations. Body slender to ellipsoidal, flexible and slightly contractile (Figs. 7A, 8A-E). Cytoplasm grayish to yellowish under low magnification. Invariably two elongate elliptical Ma nodules left of mid-body, each about 18.2×9 μm after protargol impregnation; one to five oval to spherical Mi near Ma nodules, usually 2.4×2 μm in protargol preparations. A single contractile vacuole in mid-body near left margin, about 6 μm across during diastole (Figs. 7A, 8A). Cortical granules spherical, distributed over entire cortex, more densely arranged along dorsal kineties, yellowish and approximately 1 μm across in vivo (Figs. 7B, 8B, E). Adoral zone of membranelles approximately 42% of body length in protargol preparations; base of the

DK RMR EM AZM Mi G LMR

CC A B C D

Fig. 7. Pseudocyrtohymena koreana from life (A, B) and after protargol impregnation (C, D). A, B, Ventral and dorsal view of a representative specimen showing the body shape, the ventral cirral pattern and the cortical granules of the dorsal side; arrow denotes the contractile vacuole. C, D, Ventral and dorsal view of the holotype specimen. AZM, adoral zone of membranelles; CC, caudal cirri; DK, dorsal kineties; EM, endoral membrane; G, cortical granules; LMR, left marginal cirral row; Ma, macronuclear nodules; Mi, micronucleus; PM, paroral membrane; RMR, right marginal cirral row; TC, transverse cirri. Scale bars=50 μm (cited from Jung et al., 2015).

25 INVERTEBRATE FAUNA OF KOREA Ciliates

G G

Ma CV

CC A B C DDB E

PM K2 K3 PM Ma K1 AZM

EM EM Mi

LMR

H I

TC RMR CC CC VC F G J K

Fig. 8. Pseudocyrtohymena koreana from life (A-E) and after protargol impregnation (F-K). A, B, D, E, Dorsal views of representative specimens. C, Ventral view showing Australocirrus undulating membranes pattern. F-K, Dorsal (F, I, K) and ventral (G, H, J) views of the holotype (F, G) and other specimen (H-K) showing the Australocirrus undulating membrane pattern, nuclear apparatus, postoral ventral cirri, and caudal cirri at posterior end of dorsal kinety 3. AZM, adoral zone of membranelles; CC, caudal cirri; CV, contractile vacuole; DB, dorsal bristle; EM, endoral membrane; G, cortical granules; K1-3, dorsal kineties 1-3; LMR, left marginal cirral row; Ma, macronuclear nodules; Mi, micronuclei; PM, paroral membrane; RMR, right marginal cirral row; TC, transverse cirri; VC, ventral cirri. Scale bars=50 μm (cited from Jung et al., 2015).

26 UROSTYLIDA

largest membranelles approximately 6 μm wide, cilia of membranelles approximately 13 μm long. Paroral membrane (PM) and endoral membrane (EM) in typical Australocirrus pattern, namely, distinctly curved anterior part of PM in the leftward direction; the UM intersect in mid-buccal cavity (Figs. 7C, 8G). All cirri in vivo relatively fine, frontal and transverse cirri about 15 μm long; other cirri about 10 μm long (Figs. 7A, 8A, C, D, G). Usually, three frontal, four frontoventral, one buccal, three postoral, two pretransverse, and five transverse cirri. Most specimens showed the typical oxytrichid pattern, namely, 18 frontal-ventral-transverse (FVT) cirri with 22-39 left and 25-37 right marginal cirri. Few cells showed variation in FVT cirri number, ranging from 18 to 22 due to the presence of extra postoral ventral and transverse cirri. The extra cirri very likely originated from extra anlage. Three bipolar dorsal kineties without fragmentation; two shorter dorsomarginal kineties on right cell margin, rightmost kinety distinctly shorter than other dorsal kineties. Dorsal cilia approximately 2.5 μm long in vivo (Fig. 8D, E). One to three caudal cirri posterior to dorsal kinety 3.

Distribution: Korea.

Korea: GG.

Specimen examined: GG: (Estuarine brackish water in the Yellow Sea near Incheon, South Korea: iii.2011).

Habitat: Brackish water.

Remarks: Pseudocyrtohymena koreana is the type specis of the genus as monotypy (Jung et al., 2015). While the species has the Australocirrus UM, dorsal kinety 3 is not fragmented and caudal cirri are absent in dorsal kineties 1 and 2.

Order Urostylida Jankowski, 1979 Mi-ju-ha-mo-mok (미주하모목)

Size small to large, up to 800 μm; shape, elongate-elliptical in outline, sometimes quite broad; free-swimming; somatic ventral ciliature as fronto-ventral cirri in zig-zag files, running almost full length of ventral surface between right and left files of marginal cirri and ranging from a “single” file of zig-zag or offset cirri to multiple and short files of cirri whose anterior and sometimes posterior ends are offset (=developed zig- zag) (e.g., Eschaneustyla); transverse cirri, present or absent; caudal cirri, present or absent; somatic dorsal ciliature as three or more kineties of bristle dikinetids; during division morphogenesis, zig-zag cirri differen- tiating from anlagen of many short oblique kinetofragments.

27 INVERTEBRATE FAUNA OF KOREA Ciliates

Family Pseudokeronopsidae Borror and Wicklow, 1983 Yu-sa-gag-mo-gwa (유사각모과)

Size, medium to large; shape, elongate; freeswimming; somatic ventral ciliature as frontal cirri forming a conspicuous, arc-like file that parallels the anterior left serial oral polykinetids, which may be doubled by an arc-like extension of the frontoventral zig-zag file; left and right marginal cirri as 1 (rarely 2) file(s); transverse cirri, present or absent; caudal cirri, present or absent; dorsal somatic ciliature as three or more files of bristle dikinetids; oral ciliature as for order with paroral and endoral; macronucleus, ellipsoid, typically many more than two; micronucleus, present; contractile vacuole, present at least in freshwater forms; cytoproct, likely present; feeding on bacteria, algae, and smaller protists; in marine, freshwater, and terrestrial habitats (Lynn, 2008).

Genus Apokeronopsis Shao, Hu, Warren, Al-Rasheid, Al-Quraishy and Song, 2007 Bak-gag-mo-ha-mo-chung-sok (박각모하모충속)

Key to the species of genus Apokeronopsis

1. One or two buccal cirri...... A. ovalis - More than two buccal cirri...... A. bergeri

8. ‌Apokeronopsis bergeri Li, Song, Warren, Al-Rasheid, Roberts, Yi, Al-Farraj and Hu, 2008 (Figs. 9, 10) Hwang-saek-bak-gag-mo-ha-mo-chung (황색박각모하모충)

Apokeronopsis bergeri Li, Song, Warren, Al-Rasheid, Roberts, Yi, Al-Farraj and Hu, 2008, p. 208; Jung, Baek and Min, 2011, p. 116.

Size in vivo usually 260×80 μm. Body fusiform with both ends broadly rounded (Figs. 9A, 10A); slightly contractile and flexible (Fig. 10B, C); dorsoventrally flattened. Contractile vacuole on left side of anteri- or third of body, approximately 15 μm in diameter (Figs. 9A, 10B, arrow). Cells appear yellowish green to green under low magnification. Cytoplasm opaque and colorless (Fig. 10D). About 200 oval-shaped macronuclear nodules (Figs. 9F, 10G). Two types of cortical granules: type I very small, ca. 0.3 μm across and colorless, arranged in longitudinal lines, distributed over entire body (Figs. 9B, 10D, arrowhead); type II ca.

28 PSEUDOKERONOPSIDAE: Apokeronopsis

BC DK PM EM AZM

MVR

RMR

LMR Ma TC

A C D E F

Fig. 9. Morphology and infraciliature of Apokeronopsis bergeri from life (A-D) and after protargol impregnation (E, F). A, Ventral view of a representative specimen, arrow indicates the contractile vacuole. B, The two types of cortical granules, arrow and arrowhead show the type I and type II granules, respectively. C, D, Ventral and dorsal view showing the arrangement of the cortical granules. E, F, Infraciliature of ventral and dorsal side, arrow show frontoterminal cirri. AZM, adoral zone of membranelles; BC, buccal cirri; DK, dorsal kineties; EM, endoral membrane; LMR, left marginal row; Ma, macronuclei; MVR, midventral row; PM, paroral membrane; RMR, right marginal row; TC, transverse cirri. Scale bars=100 μm (cited from Jung et al., 2011a).

2 μm across, oval, and yellow green in color, dense and irregularly distributed over entire body (Figs. 9B, arrow; C, D; 10D, arrow). Distinct adoral zone of membranelles, about 1/3 of cell length, forming a question mark, composed of about 85 membranelles, distal end extends posteriorly to near body 1/3; base of longest membranelles about 10 μm wide (Fig. 9A, E). Paroral and endoral membranes almost equal in length and spatially crossed at proximal end on different planes (Fig. 9E). Most somatic cirri relatively fine, ca. 15 μm in length. Bicorona of frontal cirri slightly enlarged, composed of 42 cirri, extending consecutively to midventral complex. Midventral complex distinctly separated rows, composed of 77 cirri, terminating near transverse cirri. Cirri of left row of both bicorona and midventral complex relatively smaller than those of right rows (Fig. 9E). Usually two frontoterminal cirri, un-

29 INVERTEBRATE FAUNA OF KOREA Ciliates

A B C

D E F G

Fig. 10. Morphology and infraciliature of Apokeronopsis bergeri from life (A-D) and after protargol impregnation (E-G). A-D, Dorsal and ventral views showing the body shape, color, contractile vacuole (arrow in B), the arrowhead and arrow in D mark the two types of cortical granules, respectively. E. Dorsal side showing the invariably three dorsal kineties. F, G, Ventral views showing the frontal cirri (bicorona) and the buccal cirral row, the general ciliature of the specimen, and the numerous densely scattered macronuclear nodules. Scale bars=100 μm (cited from Jung et al., 2011a).

derneath distal end of AZM (Fig. 9E, arrow). One row of buccal cirri consisting of 9-15 cirri, alongside of paroral membrane. Cirri in left and right marginal rows narrowly spaced, and separated posteriorly by a slightly conspicuous gap. Transverse cirri arranged in a curved row, composed of 11-18 cirri. Dorsal cilia ca. 5 μm long; invariably three bipolar dorsal kineties (Fig. 10E, arrows).

Distribution: Korea, China.

Korea: GG.

Specimen examined: GG: (Incheon Harbor: 2.xi.2010).

Habitat: Marine.

Remarks: In terms of the infraciliature, Apokeronopsis bergeri mostly resembles A. sinica. However, the former can be distinguished from the latter by the following characteristics: body shape (fusiform with nar-

30 PSEUDOKERONOPSIDAE: Apokeronopsis

rowing at cell ends vs. slender ellipsoid with widely rounded anterior end), number of adoral membranelles (75-106 vs. 41-62), buccal cirri (9-15 vs. 1-6), frontal cirri (37-47 vs. 18-29), and transverse cirri (11-18 vs. 8-13) (Liu et al., 2009). The Korean population of A. bergeri corresponds well with the original description by Li et al. (2008) and the ranges of characteristics in the morphometric comparisons are highly overlapped. However, the body size of the Korean population is slightly smaller than that of the Chinese population (ca. 260×80 vs. 300×80 μm in vivo), and the type II granules of the Chinese specimen are flattened and biconcave (similar to erythrocytes of mammals), while those of Korean specimens are slightly flattened and convex.

9. ‌Apokeronopsis ovalis (Kahl, 1932) Shao, Miao, Li, Song, Al-Rasheid, Al-Quraishy and Al-Farray, 2008 (Figs. 11, 12) Nan-hyeong-bak-gag-mo-ha-mo-chung (난형박각모하모충)

Holosticha (Keronopsis) ovalis Kahl, 1932, p. 575. Holosticha (Keronopsis) ovalis forma arenivora Kahl, 1932, p. 575. Pseudokeronopsis ovalis Borror and Wicklow, 1983, p. 124; Berger, 2006, p. 968. Apokeronopsis ovalis Shao, Miao, Li, Song, Al-Rasheid, Al-Quraishy and Al-Farraj, 2008, p. 363; Jung, Baek and Min, 2011, p. 117.

Size in vivo usually 160×55 μm. Body oval, dorsoventrally flattened, slightly contractile and flexible (Figs. 11A, 12A-D). Contractile vacuole on left side of anterior third of body, about 10 μm in diameter (Figs. 11A, 12C, arrow). Cells colorless to grayish under low magnification. Cytoplasm opaque and colorless (Fig. 12A-D). About 150 oval macronuclear nodules (Figs. 11D; 12I, arrow). Two types of cortical granules: type I very small, about 0.2 μm across and colorless, arranged in longitudinal lines, distributed over entire body (Figs. 11B, arrowhead; 12F, arrowhead); type II granules spherical, about 1.5 μm in diameter, and mostly colorless and only a few yellow green, densely and irregularly distributed over entire body (Figs. 11B, arrow; 12E, F, arrow). Distinct adoral zone of membranelles, about 1/3 of cell length, formed question mark, consisting of about 62 membranelles; base of longest membranelles about 15 μm wide (Fig. 11C). Paroral and endoral membranes almost equal in length and spatially crossed on proximal end (Fig. 11C). Most somatic cirri relatively fine, about 10 μm in length. Bicorona of frontal cirri slightly enlarged, composed of 30 cirri, extends to midventral complex with an inconspicuous gap. Midventral complex consists of about 52 cirri, terminating near transverse cirri. Invariably, two frontoterminal cirri, on distal end of AZM (Fig. 11C, arrow). One or two BC right to PM (Figs. 11C, 12K). Transverse cirri arranged in J-shaped line,

31 INVERTEBRATE FAUNA OF KOREA Ciliates

BC DK AZM PM EM

MVR LMR

RMR Ma

A B C D

Fig. 11. Morphology and infraciliature of Apokeronopsis ovalis from life (A, B) and after protargol impregnation (C, D). A, Ventral view of of a representative specimen, arrow indicates the contractile vacuole. B, Densely distributed granules, arrow and arrowhead show type II and type I granules, respectively. C, D, In- fraciliature of ventral and dorsal side and the nuclear apparatus, arrow marks the frontoterminal cirri. AZM, adoral zone of membranelles; BC, buccal cirri; DK, dorsal kineties; EM, endoral membrane; LMR, left marginal row; Ma, macronuclei; MVR, midventral row; PM, paroral membrane; RMR, right marginal row; TC, transverse cirri. Scale bars=100 μm (cited from Jung et al., 2011a).

and composed of 9-14 cirri (Figs. 11C, 12L). Left marginal row terminates posteriorly on dorsal side, composed of 30-47 cirri; RMR commencing on dorsal side, consisting of 38-55 cirri. Usually three DK (Figs. 11D; 12J, arrows); dorsal cilia about 5 μm long (Figs. 11D; 12F, double-arrowhead).

Distribution: Korea, China, and Germany.

Korea: GG.

Specimen examined: GG: (Baengyeongdo Island: 16.xi.2010).

Habitat: Marine.

Remarks: In comparison with the congeners, Apokeronopsis ovalis is most closely related to A. sinica(Liu et al., 2009). However, the former can be separated from the latter by body shape (oval vs. slender ellipsoid), the location of the anterior portion of the right marginal row (dorsal vs. ventral), and the color of the larger cortical granules (mostly colorless and a few yellow-green vs. mostly colorless and a few vermeil). The Korean population of Apokeronopsis ovalis corresponds well with the description of Shao et al. (2008a). The Chinese populations described by Shao et al. (2008a) differs from the Korean population in

32 PSEUDOKERONOPSIDAE: Apokeronopsis

A B C

E F

H I J L

Fig. 12. Morphology and infraciliature of Apokeronopsis ovalis from life (A-F) and after protargol impregnation (G-L). A-D, Dorsal (A) and ventral (B-D) views of representative specimens, body slightly contractile and flexible, arrow indicates the contractile vacuole. E, F, Type I (arrowhead) and type II (arrows) cortical granules, double-arrowhead indicates the dorsal cilia. G-L, Dorsal (G-I, K, L) and ventral (J) view showing the general ciliature, the two frontoterminal cirri, arrows in H indicate frontoterminal cirri near the distal end of the adoral zone, arrow in I denotes macronuclear nodules, and arrows in J indicate dorsal kineties, Scale bars=100 μm (cited from Jung et al., 2011a).

having one to five buccal cirri (vs. 1 or 2), and are brown to dark brown in color (vs. colorless to grayish). Shao et al. (2008a) suggested that the body color of A. ovalis is possibly reflected by green or yellow-green cortical granules. However, the Korean population is colorless and the cells have both colorless and yel-

33 INVERTEBRATE FAUNA OF KOREA Ciliates

low-green type II granules. The color of the granules in the family Pseudokeronopsidae has been known as an important characteristics (Berger, 2006; Song et al., 2006), however, Li et al. (2008) reported that the colors in A. bergeri were variable from yellow-brown to yellow-green, and that the colors can even be changed to dark-red in cultured cells. Therefore, the color of the cortical granules in A. bergeri and A. ovalis should be treated carefully as a diagnostic for species identification.

Genus Pseudokeronopsis Borror and Wicklow, 1983 Wi-gag-mo-chung-sok (위각모충속)

10. ‌Pseudokeronopsis carnea (Cohn, 1866) Wirnsberger, Larsen and Uhlig, 1987 (Figs. 13, 14) Ttung-ttung-i-hong-saeg-wi-gag-mo-chung (뚱뚱이홍색위각모충)

Oxytricha flava var. carnea Cohn, 1866, p. 288. Holosticha (Keronopsis) rubra var. carnea Kahl, 1932, p. 573. Pseudokeronopsis rubra Shi and Xu, 2003, p. 23. Pseudokeronopsis pararubra Hu, Warren and Suzuki, 2004, p. 351. Pseudokeronopsis carnea Wirnsberger, Larsen and Uhlig, 1987, p. 79, Song, Warren, Roberts, Wilbert, Li, Sun, Hu and Ma, 2006, p. 271; Baek, Jung and Min, 2011, p. 221.

Size in vivo 190-255×55-70 μm, usually 225×61.3 μm. Body slender; posterior end inconspicuously narrowed; both anterior and posterior ends rounded (Figs. 13A, 14A, B); dorsoventrally flattened. Con- tractile vacuole on left side of posterior 1/3-2/5 portion (Figs. 13A, arrowhead; 14C, arrow). Two types of cortical granules, reddish cortex due to underlying reddish-brown or orange-red cortical granules, which are around both dorsal kineties and cirri (Fig. 14E, F, G, arrowhead); colorless cortical granules, blood cell shaped, scattered throughout the cell body (Fig. 14F, G, arrow). The adoral zone of membranelles distinct, approximately 1/3 of cell length, and composed of about 69 membranelles (Fig. 14D, H). Bicorona of frontal cirri slightly enlarged, composed of about 8-12 cirral pairs, extending consecutively to midventral complex. One buccal cirrus near paroral membrane (Fig. 14H, arrow). Two frontoterminal cirri underneath distal end of AZM (Fig. 14I, arrows). Midventral complex distinctly separated rows (Fig. 14J), composed of 30-46 cirral pairs, terminating near transverse cirri. One LMR and one RMR with posterior ends not overlapped. Seven to ten TC between posterior ends of marginal cirral rows (Fig. 14K). Inconspicuous gap between midventral rows and TC. Five to seven dorsal kineties (Figs. 13D; 14L, arrows).

34 PSEUDOKERONOPSIDAE: Pseudokeronopsis

AZM DK

PM FTC EM

Ma MVR

LMR

RMR

TC A C D

Fig. 13. Morphology and infraciliature of Pseudokeronopsis carnea from life (A, B) and after protargol impregnation (C, D). A, Ventral view of a representative specimen, arrowhead denotes CV. B, The two types of cortical granules. C, D, Infraciliature of the ventral and dorsal side. AZM, adoral zone of membranelles; BC, buccal cirri; CV, contractile vacuole; DK, dorsal kineties; EM, endoral membrane; FTC, frontoterminal cirri; LMR, left marginal row; Ma, macronuclei; MVR, midventral row; PM, paroral membrane; RMR; right marginal row; TC, transverse cirri. Scale bars=100 μm (cited from Baek et al., 2011).

Distribution: Korea, China, Denmark, Germany, Mediterranean, North Sea, and Yugoslavia.

Korea: GG.

Specimen examined: GG: (Incheon harbor: 2.xi.2010).

Habitat: Marine.

Remarks: Cohn (1866) published Oxytricha flava var. carnea without any illustrations. As the former species is almost identical to Pseudokeronopsis flava, he classified it as a variety of Oxytricha flava. The deri- vation of the name was not given in the original description of P. carnea. The meaning of carnea in Latin is “fleshy.” In 1882, Kent transferred Oxytricha rubra to the genus Holosticha. Kahl (1932) classified Keron- opsis as a subgenus of Holosticha. Then, Kahl named it Holosticha (Keronopsis) rubra var. carnea. Even after several taxonomists recorded this species, they were considered it Pseudokeronopsis rubra or P. flava in

35 INVERTEBRATE FAUNA OF KOREA Ciliates

A B C D

E F G

H I K L

Fig. 14. Morphology and infraciliature of Pseudokeronopsis carnea from life (A-C, E-G) and after protargol impregnation (D, H-L). A-C, Ventral (A, B) and dorsal (C) view showing the body shape. Arrow marks the contractile vacuole. D, H-L, Ventral (D, H-K) and dorsal (L) view showing the infraciliature, the nuclear apparatus, and frontal (bicorona). Arrow in H indicates the buccal cirrus. Arrows in I mark the two frontoterminal cirri. Arrows in (L) show the dorsal kineties. E-G, Cortical granules around dorsal kineties, arrows indicate ring-shaped hollow structures, arrowheads show cortical granules; Scale bars=100 μm (cited from Baek et al., 2011).

36 PSEUDOKERONOPSIDAE: Uroleptopsis

confusion. Entz (1884) considered P. carnea as a transitional form between P. rubra and P. flava. The neotype of P. carnea was fixed by Wirnsberger et al. (1987) and until now, a Chinese population of P. carnea has been redescribed solely (Song et al., 2006). Because Pseudokeronopsis species are somewhat difficult to classify and identify among congeners, the color (as main diagnostic key) is the critical factor distinguishing P. carnea from other congeners (Hu and Song, 2001). The orange-red color of cortical granules is essential for identifying P. carnea (vs. colorless P. decolar and P. ovalis; yellow P. flavicans and P. flava; brick-red P. rubra; yellow-greenish P. sepetiben- sis; brick-red and yellow P. multinucleata). Moreover, with the exception of the color of the cortical granules, the ciliary pattern and position of the contractile vacuole support species separation (Song et al., 2002; Berger, 2006). Like the name suggests, this species has the most plump body shape among the congeners. Although the anterior end is bluntly rounded, the posterior end is inconspicuously narrowed. This species can be separated from other congeners by having: (i) more cirral pairs in both the bicorona and the midventral rows; (ii) more transverse cirri; (iii) more dorsal kineties; (iv) a contractile vacuole in the posterior half of the cell, usually in the posterior 1/3-2/5; and (v) more conspicuous pigment granules, always dark red or orange-red. The number of adoral membranelles in this species is also higher than that of other congeners. In addition, the adoral zone of membranelles is relatively long compared to body length (ratio, 1:3), and the gap between the midventral rows and the transverse cirri is almost absent. The Korean population of Pseudokeronopsis carnea differs from the Chinese population (Song et al., 2006) in having less dorsal kineties (5-7 vs. 7-8).

Genus Uroleptopsis Ehrenberg, 1831 Mang-hoing-geug-mo-chung-sok (망횡극모충속)

11. Uroleptopsis citrina Kahl, 1932 (Figs. 15, 16) Yeon-no-rang-mang-hoing-geug-mo-chung (연노랑망횡극모충)

Uroleptopsis citrina Kahl, 1932, p. 543; Kahl, 1933, p. 107; Kudo, 1950, p. 672; Borror, 1972, p. 11; Berg- er, 2004, p. 99; Baek, Jung and Min, 2011, p. 224.

Size in vivo 118-165×45-55 μm, usually 130.2×50 μm. Body shape elongate-elliptical; both anterior and posterior ends round and dorsoventrally flattened. Contractile vacuole difficult to recognize, located on the left side of usually slightly squeezed cells. Body color is lemon-yellow due to cortical granules, which are around both dorsal kineties and cirri; two types of cortical granules, blood cell shaped granules colorless and spherical ones yellowish, scattered throughout body surface and around both dorsal kineties and cirri.

37 INVERTEBRATE FAUNA OF KOREA Ciliates

FTC AZM B PM EM

MVR Ma

RMR

LMR

A C D

Fig. 15. Morphology and infraciliature of Uroleptopsis citrina from life (A, B) and after protargol impregnation (C, D). A, Ventral view of a representative specimen showing the body shape and the infraciliature; B, Two types of granules. C, D, Ventral and dorsal side view showing the infraciliature and the nuclear apparatus. AZM, adoral zone of membranelles; DK, dorsal kineties; EM, endoral membrane; FTC, frontoterminal cirri; LMR, left marginal row; Ma, macronuclei; MVR, midventral row; PM, paroral membrane; RMR; right marginal row. Scale bars=100 μm (cited from Baek et al., 2011).

(Figs. 15B, 16E, F). Adoral zone of membranelles distinct; about 1/3 of cell length and composed of about 40 membranelles; left anterior corner a minute process causing a break (Figs. 15C, 16C, D, I). Bicorona of frontal cirri slightly enlarged, composed of about 6-9 cirral pairs, extends consecutively to midventral complex (Figs. 15A, C, 16D, I). Midventral complex consists of two separate rows, composed of 26-35 cirri; middle portion consists of single cirral row (Figs. 15A, C, 16G). Two or three frontoterminal cirri underneath distal end of AZM (Figs. 15C, 16I, arrows). Invariably, three dorsal kineties (Figs. 15D; 16C, arrows). Of particular inter- est, both buccal cirrus and transverse cirri absent.

Distribution: Korea, Adriatic Sea.

Korea: GB.

38 PSEUDOKERONOPSIDAE: Uroleptopsis

A B C D

E F G H I

Fig. 16. Morphology and infraciliature of Uroleptopsis citrina from life (A, B, E, F) and after protargol impregnation (C, D, G-I). A, B, Ventral views showing the body shape; C, D, G-I Dorsal (C) and ventral (D, G-I) views showing the infraciliature and the nuclear apparatus. Arrows in C mark the invariable three dorsal kineties. Arrowheads in C, D, show the gap in the AZM. Arrow and arrowheads in E, F, indicate the two kinds of granules, respectively. Note the middle portion of the midventral row cinsists of a single cirral line (G, Arrow). Scale bars=100 μm (cited from Baek et al., 2011).

Specimen examined: GB: (Guryongpo, Pohang: xi.2008).

Habitat: Marine.

Remarks: Kahl (1932) established the genus Uroleptopsis and described firstly U. citrina. Later, Berger (2004) redescribed the morphology and morphogenesis of U. citrina from the Adriatic Sea. Uroleptopsis citrina has a gap in the adoral zone and lacks transverse cirri. The loss of the transverse cirri is the main diagnostic character to separate U. citrina from other Pseudokeronopsidae species. This species has conspicuous differences from the congener U. ignea mainly the presence/absence of the buccal cirrus and the pattern of

39 INVERTEBRATE FAUNA OF KOREA Ciliates

the midventral complex. Circumstantially, U. citrina lacks a buccal cirrus in the ordinary position, right of the paroral, while it is present in U. ignea. Also, the anterior and posterior portion of the midventral complex in this species primarily consist of ordinary midventral pairs; the middle portion is composed only of the right cirri of the cirral pairs, while only the anterior portion of the midventral complex is composed of paired cirri in U. ignea (Mihailowitsch and Wilbert, 1990). Consequently, U. ignea is transferred to the subgenus Uroleptopsis (Plesiouroleptopsis) by Berger (2004). The Korean population of U. citrina differs from the Adriatic Sea population (Berger, 2004) as follows: (1) the number of the left marginal cirri (26-41 vs. 28-49); (2) the number of the right marginal cirri (29-53 vs. 34-63); and (3) the number of cirri in the middle portion of the midventral row (8 vs. 11 on average).

Family Pseudourostylidae Jankowski, 1979 Yu-sa-mi-ju-ha-mo-chung-gwa (유사미주하모충과)

Size, medium to large; shape, elongate ovoid; free-swimming; somatic ventral ciliature as frontal cirri forming a conspicuous, arc-like file that parallels the anterior left serial oral polykinetids and a frontoventral cirral zig-zag with 1-6 files to the right of left marginal cirral file and also with several cirral files to the left of the right marginal cirri; multiple “marginal files” derive from unique anlagen during morphogenesis; transverse cirri, present or absent; caudal cirri, absent; dorsal somatic ciliature as several files of bristle dikinetids; oral ciliature as for order with paroral and endoral; macronucleus, ellipsoid, multiple; micronucleus, present; contractile vacuole, present; cytoproct, likely present; feeding on bacteria, algae, smaller protists, including testate amoebae and ciliates; in freshwater and terrestrial habitats.

Genus Pseudourostyla Borror, 1972 Yu-sa-mi-ju-ha-mo-chung-sok (유사미주하모충속)

12. Pseudourostyla cristatoides Jung, Park and Min, 2012 (Figs. 17-19) Gi-su-yu-sa-mi-ju-ha-mo-chung (기수유사미주하모충)

Pseudourostyla cristatoides Jung, Park and Min, 2012, p. 42.

Size in vivo 220-265×85-125 μm (Figs. 17, 18), on average about 243.8×89 μm in protargol preparations (Figs. 17, 19). Body ellipsoidal with both ends broadly rounded, anterior (head-like) portion slightly curved leftward; flexible and slightly contractile. Cell color grayish to colorless. Extrusomes trichocyst type,

40 PSEUDOUROSTYLIDAE: Pseudourostyla

FC DK BC AZM RMR PM FTC EM LMR

Mi Ma TC

A B C D E

Fig. 17. Morphology of Pseudourostyla cristatoides from life (A, B) and after protargol impregnation (C-E). A. Ventral view of a representative individual, arrows indicate contractile vacuoles. B. Ventral views of the process of forming contractile vacuoles. C-E. Ventral (C) and dorsal (D, E) views of the holotype specimen, arrow denotes the anteriormost midventral pair. AZM, adoral zone of membranelles; BC, buccal cirrus; DK, dorsal kineties 1; EM, endoral membrane; FC, frontal cirri forming bicorona; FTC, frontoterminal cirri; LMR, outermost left marginal row; Ma, macronucleus; Mi, micronucleus; MP, midventral pair; PM, paroral membrane; RMR, outermost right marginal row; TC, transverse cirri. Scale bars=100 μm (cited from Jung et al., 2012).

densely arranged throughout cell surface (Fig. 18E, arrows). Extruded extrusomes ca. 5-10 μm in length with club-shaped end; observed after methyl green-pyronin and occasionally after protargol impregnation (Fig. 18G, H). Two contractile vacuoles on left side at 25% and 75% of body, about 14 μm in diameter during diastole; both vacuoles with anterior and posterior collecting canals about 180-200 μm long; only one or both vacuoles recognizable at the same time (Figs. 17A, B; 18A-C, arrows). On average 78 ellipsoidal macronuclear nodules and about four oval micronuclei (Figs. 17D, 19A-E). Crawling moderately fast on bottom of Petri dish. Adoral zone of membranelles about 33% of body length in fixed specimens, base of largest membranelles about 12 μm wide, cilia of membranelles about 15 μm long. Distal end of AZM extends far posteriorly (Figs. 17A, C, 19A, B). Paroral and endoral membranes rather short, slightly curved and almost parallel (Fig. 17C).

41 INVERTEBRATE FAUNA OF KOREA Ciliates

A B C D

E F H

Fig. 18. Photomicrographs of Pseudourostyla cristatoides from life (A-F) and methyl green-pyronin staining (G, H). A-C. Dorsal views, arrows mark the contractile vacuoles. D. Ventral view showing the arrangement of cirri. E, F. Dorsal views, arrow denotes narrowly spaced extrusomes, and arrowheads indicate dorsal bristles. G, H. Extruded cortical granules (trichocyst type). Scale bars=100 μm (cited from Jung et al., 2012).

All cirri relatively fine, mostly 10-15 μm long; frontal cirri about 13 μm long; midventral, marginal and frontoterminal cirri about 10 μm long; transverse cirri 15 μm long (Figs. 17A, 18D). Frontal cirri form bicorona of 20-30 cirri separated from midventral (17-25) cirral pairs by a distinct gap near posterior frontoterminal cirrus; one buccal cirrus. Invariably two frontoterminal cirri at distal end of AZM. Two pretransverse and 6-12 transverse cirri. Five to seven left and four or five right marginal rows, number of cirri in each row decreasing gradually from inside to outside. Ten to thirteen bipolar dorsal kineties (Figs. 17E, 19B). Number of dikinetids in dorsal kineties gradually decreases from outside to inside and leftmost row have distinctly higher number of dikinetids (ca. 51). Dorsal bristles about 3 μm-long (Fig. 18F).

42 PSEUDOUROSTYLIDAE: Pseudourostyla

A B D E

Fig. 19. Photomicrographs of Pseudourostyla cristatoides after protargol impregnation. A, C. Ventral views of the holotype specimen with arrow and arrowhead indicating macronucleus and micronucleus, respectively. B. Dorsal view of the holotype specimen showing the complete dorsal kineties. Arrows mark the leftmost and the rightmost dorsal kineties. D, E. Ventral views of early dividers, arrows indicate oral primordium patches, arrowhead denotes dedifferentiated buccal cirrus. Scale bars=100 μm (cited from Jung et al., 2012).

Distribution: Korea, Adriatic Sea.

Korea: GB.

Specimen examined: GB: (Guryongpo, Pohang: ix.2008).

Habitat: Brackish water.

Remarks: Pseudourostyla cristatoides is morphologically very similar to P. cristata (Jerka-Dziadosz, 1964) Borror, 1972, type species of Pseudourostyla, in body shape and cirral pattern arrangement. However, the former species differs from the latter in the number and position of contractile vacuoles (two in 25% and 75% of body length vs. one ahead of mid-body), dorsal kineties (10-13 vs. 8), hyaline layer underneath pellicle (inconspicuous vs. conspicuous), habitat (brackish water vs. freshwater), and participation of the posterior cirri of the rear corona in FVT anlagen (yes vs. no). Berger (2006) suggested that Pseudourostyla levis Takahashi, 1973 and P. cristata are sibling species because they cannot be distinguished based on morphology. Kumar et al. (2010) described an Indian population of P. levis. However, the Indian population slightly differs from the neotype population in terms of pretransverse cirri (absent vs. present). Thus, we compared these two P. levis populations, the neotype and Indi-

43 INVERTEBRATE FAUNA OF KOREA Ciliates

an population, with P. cristatoides separately. The P. levis neotype can be distinguished from P. cristatoides based on adoral membranelles (67 vs. 84-115), frontal cirri (16 vs. 20-30), dorsal kineties (7-8 vs. 10-13), and participation of posterior cirri of rear corona in FVT anlagen (no vs. yes). Pseudourostyla levis sensu Kumar et al. (2010) differs from P. cristatoides in terms of dorsal kineties (7 vs. 10-13), pretransverse cirri (absent vs. present), contractile vacuole (1 vs. 2), and participation of the posterior cirri of the rear corona in FVT anlagen (no vs. yes).

Family Urostylidae Bütschli, 1889 Mi-ju-ha-mo-chung-gwa (미주하모과)

Some tailed forms; free-swimming; somatic ventral ciliature with several frontal cirri somewhat larger than other frontoventral cirri, and with frontoventral cirri as a single zig-zag file of paired cirri or a series of shorter files offset at their anterior and posterior ends (e.g., Bakuella, Eschaneustyla ) and typically not with additional “marginal files” on both sides of this zig-zag (cf. Pseudourostylidae); transverse cirri, may be numerous; caudal cirri, present or absent; dorsal somatic ciliature as three to many files of bristle dikinetids; oral ciliature as for order with paroral and endoral; during division morphogenesis, frontoventral cirri dif- ferentiate from a longitudinal field of more than five oblique ciliary streaks; macronucleus, ellipsoid, two to many nodules; micronucleus, present; contractile vacuole, present; cytoproct, likely present; feeding on bacteria, algae, and smaller protists, including ciliates; in marine, freshwater, and terrestrial habitats.

Genus Anteholosticha Berger, 2003 Won-jeon-yeol-ha-mo-chung-sok (원전열하모충속)

Key to the species of genus Anteholosticha

1. Two frontoterminal cirri...... A. pulchra - More than two frontoterminal cirri...... A. multicirrata

13. Anteholosticha multicirrata Park, Jung and Min, 2013 (Figs. 20-22) Da-geug-mo-won-jeon-yeol-ha-mo-chung (다극모원전열하모충)

Anteholosticha multicirrata Park, Jung and Min, 2013, p. 565.

44 UROSTYLIDAE: Anteholosticha

Size in vivo 90-125×30-45 μm, on average about 115×31 μm in protargol-impregnated specimens. Body slender to ellipsoidal, slightly flexible and noncontractile, anterior end broader than posterior end and posterior end narrowly rounded. Buccal field occupies about 40% of body length (Figs. 20A, 21A, B, E-G). About 117 ellipsoidal macronuclear nodules, each 1.6-4.8×1.6-2.4 μm in protargol impregnated specimens and about 4×2.2 μm in vivo, scattered throughout whole body (Figs. 20E, 22A, B). Contractile vacuole about 10 μm across, on left and slightly above mid-body (Fig. 21A, B). Cells colorless to greyish at low magnification. Yellow-greenish cortical granules, approximately 0.7 μm in diameter, in rows along dorsal kineties and cirri on ventral side and between rows (Figs. 20B, C, 21C, D, F). All cirri relatively fine, generally 10-

AZM FC FT PM EM DK BC

B MP Ma

RMR LMR PTC

TC A C D E

Fig. 20. Morphology of Anteholosticha multicirrata from life (A-C) and after protargol impregnation (D, E). A. Ventral view of a typical specimen. B, C. Ventral and dorsal side views showing the distribution of cortical granules. D, E. Ventral and dorsal view of the holotype specimen, showing the infraciliature and the nuclear apparatus. AZM, adoral zone of membranelles; BC, buccal cirrus; DK, dorsal kineties; EM, endoral membrane; FC, frontal cirri; FT, frontoterminal cirri; LMR, left marginal row; Ma, macronuclear nodules; MP, mid-ventral pairs; PM, paroral membrane; PTC, pretransverse cirri; RMR, right marginal row; TC, transverse cirri. Scale bars=50 μm (cited from Park et al., 2013).

45 INVERTEBRATE FAUNA OF KOREA Ciliates

A B

C D E F G

Fig. 21. Photomicrographs of Anteholosticha multicirrata from life. A, B, Ventral and dorsal views of a typical specimen, arrow marks the contractile vacuole. C, D, Dorsal and marginal view showing the cortical granules (arrows) and the dorsal bristles (arrowhead). E-G. Ventral (E, G) and dorsal (F) views showing the distribution of cortical granules (E, F) and the ventral cirral pattern. Scale bars=50 μm (cited from Park et al., 2013).

12 μm long. Adoral membranelles 30-40 in number; three frontal cirri; five to seven frontoterminal cirri near distal portion of AZM. Mid-ventral complex composed of zigzagging 14-21 cirral pairs and extends to 60% of body length. Endoral and paroral membrane almost equivalent in length. Buccal cirrus about 12 μm beneath anterior end of paroral membrane. About 39 left marginal cirri, right marginal cirri about 45 with anterior portion on dorsal side. One or two pretransverse and four to six transverse cirri. Invariably, three bipolar dorsal kineties and two dikinetids anterior to right marginal row. Bristles 1.7-2.5 μm long in vivo (Figs. 20A, D, E, 21G, 22A-E). Caudal cirri lacking. Crawling moderately fast on bottom of Petri dish.

Distribution: Korea.

Korea: GN.

Specimen examined: GN: (the littoral zone of Dong-baek park of Busan (35°09ʹN, 129°09ʹE), South Ko- rea).

46 UROSTYLIDAE: Anteholosticha

A B E F

G H I J K

Fig. 22. Photomicrographs of Anteholosticha multicirrata after protargol impregnation. A, C, D, Ventral views showing frontal (arrowheads in C), frontoterminal (arrows in C), and pretransverse (arrowhead in D) cirri. B, E, Dorsal views showing macronuclear nodules and dorsal kineties. F. Ventral view of early divider, arrow indicates the proliferation of basal body patches. G. Ventral view of late early divider, showing the formation of the adoral membranelles (arrow). H, I. Ventral and dorsal views of a middle divider specimen, showing marginal cirral row anlagen (arrows) and dorsal kineties anlagen (arrowhead). J, K. Ventral views of late divider, arrow indicates migration of frontoterminal cirri. Scale bars=50 μm (cited from Park et al., 2013).

Habitat: Marine.

Remarks: Among the ca. 40 species of the genus Anteholosticha, the following three morphologically similar congeners were compared with A. multicirrata: A. manca, A. warreni, and A. australis (Berger,

47 INVERTEBRATE FAUNA OF KOREA Ciliates

2006). Anteholosticha manca (Kahl, 1932) Berger, 2003 is very similar to A. multicirrata, i.e., they both have similar body shape, one buccal cirrus, four to six transverse cirri, three dorsal kineties. Anteholosticha manca is distinguished from A. multicirrata by the absence (vs. presence) of the pretransverse cirri, the number of the AZM (21-27 vs. 30-40), frontoterminal cirri (2-4 vs. 5-7), left marginal cirri (22-29 vs. 33-49), right marginal cirri (6-34 vs. 38-56), and the color of the cortical granules (colorless vs. yellow-greenish). Anteholosticha warreni (Song and Wilbert, 1997) Berger, 2003 can be separated from A. multicirrata by the color of the cortical granules (colorless vs. yellow-greenish), the number of the frontoterminal cirri (2 vs. 5-7), mid-ventral pairs (7-9 vs. 14-21), transverse cirri (10-12 vs. 4-6), left marginal cirri (22-27 vs. 33- 49), and right marginal cirri (21-26 vs. 38-56). Anteholosticha australis (Blatterer and Foissner, 1988) Berger, 2003 is also compared to A. multicirrata by the color of cortical granules (colorless vs. yellow-greenish), the number of the macronuclear nodules (10-16 vs. 94-142), frontoterminal cirri (2 vs. 5-7), dorsal kineties (4 vs. 3), and the terrestrial (vs. marine) habitat.

14. Anteholosticha pulchra (Kahl, 1932) Berger, 2003 (Figs. 23, 24) Hong-saeg-yet-jeon-yeol-ha-mo-chung (홍색옛전열하모충)

Keronopsis pulchra Kahl, 1932, p. 573; Kahl, 1933, p. 109. Holosticha (Keronopsis) pulchra Berger, 2001, p. 36. Anteholosticha pulchra Berger, 2003, p. 377; Berger, 2006, p. 435; Li, Song and Hu, 2007, p. 113; Park, Jung and Min, 2012, p. 21; Park, Jung and Min, 2013, p. 569.

Size in vivo 190-300×30-55 μm. Body slender, flexible, not contractile, anterior and posterior ends rounded (Figs. 23A, 24A, B). Contractile vacuole approximately 10 μm in diameter, on left side of posterior 1/4 of cell (Figs. 23A, 24B, C, arrow). Cortical granules spherical and reddish, arranged at cirral bases and around dorsal bristles, some sparsely distributed throughout cell surface, about 1 μm across (Figs. 23B, C, 24D, arrow). Adoral zone of membranelles 46-60 and occupy 25-35% of body length, proximal portion covered with thick buccal lip. Midventral row extend to transverse cirri, composed of 27-34 pairs, and form a zigzag pattern. Food vacuoles colorless and scattered in cytoplasm. Four frontal cirri, ca. 18 μm-long (Figs. 23E, 24H), two frontoterminal cirri 10 μm-long, left to anterior end of right marginal row (Fig. 24H, arrowhead), and seven to nine transverse cirri 20 μm-long (Fig. 24E, J). One left and right marginal row with about 56 and 61 cirri, respectively. Buccal cirrus near paroral membrane (Fig. 24I, arrow). Caudal cirri absent. Four bipolar dorsal kineties (Fig. 24G, K, arrows). Approximate-

48 UROSTYLIDAE: Anteholosticha

FC DK FTC AZM PM BC EM

RMR LMR

A C D E

Fig. 23. Morphology of Anteholosticha pulchra from life (A-C) and after protargol impregnation (D, E). A, Ventral view showing the body shape, arrow denotes the contractile vacuole. B, C, Pattern of cortical granules in dorsal and ventral sides, reddish cortical granules (arrow); D, E, Ventral and dorsal views showing the infraciliature. AZM, adoral zone of membranelles; BC, buccal cirrus; DK, dorsal kineties; EM, endoral membrane; FC, frontal cirri; FTC, frontoterminal cirri; LMR, left marginal row; Ma, macronuclear nodules; MP, midventral pairs; PM, paroral membrane; RMR, right marginal row; TC, transverse cirri. Scale bars=100 μm (cited from Park et al., 2012).

ly 49 scattered macronuclear nodules (Figs. 23E, 24L).

Distribution: Korea, China (Laizhou, the Yellow Sea), Germany (Kiel, the Baltic Sea).

Korea: GG.

Specimen examined: GG: (Isolated from Incheon Harbor (salinity, 30.6‰; temperature, -0.6°C; 37°26ʹN, 126°35ʹE), Incheon, Korea: i.2011).

Habitat: Marine.

Remarks: Polyphyly of the genus Anteholosticha was shown by molecular phylogenetic analysis based

49 INVERTEBRATE FAUNA OF KOREA Ciliates

A B E F G

H I J K L

Fig. 24. Morphology of Anteholosticha pulchra from life (A-E) and after protargol impregnation (F-L). A, B, Ventral and dorsal views showing the body shape, the arrangement of cortical granules (arrowheads), and the contractile vacuole (arrow). C, D, Surface view of ventral and dorsal side showing the contractile vacuole (arrow in C) and the reddish cortical granules (arrow in D). E, Ventral view showing the transverse cirri. F-J, Ventral views showing the cirral pattern including the frontal cirri (arrows in H), frontoterminal cirri (arrowhead), the buccal cirri (arrow in I) and the pretransverse and transverse cirri. G, K, Dorsal view showing the four dorsal kineties. L, Macronuclear nodules (arrow). Scale bars=100 μm (cited from Park et al., 2012).

on the SSU rDNA. Therefore, this genus should be divided into subgroups according to the relativeness of both morphology and phylogeny (Berger, 2006; Gao et al., 2010; Yi and Song, 2011). Among ca. 40 species known from this genus, the morphology of the species A. gracilis, A. xanthichroma, A. australis, A. sig-

50 UROSTYLIDAE: Bakuella

moidea and A. monilata show closest relationship with Anteholosticha pulchra. Anteholosticha pulchra can be distinguished from these species by the position of contractile vacuole, i.e., around the posterior 1/4 of body in A. pulchra, in anterior 1/3 of body in A. gracilis; ahead of mid-body in A. xanthichroma, A. australis, A. sigmoidea and A. monilata (Foissner and Didier, 1981; Foissner, 1982; Wirns- berger and Foissner, 1987; Blatterer and Foissner, 1988; Hu and Suzuki, 2004). The most similar species to A. pulchra is A. gracilis because both are marine and have four frontal and two frontoterminal cirri. However, Anteholosticha pulchra differs from A. gracilis mainly in size (190-300×30-55 μm vs. 100-150×30-40 μm in vivo), position of contractile vacuole (posterior 1/4 vs. anterior 1/3 of body), color of cortical granules (reddish vs. yellow greenish), number of dorsal kineties (four vs. three) adoral membranelles (46-60 vs. 24- 30) and pair of midventral cirri (27-34 vs. 17-24) (Hu and Suzuki, 2004). The Korean population corresponds well with the Chinese population reported by Li et al. (2007), and show high similarity in morphometric characteristics.

Genus Bakuella Agamaliev and Alekperov, 1976 Ba-ku-ha-mo-chung-sok (바쿠하모충속)

Key to the species of genus Bakuella

1. Two frontoterminal cirri...... B. (P.) litoralis - More than two frontoterminal cirri...... B. (B.) incheonensis

Subgenus Bakuella (Bakuella) Agamaliev and Alekperov, 1976 Ba-ku-ha-mo-chung-a-sok (바쿠하모충아속)

15. Bakuella (Bakuella) incheonensis Jo, Jung and Min, 2015 (Figs. 25-27) In-cheon-ba-ku-ha-mo-chung (인천바쿠하모충)

Bakuella (Bakuella) incheonensis Jo, Jung and Min, 2015, p. 800.

Size in vivo 70-105×20-40 μm in, on average 82×37 μm in protargol preparations. Body slender to elliptical, flexible and slightly contractile; dorsoventrally flattened (Figs. 25A-C, 26A-D, F). Cell yellowish to colorless. Cortical granules mainly distributed along cirral rows and dorsal kineties; yellowish, spherical to slightly ellipsoidal, about 0.7×0.5 μm in dorsal view, while ellipsoidal and about 1.0×0.7 μm in lateral

51 INVERTEBRATE FAUNA OF KOREA Ciliates

FC AZM 3 FTC PM 2 EM 1 RMR BC

MP LMR

B PF Ma Mi MV

A C D E

Fig. 25. Morphology of Bakuella (Bakuella) incheonensis from life (A-C) and after protargol impregnation (D, E). A. Ventral view of a representative individual, arrow indicates the contractile vacuole. B, C. Ven- tral and dorsal view showing cortical granulation. D, E. Ventral and dorsal view of the holotype specimen, dotted circle marks the parabuccal cirrus, arrows indicate two dikinetids anterior to the right marginal row. AZM, adoral zone of membranelles; BC, buccal cirrus; EM, endoral membrane; FC, frontal cirri; FTC, frontoterminal cirri; LMR, left marginal row; Ma, macronuclear nodules; Mi, micronuclei; MP, midventral pairs; MV, midventral row; PF, pharyngeal fibers; PM, paroral membrane; RMR, right marginal row; TC, transverse cirri; 1-3, dorsal kineties. Scale bars=50 μm (cited from Jo et al., 2016).

view (Figs. 25B, C, 26D, F-H). On average 69 scattered, irregularly ellipsoidal macronuclear nodules, measuring 2.3-7.0×1.3-2.0 μm in protargol-impregnated specimens. About five oval micronuclei measuring 2.3-3.0×1.7-2.0 μm in stained specimens (Figs. 25E, 27D). Contractile vacuole on left side at about 40% of body length, 10-12 μm in diameter during diastole (Figs. 25A, 26C). Crawling moderately fast on bottom of Petri dish. Adoral zone about 34% (29-45%) of body length in protargol-impregnated specimens, with 21-25 membranelles; distal end extends only slightly on right margin forming a question mark as in other urostylids. Buccal cavity deep and moderately wide. Undulating membranes long, slightly curved; optically intersect-

52 UROSTYLIDAE: Bakuella

A B C

D E

F G H

Fig. 26. Photomicrographs of Bakuella (Bakuella) incheonensis from life. A-C. Ventral (A) and dorsal (B, C) views, showing elliptical body shape, arrow indicates the contractile vacuole. D, F. Distribution of the cortical granules on dorsal and ventral side. E. Ventral view of the anterior body portion, right frontal cirrus is marked by arrow and the single buccal cirrus by arrowhead. G. Dorsal bristles (arrows) and cortical granules. H. Lateral view of cortical granules (arrows) at cell margin. Scale bars =50 μm (cited from Jo et al., 2016).

ing at about mid-portion of paroral; paroral approximately three-quarters of endoral membrane length (Fig. 25D). All cirri relatively fine, mostly 10-13 μm long. Three enlarged frontal cirri (Figs. 25D, 26E), invariably one buccal cirrus on right side of paroral membrane (Figs. 25D, 26E) and one parabuccal cirrus (Fig. 25D, dotted circle). Three or four frontoterminal cirri near distal end of AZM (Figs. 25D, 27C). Midventral com-

53 INVERTEBRATE FAUNA OF KOREA Ciliates

A B D E

Fig. 27. Photomicrographs of Bakuella (Bakuella) incheonensis after protargol impregnation. A, B, Ven- tral and dorsal view of the holotype specimen, showing the entire cirral pattern, oral apparatus, and dorsal kineties. C, Ventral view of ciliature of the anterior body portion, arrowheads indicate frontoterminal cirri. D, Macronuclear nodule (arrow) and micronucleus (arrowhead). E, Close up of the anterior part of three dorsal kineties (arrows). Scale bars=50 μm (cited from Jo et al., 2016).

plex composed of 7-10 inconspicuously zigzagging midventral pairs with one or two midventral rows each comprising three or four cirri and terminating at about 62% of body length (Fig. 25D). Of the 19 examined specimens, 10 with one pretransverse cirrus, while others without cirrus (Fig. 25D, no pretransverse cirrus). Four or five transverse cirri protruding beyond rear end of body (Fig. 25D). One left and one right marginal row, consisting of 20-28 and 25-32 cirri, respectively (Fig. 25D). Marginal rows terminated at level of transverse cirri and not overlapped posteriorly. Three bipolar dorsal kineties (Figs. 25E, 27E); usually two dikinetids at anterior part of right marginal cirral row (Fig. 25E). Dorsal cilia 3-4 μm long in vivo. Caudal cirri lacking.

Distribution: Korea.

Korea: GG.

Specimen examined: GG: (Incheon (37°24030ʺN, 126°38043ʺE, salinity, 4.1‰; temperature, 26.9°C): 23.vi.2014).

Habitat: Brackish water.

Remarks: Two of the seven previously described species in the subgenus Bakuella have one buccal cirrus

54 UROSTYLIDAE: Bakuella

as in B. (B.) incheonensis: B. (B.) agamalievi Borror & Wicklow, 1983 and B. (B.) subtropica Chen et al., 2013. Here, we compare B.(B.) incheonensis to the previously described populations of B. agamalievi Borror and Wicklow, 1983 (Agamaliev, 1972, 1974; Mihailowitsch and Wilbert, 1990; Song et al., 2002; Berger, 2006). According to the combined data from two populations well described by Mihailowitsch and Wil- bert (1990) and Song et al. (2002; neotype population), B. (B.) agamalievi can be distinguished from B. (B.) incheonensis by body size (97-176×40-70 μm vs. 60-100×29-50 μm in protargol-impregnated specimens), number of adoral membranelles (26-37 vs. 21-25), frontoterminal cirri (4-7 vs. 3 or 4), midventral pairs (9-18 vs. 7-10), left and right marginal cirri (30-40 vs. 20-28 and 34-47 vs. 25-32, respectively), and cortical granules (colorless or slightly greenish vs. yellowish) (Mihailowitsch and Wilbert, 1990; Song et al., 2002). This excludes the type population (Agamaliev, 1972) because an inappropriate impregnation method was used, causing misinterpretation of its morphology (Berger, 2006). Bakuella (B.) subtropica is distinguished from B. (B.) incheonensis by body size (116-208×43-125 μm vs. 60-100×29-50 μm in protargol-impregnated specimens), number of adoral membranelles (25-44 vs. 21-25), frontoterminal cirri (4-12 vs. 3 or 4), midventral pairs (9-23 vs. 7-10), length of midventral complex (80% vs. 62% of body length), left and right marginal cirri (30-54 vs. 20-28 and 28-64 vs. 25-32, respectively), macronuclear nodules (68-144 vs. 58-87), and cortical granules (1-2 μm, yellow-brownish to yellowgreenish vs. 0.7 μm, yellowish) (Chen et al., 2013).

Subgenus Bakuella (Pseudobakuella) Alekperov, 1992 Yu-sa-ba-ku-ha-mo-chung-a-sok (유사바쿠하모충아속)

16. Bakuella (Pseudobakuella) litoralis Jo, Jung and Min, 2015 (Figs. 28, 29) Yeon-an-ba-ku-ha-mo-chung (연안바쿠하모충)

Bakuella (Pseudobakuella) litoralis Jo, Jung and Min, 2015, p. 802.

Size in vivo 90-125×30-40 μm, on average 89×36 μm in protargol preparations. Body slender to elliptical, flexible and slightly contractile, dorsoventrally flattened (Figs. 28A, E, F, 29A-D, J, K). Cell slightly yellowish at low magnification due to cortical granules. Two types of cortical granules: type I granules yellowish, larger and about 0.6×0.4 μm in size, oval in dorsal and lateral views (Fig. 29G-I) and type II granules yellowish to colorless, smaller and about 0.2 μm in diameter, subglobular in dorsal and lateral views (Fig. 29G-I). Both types form longitudinal rows along and between cirral rows and dorsal kineties (Figs. 28B-D, 29G-I). On average 67 irregularly ellipsoidal, scattered macronuclear nodules, measuring 2.8-8.0×1.9-2.3

55 INVERTEBRATE FAUNA OF KOREA Ciliates

FC 2 3 FTC AZM PM RMR 1 RMR EM BC LMR

PF Mi B C Ma MV

TC A D E F

Fig. 28. Morphology of Bakuella (Pseudobakuella) litoralis from life (A-D) and after protargol impregnation (E, F). A, Ventral view of a representative individual, arrow indicates the contractile vacuole. B-D, Ventral (B) and dorsal (C, D) views of cortical granulation. E, F, Ventral and dorsal view of the holotype specimen, arrows indicate pretransverse cirri, arrowhead shows cirrus between the midventral row and pretransverse cirri, the dotted circle marks parabuccal cirri. Nuclear apparatus in (F) was illustrated from an- other typical specimen because of faint impregnation of those of the holotype. AZM, adoral zone of membranelles; BC, buccal cirri; EM, endoral membrane; FC, frontal cirri; FTC, frontoterminal cirri; LMR, left marginal row; Ma, macronuclear nodules; Mi, micronuclei; MP, midventral pairs; MV, midventral rows; PF, pharyngeal fibers; PM, paroral membrane; RMR, right marginal row; TC, transverse cirri; 1-3, dorsal kineties. Scale bars=50 μm (cited from Jo et al., 2016).

μm in protargol-impregnated specimens (Figs. 28F, 29M). Three to eight spherical or oval micronuclei, measuring 1.7-2.0×1.3-2.0 μm in protargol-impregnated specimens (Figs. 28F, 29M, arrowhead). Contractile vacuole on left side of mid-body, about 12.5 μm in diameter (Figs. 28A, 29C, D, arrows). Crawling moderately fast on bottom of Petri dish. Adoral zone consists of 25-33 membranelles and extends to about 41% (27-49%) of body length. Distal end extends only slightly on right body margin forming a question mark as in other urostylids. Buccal cavity deep and moderately wide. Undulating membranes long, slightly curved; optically intersecting in mid-portion of paroral; paroral and endoral membranes almost equal in length (Fig. 28E). All cirri relatively fine, mostly 10-15 μm long in vivo. Three enlarged frontal cirri (Figs. 28E, 29L), three

56 UROSTYLIDAE: Bakuella

E F

A B C D G

H I

J K M N

Fig. 29. Morphology of Bakuella (Pseudobakuella) litoralis from life (A-I) and after protargol impregnation (J-N). A-D, Ventral (A) and dorsal (C-D) views of representative individuals, arrows indicate the contractile vacuole. E, Ventral view of the posterior body part to show the pretransverse (arrows) and transverse cirri. F, Dorsal bristles. G-I, Arrangement of type I (arrow) and type II (arrowhead) cortical granules on dorsal (G, I) and ventral (H) side. J, L, Ventral views showing the ventral cirral pattern, Arrows denote frontal cirri, arrowheads show the frontoterminal cirri. K, N, Dorsal views showing the dorsal kineties (arrows). M, The macronucleus (arrow) and micronucleus (arrowhead) nodules. Scale bars=50 μm (cited from Jo et al., 2016).

57 INVERTEBRATE FAUNA OF KOREA Ciliates

to five buccal cirri arranged in a longitudinal row right of paroral membrane (Fig. 28E). Two to four parabuccal cirri, arranged with two or three other cirri below rightmost frontal cirrus and no or one cirrus below first midventral cirral pair (Fig. 28E, dotted circle). Invariably two frontoterminal cirri near distal end of AZM (Figs. 28E, 29L). Midventral complex composed of 10-15 zigzagging midventral pairs with one or two midventral rows each comprising 3-5 cirri and terminating at about 70% of body length (Fig. 28E). Pe- culiarly, two out of 25 specimens lack midventral row, but no other differences from typical specimens. One or two pretransverse cirri ahead of 3-6 transverse cirri (Figs. 28E, 29E). All transverse cirri protruding beyond rear end of body. One or two cirri between midventral complex and pretransverse/transverse cirri in 23 out of 25 specimens (Fig. 28E). One left and one right marginal row, consisting of 26-39 and 29-47 cirri, respectively (Fig. 28E). Anterior part of right marginal cirral row on dorsal side (Fig. 28F). Marginal rows not connected or overlapped posteriorly. Three complete dorsal kineties (Figs. 28F, 29N, arrows); usually two dikinetids ahead of anterior part of right marginal row. Dorsal cilia 3-4 μm long in vivo. Caudal cirri lacking.

Distribution: Korea.

Korea: GG.

Specimen examined: GG: (Incheon (37°24048ʺN, 126°38026ʺE, salinity, 15.0 psu; temperature unavail- able): 16.xii.2012).

Habitat: Brackish water.

Remarks: Among the 10 species of Bakuella, only two species have been designated in the subgenus Pseudobakuella by Berger (2006): B. (P.) salinarum Mihailowitsch and Wilbert, 1990 and B. (P.) walibonensis Song et al., 1992. Bakuella nilgiri Kumar et al., 2010 was not designated in any subgenera in the original description, but it usually has two to four frontoterminal cirri (Kumar et al., 2010), suggesting that, it could be assigned to the subgenus Pseudobakuella; therefore, we compare it to B. (P.) litoralis as follows: habitat (soil vs. brackish water), body size (124-158×44-77 μm vs. 70-106×22-49 μm in protargol-impregnated specimens), number of adoral membranelles (42-54 vs. 25-33), transverse cirri (6-11 vs. 3-6), midventral pairs (18-23 vs. 10-15), length of midventral complex (extended to near transverse cirri vs. to 70% of body length), left and right marginal cirri (38-56 vs. 26-39 and 49-65 vs. 29-47, respectively), and cortical granules (one type, colorless vs. two types, yellowish or yellowish to colorless). Bakuella (P.) salinarum is clearly distinguished from B. (P.) litoralis by body size (272-348×87-145 μm vs. 70-106×22-49 μm in protargol-impregnated specimens), number of AZM (47-63 vs. 25-33), buccal cirri (6-8 vs. 3-5), transverse cirri (7-12 vs. 3-6), midventral pairs (22-38 vs. 10-15), midventral rows (13-21 vs. 1 or 2), length of midventral complex (terminated close to transverse cirri vs. at 70% of body length), left and right marginal cirri (45-60 vs. 26-39 and 55-66 vs. 29-47, respectively), and macronuclear nodules (more than 100 vs. 49-84) (Mihailowitsch and Wilbert, 1990).

58 UROSTYLIDAE: Birojimia

Bakuella (P.) walibonensis can be discriminated from B. (P.) litoralis by body size (180-229×62-83 μm vs. 70-106×22-49 μm in protargol impregnated specimens), buccal cirri (5 or 6 vs. 3-5), length of midventral complex (54% vs. 70% of body length), pretransverse cirri (absent vs. present), left and right marginal cirri (42-50 vs. 26-39 and 51-66 vs. 29-47, respectively), posterior part of marginal rows (slightly overlapped vs. clearly separated), and macronuclear nodules (more than 100 vs. 49-84) (Mihailowitsch and Wilbert, 1990; Song et al., 1992).

Genus Birojimia Berger and Foissner, 1989 Bi-ro-ji-ma-ha-mo-chung-sok (비로지마하모충속)

17. Birojimia soyaensis Kim, Jung and Min, 2016 (Figs. 30-32) So-ya-bi-ro-ji-ma-ha-mo-chung (소야비로지마하모충)

Birojimia soyaensis Kim, Jung and Min, 2016, p. 136.

Size in vivo 170-200 μm×40-50 μm, with an average of 184.9 μm×42.1 μm in protargol-impregnated specimens. Body outline usually elongate elliptical, and somewhat twisted at right margin, slightly flexible, colorless to slightly grayish at low magnification (Figs. 30A, 31A-C). Macronuclear nodules size 3-9 μm×2-6 μm in vivo (on average 6.5 μm×4 μm in protargol-impregnated specimens), 53-69 in number, distributed in cytoplasm, except in anterior and posterior portion of cell. Two or three, oval to spherical micronuclei, about 5×4 μm in protargol-impregnated specimens (Figs. 30C, 31I, 32A). Cortical granules colorless, 0.4-1.2 μm across in surface view, rod-shaped in lateral view, average size in vivo 3.0 μm×1.0 μm, irregularly distributed, partially in longitudinal lines on ventral side, sparsely arranged in short longitudinal rows on dorsal side (Figs. 30D-F, 31D, F, J). Contractile vacuole in mid-body, left to midline, about 15 μm in diameter when fully extended, dividing into 2 collecting canals (Fig. 31B, C). Adoral zone composed of 37-48 membranelles, about 25-35% of body length in protargol-impregnated specimens. Bases of largest membranelles about 8 μm wide, AZM slightly curved like a “question mark” (Figs. 30B, 32A, B). Paroral and endoral membranes slightly curved, crossing each other (Figs. 30B, 32B). Pharynx conspicuous in stained specimens, with 2-3 μm short rods (Figs. 30B, 32D). Frontal and transverse cirri about 12 μm long, and other cirri about 9-10 μm long (Figs. 31A, B, D, H). Three enlarged frontal cirri, 2 frontoterminal cirri, III/2 and buccal cirrus present (Figs. 30B, 32B). Midventral complex composed of 13-17 midventral cirral pairs only, commencing close to cirrus III/2 (Figs. 30B, 32A, B). One left and four right marginal rows, including three compound ones with bristles anteriorly and cirri posteriorly on right margin; inner right marginal cirral row and left marginal cirral rows (LMR) composed of cirri only; LMR

59 INVERTEBRATE FAUNA OF KOREA Ciliates

FC DK5 FTC III/2 AZM 1 1 EM 2 BC DK2 2 PM DK1 DK4 3 D 3 Mi

DK3 4

4 Ma MP caudal cirrus on LMR ventral side caudal cirrus on dorsal side DK5 dorsal bristle row PTC cirral row on CC dorsal side TC cirral row on CC ventral side A B C E F G

Fig. 30. Morphology of Birojimia soyaensis from life (A, D-F) and after protargol-impregnation (B, C, G). A, Ventral view of a representative specimen showing the body shape and the cirral pattern. B, C, Ventral and dorsal view of the holotype specimen, showing the infraciliature and the nuclear apparatus, arrow indicates the pharyngeal fibers. D, Cortical granules (arrow) and dorsal cilia (arrowhead); E, F, Ventral and dorsal view showing the cortical granules arrangement. G, Ciliary pattern of cirral rows and dorsal kineties. AZM, adoral zone of membranelles; BC. buccal cirrus; CC, caudal cirri; DK1-5, dorsal kineties; EM, endoral membrane; FC, frontal cirri; FTC, frontoterminal cirri; LMR, left marginal cirral row; Ma, macronuclei; Mi, micronuclei; MP, midventral pairs; PM, paroral membrane; PTC, pretransverse ventral cirri; TC, transverse cirri; 1, inner right marginal cirral row; 2-4, compound rows. Scale bars=100 μm (cited from Kim et al., 2016a).

extends to center of rear body margin as J-shape. One or two pretransverse and four to eight transverse cirri (Figs. 30B, C, G, 32A-C, E, F). Eight dorsal kineties with cilia approximately 3-4 μm long in vivo, five long dorsal kineties (DK) associated with caudal cirri at rear end of cell; three shortened kineties associated with right marginal rows (compound rows) (Figs. 30B, C, F, 31G, 32A, C, E, F). Two bipolar kineties (DK1, DK2) and 3 shortened rows (rows 1 to 3) commencing from the anterior portion, while DK 3 to 5 and row 4 commencing near midbody, between DK 2 and row 3; 2 bipolar DK1 and 2 extending along left body margin (Figs. 30C, G, 32E). First and fifth dorsal kineties associated with 3 or 4 caudal cirri, second to fourth kineties combined with 1 or 2 caudal cirri. Eight to eleven caudal cirri, approximately 11 μm long in vivo

60 UROSTYLIDAE: Birojimia

A B C E

F G I J

Fig. 31. Photomicrographs of Birojimia soyaensis from life. A, D, E, Ventral views showing the body shape and the cirral pattern, arrow marks the inner right cirral row, arrowhead indicates a longitudinal row of cortical granules. B, C, Dorsal views showing the contractile vacuole and the collecting canals (arrows) F, J, Dorsal and marginal view showing the surface (arrows in F) and the lateral view of the cortical granules. G, The dorsal bristles (arrow). H, The caudal cirri in posterior body region (arrows). I - Macronuclear (arrow) and micronuclear (arrowhead) nodule; Scale bars=100 μm (cited from Kim et al., 2016a).

61 INVERTEBRATE FAUNA OF KOREA Ciliates

3 2 4 FC 1

DK5 PTC 1 III/2 FTC PM 2 EM AZM MP BC 3 LMR CC

B C 4

1 DK1

DK2 DK5 PF DK5 2 DK1 DK3 DK2 DK4 DK4 3 DK3 4 CC A D E F

Fig. 32. Photomicrographs of Birojimia soyaensis after protargol impregnation. A-D, Ventral views of the holotype specimen, showing the cirral pattern, the nuclear apparatus and the pharyngeal fibers. Note the testate amoeba inside a food vacuole. E, F, Anterior and posterior portion of dorsal side. AZM, adoral zone of membranelles; BC, buccal cirrus; CC, caudal cirri; DK, dorsal kineties; EM, endoral membrane; FC, frontal cirri; FTC, frontoterminal cirri; LMR, left marginal cirral row; Ma, macronuclei; Mi, micronuclei; MP, midventral pairs; PM, paroral membrane; PTC, pretransverse ventral cirri; TC, transverse cirri; 1, inner right marginal cirral row; 2-4, compound rows (cited from Kim et al., 2016a).

(Figs. 30C, 31H, 32F). Feeds on fungi, testate amoebae, soil particles, and small protozoa (Fig. 32A).

Distribution: Korea.

Korea: GG.

Specimen examined: GG: (Wetland soil on Soya Island, South Korea, 37°12ʹ N and 126°10ʹ E).

Habitat: Soil.

Remarks: Birojimia comprises two soil ciliates, B. terricola and B. litoralis (Foissner, 2016) with features typical of the Holostichidae, i.e., 3 frontal cirri and midventral pairs only. The Holostichidae applies to more

62 UROSTYLIDAE: Metaurostylopsis

than one category, a superfamily (Jankowski, 1979) and a subfamily (Borror and Wicklow, 1983). However, Berger (2006) used the name “Holostichidae” without any categories. Birojimia litoralis can be separated from B. soyaensis using body size (179-251 μm×40-65 μm vs. 146- 213 μm×33-65 μm); lithosome in cytoplasm (present vs. absent); number of frontoterminal cirri (2-3 vs. invariable 2); number of macronuclear nodules (116-210 vs. 53-69); number of left marginal cirral rows (2 vs. 1); number of dorsal kineties (8-11, invariable 8). However, the dorsal structure is similar between the two Birojimia species, i.e., bipolar 1 and 2 dorsal kineties extend to the posterior end of the body, and several dorsal kineties commence near the mid-body (Foissner, 2016). Berger and Foissner (1989) missed the cortical granules of the type species, B. terricola, although the granules were found in deeply stained specimens (Foissner, 2016). Birojimia soyaensis also has the cortical granules. The granules of B. terricola differ from those of B. soyaensis as follows: shape (broadly ellipsoid to lenticular vs. mostly spherical), size (2-3 μm×1-2 μm vs. 0.4-1.2 μm in diameter), and pattern of distribution (within and between cirral and bristle rows vs. irregularly distributed, partially in longitudinal rows) (Foissner, 2016). Cortical granules are important characteristics for classifying ciliates (Gong et al., 2001; Lei et al., 2005; Berger, 2006). Furthermore, caudal cirri (CC) in B. soyaensis are more numerous than those in B. terricola (8-11 vs. 2-7 in the Japanese population) (Berger and Foissner, 1989; Berger, 2006; Foissner, 2016) (Figs. 30C, 32E, F). However, futher study is necessary to convince the cortical granuation of H. terricola in vivo.

Genus Metaurostylopsis Song, Petz and Warren, 2001 Cho-mi-ju-ha-mo-chung-sok (초미주하모충속)

Key to the species of genus Metaurostylopsis

1. Smaller cortical granules colorless...... M. cheni - Smaller cortical granules reddsh...... M. struederkypkeae

18. Metaurostylopsis cheni Chen, Huang and Song, 2010 (Figs. 33, 34) Chaen-ssi-cho-mi-ju-ha-mo-chung (챈씨초미주하모충)

Metaurostylopsis cheni Chen, Huang and Song, 2011, p. 100; Kim, Park, Jung and Min, 2016, p. 469.

Size in vivo 90-120×43-50 μm. Body ellipsoidal with convex margins, flexible and yellow to greenish (Figs. 33A, 34A, C). Two types of cortical granules: large granules of oval shape, yellow to green in color,

63 INVERTEBRATE FAUNA OF KOREA Ciliates

ca. 1.5 μm across, and distributed along cirral rows and dorsal kineties; small colorless granules, irregularly scattered, ca. 0.3 μm across (Fig. 34D, F). About 57 macronuclear nodules. Three frontal and three to five frontoterminal cirri; buccal and III/2 cirrus present; five to eight transverse cirri; seven to eleven midventral pairs, additional three to five unpaired ventral cirri in a longitudinal row; three to four left and right marginal rows, first and second right marginal rows commence dorsally; three bipolar dorsal kineties and additional two dikinetids ahead of first right marginal row, dorsal cilia 3-5 μm long in vivo; caudal cirri lacking (Figs. 33B, C, 34G, H).

Distribution: Korea, China.

Korea: GG, GN.

FC AZM DK FTC PM EM MP

RMR

LMR Ma

TC A B C

Fig. 33. Morphology of Metaurostylopsis cheni from life (A) and after protargol impregnation (B, C). A, Ventral view of a typical specimen; B, C, Cirral base in ventral and dorsal views; AZM, adoral zone of membranelles; DK, dorsal kineties; EM, endoral membrane; FC, frontal cirri; FTC, frontoterminal cirri; LMR, left marginal row; Ma, macronuclear nodules; MR, midventral rows; MP, midventral pairs; PM, paroral membrane; RMR, right marginal row. TC, transverse cirri. Scale bars=50 μm (cited from Kim et al., 2016b).

64 UROSTYLIDAE: Metaurostylopsis

Specimen examined: GN: (Mokpo Harbor (salinity, 21‰; 34°47ʹN, 126°23ʹE): vi.2011) and GG: (Yongyu- dong, Incheon (salinity, 30‰; 37°26ʹN 126°24ʹE): iii.2015).

Habitat: Marine.

Remarks: There are six species in this genus: the type species Metaurostylopsis marina Song et al., 2001;

D CV

A B C E

3 2 RMR 1 FC AZM III/2

LMR FTC

BC MP

TC F G H I

Fig. 34. Photomicrographs of Metaurostylopsis cheni from life (A-F) and after protargol impregnation (G-I). A, B, C, ventral views showing the body shape, the cirral pattern and the contractile vacuole. D, E, F, Dis- tribution of large cortical granules (arrowhead in E) and small cortical granules (arrowheads in F), arrow denotes marginal cirri in E and dorsal bristles in F. G, H, Ventral and dorsal views showing the ciliary pattern, arrows mark the two dikinetids anterior to the first right marginal row on dorsal surface. I, Anterior region of ventral surface showing the frontal, frtontoterminal, buccal cirri. AZM, adoral zone of membranelles; BC, buccal cirrus; FC, frontal cirri; FTC, frontoterminal cirri; LMR, left marginal row; MP, midventral pairs; RMR, right marginal row; TC, transverse cirri; 1-3, dorsal kineties 1-3. Scale bars=100 μm (cited from Kim et al., 2016b).

65 INVERTEBRATE FAUNA OF KOREA Ciliates

M. rubra Song & Wilbert, 2002; M. salina Lei et al., 2005; M. struederkypkeae Shao et al., 2008; M. cheni Chen et al., 2011; and M. antarctica Jung et al., 2011b (Song et al., 2001; Berger, 2006; Shao et al., 2008b; Chen et al., 2011a; Jung et al., 2011b; Lu et al., 2016). We used the morphometric data of the Mokpo population to make comparisons with congeners. Metaurostylopsis cheni differs from M. struederkypkeae in the color of the cortical granules (yellowish to greenish vs. reddish) and in the number of frontoterminal cirri (3-5 vs. 4-8), midventral pairs (7-11 vs. 12- 20), cirri in midventral row (3-5 vs. 6-9) and in left marginal rows (3-4 vs. 5-7 in). Metaurostylopsis cheni and M. antarctica both have two types of cortical granules. However, Metaurosty- lopsis cheni can be separated from M. antarctica by the number of transverse cirri (5-8 vs. 2), left marginal rows (3-4 vs. 2), and right marginal rows (3-4 vs. 1).

19. ‌Metaurostylopsis struederkypkeae Shao, Song, Al-Rasheid, Yi, Chen, Al-Farraj and Al-Quraishy, 2008 (Figs. 35, 36) Jag-eun-hong-saek-cho-mi-ju-ha-mo-chung (작은홍색초미주하모충)

Metaurostylopsis struederkypkeae Shao, Song, Al-Rasheid, Yi, Chen, Al-Farraj and Al-Quraishy, 2008, p. 289; Park, Jung and Min, 2012, p. 25. Metaurostylopsis parastruederkypkeae Lu, Wang, Huang, Shi and Chen, 2016, p. 874.

Size in vivo 80-110 ×40-50 μm. Body slender with anterior and posterior ends rounded; slightly contractile (Figs. 35A, 36A-C). Contractile vacuole approximately 10 μm in diameter on left side of mid-body (Fig. 36C, arrow). Two types of cortical granules: one small and reddish, approximately 0.5 μm across, spread irregularly on surface (Figs. 35B, C, 36D, arrowhead), and other type yellow green, approximately 1.5 μm across, at base of cirri, clustered along cirral rows and dorsal bristles (Figs. 35B, C, 36D, arrow). Cells appear reddish under low magnification due to cortical granules. Macronuclear nodules, ovoid and ellipsoid shape, ca. 82 in number. Lengths of transverse and frontal cirri 15 μm and 13 μm, respectively. Other somatic cirri ca. 10 μm long. Four frontal cirri and four to eight frontoterminal cirri near distal portion of AZM (Fig. 36H, arrow). Two to six transverse cirri and one buccal cirrus near middle of paroral membrane (Fig. 36H, arrowhead). Five to seven left and three to five right marginal rows (Fig. 36F). 12-20 midventral pairs, and six to nine unpaired midventral cirri between midventral pairs and transverse cirri. Three dorsal kineties (Fig. 36G, arrows), and two other dikinetids ahead of rightmost right marginal row on dorsal side (Fig. 36G, arrowheads). Adoral membranelles 25-36 in number and AZM ca. 35-45% in length. Paroral and endoral membrane equal in length.

Distribution: Korea, China.

66 UROSTYLIDAE: Metaurostylopsis

FC AZM FTC PM EM DK

MVR B

RMR

Ma LMR TC A C D E F G

Fig. 35. Morphology of Metaurostylopsis struederkypkeae from life (A-C) and after protargol impregnation (D-G). A, Ventral view showing the contractile vacuole (arrow). B, C, Ventral and dorsal surface view showing the large, yellow green cortical granules (arrow) and the small reddish cortical granules (arrowhead); D, E, Ventral and dorsal view showing the arrangement of the yellow green cortical granules; F, G, Cirral base on ventral and dorsal side. AZM, adoral zone of membranelles; DK, dorsal kineties; EM, endoral membrane; FC, frontal cirri; FTC, frontoterminal cirri; LMR, left marginal row; Ma, macronuclear nodules; MP, midventral pairs; MVR, midventral row; PM, paroral membrane; RMR, right marginal row; TC, transverse cirri. Scale bars=50 μm (cited from Park et al., 2012).

Korea: GW.

Specimen examined: GW: (Youngrang (salinity, 14.8‰; temperature, 18.3°C; 38°13ʹN, 128°35ʹE), Sok- cho, Korea: vi.2011).

Habitat: Marine.

Remarks: Metaurostylopsis struederkypkeae is similar to M. rubra in having reddish cell color. How- ever, M. struederkypkeae is distinguished from M. rubra by the body size (80-110 ×40-50 μm vs. 150- 300×50-90 μm in vivo), the number of right marginal rows (3-5 vs. 6-7), and the types of cortical granules (two vs. one) (Song and Wilbert, 2002). Metaurostylopsis struederkypkeae is distinguished from M. marina by the body shape (slender vs. oval), the cell color (reddish vs. colorless), and the types of cortical granules (two vs. one) (Song et al., 2001). The Korean population of M. struederkypkeae corresponds well with the original description of Shao et al. (2008b). However, the Korean population differs from the Chinese population by the higher number of left and right marginal rows, midventral pairs, and macronuclear nodules (Shao et al., 2008b). Because of

67 INVERTEBRATE FAUNA OF KOREA Ciliates

A B C

F G H E

Fig. 36. Photomicrographs of Metaurostylopsis struederkypkeae from life (A-D) and after protargol impregnation (E-H). A-C, Ventral (A, C) and dorsal (B) view showing the body shape, arrow marks the contractile vacuole; D, Large yellow green cortical granules (arrow) and small reddish cortical granules (arrowhead). E, F, H, Ventral views showing the cirral pattern, arrowhead marks the buccal cirrus and arrow denotes the frontoterminal cirri. G, Dorsal view showing the typically three dorsal kineties (arrows) and two dikinetids (arrowheads) ahead of right marginal row. Scale bars=50 μm (cited from Park et al., 2012).

these differences, Lu et al. (2016) established a new species M. parastruederkypkeae and considered the Ko- rean population a junior synonym of the new species. However, M. parastruederkypkeae slightly overlaps the morphological attributes with M. struederkypkeae, and the Korean population has smaller size than M. parastruederkypkeae (80-110 ×40-50 μm vs. 165-200×45-60 μm in vivo). Therefore, here we refrain the synonymization of the Korean population.

68 UROSTYLIDAE: Pseudoamphisiella

Genus Pseudoamphisiella Song, 1996 Wi-yang-yeol-ha-mo-chung-sok (위양열하모충속)

20. ‌Pseudoamphisiella alveolata (Kahl, 1932) Song and Warren, 2000 (Figs. 37, 38) Yu-mag-wi-yang-yeol-ha-mo-chung (유막위양열하모충)

Holosticha alveolata Kahl, 1932, p. 581. Holosticha alviolata Carey, 1992, p. 181. Pseudoamphisiella alveolata Song and Warren, 2000, p. 453; Hu and Suzuki, 2006, p. 44; Shao, Song, War- ren, Al-Rasheid, Yi and Gong, 2006, p. 389; Jung and Min, 2009, p. 233.

Size in vivo 100-213×50-78 μm, usually 135×67 μm. Body generally elongate and contractile, thus

EM AZM FC PM BC RMR LMR Ma

VR2 Mi VR1

DK TC

A B CC C

Fig. 37. Morphology and infraciliature of Pseudoamphisiella alveolata from life (A) and after protargol impregnation (B, C). A, Ventral view showing the body shape, the cirral pattern and the alveolar seam. B, C, Infraciliature of ventral and dorsal side, arrows show extra right marginal cirri. AZM, adoral zone of membranelles; BC, buccal cirri; DK, dorsal kineties; EM, endoral membrane; FC, frontal cirri; LMR, left marginal row; Ma, macronuclear nodules; Mi, micronucleus; PM, paroral membrane; RMR, right marginal row; TC, transverse cirri; VR1, 2, ventral rows. Scale bar=60 μm (cited from Jung and Min, 2009).

69 INVERTEBRATE FAUNA OF KOREA Ciliates

B C

AZM

VR1

VR2 Ma RMR Mi LMR

E G TC

F EM

I J K

70 UROSTYLIDAE: Pseudoamphisiella

variable in shape and size, extended shape in motion resembling a sigmoid; contracted cells oval (Fig. 37A-C); dorsoventrally flattened. Cell surface covered by conspicuous alveolar seam, 3-4 μm in depth, with small, bar-like extrusomes sparsely arranged, ca 1.5×0.5 μm (Figs. 37A, 38A, C-E, arrow); extrusome-linkage forming a cell surface polygon (Fig. 38D). Neither CV nor food vacuoles observed in cytoplasm. Adoral zone of membranelles distinct, about 1/3 of cell length, composed of about 58 membranelles (Figs. 37A, B, 38C, G, H); cilia of adoral membranelles short, ca 7-10 μm long. Two elongated Ma in center of body, 19-32×14-21 μm in size (Figs. 37C, 38G, H). Two to seven scattered Mi, about 4 μm in diameter (Fig. 38H, J). Three distinct FC, near AZM (Fig. 37B). Two BC (Fig. 38G, K). VR2 parallel to RMR, lying hor- izontally derived from the ventral groove; anterior VR1 close to rightmost FC; cirri of VR1, ca 6-8 μm in length (Fig. 38G). LMR, CC, and extra marginal cirri arranged in the same line, which makes it difficult to distinguish one from the other (Fig. 37B, arrows, extra marginal cirri). TC highly developed and arranged in a J-shaped row. Dorsal kineties bipolar and curved anteriorly (Fig. 37C); two to three kineties on the lateral side for protargol-impregnated specimens (Fig. 37B); dorsal cilia about 3 μm long.

Distribution: Korea, China, Germany, Japan.

Korea: GG.

Specimen examined: GG: (the Incheon harbor: 24.vii.2008).

Habitat: Marine.

Remarks: Pseudoamphisiella Song, 1996 has a unique cirral pattern: the origin of the right marginal cirri and the absence of FT distinguish it from other hypotrichs (Song, 1996; Song et al., 1997). Song et al. (1997) suggested a new family, Pseudoamphisiellidae. Although Berger (2006) and Lynn (2008) assigned this genus to Urostylidae, systematic positioning based on molecular analyses showed that Pseudoamphisiellidae clustered away from Urostylidae. The issue, therefore remains unclear (Shao et al., 2006; Yi et al., 2008). Pseudoamphisiella alveolata has two conspicuous Ma that can easily be separated from the two congeners: P. lacazei has 25-47 Ma and lacks the alveolar seam, whereas P. quadrinucleata has four Ma. Kahl (1932) described P. alveolata with sufficient morphological features for identification, matching well the present population, mainly in terms of its conspicuous alveolar seam, the two Ma, the three FC, the two

Fig. 38. Morphology and infraciliature of Pseudoamphisiella alveolata from life (A-F) and after protargol impregnation (G-K). A, C, E, Ventral views showing the body shape and the alveolar seam (arrow). B, D, Dorsal views. Note the cortical granules form polygonal structures. F, The macronucleus. G, H, K, Infracil- iature of ventral side, arrows mark extra right marginal cirri. I, Dorsal side showing the dorsal kineties (arrows). J, Macronucleus and micronucleus. Scale bars=60 μm (cited from Jung and Min, 2009).

71 INVERTEBRATE FAUNA OF KOREA Ciliates

BC, and the well-developed J-shaped TC. Furthermore, the present population has a longer body (149 vs. 96.6 μm) and a higher number of left marginal cirri (24.7 vs. 17) compared to the Chinese population (Song and Warren, 2000).

Family Kahliellidae Tuffrau, 1979 Manh-eun-bok-geug-mo-yeol-gwa (많은복극모열과)

Size, medium to large; shape, elongate ovoid; free-swimming; somatic ventral ciliature with at least two, typically more than two, ventral cirral files, often not distinctly different from right and left marginal cirral files; ventral cirral files may be preserved through a variable number of cell divisions (=cell generations) before being resorbed and replaced through additional new (=neokinetal) anlagen; transverse cirri, typically absent; caudal cirri, typically absent; dorsal ciliature as several files of dikinetids; oral ciliature as for order with paroral and endoral; macronucleus, two to many nodules; micronuclei, several to many; contractile vacuole, present; cytoproct, likely present; feeding on bacteria, microalgae, and smaller protists; in marine, freshwater, and terrestrial habitats.

Genus Pseudouroleptus Hemberger, 1985 Yu-sa-dan-mi-ha-mo-chung-sok (유사단미하모충속)

21. Pseudouroleptus jejuensis Jung, Park and Min, 2014 (Figs. 39-41) Je-ju-yu-sa-dan-mi-ha-mo-chung (제주유사단미하모충)

Pseudouroleptus jejuensis Jung, Park and Min, 2014, p. 196.

Size in vivo 220-300×35-55 μm in raw cultures, usually about 260×45 μm in environmental samples; posterior body portion usually slightly curved rightwards in protargol preparations. Length:width ratio in vivo moderately variable (5.4-6.3:1). Body cylindrical to elliptical with tail-like posterior portion (Figs. 39A, B, D, 40A, H); body shape straight in fast-moving behavior and slightly sigmoidal when feeding (Fig. 40H). Invariably, two ellipsoidal macronuclear nodules on left of midline behind buccal vertex, on average 25×8 μm in protargol-impregnated specimens. Two to four ellipsoidal micronuclei near or attached to macronuclear nodules, on average 6×4 μm in silver preparations (Figs. 39A, 40D, 41I). Contractile vacuole slightly above mid-body, without distinct collecting canals, on average 18×13 μm when fully extended (Figs.

72 KAHLIELLIDAE: Pseudouroleptus

1 2 3 AZM RMR PM BC 5

RFVR G EM G

4 LFVR

RFVR

LMR RMR

CC A D E F

Fig. 39. Pseudouroleptus jejuensis from life (A-D) and after protargol impregnation (E, F). A, Ventral view of a representative specimen, arrow indicates contractile vacuole. B, C, Arrangement of cortical granules on dorsal side and cell margin. D, Ventral view of a specimen gliding for feeding, showing a slightly curved body shape. E, F, Dorsal and ventral views of the holotype specimen. Arrow denotes postperistomial ventral cirrus. AZM, adoral zone of membranelles; BC, buccal cirrus; CC, caudal cirri; 1-5, dorsal kineties 1-5; EM, endoral membrane; G, cortical granules; LFVR, left frontoventral row; LMR, left marginal row; PM, paroral membrane; RFVR, right frontoventral row; RMR, right marginal row. Scale bars =100 μm (cited from Jung et al., 2014).

39A, 40A). Cortex flexible; cortical granules densely arranged in narrow vertical stripes, colourless, about 1.3 μm in diameter (Figs. 39B, C, 40E, G, I, J). Cytoplasm colourless, with 8-16 μm-sized food vacuoles usually in posterior half of cell. Feeds on bacteria, testate amoebae, diatoms, and organic soil particles. Glides moderately fast on bottom of Petri dish.

73 INVERTEBRATE FAUNA OF KOREA Ciliates

D E

A B C F G

I J

Fig. 40. Pseudouroleptus jejuensis from life. A-C, H, Dorsal (A, B) and ventral (C, H) views, arrow marks the contractile vacuole. D, Ventral view showing macronucleus (arrow) and micronucleus (arrowhead). E, G, I, J, Cortical granules (arrows) of dorsal side (E, I), ventral side (J), and body margin (G); dorsal bristles (double arrowhead) and postperistomial cirrus (arrowhead) denoted in J. F, Caudal cirri in dorsal view. CC, caudal cirri. Scale bars=130 μm (cited from Jung et al., 2014).

74 KAHLIELLIDAE: Pseudouroleptus

5 C

A B E F MI MI MI CC CC CC

CC CC CC MA MA G H I J

Fig. 41. Pseudouroleptus jejuensis during interphase (A-D, G-I) and ontogenesis (E, F, J) after protargol impregnation. A-C, Dorsal view (A) and ventral views (B, C), arrow indicates postperistomial cirrus. D, Dorsal view showing basal bodies (asterisks) in dorsal kinety 4. E, F, Dorsal views of late dividers, asterisks denote dorsal kinety 4 developed by multiple fragmentation of dorsal kinety anlage (DK) 3. G, H, J, Dorsal views showing caudal cirri developed from DK 1, 2 while DK 3 does not participate in the formation of these caudal cirri during ontogenesis; I - ventral view showing macronuclear nodules and micronuclei. CC, caudal cirri; MA, macronuclear nodules; MI. micronuclei. Scale bars=100 μm (cited from Jung et al., 2014).

75 INVERTEBRATE FAUNA OF KOREA Ciliates

All cirri, except for frontal and buccal cirri, 15-20 μm long in vivo; frontal and buccal cirri 18-25 μm long in vivo, and composed of distinctly more basal bodies than other cirri (Figs. 39F, 40B). Marginal and frontoventral cirri similar-sized and evenly spaced within the rows, but the intervals and size becoming slightly wider and smaller, respectively, at posterior body portion (Fig. 39F). Right marginal and right frontoventral row commence on dorsal side. Dorsal bristles 3-4 μm long in vivo, 5 dorsal kineties; dorsal kinety 3 multiple-fragmented and not associated with forming caudal cirri; dikinetids of dorsal kinety 4 sparsely arranged in a row and rarely appearing in 2 rows because of the scattered distribution pattern; here we considered them as a single row (Figs. 39E, 41D-F). Four to seven caudal cirri developed from dorsal kineties 1 and 2 (Fig. 41G, H, J). Late dividers observed and support the above features (Fig. 41E, F, J). Oral apparatus oxytrichid pattern (Berger, 1999), i.e., undulating membranes Oxytricha pattern (optically crossing at posterior half) and adoral zone of membranelles 30% of body length on average; shaped like a question mark, largest membranelles about 10 μm wide in vivo and in protargol impregnation; cilia about 15-20 μm long in vivo. Buccal lip distinct (Fig. 40C) and very likely angular (for review of oral apparatus, see Foissner and Al-Rasheid (2006)).

Distribution: Korea.

Korea: JJ.

Specimen examined: JJ: (Soil with the litter of tree, Jeju Island, South Korea, N33°18ʹ22ʺ E126°15ʹ42ʺ).

Habitat: Soil.

Remarks: Pseudouroleptus caudatus is the sole species in the genus and consists of two subspecies (for review of the genus Pseudouroleptus, see Berger, 2008): Pseudouroleptus caudatus caudatus Hemberg- er, 1985 and P. caudatus namibiensis Foissner, Agatha and Berger, 2002. Pseudouroleptus jejuensis differs from these subspecies mainly by the number of dorsal kineties, which include an additional dorsal kinety in comparison with the other two subspecies. The detailed comparison is discussed below. Pseudouroleptus caudatus caudatus is the nominotypical subspecies and the most similar taxon to P. jejuensis. However, they can be separated from each other by the number of dorsal kineties (4 vs. 5) the development of caudal cirri from dorsal kinety 3 anlage (present vs. absent), and the number of the caudal cirri (one in dorsal kinety 1 vs. 3-5 in kineties 1 and 2 (Hemberger, 1982; Berger, 1999; Küppers and Claps, 2013; Jung et al., 2014). Pseudouroleptus caudatus namibiensis can be distinguished from P. jejuensis by having fewer adoral membranelles (33-51 vs. 52-62), right frontoventral cirri (20-31 vs. 46-58), dorsal kineties (4 vs. 5), and caudal cirri (1-4 vs. 4-7). The right frontoventral row is distinctly shorter in P. caudatus namibiensis than in P. jejuensis; this difference in length results in the different number of cirri. The ontogenesis is almost identical in both P. caudatus caudatus and P. jejuensis with the exception of the following characteristics: i) the number of caudal cirri developed from dorsal kineties 1 and 3; and ii) the

76 UROSTYLIDAE: Arcuseries

number of dorsal kineties developed from dorsal kinety 3. Although Hemberger (1982) described these numbers of P. caudatus caudatus in the text without providing any illustrations.

Incertae sedis in order Urostylida

Genus Arcuseries Huang, Chen, Song and Berger, 2014 Hwin-hoing-geug-mo-chung-sok (휜횡극모충속)

22. ‌Arcuseries petzi (Shao, Gao, Hu, Al-Rasheid and Warren, 2011) Huang, Chen, Song and Berger, 2014 (Fig. 42) Pe-cheu-ssi-hwin-hoing-geug-mo-chung (페츠씨휜횡극모충)

Anteholosticha petzi Shao, Gao, Hu, Al-Rasheid and Warren, 2011, p. 255; Kim, Jung and Min, 2013, p. 145. Arcuseries petzi Huang, Chen, Song and Berger, 2014, p. 345.

Size in vivo about 75×43 μm. Body outline variable, usually oval and shield-like, flexible and highly contractile (Fig. 42A, B, K-M). Contractile vacuole absent. Approximately 34-49 macronuclei and one or two micronuclei (Fig. 42H, M). Three types of cortical granules: type I, mitochondria-like, about 4×2 μm in size and colorless (Fig. 42D, P, arrow); type II granules approximately 1 μm in diameter, partially gath- ered and weak gray in color; arranged in rows along cirri (Fig. 42D, E, F, O, P, arrowhead); type III granules about 0.5 μm in diameter and gray in color (Fig. 42D, P, double arrowhead). Cytoplasm colorless or slightly gray (Fig. 42D). Adoral zone of membranelles occupy 25-40% of body length (Fig. 42A, G, K, L). Both PM and EM either straight or slightly curved (Fig. 42L). Three enlarged FC (Fig. 42I, double arrowheads, L), two FTC close to distal end of AZM (Fig. 42I, arrowheads), and one BC near PM (Fig. 42I, arrow, L). Midventral complex form “Zig-zag” pattern and composed of 8-12 pairs (Fig. 42G, L). Two pretransverse cirri ahead of 8-12 TC (Fig. 42L). One right and one left marginal rows distinctly separated posteriorly (Fig. 42K). Three bipolar DK on dorsal side (Fig. 42H, M, arrowhead) and a single basal body ahead of RMR (Fig. 42J, arrowhead).

Distribution: Korea, China.

Korea: GG.

Specimen examined: GG: (Incheon Harbor in South Korea: 20.i.2011).

77 INVERTEBRATE FAUNA OF KOREA Ciliates

Habitat: Marine.

Remarks: Arcuseries petzi was first reported by Shao et al. (2011) in the Jiaozhou Bay of Qingdao, China as Anteholosticha petzi. After that, Huang et al. (2014) established the genus Arcuseries and transfered the species as type species. The Korean populations was originally reported as Anteholosticha petzi (Kim et al., 2013). Body outline and distributional pattern of cirri in Arcuseries petzi are very similar to those of Arcu-

A B C D

E I

F G H J

FC EM FTC AZM BC DK

Mi LMR Ma RMR PTC TC

K L M O P

78 LITOSTOMATEA

series scutellum (Cohn, 1866) Huang et al., 2014 as described by Berger (2003). Arcuseries petzi, however, has more cirri than A. scutellum as follows: MP (17-25 vs. 12-14), RMR (28-42 vs. 10-18), and LMR (20-36 vs. 11-17) (Chen et al., 2010). Arcuseries warreni (Song and Wilbert, 1997) Huang et al., 2014 also shows similar morphology to A. petzi but only contains one type of cortical granules and a fewer marginal cirri (22-27 vs. 20-36 in LMR; 21-26 vs. 28-42 in RMR) (Hu et al., 2000; Berger, 2006; Shao et al., 2011). The Korean population of A. petzi, therefore, is similar to the Chinese population described by Shao et al. (2011). However, it differs from the Chinese population in the color of cortical granules, which are not red- brown to brick-red as previously described, the smaller cell size (72×43 μm vs. 102×64 μm, on average), and the lower number of Ma (42 vs. 115).

Class Litostomatea Small and Lynn, 1981 Yeol-gu-seom-mo-chung-gang (열구섬모충강)

Size, small to large; shape, varied; free-swimming; alveoli, poorly to well-developed; somatic ciliation, holotrichous to sparse in pleurostomes and some endosymbionts; somatic monokinetids, typical, with laterally directed kinetodesmal fibril that does not overlap those of adjacent kineties, slightly convergent postciliary ribbon, and two transverse ribbons, one of which is tangential to the kinetosome perimeter and extends anteriorly into the somatic ridge to the left of the kinetid while the other transverse ribbon is radial to the kinetosome perimeter and extends transversely into the adjacent somatic ridge; one to several dorsal somatic kineties differentiated as a brosse or brush kinetids with specialized dikinetids bearing clavate cilia; lamina corticalis or ecto-endoplasmic fibrillar layer often present and well-developed; oral ciliature as simple kinetids from which nematodesmata arise to support the cytopharynx, but nematodesmata may also arise from

Fig. 42. Morphology of Arcuseries petzi from life (A-F, K, N-P) and after protargol impregnation (G-J, L, M). A-C, K, Ventral (A, C) and dorsal (B) view showing the variable outline. D-F, Surface views showing the cortical granule types, type 1 (arrows), type II (arrowheads), and type III (double arroeheads). G, I, Infra- ciliature of the ventral side, arrow denotes buccal cirrus, arrowheads mark the FTC, and double arrowheads show the FC. H, J, Infraciliature of the dorsal side showing the dorsal kineties and the dikinetid ahead of RMR. L, M, Infraciliature of the ventral and dorsal side; N, Variable body shapes. O, P, The arrangement of type I (arrow), and type II (arrowhead), type III (double arrowhead) cortical granules on the dorsal side. AZM, adoral zone of membranelles; BC, buccal cirrus; DK, dorsal kineties; EM, endoral membrane; FC, frontal cirri; FTC, frontoterminal cirri; LMR, left marginal row; Ma, macronuclei; Mi, micronuclei; MP, midventral pairs; PM, paroral membrane; PTC, pretransverse cirri; RMR, right marginal row; TC, transverse cirri. Scale bars=50 μm (cited from Kim et al., 2013).

79 INVERTEBRATE FAUNA OF KOREA Ciliates

so-called “oralized” somatic kinetids adjacent to the oral region, and in some symbionts, oral ciliature is or- ganized into polykinetid-like structures called syncilia; stomatogenesis, telokinetal; macronucleus, typically single, variously shaped from globular to band-shaped or moniliform; micronucleus, present; conjugation, temporary; contractile vacuole, present; cytoproct, present; feeding, extremely diverse, on bacteria and plant debris in some symbionts to carnivorous in others; in marine, freshwater, and terrestrial habitats, free-living and as endosymbionts in wide variety of vertebrates, especially; two subclasses.

Subclass Haptoria Corliss, 1974 Dok-po-seom-mo-chung-a-gang (독포섬모충아강)

Size, small to large; shape, variable, some species equipped with proboscis and a few species with non-suctorial tentacles; free-swimming; poorly developed alveoli; somatic ciliation, holotrichous, but reduced to girdles in some forms, and sparse in pleurostomes; somatic kinetid as for the class, but postciliary microtubules overlapping longitudinally; extrusomes as somatic mucocysts, clathrocysts, and lepidosomes, and oral and/or somatic toxicysts; oral region, typically anterior, with cytostome, apical or subapical, oval or slit-like, rarely permanently open, so that the cytopharynx becomes eversible in some species; oral dikinetids, rarely monokinetids, on border of cytostome-cytopharynx, typically with outer or posterior kinetosome bearing a slightly longer cilium and inner or anterior nonciliated kinetosome with a transverse microtubular ribbon that extends anteriorly and then reflects posteriorly to support the cytopharynx; cytopharynx, supported by the rhabdos, which is formed by bulge microtubules and transverse microtubular ribbons and nematodesmata arising from oral dikinetids; toxicysts localized in or near the oral area, typically between the oral transverse ribbons and bulge microtubules of the rhabdos; stomatogenesis, telokinetal; conjugation, temporary; rapacious carnivores of flagellates, ciliates, and other protists; two orders and one order incertae sedis.

Order Pleurostomatida Schewiakoff, 1896 Cheuk-gu-seom-mo-chung-mok (측구섬모충목)

Size, medium to large; shape, leaf-like or laterally compressed, sometimes with lengthy, attenuated anterior end; free-swimming, typically gliding on the substrate; somatic ciliation on both sides of the body, typically more densely on the right side; brosse, dorsal, and integrated in one or two dorsolateral kineties; oral region, ventral and elongated, with oral kinetids as left and right components extending along the ventral edge of the laterally flattened body, bordering a ventor slit-like cytostome, surrounded by toxicysts; micronucleus lying between two macronuclear nodules; voracious carnivores; in marine, freshwater, and rarely terrestrial habitats; two families.

80 LITONOTIDAE: Litonotus

Family Litonotidae Kent, 1882 Hae-byeon-chung-gwa (해변충과)

Size, typically medium to large; shape, flattened ovoid with narrowing at the anterior and posterior ends; free-swimming, typically gliding on the substrate; somatic ciliation, holotrichous, with right somatic kineties gradually terminating along rightmost perioral kinety, thus spica absent, and with one or two dorsolateral kineties in some forms; extrusomes as somatic mucocysts and somatic and/or oral toxicysts, but toxicysts in some forms distributed on the perimeter of the flattened body in protuberances (e.g., Loxophyllum ); oral region along the ventral edge, with two right perioral kineties and one left perioral kinety, with rightmost perioral kinety of monokinetids and other kineties of dikinetids; macronucleus, typically two ellipsoid nodules; micronucleus in between macronuclear nodules; contractile vacuole, present; cytoproct (?); feeding on flagellates and smaller protists; in marine, freshwater, and terrestrial habitats, with some species planktonic; five genera.

Genus Litonotus Wresniowski, 1870 Hae-byeon-chung-sok (해변충속)

Key to the species of genus Litonotus

1. Two macronuclear nodules...... L. paracygnus - Moniliform macronuclear nodules...... L. pictus

23. Litonotus paracygnus Song, 1994 (Figs. 43, 44) Go-ni-hae-byeon-chung (고니해변충)

Litonotus paracygnus Song, 1994, p. 131, figs. 1-11; Kim and Min, 2009, p. 168, figs. 1, 2.

Body size variable, about 150-300×40-60 μm in vivo. Cells spindle-shaped; anterior region resembling the neck of a swan and highly contractile. Laterally compressed about 3:1; left side with conspicuous hump and six longitudinal furrows (Figs. 43A, B, 44A-C, H). Right side with ordinary somatic cilia, left somatic cilia difficult to observe in vivo (Fig. 44E-G). Cytoplasm gray to bright yellow, with numerous tiny cortical granules. Body color become faint after several days in raw culture (Fig. 44A-G). Extrusomes bar-shaped, about 4-6 μm long, distributed on anterior region of ventral margin only, some scattered in cytoplasm (Figs. 43A, 44J). Two spherical to ovoid macronuclear nodules, about 8-18×8-13 μm after fixation, near mid- body, usually recognizable in vivo (Figs. 43C, 44D, H, J-L). Single micronucleus, ca 2 μm long, between

81 INVERTEBRATE FAUNA OF KOREA Ciliates

PK2 DB PK1 PK3

A C D

Fig. 43. Morphology of Litonotus paracygnus from life (A, B) and after protargol impregnation (C, D). A, Right view of a typical individual; B, Contractile anterior region; C, D, The infraciliature of the left (C) and right (D) sides. Scale bars=70 μm (A), 50 μm (C, D) (cited from Kim and Min, 2009).

macronuclear nodules (Figs. 43C, 44J-L). Two to four contratile vacuoles in posterior body portion (Figs. 43A, 44G). Usually gliding slowly on substrate or swimming with rapid rotation. Infraciliature shown in Figures 43C-D and 44F, I, J-L. Three perioral kineties: PK1, left of oral slit, consisted of dikinetids in anterior half, subsequently monokinetids to posterior region (Fig. 43C); PK2 and 3 right of cytostome, PK2 consisting of dikinetids, PK3 composed of monokinetids, terminated at posterior end of cell (Figs. 43D, 44I). Dorsal brush kinety (DB) extends nearly to posterior end, composed of dikinetids in anterior half (Fig. 43C). About 11-14 right kineties including PK2 and 3 gradually shortened ante-

82 LITONOTIDAE: Litonotus

A B C D

E F G H

I J K L

Fig. 44. Photographs of Litonotus paracygnus from life (A-G) and after protargol impregnation (H-L). A-D, H, Shape variants; E, Left of anterior region; F, I, Arrows mark perioral kineties and arrowheads kineties on the right side; G, Arrows indicate contractile vacuoles on the posterior; J, The middle region of the body shows the extrusomes (arrow) and nuclei; K, L, View right (K) and left (L) side, arrows indicate somatic kineties. Scale bars=100 μm (cited from Kim and Min, 2009).

riorly to right side (Figs. 43D, 44K). Left side with seven kineties including PK1 and DB (Figs. 43C, 44L). Nematodesmata not observed.

83 INVERTEBRATE FAUNA OF KOREA Ciliates

Distribution: Korea, China.

Korea: GW.

Specimen examined: GW: (the coastal waters of Yeonggeumjeong (38°12ʹN and 128°36ʹE), Bongpoport (38°17ʹN and 128°33ʹE), Gangwon-do in the East Sea of the Republic of Korea (Yeonggeumjeong, 15.2°C, ca 23.2 psu, pH ca 8.5; Bongpo-port, 14.1°C, ca 23.0 psu, pH ca 8.3): 18.iii.2008).

Habitat: Marine.

Remarks: Litonotus paracygnus was originally reported from the Yellow Sea, China (Song, 1994). Char- acteristics of the Korean population correspond well with the original description by Song (1994) in most respects, such as the body shape, size, the number and shape of nuclei, the distribution of extrusomes, the existence of furrows, and the marine habitat (Figs. 43A-C, 44A). This population, however, differs slightly from the Chinese one in the number of left (7 vs. 8-9) somatic kineties, and the number of contractile vacuoles (1-4 vs. 1). Litonotus paracygnus is most similar to L. cygnus mainly because of the contraction and expansion of the neck region, the possession of nuclei and the distribution of extrusomes. However, L. paracygnus can be distinguished from L. cygnus by the number of dikinetosomes in dorsal brush (many vs. 6-13) and the left side furrows (present vs. absent) (Song, 1994; Foissner et al., 1995). In spite of that, L. cygnus is only clearly described in terms of the infraciliature by Foissner (1984). For these reasons, distinguishing between the two species is still difficult. A reinvestigation of the infraciliature and molecular studies from L. cygnus is necessary.

24. Litonotus pictus Gruber, 1884 (Figs. 45-47) No-rang-hae-byeon-chung (노랑해변충)

Litonotus pictus Gruber, 1884, p. 521, figs. 52-53; Khal, 1931, p. 190, figs. S. 187, 22; Khal, 1933, p. c 62, figs. 5.16, 5.19; Kim and Min, 2009, p. 171, figs. 3-5.

Body size extremely variable, about 200-600 μm long in vivo (Figs. 45B; 46A, B). Cells slender lanceo- late-shaped with rounded posterior end, highly contractile with many longitudinal ridges within the ciliary rows of right side; left side with an inconspicuous weak hump; laterally compressed about 3:1 (Figs. 45A, B; 46A-C, F). Somatic cilia, 6-8 μm long, of right side visually developed (Fig. 46J); left somatic cilia difficult to detect in vivo. Cytoplasm yellow to yellow-brownish (Fig. 46), with numerous tiny cortical granules arranged regularly on right side, dot-like cortical granules along ciliary rows on both sides (Figs. 45G, H, 46N); irregularly arranged on left side between ciliary rows (Figs. 45I, 46O). Extrusomes bar-shaped, about 3-10 μm, on anterior region of ventral margin only, some scattered in cytoplasm (Figs. 45A, C, 46M, 47J, K). Macronucleus

84 LITONOTIDAE: Litonotus

PK1 PK2 DB PK3

E F

A D H I

Fig. 45. Morphology of Litonotus pictus drawn from life (A, B, G-I) and after protargol impregnation (C- F). A, Left view of a typical individual; B, Shape variants; C, Extrusomes and nematodesmata; D, Variants of macronuclear nodules; E, F, The infraciliature of left (E) and right (F) sides; G-I, The arrangement of pigment granules on right (G, H) and left (I) sides. Scale bars=100 μm (cited from Kim and Min, 2009).

consisted of two types: Type 1, moniliform with 12-21 nodules, elongated to ovoid macronuclear nodules, each about 9-25×5-18 μm after fixation (Figs. 45A, D, E, 46K, 47A, B, E); Type 2, a long vermiform (Figs. 45D, 47C, D), lean to the ventral region, usually detectable in vivo using differential interference contrast microscopy (Fig. 46K). Micronucleus not observed. Typically one large contratile vacuole, subterminally, several satellites, ca 10, along both boundaries of left side hump (Figs. 45A; 46L); frequently, exhausted in-

85 INVERTEBRATE FAUNA OF KOREA Ciliates

A B C

D E G

H I M

J K L O

Fig. 46. Photographs of Litonotus pictus from life. A-G, Shape variants and movement; H, I, Arrows mark contractile vacuoles in exhausted individuals; J, Arrowheads indicate cilia; K, L, View of the posterior region showings macronuclear nodules (arrowheads) and contractile vacuoles (arrows); M, Left of anterior region, arrows indicate extrusomes; N, O, Right and left sides; arrows indicate pigment granules and arrowheads mark kineties. Scale bars=100 μm (cited from Kim and Min, 2009).

dividuals exhibit several large vacuoles all over body (Fig. 46H, I). Numerous large lumps of prey existed in cytoplasm (Fig. 47D, F). Usually gliding slowly on substrate, swimming with rapid rotation or twisting (Fig.

86 LITONOTIDAE: Litonotus

A E

B F

G H I J L

Fig. 47. Photographs of Litonotus pictus after protargol impregnation. A, B, Different body shapes with moniliform macronucleus. C-E, Shape variants of macronuclear nodules, long vermiform (arrows in D) and ovoid (arrows in E). F, Numerous large lumps of prey; G, H, Right and left side view, arrows indicate somatic kineties; I, J, The anterior region, showing the dorsal brush kinety (arrowheads) and extrusomes (arrows); K, Arrows mark extrusomes scattered in the cytoplasm; L, Arrowheads indicate nematodesmata. Scale bars=100 μm (cited from Kim and Min, 2009).

46A-G). Infraciliature as shown in Figs. 45C, E, F and 47G-I, L. Three perioral kineties: PK1, left of oral slit, consists of dikinetids in anterior 2/3 of its length (Fig. 45E); PK2 and 3 right to cytostome, PK2 consists of dikinetids throughout, PK3 composed of monokinetids, terminated at posterior end cell (Fig. 45F). Dorsal brush kinety (DB) extends to nearly posterior end, composed of regularly spaced dikinetids (Figs. 45E; 47I, arrowheads). About 18-26 right kineties including PK2 and 3 (mean 22.5) closely spaced, anteriorly shortened gradually to right side (Figs. 45F; 46N; 47G). Left side, about 7-11 kineties including PK1 and DB (Figs. 45E; 46O; 47H-I). Nematodesmata highly prominent and extending along cytopharynx into cytoplasm, about 110-320 μm long (Figs. 45C; 47L, arrowheads).

87 INVERTEBRATE FAUNA OF KOREA Ciliates

Distribution: Korea, Germany.

Korea: CN.

Specimen examined: CN: (the Iwon tide embankment near Ganwol-do (36°54ʹN and 126°16ʹE) of Chung cheongnam-do in the Yellow Sea of the Republic of Korea: 11.iii.2008).

Habitat: Marine.

Remarks: The population used in this study corresponds well with the original description by Gruber(1884) and the subsequent description by Khal (1931, 1933) in most respects, i.e., the body size, body shape, distribution of extrusomes, body color, macronuclear nodules and habitat. However, this population differs slightly in terms of the number of contractile vacuoles; Litonotus pictus by Gruber (1884) showed only one on subterminal region. Generally, shape of the contractile vacuoles frequently changes in vivo and contractile vacuoles, as satellites are sometimes especially difficult to observe. These are considered population differences.

Genus Loxophyllum Dujardin, 1841 Sa-yeop-mo-chung-sok (사엽모충속)

Key to the species of genus Loxophyllum

1. Several contractile vacuoles...... L. perihoplophorum - One contractile vacuole...... L. rostratum

25. Loxophyllum perihoplophorum Buddenbrock, 1920 (Figs. 48, 49) Neolb-eun-te-du-ri-na-mut-ip-seom-mo-chung (넓은테두리나뭇잎섬모충)

Loxophyllum perihoplophorum Buddenbrock, 1920, p. 347, fig. 7; Kahl, 1931, p. 200, figs. S196, 6; Wu, Chen, Yi, Li, Warren and Lin, 2014, p. 119, figs. 5, 6; Kim and Min, 2015, p. 278, figs. 1A-D, 2.

Size in vivo 200-650×50-100 μm. Body slender with leaf-shaped outline, anterior end hooked toward dorsal side; body flexible and contractile. Length ratio of fully extended to most contracted cells about 2-3:1, a thin and wide Ex-belted zone enclosed; highly shrunken after protargol staining, about 115-350 μm in length (Figs. 48A, B, 49A, D, F). Laterally compressed at a ratio of about 2-3:1, right side flat, left slightly vaulted and has 4-5 longitudinal furrows (Fig. 48A). Two Ma connected by thread-like funiculus, dumbbellshaped, in body center, usually detectable in live specimens; each nodule egg-shaped, about 30×15 μm after fixation (Fig. 49C, I). One Mi between Ma nod-

88 LITONOTIDAE: Loxophyllum

PK2 PK1 DB PK3 Ex

A B C D

Fig. 48. Morphology of Loxophyllum perihoplophorum (A-D) from live and protargol stained specimens. A, Left view of a typical live individual; B, Nuclei, extrusomes, warts and nematodesmata with protargol staining; C, D, Ciliary pattern after protargol staining, left (C) and right (D) sides. DB, dorsal brush kinety; Ex, extrusome; Ma, macronuclear nodule; Mi, micronucleus; PK, perioral kinety; Wa, wart. Scale bars=100 μm (cited from Kim and Min, 2015).

ules; globular, ca. 2-5 μm across (Fig. 49I). Approximately 7-9 CV settled along dorsal region, size variable; a few FV recognized in vivo (Fig. 49E). Extrusomes thin, bar-shaped, about 6-10 μm long, recognizable in live cells under optimal conditions; evenly distributed along outline of entire body, and clustered into ca. 10 Warts along anterior 2/3 of dorsal margin; some scattered in cytoplasm (Figs. 48A, B, 49F, J). Cytoplasm grayish; central portion of the body opaque, with numerous tiny shiny globules; cortical granules not observed (Fig. 49C). Movement by crawling along substrates or swimming with fast rotation and twisting. Ciliary pattern typical of Loxophyllum (Figs. 48C, D, 49G, H, K, L). Three PK around oral slit, PK1 on left, and PK2, and 3 on right; kinetid rows more tightly packed than somatic kineties; PK1 contains dense dikinetids in anterior 1/3, and a continuous row of monokinetids extending to posterior end; PK2 and 3 en- tirely composed of monokinetids. Dorsal brush on dorsolateral area, with dense dikinetids in anterior 2/5, and a continuous row of monokinetids extending to posterior end. All somatic kineties composed of monokinetids; 19-22 kineties on right side, including PK2 and PK3; 9-11 kineties on left side, with PK1 and

89 INVERTEBRATE FAUNA OF KOREA Ciliates

A B

D G H

I J

C E F K L

Fig. 49. Photographs of Loxophyllum perihoplophorum from live (A-E) and protargol stained (F-L) specimens. A, B, View of live specimen; C, Macronuclear nodules (arrows) and thin and wide extrusome-belted zone (arrowheads); D, Beak-like anterior region (arrow); E, Posterior region, contractile vacuoles (arrowheads) and food vacuole (arrow); F, Appearance of protargol stained specimen; G, Dorsal brush kinety (arrowheads); H, Right view of anterior region, perioral kineties (arrowheads); I, Nuclear apparatus, micronucleus (arrow); J, Warts (arrowheads); K, L, Posterior region, left somatic kineties (arrows in K) and right somatic kineties (arrows in L). Scale bars=100 μm (cited from Kim and Min, 2015).

DB. Nematodesmata stretches to 2/3 of body (Fig. 48B).

Distribution: Korea, Germany, China.

Korea: GB.

Specimen examined: GB: (the coastal waters of Hajeo-ri (36°23ʹN and 129°24ʹE), Gyeongsangbuk-do in the East Sea: 28.iii-24.vi.2008).

Habitat: Marine.

Remarks: Loxophyllum perihoplophorum was originally described by Buddenbrock (1920) and redescribed by Kahl (1931) and Wu et al. (2014). Characteristics of the Korean population correspond very well with Buddenbrock (1920) and Kahl (1931) in most respects, such as habitat, body shape and size, the distribution of extrusomes, the number of nuclei, contractile vacuoles, somatic kineties and warts. However, the Korean population differs from the Chinese population in the distribution of extrusomes along the dorsal

90 LITONOTIDAE: Loxophyllum

margin (warts in anterior half and ordinarily distributed extrusomes in posterior half vs. warts throughout dorsal margin) and habitat (marine vs. brackish). Nevertheless, the two populations show 99.6% similarity in SSU rDNA sequences (Korean population, GenBank accession No. KT880227-KT880228; Chinese population, KC493570).

26. Loxophyllum rostratum Cohn, 1866 (Figs. 50, 51) Bu-ri-na-mut-ip-seom-mo-chung (부리나뭇잎섬모충)

Loxophyllum rostratum Cohn, 1866, p. 280, figs. 8-11; Song, 1993, p. 44, figs. 1, 2; Petz, Song and Wil- bert, 1995, p. 55, fig. 17; Lin, Li, Gong, Warren and Song, 2008, p. 331, figs. 1-16; Kim and Min, 2015, p. 280, figs. 1E-H, 3.

Size in vivo 100-130×45-65 μm. Body oblate with leaf-shaped outline; convex ventral side and sigmoidal dorsal side; beak-like anterior end hooked toward dorsal side; winding dorsal-neck region, about 15-25 μm in length; body contractile, slightly shrunken after protargol staining (Figs. 50A-D, 51A, B). Laterally compressed at a ratio of about 2-3:1, right side flat, left side notably vaulted and with 4-5 conspicuous longitudinal furrows (Fig. 51A, F). Two ovoid to elongate Ma nodules connected by thread-like funiculus in body center, usually detectable in live specimens, about 10-22×5-11 μm after fixation (Fig. 51D, H). One Mi between Ma nodules; globular, ca. 2-5 μm across. One terminal CV recognized. Extrusomes thin, bar-shaped, about 4-7 μm long, recognizable in live cells under optimal conditions; evenly distributed along entire ventral margin, and clustered into 9-10 Wa on dorsal margin; some scattered in cytoplasm (Figs. 50E, F, 51C, E, J). Cytoplasm slightly grayish with numerous shining lipid globules and particles; dot-shaped cortical granules detected on pellicle, densely placed between rows of right somatic kineties (Fig. 51A-G). Movement by slow gliding, flexible crawling along substrates, or swimming with fast rotation and twisting. Ciliary pattern typical of Loxophyllum (Figs. 50G, H, 51G, I, K, L). Three PK placed around oral slit, PK1 on left, and PK2-3 on right; kinetid rows more tightly packed than somatic kineties; PK1 contains dense dikinetids in anterior 2/3, and a continuous row of monokinetids reaching to posterior end; dikinetidal PK2 and monokinetidal PK3 reaching to posterior end. Dorsal brush on dorsolateral area, with dense dikinetids in anterior 5/6, and a continuous row of monokinetids reaching to posterior end. All somatic kineties composed of monokinetids; 15-19 kineties on right side, including PK2 and PK3; 7-8 kineties on left side, with PK1 and DB. Nematodesmata not detected.

Distribution: Korea, Antarctica, China, Germany.

Korea: GW.

91 INVERTEBRATE FAUNA OF KOREA Ciliates

PK2 DB PK3 PK1 Ex

A B C D

Fig. 50. Morphology of Loxophyllum rostratum (A-D) drawn from live and protargol stained specimens. A, Left view of a typical live individual; B, Nuclei, extrusomes, warts and nematodesmata with protargol staining; C, D, Ciliary pattern after protargol staining, left (C, G) and right (D, H) sides. DB, dorsal brush kinety; Ex, extrusome; Ma, macronuclear nodule; Mi, micronucleus; PK, perioral kinety; Wa, wart. Scale bars=50 μm (cited from Kim and Min, 2015).

Specimen examined: GW: (the coastal waters of Munam 2-ri (38°17ʹN, 128°33ʹE), Gangwon-do in the East Sea (9.2°C, 34.2 psu, and pH 8.3): 12-19.iii.2008).

Habitat: Marine.

Remarks: Loxophyllum rostratum was originally described from an aquarium population based on live observation by Cohn (1866). Several redescriptions based on protargol staining have improved the definition of L. rostratum (Song, 1993; Petz et al., 1995; Lin et al., 2008). The Korean population corresponds well with the characteristics of the original description and the subsequent studies. However, the Korean population shows a small difference from the Chinese population (Song, 1993) in body size (100-130 μm vs. 150- 250 μm) and the Weddell Sea population (Petz et al., 1995) in the number of warts (9-10 vs. ca. 12).

92 PHYLLOPHARYNGEA

B C I J

D E

A F G H K L

Fig. 51. Photographs of Loxophyllum rostratum from live (A-G) and protargol stained (H-L) specimens. A, Left view of live specimen; B, Beak-like anterior region (arrow) and winding neck-dorsal portion (arrowhead); C, Warts (arrowheads) in anterior region; D, Macronuclear nodules (arrows); E, Extrusomes (arrows) and warts (arrowheads); F, Furrows (arrows); G, Somatic kineties (arrows); H, Appearance of protargol stained specimen; I, Anterior region, perioral kineties (arrowheads); J, Extrusomes in body (arrows); K, L, Middle region, left somatic kineties (arrows in K) and right somatic kineties (arrows in L). Scale bars=80 μm (cited from Kim and Min, 2015).

Class Phyllopharyngea de Puytorac, Batisse, Bohatier, Corliss, Deroux, Didier, Dragesco, Fryd-Versavel, Grain, Grolière, Hovasse, Iftode, Laval, Rogue, Savoie and Tuffrau, 1974 Yeop-sang-in-du-seom-mo-chung-gang (엽상인두섬모충강)

Size, small to large; shape, extremely variable, globular to ellipsoid to bizarre spinous and tentacle forms; free-swimming and sessile or both, depending on the life cycle stages (e.g. free-swimming dispersal larval forms of sessile chonotrichs and suctorians); alveoli, generally well-developed, especially on non-ciliated surfaces; somatic kineties, typically arranged in two fields, which may be continuous over the body surface of ciliated stages; somatic kinetids as monokinetids that each have a lateral kinetodesmal fibril, a reduced or absent transverse microtubular ribbon, usually accompanied by a left-directed transverse fiber, and a somewhat convergent postciliary ribbon extended posteriorly to accompany ribbons of more anterior monokinetids; ribbon-like subkinetal nematodesmata arise from somatic monokinetids, extending beneath kineties as subkinetal ribbons , which in cyrtophorids and chonotrichs probably extend anteriorly and in rhynchodids

93 INVERTEBRATE FAUNA OF KOREA Ciliates

and suctorians probably extend posteriorly; extrusomes vary with subclass (e.g., acmocysts in rhynchodians; haptocysts in suctorian tentacles); oral region with radially arranged microtubular ribbons, the phyllae, sup- porting the cytopharynx; “cytopharynx” may be restricted to a tentacle in the suctoria or a tentacle-like tube in the rhynchodia; stomatogenesis, mixokinetal or merotelokinetal; macronucleus, homomerous in rhynchodians and suctorians, and heteromerous in cyrtophorians and chonotrichs; conjugation, temporary or total, the latter may involve micro- and macroconjugants; micronucleus, single to many; contractile vacuoles, common; cytoproct, apparently absent in suctoria and many chonotrichs; feeding strategies, diverse, from algivorous and bacterivorous in cyrtophorians to carnivorous on other ciliates in suctorians; encystment, common; in marine, freshwater, and terrestrial habitats, distributed widely, with many suctorian species as epibionts on a wide diversity of aquatic invertebrates and some vertebrates, chonotrichs primarily restricted to the appendages of crustaceans , and rhynchodians typically as ectoparasites on invertebrates; four subclasses.

Subclass Cyrtophoria Fauré-Fremiet in Corliss, 1956 Gok-gwan-in-du-seom-mo-chung-a-gang (곡관인두섬모충아강)

Size, small to large; shape, frequently dorsoventrally flattened; free-swimming, may be sessile but usually not sedentary, often thigmotactic, sometimes using an adhesive organelle at the posterior end; alveoli, well-developed, revealed as a complex argyrome on the dorsal surface; somatic ciliature predominantly restricted to ventral surface with preoral suture skewed far to left and with rightmost somatic kinety often divided into a dorsal kinetofragment and a midventral kinetofragment; oral ciliature typically composed of one preoral kinety and two circumoral kineties as several short double files of kinetosomes located anteriad to the cytostome; cytopharyngeal apparatus a complex cyrtos with phyllae surrounded by rod-shaped nematodesmata; stomatogenesis, merotelokinetal, but involving extensive morphogenetic movements of preoral and circumoral kineties; macronucleus heteromerous; conjugation, temporary; feeding on bacteria and algae, with some parasitic species possibly ingesting epithelial tissues of host, such as fish; in marine and freshwater habitats, broadly distributed, mostly marine, with numerous free-living forms and many epibionts of which a few species are parasites on fish; two orders.

Order Dysteriida Deroux, 1976 Nap-jak-seom-mo-chung-mok (납작섬모충목)

Size, small to large; shape, typically laterally compressed with dorsal surface rounded, in extreme;

94 DYSTERIIDAE: Dysteria

free-swimming, but often temporarily attached; ventral cilia not thigmotactic, but ciliate attached to substrate by non-ciliated adhesive region or by flexible podite (except Atelepithites); macronucleus, juxtaposed heteromerous; widespread and numerous, mainly marine, but some Ectosymbiotic forms with members of the Family Kyaroikeidae exclusively on cetaceans; four families.

Family Dysteriidae Claparède and Lachmann, 1858 Nap-jak-seom-mo-chung-gwa (납작섬모충과)

Size small; shape, ovoid to almost rectangular, may be conspicuously laterally compressed; freeswimming; somatic ciliature, typically reduced, with left ventral somatic kineties as midventral postoral field, typically separated from an anterior preoral field; flexible podite used for attachment; oral ciliature as two or more small kinetofragments disposed around the cytostome; nematodesmata of cyrtos reduced to six or fewer, with cytopharyngeal capitula or “teeth” often prominent; macronucleus, juxtaposed heteromerous, globular to ellipsoid; micronucleus, present; contractile vacuole present, may be multiple; cytoproct (?); feeding on bacteria and microalgae; in marine and freshwater habitats, widely distributed, mainly in marine habitats, and frequently as symphorionts; seven genera.

Genus Dysteria Huxley, 1857 Nap-jak-seom-mo-chung-sok (납작섬모충속)

Key to the species of genus Dysteria

1. Gradually shortened right kineties...... 2 - Shortened innermost row of right kinety...... 3 2. Five to six right kineties...... D. brasiliensis - Seven to eight right kineties...... D. lanceolata 3. Five right kineties...... D. nabia - Four right kineties...... D. ovalis

27. Dysteria brasiliensis Faria, Cunha and Pinto, 1922 (Fig. 52) Kko-ri-nap-jak-chung (꼬리납작충)

Dysteria brasiliensis Faria, Cunha and Pinto, 1922, p. 196, fig. 25; Gong, Song, Warren, Lin and Roberts,

95 INVERTEBRATE FAUNA OF KOREA Ciliates

2007, p. 157, figs. 8-9; Park and Min, 2015, p. 190, fig. 1.

Normal type: Marine Dysteria, size approximately 105 μm×47 μm in vivo; dorsal spine present; six right kineties; macronucleus approximately 33 μm×15 μm in vivo; two ventral contractile vacuoles; ectosymbiotic bacteria rod-shaped. Small-sized type: Marine Dysteria, size approximately 59 μm×33 μm in vivo; dorsal spine absent; five right kineties; macronucleus approximately 23 μm×13 μm in vivo; two ventral contractile vacuoles; ectosymbiotic bacteria rod-shaped.

Distribution: Korea, Brazil, China.

Korea: GG.

Specimen examined: GG: (Incheon Harbor, the Yellow Sea, Korea (37°26ʹN, 126°35ʹE). Habitat: Marine.

Remarks: This species was originally reported by Faria et al. (1922). Gong et al. (2007) re-described the species as three types (normal type, small-sized type, and elongate type) according to size and body outline. In the present study, we identified two types of D. brasiliensis, i.e., normal and small-sized type, in the same population; our normal and small-sized types correspond well with the two previously described types of Chinese isolate (Gong et al., 2007). However, the normal type in our population differs from that of the Chi- nese isolate in the cell size (90-126 μm×44-52 μm vs. 120-140 μm×46-60 μm) and the number of right kineties (six vs. five). We considered the slightly different cell size and number of right kineties to be population variations in D. brasiliensis.

28. Dysteria lanceolata Claparède and Lachmann, 1859 (Fig. 53) Chang-nap-jak-chung (창납작충)

Dysteria laceolata Chen, Gong, Al-Rasheid, Farraj and Song, 2011, p. 106, figs. 1-34; Park and Min, 2015, p. 192, fig. 2.

Cell size approximately 51 μm×37 μm in vivo; body oval in outline; seven to eight right kineties, three outermost kineties extending to dorso-apically; macronucleus 23 μm×15 μm in vivo; two ventral contractile vacuoles.

Distribution: Korea, Brazil, China.

Korea: GG.

Specimen examined: GG (Incheon Harbor, the Yellow Sea, Korea (37°26ʹN, 126°35ʹE).

96 DYSTERIIDAE: Dysteria

Pr Lf Co TF

EF Ma

A B C D E

G I

F H J K

Fig. 52. Dysteria brasiliensis (normal and small-sized type) from life (A, B, F-H), after protargol (C, D, I, K), and silver nitrate impregnation (E, J). A, B, left side view of two individuals with differing body size and shape, normal type (A) and small-sized type (B), showing two contractile vacuoles (arrowheads); C, D, left side view showing the infraciliature, arrowheads indicate the kinetosome-like granules at the base of the podite (C) and glandule (D); E, left side view showing the silverline system; F, G, left lateral view of two typical individuals; H, left side view showing ectosymbiotic bacteria; I, K, left side view of two type of specimens, arrowheads indicate right kineties of small-sized type and arrow indicates glandule; J, left lateral view showing the silverline system. Co, circumoral kineties; CVP, contractile vacuole pore; G, glandule; EF, equatorial fragment; Lf, left frontal kineties; LK, left kineties; Ma, macronucleus; P, podite; Pr, preoral kineties; RK, right kineties; TF, terminal fragment. Scale bars=40 μm (cited from Park and Min, 2015).

97 INVERTEBRATE FAUNA OF KOREA Ciliates

Co TF RK Lf Pr

CVP EF LK Ma

P G

A B C D

E F G H

Fig. 53. Dysteria lanceolata from life (A, E), after protargol (B, C, F, G), and silver nitrate impregnation (D, H). A, left side view; B, C, left side view of two individuals with differing number of right kineties, arrowheads indicate rows of right kineties; D, left side view showing the silverline system, arrowheads indicate the tiny argentophilic granules. E, left lateral view of typical individual; F, G, left side view of two specimens which have different number of right kineties, arrowheads indicate right kineties of having seven (F) and eight (G), arrows show two contractile vacuoles (F) and one short row under end of frontoventral kineties and terminal fragment (G); H, left lateral view showing the silverline system. Scale bars=30 μm (cited from Park and Min, 2015).

Habitat: Marine.

Remarks: Dysteria lanceolata was recently collected and described by Chen et al. (2011b) from China based on its body shape, size, and infraciliature. The Korean isolate of D. lanceolata is slightly smaller than the Chinese isolate (49-53×34-38 μm vs. 60-80×30-60 μm in vivo) and has slightly more right kineties (seven to eight vs. six to seven). However, most other features correspond well in both isolates as follows: oval body shape, presence of groove and rod-shaped ectosymbiotic bacteria on surface of plate, and three frontoventral kineties (vs. two to three in Chinese isolate).

98 DYSTERIIDAE: Dysteria

29. Dysteria nabia Park and Min, 2014 (Figs. 54-56) Na-bi-nap-jak-chung (나비납작충)

Dysteria nabia Park and Min, 2014, pp. 257-268, figs. 1A-F, 2A-I, 3A-J.

Size in vivo 74-113 ×42-49 μm, on average 94×45 μm. Body bilaterally flattened with oval to elliptical outline, ventral and dorsal sides almost parallel. In dividing cells, body form rectangular in outline. Anterior margin blunt, posterior blunt or round. Left plate concave and right plate convex. Right plate slightly wider than left plate (Figs. 54A, B, 55A-C). Under high magnification, one equatorial transverse strip on surface of both plates (Figs. 55C, D, 56B). Podite large and dagger-shaped, approximately 18 μm long in vivo, subcaudally on left ventral side (Figs. 54A-E, 55A-C). Glandule near base of podite, approximately 8 μm in diameter (Fig. 55E). Cilia restricted to ventral and apical grooves between left and right plates, approximately 12 μm long in vivo. Five right kineties even distinct in vivo (Figs. 54C, D, 55F, 56A). Cytoplasm colorless to grayish and light brown, containing several food vacuoles, approximately 3-11 μm in diameter, and numerous small granules, possibly lipid droplets (Figs. 54A, B, 55A-I). Cytostome in anterior 1/6-1/7 of body, located ventrally. Cytopharynx conspicuous in vivo, longitudinally oriented and extends to posterior end of cell, supported by 2 relatively strong nematodesmal rods, tipped with one complex tooth (Figs. 54C, D, 56D). Two ventral contractile vacuoles, approximately 8 μm in diameter in vivo, one in anterior 1/3-1/4 of body, the other in posterior 1/3-1/4 of body (Figs. 54A-D, 55H, 56A, G). Macronucleus in mid-body, elongate, approximately 33×15 μm in vivo, characteristically heteromerous, with posterior part more hyaline than anterior (Figs. 54A-D, 55E, G, 56A). Micronucleus not detected. Locomotion by slowly and wobbly crawling. Infraciliature as shown in Figs. 54C, D, 55F, 56A, C-I. Five right kineties, with the innermost row conspicuously shortened. Two outermost right kineties approximately equal in length, extending anteriorly to dorsal margin; outermost kinety consists of approximately 188 basal bodies (monokineties), comprising of 2-6 (average 4) basal body pairs (monokinety pairs). A single innermost right kinety, with 18-28 basal bodies, located in posterior 1/3-1/4 of body (Figs. 54C, D, 55F). The remaining two right kineties gradually shortened from right to left (Figs. 54C, D, 55F, 56A). Five to seven densely arranged, parallel and monokinetidal left kineties in mid-body and close to right kineties (Figs. 54C, D, 56A, D). Terminal fragment antero-dorsally located, and forming hook-like shape comprising 6-10 basal bodies. Equatorial fragment composed of 10-33 basal bodies. Two to three basal body pairs antero-dorsally located under two outermost right kineties (Figs. 54C, D, 56C). Four to six kinetosome-like granules near base of podite (Figs. 54C-E, 56A, G). Arrangement of kineties in oral field typical of the genus: two parallel circumoral kineties slightly curved to left; preoral kinety obliquely positioned in anterior region; usually three left frontal kineties, on right of

99 INVERTEBRATE FAUNA OF KOREA Ciliates

TF Pr RK Co

EF Ma

LK CVP

P A B C

D E F

Fig. 54. Morphology of Dysteria nabia from life (A, B), after protargol (C-E), and silver nitrate impregnation (F). A, B, left side view of two individuals with differing body size and shape; C, D, left side view showing the infraciliature, arrowheads indicate the kinetosome-like granules at the base of the podite; E, left side view of late-stage divider, showing the anlagen for the left kineties (arrows), the contractile vacuole pores (arrowheads), and the anlagen for terminal fragments in the opisthe (double-headed arrow); F, left side view showing the silverline system, arrowhead indicates the equatorial transverse stripe. Co, circumoral kineties; CVP, contractile vacuole pore; EF, equatorial fragment; Lf, left frontal kineties; LK, left kineties; Ma, macronucleus; P, podite; Pr, preoral kineties; RK, right kineties; TF, terminal fragment. Scale bars=40 μm (cited from Park and Min, 2014).

100 DYSTERIIDAE: Dysteria

C D

Ma Ma

E F G H I

Fig. 55. Photomicrographs of living specimens of Dysteria nabia. A-D, Left side views showing the body shape variations, arrows in (A) and (B) indicate the cytopharyngeal rod, podite, arrows in (C) and (D) show the equatorial transverse stripe, arrowheads in (A-C) indicate the groove on the left plate and arrowhead in (D) mark the complex tooth. E, Left side view, arrow indicates the contractile vacuole pore and arrowhead the glandule. F, The posterior portion of the right kineties, arrowheads indicate the innermost right kinety. G, Left side view, arrow indicates the contractile vacuole pore and arrowhead the left kineties. H-I, Left side view, arrowheads indicate the contractile vacuole pore and protuberances on the margins of the right kineties, respectively. Scale bars=50 μm (cited from Park and Min, 2014).

circumoral kineties. Cirumoral kineties and preoral kinety consisting of dikinetids (Figs. 54C-E, 56E, F, H-I). After protargol impregnation, several straight stripes were detected on surface of plates (Fig. 56B).

101 INVERTEBRATE FAUNA OF KOREA Ciliates

A C D Pr Lf

Co E

G I J

Fig. 56. Photomicrographs of Dysteria nabia after protargol impregnation (A-I) and after silver nitrate impregnation (J). A, left lateral view, arrow indicates the kinetosome-like granules and arrowheads indicate the contractile vacuole pore; B, left side view, arrows indicate the equatorial transverse stripe and arrowheads the fine stripes; C, left view of the anterior portion, arrowhead indicates the short row near the anterior end of the frontoventral kineties; D, cytopharynx, arrowhead indicates the left kineties; E, F, anterior portion, showing details of the oral ciliature; G, left side view, arrow indicates the kinetosome-like granules and arrowheads the contractile vacuole pore; H, I, oral ciliature on the left side of the late divider, arrowheads in (H) and (I) indicate the left frontal kineties in the proter and opisthe, respectively; J, left lateral view showing the silverline system, arrowheads indicate the equatorial transverse stripe. Co, circumoral kineties; Cy, cytopharynx; Lf, left frontal kineties; Ma, macronucleus; Pr, preoral kineties. Scale bars=50 μm (cited from Park and Min, 2014).

102 DYSTERIIDAE: Dysteria

Distribution: Korea, China.

Korea: GG.

Specimen examined: GG: (Marine waters with mussels and seaweeds from Incheon Harbor (37°26ʹN, 126°35ʹE), the Yellow Sea, South Korea).

Habitat: Marine.

Remarks: Dysteria nabia closely resembles D. ovalis (Gourret and Roeser, 1886) Kahl, 1931, D. pectinata (Nowlin, 1913) Kahl, 1931, D. procera Kahl, 1931, and D. proraefrons Clark, 1865 in terms of body size, shape, cytopharynx length, shortened innermost row of right kineties, and marine habitat. However, D. nabia differs from D. pectinata in several features, namely, the body size (74-113 ×42-49 μm vs. 60- 100×30-55 μm), shape (oval to elliptical with ventral and dorsal sides almost parallel vs. body semi-oval in with ventral side straight and dorsal convex), the presence (vs. absence) of a groove on the posterior left lateral side in vivo, the right kineties number (5 vs. 7), and the number of basal bodies in the equatorial fragment (ca. 17 vs. ca. 10) (Gong et al., 2007). Dysteria procera is similar to D. nabia in body size (80- 110 ×25-40 μm vs. 74-113 ×42-49 μm), but has fewer right kineties (3 vs. 5), fewer basal bodies in the equatorial fragment (3-15 vs. 10-33), and a smaller macronucleus (24-36×8-12 μm vs. 35-47×16-25 μm) (Gong and Song, 2003). Dysteria proraefrons can also be distinguished from D. nabia by the slightly smaller body size (60-90×30-50 μm vs. 74-113 ×42-49 μm), the larger number of right kineties (6 vs. 5), the smaller number of basal bodies in the equatorial fragment (2-11 vs. 10-33), and the smaller macronucleus (20-45×6-15 μm vs. 35-47×16-25 μm) (Pan et al., 2011). Dysteria ovalis has four right kineties (vs. 5 in D. nabia) and a different pattern of oral kineties (Fauré-Fremiet, 1965). Dysteria nabia must also be compared with some of 17 earlier described species that have not been described by using modern methods. Two other closely related species that resemble D. nuobia in terms of body size, number of contractile vacuoles, and absence of a dorsal spine: D. meridionalis Dragesco, 1965 and D. astyla (Maskell, 1877). Dysteria meridionalis closely resembles D. nabia in terms of length in vivo (96 μm vs. 74-113 μm) and the presence of two contractile vacuoles; however, it has 12 (vs. 5) right kineties (Dragesco, 1966). Dysteria astyla is similar to D. nabia in terms of shape (oval vs. oval to elliptical) and the presence of two ventral contractile vacuoles; however, it has a smaller body (70×17.5 μm vs. 74-113 ×42- 49 μm) and occurs in a different habitat (freshwater vs. marine). Dysteria astyla lacks the podite and only about 18 μm long in vivo (Kahl, 1931). Further, D. nabia should be compared with three other species, namely, Dysteria angustata (Claparède and Lachmann, 1858) Kahl, 1931, D. reesi Kahl, 1931, and D. sulcata (Claparede and Lachmann, 1858) Kahl, 1931. The body size and infraciliature for D. angustata are not available, however, this species can be distinguished from D. nabia by its narrow, neck-like anterior margin whereas the ventral and dorsal sides of the anterior margin in D. nabia are parallel (Kahl, 1931). Dysteria sulcata differs from D. nabia by its larger body size (150 μm vs. 74-113 ×42-49 μm) and the presence (vs. absence) of four ribs on the right plate (Kahl,

103 INVERTEBRATE FAUNA OF KOREA Ciliates

1931). Dysteria reesi differs from D. nabia in its smaller body size (59-68 μm vs. 74-113 ×42-49 μm), the presence (vs. absence) of conspicuous pigment spot in the left anterior end, and the location of the podite (posterior 1/4 of body vs. subcaudally) (Kahl, 1931).

30. Dysteria ovalis (Gourret and Roeser, 1886) Kahl, 1931 (Fig. 57) Dung-geun-nap-jak-chung (둥근납작충)

Aegyria angustata var. ovalis Gourret and Roeser, 1886, p. 508, Pl. 33, fig. 2. Dysteria ovalis Kahl, 1931, p. 256, figs. S 252, 7; Fauré-Fremiet, 1965, p. 6681, fig. 11; Park and Min, 2015, p. 193, fig. 3A, D-H.

Size in vivo approximately 58 μm×29 μm. Body oval in outline; four right kineties, one innermost kinety conspicuously shortened; macronucleus 19 μm×13 μm in vivo; two ventral contractile vacuoles. Silverlines show irregular and rather large reticulate, with equatorial transverse stripe.

Distribution: Korea, France.

Korea: GW.

Specimen examined: GW: (Geojin Harbor, Gangwon-do, the East Sea, Korea (salinity, 32.3 psu; temperature, 22.6℃; pH 8.0; 38°26ʹN, 128°27ʹE): 25.ix.2008). Habitat: Marine.

Remarks: Dysteria ovalis was originally reported by Gourret and Roeser (1886) and was subsequently described by Kahl (1931) (Fig. 57B, C). Later, Fauré-Fremiet (1965) described the infraciliature of D. ovalis. Our population corresponds well with the isolate reported by Fauré-Fremiet (1965) in terms of the cell size, infraciliature, and silverline structure (Fig. 57A-H; Kahl, 1931; Fauré-Fremiet, 1965).

104 DYSTERIIDAE: Dysteria

Co Pr TF Co Lf Pr

RK CVP Lf Ma B EF

LK CVP

P A C D E

F G H

Fig. 57. Dysteria ovalis after protargol (A, E-G), and silver nitrate impregnation (D, H) and previously reported D. ovalis (Gourret and Roeser, 1886) Kahl, 1931 (B, C). A, left side view, arrowhead indicates innermost shorten row of right kineties; B, C, left side view of previous reported two, B, from Kahl, 1931 and C, from Fauré-Fremiet, 1965; D, left side view showing the silverline system; E, F, left lateral view of two individuals, arrowheads indicate ventral contractile vacuoles and arrow show innermost shorten row of right kineties; G, left side view showing equatorial fragment; H, left lateral view showing the silverline system, arrowheads indicate the equatorial transverse stripe. Co, circumoral kineties; CVP, contractile vacuole pore; EF, equatorial fragment; Lf, left frontal kineties; LK, left kineties; Ma, macronucleus; P, podite; Pr, preoral kineties; RK, right kineties; TF, terminal fragment. Scale bars=40 μm (cited from Park and Min, 2015).

105 INVERTEBRATE FAUNA OF KOREA Ciliates

LITERATURES CITED

Agamaliev, F.G., 1972. Ciliates from microbenthos of the islands of Apšeronskij and Bakinskij archipelagos of the Caspian Sea. Acta Protozool., 10: 1-27. Agamaliev, F.G., 1974. Ciliates of the solid surface overgrowth of the Caspian Sea. Acta Protozool., 13: 53-83. Baek, Y.-S., Jung, J.-H. and Min, G.-S., 2011. Redescription of two marine ciliates (Ciliophora: Urostylida: Pseudokeronopsidae), Pseudokeronopsis carnea and Uroleptopsis citrina, from Korea. Korean J. Syst. Zool., 27: 220-227. Berger, H., 1999. Monograph of the Oxytrichidae (Ciliophora, Hypotrichia). Monogr. Biol. 78: i-xii, 1-1080. Berger, H., 2001. Catalogue of ciliate names 1. Hypotrichs. Verlag Helmut Berger, Salzburg. Berger, H., 2003. Redefinition of Holosticha Wrzesniowski, 1877 (Ciliophora, Hypotricha). Eur. J. Protistol. 39: 373-379. Berger, H., 2004. Uroleptopsis Kahl, 1932 (Ciliophora : Hypotricha): Morphology and cell division of type species, redefinition, and phylogenetic relationships. Acta Protozool., 43: 99-121. Berger, H., 2006. Monograph of the Urostyloidea (Ciliophora, Hypotricha). Monogr. Biol. 85: i-xv, 1-1303. Berger, H., 2008. Monograph of the Amphisiellidae and Trachelostylidae (Ciliophora, Hypotricha). Monogr. Biol. 88: i-xvi, 1-737. Berger, H. and Foissner, W., 1989. Morphology and biometry of some soil hypotrichs (Protozoa, Ciliophora) from Europe and Japan. Bull. Brit. Mus. (Nat. Hist.). Zool., 55: 19-46. Blatterer, H. and Foissner, W., 1988. Beitrag zur terricolen Ciliatenfauna (Protozoa: Ciliophora) Australiens. Stapfia, 17: 1-84. Borror, A.C., 1962. Euplotes minuta Yocm (Ciliophora, Hypotrichida). J. Protozool., 9: 271-273. Borror, A.C., 1972. Revision of the order Hypotrichida (Ciliophora, Protozoa). J. Eukaryot. Microbiol., 19: 1-23. Borror, A.C. and Hill, B.F., 1995. The order Euplotida (Ciliophora): taxonomy, with division of Euplotes into several genera. J. Eukaryot. Microbiol., 42: 457-466. Borror, A.C. and Wicklow, B.J., 1983. The suborder Urostylina Jankowski (Ciliophora, Hypotrichida): Mor- phology, systematics and identification of species. Acta Protozool., 22: 97-126. Buddenbrock, W., 1920. Beobachtungen über einige neue oder wenig bekannte marine Infusorien. Arch. Protistenk. Bd., 41: 341-364. Carey, P.G., 1992. Marine interstitial ciliates. An illustrated key. Chapman & Hall, London New York Tokyo Melbourne Madras. Chen, X., Huang, J. and Song, W., 2011a. Ontogeny and phylogeny of Metaurostylopsis cheni sp. n. (Proto- zoa, Ciliophora), with estimating the systematic position of Metaurostylopsis. Zool. Scr., 40: 99-111. Chen, X., Gong, J., Al-Rasheid, K.A.S., Farraj, S.A. and Song, W., 2011b. New contribution to the morpho-

106 LITERATURES CITED

logical taxonomy of three marine cyrtophorid ciliates from the Yellow Sea, China (Ciliophora: Cyrto- phorida). Acta Protozool., 50: 105-119. Chen, X., Hu, X., Lin, X., Al-Rasheid, K.A.S., Ma, H. and Miao, M., 2013. Morphology, ontogeny and molecular phylogeny of a new brackish water ciliate Bakuella subtropica sp. n. (Ciliophora, Hypotricha) from southern China. Eur. J. Protistol., 49: 611-622. Chen, X., Gao, S., Song, W., Al-Rasheid, K.A.S., Warren, A., Gong, J. and Lin, X., 2010. Parabirojimia multinucleata spec. nov. and Anteholosticha scutellum (Cohn, 1866) Berger, 2003, marine ciliates (Cilio- phora, Hypotrichida) from tropical waters in southern China, with notes on their small-subunit rRNA gene sequences. Int. J. Syst. Evol. Microbiol., 60: 234-243. Choi, J.K., 2015. Invertebrate fauna of Korea. Volume 1, Number 2. Ciliophora: Postciliodesmatophora, Intramacronucleata. Marine ciliates. National Institute of Biological Resources, Ministry of Environ- ment. Cohn, F., 1866. Neue Infusorien im Seeaquarium. Zeitschrift für Wissenschaftliche Zoologie, 16: 253-302, Tafeln XIV, XV. Curds, C.R., 1975. A guide to the species of the genus Euplotes (Hypotrichida, Ciliatea). Bulletin of the British Museum (National History) Zoology, 28: 1-63. Dragesco, J., 1966. Obsevation sur quelques Cilies libres. Arch. Protistenkd., 109: 155-206. Dragesco, J. and Dragesco-Kernéis, A., 1986. Ciliés libres de l’Afrique intertropicale. Introduction à la con- naissance et à l’étude des ciliés. Faune tropicale, (Éditions de l’ORSTOM) 26: 1-559. Entz, G., 1884. Über Infusorien des Golfes von Neapel. Mitt. zool. Stn Neapel 5: 289-444, Tafeln, 220- 225. Faria, J.G., da Cunha, A.M. and Pinto, C., 1922. Estudos sobre protozoarios do mar. Memaorias do Instituto Oswaldo Cruz, 15: 186-208. Fauré-Fremiet, E., 1965. Morphologie des Dysteriidæ (Ciliata Cyrtophorina). Comptes Rendus de l’Académie des Sciences, Paris, 260: 6679-6684. Foissner, W., 1982. Ecology and taxonomy of the hypotrichida (Protozoa: Ciliophora) of some Austrian soil. Arch. Protistenkd., 126: 19-143. Foissner, W., 1984. Taxonomie und Ökologie einiger Ciliaten (Protozoa, Ciliophora) des Saprobiensystems. I: Genera Litonotus, Amphileptus, Opisthodon. Hydrobiologia, 119: 193-208. Foissner, W., 2014. An update of ‘basic light and scanning electron microscopic methods for taxonomic studies of ciliated protozoa’. Int. J. Syst. Evol. Microbiol., 64: 271-292. Foissner, W., 2016. Terrestrial and semiterrestrial ciliates (Protozoa, Ciliophora) from Venezuela and Galápagos. Denisia, 35: 1-912. Foissner, W. and Al-Rasheid, K., 2006. A unified organization of the stichotrichine oral apparatus, including a description of the buccal seal (Ciliophora: Spirotrichea). Acta Protozool., 45: 1-16. Foissner, W. and Didier, P., 1981. Morphologie und infraciliatur einiger kinetofragminophorer und hypotricher ciliaten aus den Fliessgewässern von Besse-en-Chandesse (Frankreich). Annales de la Station limnologique de Besse, 15: 254-275. Foissner, W., Agatha, S. and Berger, H., 2002. Soil ciliates (Protozoa, Ciliophora) from Namibia (Southwest

107 INVERTEBRATE FAUNA OF KOREA Ciliates

Africa), with emphasis on two contrasting environments, the Etosha region and the Namib desert. Part I: Text and line drawings. Denisia, 5: 1-1063. Foissner, W., Blatterer, H., Berger, H. and Kohmann, F., 1995. Taxonomische und ökologische Revision der Ciliaten des Saprobiensystems - Band IV: Gymnostomatea, Loxodes, Suctoria. Bayerischen Landesamtes für Wasserwirtschaft, 1/95: 318-325. Foissner, W., Chao, A. and Katz, L.A., 2008. Diversity and geographic distribution of ciliates (Protista: Cil- iophora). Biodivers. Conserv., 17: 345-363. Gao, F., Yi, Z., Gong, J., Al-Rasheid, K.A.S. and Song, W., 2010. Molecular phylogeny and species separation of five morphologically similar Holosticha-complex ciliates (Protozoa, Ciliophora) using ARDRA riboprinting and multigene sequence data. Chin. J. Oceanol. Limnol., 28: 542-548. Gao, F., Warren, A., Zhang, Q., Gong, J., Miao, M., Sun, P., Xu, D., Huang, J., Yi, Z. and Song, W., 2016. The all-data-based evolutionary hypothesis of ciliated protists with a revised classification of the phylum Ciliophora (Eukaryota, Alveolata). Scientific Reports, 6: 24874. Gong, J. and Song, W., 2003. Morphology and infraciliature of two marine benthic ciliates, Dysteria procera Kahl, 1931 and Dysteria magna nov. spec. (Protozoa, Ciliophora, Cyrtophorida), from China. Eur. J. Protistol., 39: 301-309. Gong, J., Song, W., Hu, X., Ma, H. and Zhu, M., 2001. Morphology and infraciliature of Holosticha brad- buryae nov. spec. (Ciliophora, Hypotrichida) from the Yellow Sea, China. Hydrobiologia, 464: 63-69. Gong, J., Song, W., Warren, A., Lin, X. and Roberts, D.M., 2007. Microscopical observations on four marine Dysteria species (Ciliophora, Cyrtophorida). Eur. J. Protistol., 43: 147-161. Gourret, P. and Roeser, P., 1886. Les protozoaires du Vieux-Port de Marseille. Arch. Zool. Exp. Gen., 4: 507-511. Gruber, A., 1884. Die Protozoen des Hafens von Genua. Nova Acta Leop. Carol., 46: 473-539. Hemberger, H., 1982. Revision der Ordnung Hypotrichida Stein (Ciliophora, Protozoa) an Hand von Protar- golpräparaten und Morphogenesedarstellungen. Dissertation, Universität Bonn. Hemberger, H., 1985. Neue Gattungen und Arten hypotricher Ciliaten. Arch. Protistenkd., 130: 397–417. Hu, X. and Song, W., 2001. Morphological redescription and morphogenesis of the marine ciliate, Pseu- dokeronopsis rubra (Ciliophora: Hypotrichida). Acta Protozool., 40: 107-115. Hu, X. and Suzuki, T., 2004. A new species of Holosticha (Cillophora: Hypotrichida) from the coastal waters of Nagasaki, Japan: Holosticha nagasakiensis sp. nov. J. Mar. Biolog. Assoc. U.K., 84: 9-13. Hu, X. and Suzuki, T., 2006. Observation on a Japanese population of Pseudoamphisiella alveolata (Kahl, 1932) Song et Warren, 2000 (Ciliophora: Hypotrichida): Morphology and morphogenesis. Acta Protozo- ol., 45: 41-52. Hu, X., Song, W. and Warren, A., 2000. Divisional morphogenesis in the marine ciliate Holosticha warreni (Ciliophora: Hypotrichida). J. Mar. Biolog. Assoc. U.K., 80: 785-788. Hu, X., Warren, A. and Suzuki, T., 2004. Morphology and morphogenesis of two marine ciliates, Pseu- dokeronopsis pararubra sp. n. and Amphisiella annulata from China and Japan (Protozoa : Ciliophora). Acta Protozool., 43: 351-368. Huang, J., Chen, Z., Song, W. and Berger, H., 2014. Three-gene based phylogeny of the Urostyloidea (Pro-

108 LITERATURES CITED

tista, Ciliophora, Hypotricha), with notes on classification of some core taxa. Mol. Phylogenet. Evol., 70: 337-347. Jankowski, A., 1979. Revision of the order Hypotrichida Stein, 1859. Generic catalogue, phylogeny, taxonomy. Trudy Zoologicheskogo instituta, Leningrad, 86: 48-85. Jankowski, A.W., 1989. Replacement of unacceptable generic names in the phylum Ciliophora. Vestnik Zoologii 1989: 86. Jerka-Dziadosz, M., 1964. Urostyla cristata sp. n. (Urostylidae, Hypotrichida): the morphology and morphogenesis. Acta Protozool., 2: 123-128, Plates I, II. Jo, E., Jung, J.-H. and Min, G.-S., 2015. Morphology and molecular phylogeny of two new brackish water ciliates of Bakuella (Ciliophora: Urostylida: Bakuellidae) from South Korea. J. Eukaryot. Microbiol., 62: 799-809. Jung, J.-H. and Min, G.-S., 2009. New record of two species in stichotrichous ciliates (Ciliophora: Stichotri- chia) from Korea. Korean J. Syst. Zool., 25: 227-236. Jung, J.-H., Baek, Y.-S. and Min, G.-S., 2011a. New record of two Apokeronopsis species (Ciliophora: Uro- stylida: Pseudokeronopsidae) from Korea. Korean J. Syst. Zool., 27: 115-122. Jung, J.-H., Park, K.-M. and Min, G.-S., 2012. Morphology, morphogenesis, and molecular phylogeny of a new brackish water ciliate, Pseudourostyla cristatoides n. sp., from Songjiho lagoon on the coast of East Sea, South Korea. Zootaxa, 3334: 42-54. Jung, J.-H., Park, K.-M. and Min, G.-S., 2014. Morphology and molecular phylogeny of Pseudouroleptus jejuensis nov. spec., a new soil ciliate (Ciliophora, Spirotrichea) from South Korea. Acta Protozool., 53: 195-206. Jung, J.-H., Park, K.-M. and Min, G.-S., 2015. Morphology and molecular phylogeny of Pseudocyrtohyme- na koreana n. g., n. sp. and Antarctic Neokeronopsis asiatica Foissner et al., 2010 (Ciliophora, Sporado- trichida), with a brief discussion of the Cyrtohymena undulating membranes pattern. J. Eukaryot. Micro- biol., 62: 280-297. Jung, J.-H., Baek, Y.-S., Kim, S., Choi, H.-G. and Min, G.-S., 2011b. A new marine ciliate, Metaurostylop- sis antarctica nov. spec. (Ciliophora, Urostylida) from the Antarctic Ocean. Acta Protozool., 50: 289- 300. Jung, J.-H., Park, M.-H., Kim, S.Y., Choi, J.M., Min, G.-S. and Kim, Y.-O., 2017. Checklist of Korean ciliates (Protozoa: Ciliophora). J. Species Res., 6: 241-257. Kahl, A., 1931. Urtiere oder Protozoa I: Wimpertiere oder Ciliata (Infusoria) 2. Holotricha außer den im 1. Teil behandelten Prostomata. Tierwelt Dtl., 21: 181-398. Kahl, A., 1932. Urtiere oder Protozoa I: Wimpertiere oder Ciliata (Infusoria) 3. Spirotricha. Tierwelt Dtl., 25: 399-650.

Kahl, A., 1933. Ciliata libera et ectocommensalia. Tierwelt N.- u. Ostsee Lieferung, 23 (Teil II. c3): 29-146. Kent, W.S., 1880-1882. A manual of the infusoria: including a description of all known flagellate, ciliate, and tentaculiferous protozoa, British and foreign, and an account of the organization and affinities of the sponges. Volumes I-III. D. Bogue, London (Vol. I 1880: 1-472; Vol. II 1881: 473-720; Vol. II 1882: 721-913; Vol. III 1882: Plates I-LI).

109 INVERTEBRATE FAUNA OF KOREA Ciliates

Kim, K.-S., Jung, J.-H. and Min, G.-S., 2013. New record of two marine ciliates (Ciliophora: Spirotrichea) in South Korea. Anim. Syst. Evol. Divers., 29: 144-151. Kim, K.-S., Jung, J.-H. and Min, G.-S., 2016a. A new soil ciliate, Birojimia soyaensis nov. spec. (Ciliopho- ra: Urostylida) from South Korea. Acta Protozool., 55: 135-144. Kim, K.-S., Park, K.-M., Jung, J.-H. and Min, G.-S., 2016b. First description of three ciliates (Ciliophora: Stichotrichia) from Korea. J. Species Res., 5: 468-476. Kim, S.-J. and Min, G.-S., 2009. Taxonomic study of pooly-known marine pleurostomatid ciliates of Litonotus paracygnus and L. pictus (Ciliophora: Pleurostomatida) from Korea. Korean J. Syst. Zool., 25: 167-178. Kim, S.-J. and Min, G.-S., 2011. First record of three Uronychia species (Ciliophora: Spirotrichea: Euploti- da) from Korea. Korean J. Syst. Zool., 27: 25-33. Kim, S.-J. and Min, G.-S., 2015. Taxonomic redescription of Loxophyllum perihoplophorum and L. rostratum (Ciliophora: Pleurostomatida) from Korea. Anim. Syst. Evol. Divers., 31: 277-283. Kudo, R.R., 1950. Protozoology. Thomas Publisher, Springfield. Küppers, G.C. and Claps, M.C., 2013. Hypotrichous ciliates (Protozoa: Ciliophora) from a temporary pond in Argentina, with redescription of Apoamphisiella hymenophora (Stokes, 1886) Berger, 1999. Zootaxa, 3626: 55-76. Kumar, S., Kamra, K. and Sapra, G.R., 2010. Ciliates of the Silent Valley National Park, India: Urostyloid hypotrichs of the region with a note on the habitat. Acta Protozool., 49: 339-364. Kwon, C.B., Kang, Y.S. and Shin, M.K., 2007. Two newly recorded estuarine ciliates, Euplotes vannus and E. parawoodruffi (Ciliophora: Spirotrichea: Euplotida) from Korea. Korean J. Syst. Zool., 23: 229-235. Lei, Y., Choi, J.K., Xu, K. and Petz, W., 2005. Morphology and infraciliature of three species of Metauro- stylopsis (Ciliophora, Stichotrichia): M. songi n. sp., M. salina n. sp., and M. marina (Kahl, 1932) from sediments, saline ponds, and coastal waters. J. Eukaryot. Microbiol., 52: 1-10. Li, L., Song, W. and Hu, X., 2007. Two marine hypotrichs from north China, with description of Spiroam- phisiella hembergeri gen. nov., spec. nov. (Ciliophora, hypotricha). Acta Protozool., 46: 107-120. Li, L., Song, W., Warren, A., Al-Rasheid, K.A.S., Roberts, D., Yi, Z., Al-Farraj, S.A. and Hu, X., 2008. Morphology and morphogenesis of a new marine ciliate, Apokeronopsis bergeri nov. spec. (Ciliophora, Hypotrichida), from the Yellow Sea, China. Eur. J. Protistol., 44: 208-219. Lin, X., Li, J., Gong, J., Warren, A. and Song, W., 2008. Taxonomic studies on three marine pleurostomatid ciliates, Litonotus bergeri nov. spec., L. blattereri nov. spec. and L. petzi nov. spec. (Ciliophora, Pleu- rostomatida) from North China Sea. Eur. J. Protistol., 44: 91-102. Liu, W., Li, J., Gao, S., Shao, C., Gong, J., Lin, X., Liu, H. and Song, W., 2009. Morphological studies and molecular data on a new marine ciliate, Apokeronopsis sinica n. sp. (Ciliophora: Urostylida), from the South China Sea. Zootaxa, 2005: 57-66. Lu, B., Wang, C., Huang, J., Shi, Y. and Chen, X., 2016. Morphology and SSU rDNA sequence analysis of two hypotrichous ciliates (Protozoa, Ciliophora, Hypotrichia) including the new species Metaurostylop- sis parastruederkypkeae n. sp. J. Ocean Univ. China, 15: 866-878. Lynn, D.H., 2008. The ciliated protozoa: Characterization, classification, and guide to the literature. Spring-

110 LITERATURES CITED

er, New York. Mihailowitsch, B. and Wilbert, N., 1990. Bakuella salinarum nov. spec. und Pseudokeronopsis ignea nov. spec. (Ciliata, Hypotrichida) aus einem solebelasteten Fließgewässer des östlichen Münsterlandes, BRD. Arch. Protistenk., 138: 207-219. Pan, X., Bourland, W.A. and Song, W., 2013. Protargol synthesis: An in-house protocol. J. Eukaryot. Micro- biol., 60: 609-614. Park, M.-H., Kim, S.-J. and Min, G.-S., 2015. New records of three dysteriids (Ciliophora: Pyllopharyngea) from Korea. Korean J. Environ. Biol., 33: 189-196. Park, M.-H. and Min, G-S., 2014. A new marine cyrtophorid ciliate, Dysteria nabia nov. spec. (Ciliophora: Phyllopharyngea: Cyrtophorida: Dysteriidae), from South Korea. Acta Protozool., 53: 257-268. Park, K.-M., Jung, J.-H. and Min, G.-S., 2012. Redescription of two urostylid ciliates (Ciliophora: Urostyli- da), Anteholosticha pulchra and Metaurostylopsis struederkypkeae from Korea. Anim. Syst. Evol. Div- ers., 28: 20-28. Park, K.-M., Jung, J.-H. and Min, G.-S., 2013. Morphology, morphogenesis, and molecular phylogeny of Anteholosticha multicirrata n. sp. (Ciliophora, Spirotrichea) with a note on morphogenesis of A. pulchra (Kahl, 1932) Berger, 2003. J. Eukaryot. Microbiol., 60: 564-577. Park, M.-H., Kim, S.-J. and Min, G.-S., 2010. First record of two Euplotes ciliates (Ciliophora: Spirotrichea: Euplotida) from Korea. Korean J. Syst. Zool., 26: 21-27. Petz, W., Song, W. and Wilbert, N., 1995. Taxonomy and ecology of the ciliate fauna (Protozoa, Ciliophora) in the endopagial and pelagial of the Weddell Sea, Antarctica. Stapfia, 40: 1-223. Shao, C., Gao, F., Hu, X., Al-Rasheid, K.A. and Warren, A., 2011. Ontogenesis and molecular phylogeny of a new marine urostylid ciliate, Anteholosticha petzi n. sp. (Ciliophora, Urostylida). J. Eukaryot. Microbi- ol., 58: 254-265. Shao, C., Song, W., Warren, A., Al-Rasheid, K.A.S., Yi, Z. and Gong, J., 2006. Morphogenesis of the marine ciliate, Pseudoamphisiella alveolata (Kahl, 1932) Song & Warren, 2000 (Ciliophora, Stichotrich- ia, Urostylida) during binary fission. J. Eukaryot. Microbiol., 53: 388-396. Shao, C., Miao, M., Li, L., Song, W., Al-Rasheid, K.A.S., Al-Quraishy, S.A. and Al-Farraj, S.A., 2008a. Morphogenesis and morphological redescription of a poorly known ciliate Apokeronopsis ovalis (Kahl, 1932) nov comb. (Ciliophora: Urostylida). Acta Protozool., 47: 363-376. Shao, C., Song, W., Al-Rasheid, K.A.S., Yi, Z., Chen, X., Al-Farraj, S.A. and Al-Quraishy, S.A., 2008b. Morphology and infraciliature of two new marine urostylid ciliates: Metaurostylopsis struederkypkeae n. sp. and Thigmokeronopsis stoecki n. sp. (Ciliophora, Hypotrichida) from China. J. Eukaryot. Microbiol., 55: 289-296. Shen, Z., Shao, C,, Gao, S., Lin, X., Li, J., Hu, X. and Song, W., 2009. Description of the rare marine ciliate, Uronychia multicirrus Song, 1997 (Ciliophora; Euplotida) based on morphology, morphogenesis and SS rRNA gene sequence. J. Eukaryot. Microbiol., 56: 296-304. Shi, X. and Xu, R., 2003. Morphology and infraciliature of Pseudokeronopsis rubra in Jieshi waters of south China sea. Journal of Tropical Oceanography, 22: 23-30 (in Chinese with English summary). Shin, M.K., 2012. Invertebrate fauna of Korea. Volume 1, Number 1. Ciliophora: Intramacronucleata:

111 INVERTEBRATE FAUNA OF KOREA Ciliates

Spirotrichea: Stichotrichia. Stichotrichs. National Institute of Biological Resources, Ministry of Environ- ment. Song, W., 1993. Studies on the morphology and systematic status of Loxophyllum rostratum Cohn, 1866 (Ciliophora, Pleurostomatida). J. Oceanogr. Huanghai Bohai Sea, 11: 44-49 (in Chinese with English summary). Song, W., 1994. Morphology and infraciliature of a new marine ciliate, Litonotus paracygnus nov. sp. (Cil- iophora, Pleurostomatida). Acta Zool. Sin., 40: 131-136 (in Chinese with English summary). Song, W., 1996. Description of the marine ciliate Pseudoamphisiella lacazei (Maupas, 1883) nov. gen., nov. comb. (Protozoa, Ciliophora, Hypotrichida). Oceanol. Limnol. Sin., 27: 18-22. Song, W., 1997. On the morphology and infraciliature of a new marine hypotrichous ciliate, Uronychia multicirrus sp. n. (Ciliophora, Hypotrichida). Acta Protozool., 36: 279-285. Song, W., 1999. Redefinition of the marine ciliate genus, Uronychia. Progress in Protozoology (Eds., Song, W., Xu, K., Shi, X., Hu, X., Lei, Y., Wei, J., Chen, Z., Shi, X. and Wang, M.). Qingdao Ocean University Press, Qingdao, 177-187. Song, W., 2001. Morphology and morphogenesis of the marine ciliate Ponturostyla enigmatica (Dragesco & Dragesco-Kernéis, 1986) Jankowski, 1989 (Ciliophora, Hypotrichida, Oxytrichidae). Eur. J. Protistol., 37: 181-197. Song, W. and Warren, A., 2000. Pseudoamphisiella alveolata (Kahl, 1932) nov. comb., a large marine hypotrichous ciliate from China (Protozoa, Ciliophora, Hypotrichida). Eur. J. Protistol., 36: 451-457. Song, W. and Wilbert, N., 1997. Morphological investigations on some free living ciliates (Protozoa, Cilio- phora) from China Sea with description of a new hypotrichous genus, Hemigastrostyla nov. gen. Arch. Protistenkd., 148: 413-444. Song, W. and Wilbert, N., 2002. Faunistic studies on marine ciliates from the Antarctic benthic area, including descriptions of one epizoic form, 6 new species and, 2 new genera (Protozoa: Ciliophora). Acta Pro- tozool., 41: 23-61. Song, W., Petz, W. and Warren, A., 2001. Morphology and morphogenesis of the poorly-known marine urostylid ciliate, Metaurostylopsis marina (Kahl, 1932) nov. gen., nov. comb. (Protozoa, Ciliophora, Hypo- trichida). Eur. J. Protistol., 37: 63-76. Song, W., Warren, A. and Hu, X., 1997. Morphology and morphogenesis of Pseudoamphisiella lacazei (Maupas, 1883) Song, 1996 with suggestion of establishment of a new family Pseudoamphisiellidae nov. fam. (Ciliophora, Hypotrichida). Arch. Protistenkd., 147: 265-276. Song, W., Wilbert, N. and Berger, H., 1992. Morphology and morphogenesis of the soil ciliate Bakuella edaphoni nov. spec. and revision of the genus Bakuella Agamaliev & Alekperov, 1976 (Ciliophora, Hypotrichida) Bull. Br. Mus. nat. Hist. (Zool.), 58: 133-148. Song, W., Wilbert, N. and Warren, A., 2002. New contribution to the morphology and taxonomy of four marine hypotrichous ciliates from Qingdao, China (Protozoa: Ciliophora). Acta Protozool., 41: 145-162. Song, W., Wilbert, N., Chen, Z. and Shi, X., 2004. Considerations on the systematic position of Uronychia and related euplotids based on the data of ontogeny and 18S rRNA gene sequence analyses, with morphogenetic redescription of Uronychia setigera Calkins, 1902 (Ciliophora: Euplotida). Acta Protozool., 43: 313-328.

112 LITERATURES CITED

Song, W., Warren, A., Roberts, D., Wilbert, N., Li, L., Sun, P., Hu, X. and Ma, H., 2006. Comparison and redefinition of four marine, coloured Pseudokeronopsis spp. (Ciliophora: Hypotrichida), with emphasis on their living morphology. Acta Protozool., 45: 271-287. Takahashi, T., 1973. Mating types and two conjugation types of Pseudourostyla levis sp. n. (Ciliata). J. Sci. Hiroshima Univ. Series B. Division I. Zoology, 24: 145-163, Plates I, II. Wirnsberger, E. and Foissner, W., 1987. Morphologie von Holosticha xanthichroma sp. n. und die variabil- ität der infraciliatur in der gattung Holosticha (Ciliophora, Hypotrichida). Acta Protozool., 26: 1-8. Wirnsberger, E., Larsen, H.F. and Uhlig, G., 1987. Rediagnosis of closely related pigmented marine species of the genus Pseudokeronopsis (Ciliophora, Hypotrichida). Europ. J. Protistol., 23: 76-88. Wu, L., Chen, R., Yi, Z., Li, J., Warren, A. and Lin, X., 2014. The morphology of three Loxophyllum species (Ciliophora, Pleurostomatida) from Southern China, L. lembum sp. n., L. vesiculosum sp. n. and L. perihoplophorum Buddenbrock, 1920, with notes on the molecular phylogeny of Lophyllum. J. Eukaryot. Microbiol., 61: 115-125. Yi, Z. and Song, W., 2011. Evolution of the order Urostylida (Protozoa, Ciliophora): New hypotheses based on multi-gene information and identification of localized incongruence. PLoS ONE, 6: e17471. Yi, Z., Song, W., Warren, A., Roberts, D.M., Al-Rasheid, K.A.S., Chen, Z., Al-Farraj, S.A. and Hu, X., 2008. A molecular phylogenetic investigation of Pseudoamphisiella and Parabirojimia (Protozoa, Cilio- phora, Spirotrichea), two genera with ambiguous systematic positions. Eur. J. Protistol., 44: 45-53. Yocom, H.B., 1930. Two new species of Euplotes from Puget Sound. Pub. Puget Sound Biol. Sta., 7: 241- 248. Young, D.B., 1922. A contribution to the morphology and physiology of the genus Uronychia. J. Exp. Zool., 36: 352-395.

113 INVERTEBRATE FAUNA OF KOREA Ciliates

INDEX TO KOREAN NAMES

ㄱ 말총충과 14 말총충속 15 강모말총충 19 망횡극모충속 37 고니해변충 81 미주하모과 44 곡관인두섬모충아강 94 미주하모목 27 기수유사미주하모충 40 꼬리납작충 95 ㅂ

ㄴ 바다미주하모충속 22 바쿠하모충속 51 나비납작충 99 바쿠하모충아속 51 난형박각모하모충 31 박각모하모충속 28 납작섬모충과 95 벼슬머리자라하모충 10 납작섬모충속 95 부리나뭇잎섬모충 91 내핵아문 8 비로지마하모충속 59 넓은테두리나뭇잎섬모충 88 노랑해변충 84 ㅅ

ㄷ 사엽모충속 88 산포하모목 21 다극모말총충 17 선모충강 8 다극모원전열하모충 44 소야비로지마하모충 59 독포섬모충아강 80 신비바다미주하모충 22 둥근납작충 104 쌍핵말총충 15 뚱뚱이홍색위각모충 34

ㅇ ㅁ 연노랑망횡극모충 37 많은복극모열과 72 연안바쿠하모충 55

114 INDEX TO KOREAN NAMES

열구섬모충강 79 ㅊ 열하모충아강 21 엽상인두섬모충강 93 창납작충 96 원전열하모충속 44 챈씨초미주하모충 63 위각모충속 34 첨모하모충과 22 위양열하모충속 69 초미주하모충속 63 유막위양열하모충 69 측구섬모충목 80 유사각모과 28 유사관막하모충속 24 ㅍ 유사단미하모충속 72 유사미주하모충과 40 페츠씨휜횡극모충 77 유사미주하모충속 40 유사바쿠하모충아속 55 인천바쿠하모충 51 ㅎ

하모충아강 9 ㅈ 한국유사관막하모충 25 해변충과 81 자라하모충과 10 해변충속 81 자라하모충목 9 홍색옛전열하모충 48 자라하모충속 10 황색박각모하모충 28 자라하모충아목 9 휜횡극모충속 77 작은자라하모충 12 작은홍색초미주하모충 66 제주유사단미하모충 72

115 INVERTEBRATE FAUNA OF KOREA Ciliates

INDEX TO SCIENTIFIC NAMES

A ovalis 104 Dysteriida 94 Anteholosticha 44 Dysteriidae 95 multicirrata 44 pulchra 48 Apokeronopsis 28 E bergeri 28 ovalis 31 Euplotes 10 Arcuseries 77 cristatus 10 petzi 77 minuta 12 Euplotida 9 Euplotidae 10 B Euplotina 9

Bakuella 51 (Bakuella) incheonensis 51 H (Pseudobakuella) litoralis 55 Birojimia 59 Haptoria 80 soyaensis 59 Hypotrichia 9

C I

Cyrtophoria 94 Incertae sedis in order Urostylida 77 Intramacronucleata 8 D

Dysteria 95 K brasiliensis 95 lanceolata 96 Kahliellidae 72 nabia 99

116 INDEX TO SCIENTIFIC NAMES

L alveolata 69 Pseudocyrtohymena 24 Litonotidae 81 koreana 25 Litonotus 81 Pseudokeronopsidae 28 paracygnus 81 Pseudokeronopsis 34 pictus 84 carnea 34 Litostomatea 79 Pseudouroleptus 72 Loxophyllum 88 jejuensis 72 perihoplophorum 88 Pseudourostyla 40 rostratum 91 cristatoides 40 Pseudourostylidae 40

M S Metaurostylopsis 63 cheni 63 Spirotrichea 8 struederkypkeae 66 Sporadotrichida 21 Stichotrichia 21

O U Oxytrichidae 22 Uroleptopsis 37 citrina 37 P Uronychia 15 binucleata 15 Phyllopharyngea 93 multicirrus 17 Pleurostomatida 80 setigera 19 Ponturostyla 22 Uronychiidae 14 enigmatica 22 Urostylida 27 Pseudoamphisiella 69 Urostylidae 44

117

Invertebrate Fauna of Korea Vol. 1, No. 3 Ciliates NIBR ) set ( 3 8 00- 346- 96470 94555- 6811- 89- 89- 113468 Not for sale / No charge 978- 978-

BN BN IS IS 788968 9 Marine Ciliates 2 Marine 3 Ciliates Stichotrichs Ciliophora 1 Stichotrichs

1 No. 1 No. 1 No.

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