New Records of Three Dysteriids (Ciliophora: Pyllopharyngea) from Korea

Korean J. Environ. Biol. 33(2) : 189~196(2015) http://dx.doi.org/10.11626/KJEB.2015.33.2.189

INTRODUCTION

To date, more than 240 ciliate species (including parasitic ciliates), mainly belonging to the class Spirotrichea, have been reported from Korea (The Korean Society of Systema­

tic Zoology 1997; Kwon 2009; Jung et al. 2012; Shin 2012;

Jung 2013; Park and Min 2014; Lee et al. 2015; Nam et al.

2015 etc).

Most species of dysteriid ciliates (Ciliophora: Phyllopha­

ryngea) are found in marine benthic habitats. Dysteria spe­

cies are characterized by a laterally flattened body shape, oral structure with conspicuous cytopharynx, and restricted ciliature in the anterior and ventral regions (Kahl 1931;

Deroux 1965; Dragesco 1966; Wilbert 1971; Song and Wil­

bert 2002; Chen et al. 2011). To date, more than 30 Dyste- ria morphospecies have been investigated (Fauré­Fremiet 1965; Petz et al. 1995; Gong et al. 2002, 2003, 2007; Song and Wilbert 2002; Gong and Song 2003, 2004; Hu and Su­

zuki 2005; Wilbert and Song 2005; Chen et al. 2011; Pan et al. 2011; Park and Min 2014). However, only one species

­ Dysteria nabia Park & Min, 2014 ­ has previously been recorded in Korea.

MATERIALS AND METHODS Sample collection, observation, and identification The dysteriid ciliates were collected by filtering the wash­

ed seawaters of mussels and seaweeds that were sampled from harbors. The obtained samples were maintained in Pe­

tri dishes at room temperature. We observed the specimens by using bright­field and differential interference contrast microscopy, at magnifications of ×50 to ×1000. We used the protocol of Foissner (1991) to reveal the infraciliature.

We used the Chatton­Lwoff method to reveal the silverline systems for the three dysteriids (Corliss 1953). We counted and measured the stained specimens at a magnification of

× 1000 (DM2500; Leica, Wetzlar, Germany). Terminology follows that of Corliss (1979), Gong and Song (2004), and Chen et al. (2011).

All specimens were deposited in the National Institute of Biological Resources (NIBR), Korea.

RESULTS AND DISCUSSION Class Phyllopharyngea de Puytorac et al., 1974 Order Dysteriida Deroux, 1970

* Corresponding author: Gi­Sik Min, Tel. 032­860­7692, Fax. 032­874­6737, E­mail. [email protected]

ⓒ2015. Korean Society of Environmental Biology.

New Records of Three Dysteriids (Ciliophora: Pyllopharyngea) from Korea

Mi­Hyun Park and Gi­Sik Min*

Department of Biological Sciences, Inha University, Incheon 402-751, Korea

Abstract - We verified three ciliates -

Claparède and Lachmann, 1859, and Dysteria ovalis (Gourret and Roeser, 1886) Kahl, 1931 - as previously unrecorded species in Korea. These three ciliates were collected from Incheon Harbor and Geojin Harbor in Korea. We describe the three species based on live observations, protargol- impregnated specimens, and silver nitrate-impregnated specimens.

Key words: ciliates, Dysteria brasiliensis, Dysteria lanceolata, Dysteria ovalis, Korea, morphology

Family Dysteriidae Claparède & Lachmann, 1858

Genus Dysteria Huxley, 1857

1.

1922

(Fig. 1A-K; Table 1)

Dysteria brasiliensis Faria et al. 1922, p. 196, Fig. 25;

Fig. 1. Dysteria brasiliensis(normal and small­sized type) from life(A, B, F­H), 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 small­sized type(B), showing two contractile vacuoles(arrowheads); C, D ­ left side view showing the infraciliature, arrowheads indicate the kinetosome­like 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 in­

dividuals; H ­ left side view showing ectosymbiotic bacteria; I, K ­ left side view of two type of specimens, arrowheads indicate right kineties of small­sized type and arrow indicates glandule; J ­ left lateral view showing the silverline system. Co ­ circumoral kineties, 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: 40μm.

A B C D E

Lf Pr

Co TF

Ma RK

EF

P

LK

G I

F H J K

Gong et al. 2007, p. 157, Figs. 8­9.

Material examined: On September 27, 2011 at Incheon Harbor, the Yellow Sea, Korea (37˚26′N, 126˚35′E).

Diagnosis: (i) Normal type: Marine Dysteria, size approx­

imately 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 bac­

teria rod­shaped.

(ii) Small­sized type: Marine Dysteria, size approximate­

ly 59 μm×33 μm in vivo; dorsal spine absent; five right ki­

neties; macronucleus approximately 23 μm×13 μm in vivo;

two ventral contractile vacuoles; ectosymbiotic bacteria rod­shaped.

Remarks: This species was originally reported by Faria et al. (1922). Gong et al. (2007) re­described the species as three types (normal type, small­sized 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 small­sized type, in the same population; our normal and small­sized types correspond well with the two previously described types of Chinese isolate (Gong et al. 2007). How­

ever, the normal type in our population differs from that of the Chinese isolate in terms of the cell size and number of right kineties ­ cell size approximately 90~126 μm×44~52 μm in our population and 120~140 μm×46~60 μm in the Chinese isolate; six right kineties in our population and five right kineties in the Chinese isolate (Table 1, Fig. 1A­K;

Gong et al. 2007). We considered the slightly different cell size and number of right kineties to be variations of D. bra- siliensis.

Habitat: Marine waters with mussels and seaweeds.

World distribution: Brazil, China, Korea.

Deposition: NIBRPR0000106074­NIBRPR0000106075.

Identifiers: Mi­Hyun Park and Gi­Sik Min.

Table 1. Morphometric characteristics of Dysteria brasiliensis: normal type(upper row) and small­sized type(lower row) based on protar­

gol­impregnated specimens.

Type Mean Min Max SD SE CV n

Body, length Normal 95.0 62.4 118.0 16.7 4.0 17.6 17.0

Small 60.0 53.0 67.0 5.5 1.9 9.1 8.0

Body, width Normal 41.6 30.4 48.0 5.1 1.2 12.3 17.0

Small 34.4 31.0 38.0 2.3 0.8 6.6 8.0

Right kineties, number Normal 6.0 6.0 6.0 0.0 0.0 0.0 12.0

Small 5.0 5.0 5.0 0.0 0.0 0.0 8.0

Frontoventral kineties, number Normal 2.0 2.0 2.0 0.0 0.0 0.0 12.0

Small 2.0 2.0 2.0 0.0 0.0 0.0 8.0

Left equatorial kineties, number Normal 7.1 6.0 8.0 0.7 0.2 9.9 11.0

Small 6.5 6.0 7.0 0.7 0.5 10.9 2.0

Kinetosomes in the outermost

right kinety, number Normal 239.8 218.0 251.0 13.0 5.3 5.4 6.0

Small - - - -

Kinetosomes in terminal

fragment, number Normal 13.1 10.0 18.0 2.3 0.7 17.6 11.0

Small 8.8 8.0 10.0 1.0 0.5 10.9 4.0

Kinetosomes in equatorial

fragment, number Normal 16.6 11.0 26.0 5.2 1.6 31.3 10.0

Small 10.2 8.0 15.0 2.6 1.1 26.0 6.0

Macronucleus, length Normal 31.5 20.8 41.6 4.8 1.2 15.2 17.0

Small 20.1 18.0 25.0 2.5 0.9 12.3 7.0

Macronucleus, width Normal 12.2 8.0 19.2 3.2 0.8 26.4 17.0

Small 9.7 9.0 10.0 0.5 0.2 5.0 7.0

Glandule, diameter Normal 8.6 6.4 12.8 2.0 0.6 23.4 10.0

Small 6.0 6.0 6.0 0.0 0.0 0.0 3.0

Kinetosome­like granule,

number Normal 8.8 6.0 11.0 1.8 0.6 20.8 11.0

Small 4.4 3.0 6.0 1.5 0.7 34.5 5.0

Podite, length Normal 11.1 10.0 12.0 0.9 0.3 8.1 7.0

Small 12.0 12.0 12.0 0.0 0.0 0.0 1.0

CV - coefficient of variation in %; Max - maximum; Mean - arithmetic mean; Min - minimum; n - number of individuals examined; SD - standard deviation; SE

­ standard error of the mean. All measurements inμm.

2.

1859

(

) (Figs. 2A-H; Table 2)

Dysteria laceolata Chen et al. 2011, p. 106, Figs. 1­34.

Material examined: On February 9, 2011 at Incheon Har­

bor, the Yellow Sea, Korea (37˚26′N, 126˚35′E).

Diagnosis: Cell size approximately 51 μm×37 μm in vivo;

body oval in outline; seven to eight right kineties, three out­

ermost kineties extending to dorso­apically; macronucleus 23 μm×15 μm in vivo; two ventral contractile vacuoles.

Remarks: Dysteria lanceolata was recently collected from China and was re­described by Chen et al. (2011) based on its body shape, size, and infraciliature. The D. lanceolata

isolate identified in our present study is slightly smaller than the Chinese isolate (49~53 μm×34~38 μm vs. 60~80 μm

× 30~60 μm) in vivo and has seven to eight right kineties (vs. six to seven right kineties in the Chinese isolate). How­

ever, most other features correspond well with those of the Chinese isolate as follows: oval body shape; presence of groove and rod­shaped ectosymbiotic bacteria on surface of plate; and three frontoventral kineties (cf. two to three in Chinese isolate) (Table 2, Fig. 2A­H; Chen et al. 2011).

Habitat: Marine waters with mussels and seaweeds.

World distribution: France, China, Korea.

Deposition: NIBRPR0000106076­NIBRPR0000106077.

Identifiers: Mi­Hyun Park and Gi­Sik Min.

Fig. 2. 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. Co ­ circumoral kineties, CVP ­ contractile vacuole pore; EF ­ equatorial fragment, G ­ glandule; Lf ­ left frontal kineties, LK ­ left kineties, Ma ­ macronucleus, P ­ podite, Pr ­ preoral kineties, RK ­ right kineties, TF ­ terminal fragment. Scale bars: 30μm.

A B C D

RK Co

Lf Pr TF

EF Ma CVP

P G

LK

E F G H

3.

Min, 2014

(

) Dysteria nabia Park & Min 2014, p. 258, Figs. 1A­F, 2A­I,

3A­J.

4.

(Gourret and Roeser, 1886) Kahl, 1931

(

) (Fig. 3A, D-H; Table 2) Dysteria ovalis Kahl 1931, p. 256, Figs. S 252, 7; Fauré­

Fremiet 1965, p. 6681, Fig. 11.

Material examined: On September 25, 2008 at Geojin Har­

bor, Gangwon­do, the East Sea, Korea (salinity, 32.3 psu;

temperature, 22.6˚C; pH 8.0; 38˚26′N, 128˚27′E).

Diagnosis: Cell size 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 trans­

verse stripe.

Remarks: Dysteria ovalis was originally reported by Gour­

ret and Roeser (1886) and was subsequently described by Kahl (1931) (Fig. 3B, C). After then, Fauré­Fremiet (1965) described the infraciliature of D. ovalis. Our population corresponds well with the isolate reported by Fauré­Fremiet (1965) in terms of the cell size, infraciliature, and silverline structure (Table 2, Fig. 3A­H; Kahl 1931, Fauré­Fremiet 1965).

Habitat: Marine waters with mussels and seaweeds.

World distribution: France, Korea.

Deposition: NIBRPR0000106078­NIBRPR0000106079.

Identifiers: Mi­Hyun Park and Gi­Sik Min.

Key to the Korean species of the genus Dysteria 1. Four right kineties ···

···D. ovalis (Gourret and Roeser, 1886) Kahl, 1931

mens.

Species Mean Min Max SD SE CV n

Body, length DL 56.8 48.0 68.0 6.3 1.4 11.2 20.0

DO 58.4 48.0 66.0 5.8 1.6 10.0 14.0

Body, width DL 36.6 31.0 47.0 4.5 1.0 12.2 20.0

DO 28.5 23.0 33.0 3.8 1.1 13.5 13.0

Right kineties, number DL 7.4 7.0 8.0 0.5 0.2 6.9 11.0

DO 4.0 4.0 4.0 0.0 0.0 0.0 13.0

Frontoventral kineties, number DL 3.0 3.0 3.0 0.0 0.0 0.0 20.0

DO 2.0 2.0 2.0 0.0 0.0 0.0 13.0

Left equatorial kineties, number DL 5.4 5.0 6.0 0.5 0.1 9.4 17.0

DO 5.7 4.0 9.0 1.5 0.4 27.2 13.0

Kinetiosomes in the outermost

right kinety, number DL - - - -

DO 112.8 106.0 118.0 5.0 2.2 4.4 5.0

Kinetiosomes in the innermost

right kinety, number DL - - - -

DO 11.4 9.0 13.0 1.4 0.5 12.4 8.0

Kinetosomes in terminal

fragment, number DL 18.5 14.0 23.0 3.2 1.3 17.3 6.0

DO 8.4 7.0 10.0 1.1 0.4 13.5 7.0

Kinetosomes in equatorial

fragment, number DL 15.3 9.0 24.0 5.0 1.6 32.5 10.0

DO 6.5 5.0 9.0 1.4 0.5 21.8 8.0

Macronucleus, length DL 24.5 19.0 31.0 2.9 0.6 11.7 20.0

DO 19.4 15.0 23.0 2.4 0.7 12.6 14.0

Macronucleus, width DL 13.5 9.0 17.0 2.4 0.5 17.4 20.0

DO 12.8 9.0 16.0 2.2 0.6 16.9 14.0

Glandule, diameter DL 7.2 6.0 9.0 1.0 0.2 13.4 20.0

DO - - - -

Podite, length DL 14.3 11.0 16.0 1.3 0.3 9.4 20.0

DO 13.4 12.0 15.0 1.1 0.5 8.5 5.0

CV - coefficient of variation in %; Max - maximum; Mean - arithmetic mean; Min - minimum; n - number of individuals examined; SD - standard deviation; SE

­ standard error of the mean. All measurements inμm.

- More than four right kineties ···2 2. Five or six right kineties ···3 - More than six right kineties ···

···D. lanceolata Claparède and Lachmann, 1859 3. Right kinety 5 terminates anteriorly in posterior 1/4 of

body···D. nabia Park & Min, 2014

1886) Kahl, 1931(B, C). A ­ left side view, arrowhead indicates innermost shorten row of right kineties; B, C ­ left side view of previ­

ous reported two, B, from Kahl 1931 and C, from Fauré­Fremiet 1965; D ­ left side view showing the silverline system. E, F ­ left lat­

eral 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: 40μm.

B

A C D E

LfPr

Co Co

Pr

Lf TF

RK Ma EF

P

LK CVP

CVP

F G H

- Right kinety 5 or 6 terminates anteriorly at cytostome level or over equatorial transverse stripe ···

···D. brasiliensis Faria et al., 1922

ACKNOWLEDGEMENT

This work was supported by the grants from the National Institute of Biological Resources (NIBR), funded by the Ministry of Environment (MOE) of the Republic of Korea (NIBR NO. 2013­02­001).

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Received: 14 May 2015 Revised: 11 June 2015 Revision accepted: 11 June 2015