Two Newly Recorded Vorticellid Species

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INTRODUCTION

The family Vorticellidae Ehrenberg, 1838 is one of highly diverse taxa within the group Peritrichia and is characterized by zooid, contractible, and helically twisted spasmoneme (Ehrenberg, 1838; Corliss, 1979; Warren, 1986; Lynn, 2008;

Sun et al., 2011). Carchesium Ehrenberg, 1831 and Vorticel- la Linnaeus, 1767 are members of Vorticellidae and com- monly found in eutrophic freshwater environments. Carche- sium and Vorticella are distinguishable from each other by the key character of colonial versus solitary life form(Cor- liss, 1979; Lynn and Small, 2000; Lynn, 2008). According to Gentekaki and Lynn(2010), Carchesium polypinum complex might be firstly described by Leeuwenhoek in 1676 and Linnaeus(1758) officially described. Thereafter, many researchers redescribed C. polypinum(Esteban and Fernán- dez-Galiano, 1989; Foissner et al., 1992; Shi et al., 2001;

Dias et al., 2010). However, populations of C. carchesium had enormous amount of genetic differences but could not

distinguishable based on the morphology. Therefore, it was designated as a cryptic species complex(Gentekaki and Lynn, 2010). We collected the two species from Jindo Island and other places with morphological redescriptions. Carchesium polypinum complex and Vorticella campanula Ehrenberg, 1831 are newly described species in Korea.

MATERIALS AND METHODS

Carchesium polypinum complex were collected from a small freshwater pond on Gahak-ri, Jisan-myeon, Mt. Geupchisan of Jindo Island(34°24′07″N, 126°06′42″E) on 8 Jul 2016 and a small pond next to a stream in Habuk-myeon, Yang- san-si(35°29′12″N, 129°03′25″E) on 22 Nov 2013. Vorti- cella campanula was collected with debris and freshwater in an agricultural pond in Na-ri, Gunnae-myeon, Jindo Island (34°33′45″N, 126°16′02″E) on 9 Jul 2016 and a freshwater pond in Gangdong-dong, Gangseo-gu, Busan(35°12′43″N, Review article

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*To whom correspondence should be addressed Tel: 82-52-259-2396, Fax: 82-52-259-1694 E-mail: mkshin@ulsan.ac.kr

Two Newly Recorded Vorticellid Species

(Ciliophora, Oligohymenophorea, Peritrichia) from Jindo Island with Other Populations in Korea

Ji Hye Kim, Mann Kyoon Shin*

Department of Biological Science, University of Ulsan, Ulsan 44610, Korea

ABSTRACT

Carchesium polypinum and Vorticella campanula were collected in freshwater ponds and reservoirs on Jindo Island and other places in Korea. These two vorticellids are newly recorded in Korea. The two species are described using live and silver impregnated cell observations, morphometry, line drawings, and microphotographs. Characterizations were based on the following diagnostic features: Carchesium polypinum was observed mainly as a funnel to fan- shaped colony, basically dichotomous branching pattern, discontinuous spasmoneme, subconical shaped zooid, J shaped macronucleus, ventrally positioned single contractile vacuole, and pellicular striation with 61-80 rows between the peristomial lip and aboral ciliary wreath, and 18-30 rows between the aboral ciliary wreath and scopula.

Vorticella campanula was conspicuously characterized by the broadly bulged peristomial lip, wide conical shaped zooid, J or S shaped macronucleus, ventrally positioned single contractile vacuole and pellicular striation with 64- 75 rows between the peristomial lip and aboral ciliary wreath, and 27-41 rows between the aboral ciliary wreath and scopula. We provide redescriptions of two well-known vorticellids with detailed drawings and descriptions of oral ciliatures from Jindo Island and other places on the Korean peninsula.

Keywords: Carchesium, Vorticella, morphology, redescription, freshwater

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128°55′59″E) on 29 Nov 2013. Water samples were collected and transferred with debris in raw cultural petri dishes and then maintained at room temperature in a laboratory for one to five days. The cells were cultured using wheat grains added in raw cultural Petri dishes for enrichment of bacteria and ciliates(Foissner et al., 2009). Silver staining methods was performed by Wilbert(1975) and Foissner(1991). The two species were described by live and silver impregnated cells observations using a stereo microscope(SMZ800;

Nikon, Tokyo, Japan) and an optical microscope(Axio Im- ager A1; Carl Zeiss, Oberkochen, Germany), morphometry, line drawings, and microphotographs using a CCD camera (Axio Cam MRc; Carl Zeiss). Classification and terminolo- gy follows Lynn(2008) and Ji et al.(2015).

SYSTEMATIC ACCOUNTS Phylum Ciliophora Doflein, 1901

Class Oligohymenophorea de Puytorac, Batisse, Bohatier, Corliss, Deroux, Didier, 1974

Subclass Peritrichia Stein, 1859 Order Sessilida Kahl, 1933

Family Vorticellidae Ehrenberg, 1838 Genus Carchesium Ehrenberg, 1830

1. Carchesium polypinum complex(Table 1, Figs. 1, 2) Sertularia polypina Linnaeus, 1758: 816.

Carchesium polypinum: Ehrenberg, 1830: 41; Stein, 1854:

78; Kahl, 1935: 738; Foissner and Schiffmann, 1974: 491, 504; Esteban and Fernández-Galiano, 1989: 345; Foissner et al., 1992: 137; Shi et al., 2001: 13; Dias et al., 2010:

483.

Description. Colony outline funnel and fan-shaped, approx- imately 2,000μm high and contain 10-50 zooids(Figs. 1F, 2A, B). Macrozooid absent. Stalk flexible and contractile, primary stalk dichotomously branched, secondary to terminal stalks polychotomously or irregularly branched(Figs.

1B, F, 2A, B). Stalk surface smooth, gap between holdfast and starting point of spasmoneme on primary stalk approximately 80μm, primary stalk diameter about 35μm, terminal

Table 1. Morphometry of Carchesium polypinum complex(Cp.) from Jindo Island(Jin.) and Yangsan-si(Yang.) and Vorticella cam- panulla Ehrenberg, 1831(Vc.) from Jindo Island(Jin.) and Busan(Bus.)

Character SP P Mean MIN MAX MED SD SE CV n

Body, length(μm) Cp. Jin. 123 100 140 123 10.9 3.3 8.8 11

Yang. 69 51 82 72 9.5 2.7 13.8 12

Vc. Jin. 78 70 90 79 7.8 2.9 10.0 7

Bus. 67 55 84 67 7.2 1.6 10.7 19

Body, width(μm) Cp. Jin. 70 60 80 70 5.7 1.7 8.1 11

Yang. 39 31 46 38 4.5 1.3 11.6 12

Vc. Jin. 55 51 60 54 3.6 1.4 6.5 7

Bus. 55 46 66 55 5.1 1.2 9.3 19

Peristomial lip, diameter(μm) Cp. Jin. 79 70 95 76.5 7.8 2.5 9.9 10

Yang. 60 49 71 58 6.1 1.8 10.3 11

Vc. Jin. 86 74 104 85 12.7 4.8 14.8 7

Bus. 77 66 91 77 6.4 1.5 8.3 19

Peristomial lip, thickness(μm) Cp. Jin. 8 6 9 8.5 1.4 0.5 17.2 8

Yang. 9 6 12 8.5 1.8 0.6 20.0 8

Vc. Jin. 5 4.6 6.8 5.3 0.9 0.4 15.7 5

Bus. 6 3.8 10.4 5.4 1.4 0.3 25.2 19

Scopula, diameter(μm) Cp. Jin. 8 6 9 8 1.1 0.5 15.0 5

Yang. 9 8 10 9 0.8 0.4 9.5 5

Vc. Jin. 6 5.7 7.3 6.2 0.7 0.3 10.5 5

Bus. 7 5.5 7.9 6.9 0.7 0.2 11.0 19

Number of silverlines, peristomial

lip to aboral ciliary wreath Cp. Jin. 69 61 80 68 6.9 3.1 10.0 5

Yang. 70 65 75 71 5.0 2.9 7.2 3

Vc. Jin. 73 70 75 73 1.8 0.8 2.5 5

Bus. 67 64 74 66 4.0 1.8 5.9 5

Number of silverlines, aboral ciliary

wreath to scopula Cp. Jin. 26 18 30 28 5.0 2.2 19.6 5

Yang. 22 21 22 21.5 0.7 0.5 3.3 2

Vc. Jin. 29 27 31 28.5 2.1 1.0 7.2 4

Bus. 35 29 41 35 5.1 2.3 14.5 5

Measurements are in μm.

SP, species; P, population; MIN, minimum value; MAX, maximum value; MED, medium value; SD, standard deviation; SE, standard error; CV, coefficient of variance; n, sample size.

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stalk diameter about 9μm. Spasmoneme discontinuous on each branching points(Figs. 1B, F, 2D). Zooids located dis- tal end of terminal stalk(Figs. 1F, 2A, B).

Zooids subconical to inverted bell-shape, length 100-140 μm in Jindo population and 51-82μm in Yangsan population, width 60-80μm in Jindo population and 31-46μm in Yangsan population, zooids relatively symmetrical, sometimes asymmetrical caused by movement or food vacuoles (Table 1, Figs. 1A, C, 2C). Peristomial lip single-layered, diameter 49-95μm, thickness approximately 8μm(Table 1, Figs. 1A-C, E, 2C). Epistomial disc flattened(Figs. 1A, 2C). Pellicle striped horizontally(Fig. 2F).

Cytoplasm predominantly colorless, sometimes brownish to grayish caused by food vacuolar color on low magnification(Fig. 2A-C). Single contractile vacuole located ventral side of infundibulum(Figs. 1A, 2C). Macronucleus longitudinally arranged and forming J or S shape(Figs. 1A-C, E, 2E).Oral ciliature composed of parallel polykinety and haplokinety and turned one and a half times around peristome

and one and a half additional turns on infundibular wall (Figs. 1D, 2E). Epistomial membrane fragmented, located near oral opening and consisted of approximately 10 serial kinetids(Fig. 1D). Germinal kinety parallel to haplokinety and length approximately half of infundibulum(Figs. 1D, 2E). Three infundibular polykinety 1-3(P1-3) consisted of three distinct rows, respectively(Fig. 1D). P1 spirally curved along wall of infundibulum and terminated at posterior half of P3. P2 diverged from P1 near oral opening and terminated in between P1 and P3(Figs. 1D, 2E). P3 commenced near posterior half of P2 and terminated at posterior end of P1 (Fig. 1D). P1 and P3 adjoined abstomally and terminated similar position(Fig. 1D). P2 terminated at the junction of P1 and P3(Fig. 1D). Aboral ciliary wreath composed of din- kinetids, indistinct in vivo, horizontally arranged and located posteriad 3/4 of body length(Fig. 2E, F).

Pellicular striations arranged horizontally and densely, number of striations on zooids 61-80 rows between peristomial lip and aboral ciliary wreath, 18-30 rows between aboral ciliary wreath and scopula(Table 1, Fig. 2F).

Fig. 1. Carchesium polypinum complex in vivo(A-C, E, F) and oral ciliature after protargol impregnation(D). A, Typical zooid; B, Ar- rangement of zooid on stalk and discontinuous spasmoneme(arrowhead); C, E, Various shapes of zooids; D, Detail of oral ciliature and infundibular polykinety 1-3(arrow denotes terminal end of row 1 in P3); F, Shape of colony. A, aboral ciliary wreath; CV, contractile vacuoles; ED, epistomial disc; EM, epistomial membrane; GK, germinal kinety; HK, haplokinety; IF, infundibulum; MA, macronuclei; P1-3, infundibular polykinety 1-3; PK, polykinety; PL, peristomial lips; SP, spasmoneme; ST, stalk. Scale bars: A, C=50 μm, B=100μm, F=500μm.

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Distribution. Austria, Brazil, Canada, China, Denmark, Germany, Japan, Spain, USA, and Korea(present study).

Remarks. Carchesium polypinum complex is common in eutrophic freshwater environments and has worldwide dis-

tribution. Gentekaki and Lynn(2010) assessed that C. polyp- inum consisted of three cryptic species at least, based on the criteria of mitochondrial and nuclear genes(cytochrome c oxidase subunit I and small subunit ribosomal RNA genes),

Fig. 2. Microphotographs of Carchesium polypinum complex in vivo(A-D) protargol impregnated(E) and silver nitrate impregnated(F) specimens. A, B, Typical shapes of colony; C, Arrangement and structure of zooids; D, Discontinuous spasmoneme; E, Oral ciliature and macronucleus(arrow indicate terminal end of row 1 in P3). A, aboral ciliary wreath; CV, contractile vacuoles; HK, haplokinety;

IF, infundibulum; MA, macronucleus; OO, oral opening; PK, polykinety; PL, peristomial lip; SC, scopula; SP, spasmoneme; ST, stalk.

Scale bars: A, B=500μm, C=100μm, D=40μm.

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but major morphological differences could not be found to differentiate them as distinct species. Consequently, C.

polypinum is now termed a “species complex.” Description of the original population named Sertularia polypina was done by Linnaeus(1758), with no illustrations but matches the Korean populations according to their discontinuous spasmoneme.

Two Korean populations of Carchesium polypinum were slightly different in the range of body size, respectively (Table 1). Carchesium polypinum of Jindo population was larger than Yangsan population but the other characters were same. The two Korean populations were similar to Austrian population in terms of branching pattern of colony, size and shape of zooid, and pattern of infundibular polykinety 1-3 (Foissner et al., 1992). The Chinese(Wuhan) and Korean (Jindo) populations were silimilar in length of zooid(100- 130μm vs. 100-140μm). However, the Chinese(Wuhan) and Korean(Yangsan) populations were different in the size (100-130μm vs. 51-82μm)(Shi et al., 2001). The Chinese population was also different to the two Korean populations in the adjoined part of infundibular polykinety 1 and 3(shorter vs. longer)(Shi et al., 2001). The Brazilian(São Pedro stream) population was different to the two Korean populations in the habitat(epizoic vs. benthic vs. benthic) and the length of zooid(70-110μm vs. 51-140μm)(Dias et

al., 2010).

Genus Vorticella Linnaeus, 1767

2. ‌‌Vorticella campanula Ehrenberg, 1831(Table 1, ‌ Figs. 3, 4)

Vorticella campanula Ehrenberg, 1831: 92; 1838: 272; No- land and Finley, 1931: 105; Foissner and Schiffmann, 1974: 500; Warren, 1986: 55; Foissner et al., 1992: 105;

Shi et al., 2003: 64; Qi and Shi, 2008: 9081.

Description. Zooids subconical to inverted bell-shape, length 58-85μm with conspicuously wide peristomial lip, zooid width 45-66μm, asymmetrical shaped. Peristomial lip single- layered, diameter 73-104μm, thickness approximately 6μm (Table 1, Figs. 3A-D, 4A-C). Epistomial disc conspicuously protruded(Figs. 3A-D, 4A-C). Pellicle striped horizontally but weak in live observation.

Cytoplasm predominantly colorless, colored dark, on low magnification, caused by orange to gray food vacuoles(Fig.

4A-C). Single contractile vacuole located ventral side of infundibulum(Figs. 3A-D, 4C). Macronucleus longitudinally arranged and forming J or S shape(Figs. 3A, 4E, F).

Swarmer cylindrical shaped, length approximately 60μm, width approximately 40μm(Fig. 4A). Movement of swarm-

Fig. 3. Vorticella campanula Ehrenberg, 1831 in vivo(A-D), protargol impregnated(E). A, Typical shape of zooid; B-D, Shape vari- ations of zooid; E, Details of oral ciliature and infundibular polykinety 1-3(arrowhead indicate shorter row 1 of P3). A, aboral ciliary wreath; CV, contractile vacuole; ED, epistomial disc; EM, epistomial membrane; GK, germinal kinety; HK, haplokinety; IF, infundibulum; MA, macronuclei; P1-3, infundibular polykinety 1-3; PK, polykinety; PL, peristomial lips; ST, stalk. Scale bar: A=30μm.

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er, swimming posteriad with cilia of aboral ciliary wreath.

Oral ciliature composed of polykinety and haplokinety parallelly and turned one and one-fourth around peristome and one and a half additional turns on infundibular wall (Figs. 3E, 4E, F). Epistomial membrane fragmented, located near oral opening and consisted of approximately serial 7-8 kinetids(Figs. 3E, 4F). Germinal kinety parallel to haplokinety and terminated on the same level of infundibular polykinety 2(Fig. 3E). Three infundibular polykinety 1-3(P1- 3) consisted of three distinct rows, respectively(Fig. 3E). P1 spirally curved along wall of infundibulum and terminated at same level of P3(Figs. 3E, 4E, F). P2 and P1 diverged near oral opening, and P2 terminated at the junction of P1 and P3(Figs. 3E, 4E). P3 commenced near posterior one

third of P2 and terminated at same level of P1 and row 1 of P3 terminated at merging point between P1 and P3(Figs.

3E, 4E). Aboral ciliary wreath composed of dinkinetids, in- distinct in vivo, horizontally arranged and located posteriad 3/4 of body length(Fig. 4G).

Pellicular striations arranged horizontally and densely, number of striations on zooids 64-74 rows between peristomial lip and aboral ciliary wreath, 27-41 rows between aboral ciliary wreath and scopula(Table 1, Fig. 4G).

Distribution. Africa, Austria, China, England, Germany, Netherland, USA, and Korea(present study).

Remarks. Vorticella campanula Ehrenberg, 1831 was main- ly characterized by broadly bulged peristomial lip rather than body width. The two Korean populations of V. campan-

Fig. 4. Microphotographs of Vorticella campanula Ehrenberg, 1831 in vivo(A-D), protargol impregnated(E, F) and silver nitrate impregnated(G) specimens. A, Pseudocolony of zooids(arrow indicates swarmer); B, Typical zooid shape and structure; C, Different shape of zooid and contractile vacuole; D, Stalk and spasmoneme, mitochondrial band; E, Infundibular polykinety 1-3(arrow denote terminal end of row 1 in P3); F, Typical zooid to show details with peristomial lip, epistomial disc and contractile vacuole; F, Terminal part of infundibular polykinety 1-3 and epistomial membrane; G, Silver nitrate impregnated silverlines with aboral ciliary wreath.

A, aboral ciliary wreath; CV, contractile vacuole; ED, epistomial disc; EM, epistomial membrane; FV, food vacuole; IF, infundibulum;

MA, macronuclei; OO, oral opening; P1-3, infundibular polykinety 1-3; PL, peristomial lip; SC, scopula. Scale bars: A=200μm, B, C=30μm, D=10μm.

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ula where collected from Jindo and Busan were morpho- logically same. The two Korean populations conspicuously matched with the zooid shape of the original population (Ehrenberg, 1831). Noland and Finley(1931)’s population was similar to our Korean populations in its conspicuous oral opening, oval shaped body when strongly contracted, and contractile vacuolar position. The German population was also morphologically well matched with the Korean populations(Kahl, 1935).

The Korean and Austrian populations were slightly different in the length of row 1 on infundibular polykinety 3 (shorter vs. longer)(Foissner et al., 1992). The Korean populations were same in every character to the Chinese population(Shi et al., 2003). The pattern of infundibular polykinety in the swammer of other Chinese population was identical to that of Korean population(Qi and Shi, 2008).

Vorticella campanula is closely related to V. marginata Stiller, 1931 but their main differences include macronucleus shape(longitudinal J vs. horizontal U) and the mar- ginal side of its peristomial lip(flattened vs. inverted)(Kahl, 1935; Warren, 1986; Foissner et al., 1992).

ACKNOWLEDGMENTS

This study was supported by the grants from the National Institute of Ecology, funded by the Ministry of Environ- ment of the Republic of Korea and the Basic Science Re- search Program through the National Research Foundation of Korea(NRF) funded by the Ministry of Education(NRF- 2016R1D1A2B03933285, 2015R1D1A09058911).

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Received November 7, 2016 Revised November 24, 2016 Accepted November 25, 2016