Two Newly Recorded Vorticellid Species (Ciliophora, Oligohymenophorea, Peritrichia) from Jindo Island with Other Populations in Korea

2016·4.6 MB·

by  Ji Hye Kim

Anim. Syst. Evol. Divers. Special Issue, No. 9: 10-17, December 2016
https://doi.org/10.5635/ASED.2016.SIN9.042
Review article
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
INTRODUCTION distinguishable based on the morphology. Therefore, it was
designated as a cryptic species complex (Gentekaki and Lynn,
The family Vorticellidae Ehrenberg, 1838 is one of highly 2010). We collected the two species from Jindo Island and
diverse taxa within the group Peritrichia and is characterized other places with morphological redescriptions. Carchesium
by zooid, contractible, and helically twisted spasmoneme polypinum complex and Vorticella campanula Ehrenberg,
(Ehrenberg, 1838; Corliss, 1979; Warren, 1986; Lynn, 2008; 1831 are newly described species in Korea.
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- MATERIALS AND METHODS
sium and Vorticella are distinguishable from each other by
the key character of colonial versus solitary life form (Cor- Carchesium polypinum complex were collected from a small
liss, 1979; Lynn and Small, 2000; Lynn, 2008). According freshwater pond on Gahak-ri, Jisan-myeon, Mt. Geupchisan
to Gentekaki and Lynn (2010), Carchesium polypinum com- of Jindo Island (34°24′07″N, 126°06′42″E) on 8 Jul 2016
plex might be firstly described by Leeuwenhoek in 1676 and a small pond next to a stream in Habuk-myeon, Yang-
and Linnaeus (1758) officially described. Thereafter, many san-si (35°29′12″N, 129°03′25″E) on 22 Nov 2013. Vorti-
researchers redescribed C. polypinum (Esteban and Fernán- cella campanula was collected with debris and freshwater in
dez-Galiano, 1989; Foissner et al., 1992; Shi et al., 2001; an agricultural pond in Na-ri, Gunnae-myeon, Jindo Island
Dias et al., 2010). However, populations of C. carchesium (34°33′45″N, 126°16′02″E) on 9 Jul 2016 and a freshwater
had enormous amount of genetic differences but could not pond in Gangdong-dong, Gangseo-gu, Busan (35°12′43″N,
This is an Open Access article distributed under the terms of the Creative *To whom correspondence should be addressed
Commons Attribution Non-Commercial License (http://creativecommons.org/ Tel: [phone], Fax: [phone]
licenses/by-nc/3.0/) which permits unrestricted non-commercial use, distribution, E-mail: [email protected]
and reproduction in any medium, provided the original work is properly cited.
pISSN 2234-6953 eISSN 2234-8190 Copyright The Korean Society of Systematic Zoology
Two Vorticellid Species in Korea
128°55′59″E) on 29 Nov 2013. Water samples were collect- Subclass Peritrichia Stein, 1859
ed and transferred with debris in raw cultural petri dishes Order Sessilida Kahl, 1933
and then maintained at room temperature in a laboratory for Family Vorticellidae Ehrenberg, 1838
one to five days. The cells were cultured using wheat grains Genus Carchesium Ehrenberg, 1830
added in raw cultural Petri dishes for enrichment of bacteria
and ciliates (Foissner et al., 2009). Silver staining methods 1. Carchesium polypinum complex (Table 1, Figs. 1, 2)
was performed by Wilbert (1975) and Foissner (1991). The Sertularia polypina Linnaeus, 1758: 816.
two species were described by live and silver impregnat- Carchesium polypinum: Ehrenberg, 1830: 41; Stein, 1854:
ed cells observations using a stereo microscope (SMZ800; 78; Kahl, 1935: 738; Foissner and Schiffmann, 1974: 491,
Nikon, Tokyo, Japan) and an optical microscope (Axio Im- 504; Esteban and Fernández-Galiano, 1989: 345; Foissner
ager A1; Carl Zeiss, Oberkochen, Germany), morphometry, et al., 1992: 137; Shi et al., 2001: 13; Dias et al., 2010:
line drawings, and microphotographs using a CCD camera 483.
(Axio Cam MRc; Carl Zeiss). Classification and terminolo-
gy follows Lynn (2008) and Ji et al. (2015). Description. Colony outline funnel and fan-shaped, approx-
imately 2,000 μm high and contain 10-50 zooids (Figs. 1F,
2A, B). Macrozooid absent. Stalk flexible and contractile,
SYSTEMATIC ACCOUNTS primary stalk dichotomously branched, secondary to termi-
nal stalks polychotomously or irregularly branched (Figs.
Phylum Ciliophora Doflein, 1901 1B, F, 2A, B). Stalk surface smooth, gap between holdfast
Class Oligohymenophorea de Puytorac, Batisse, Bohatier, and starting point of spasmoneme on primary stalk approxi-
Corliss, Deroux, Didier, 1974 mately 80 μm, primary stalk diameter about 35 μm, 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 Cp. Jin. 69 61 80 68 6.9 3.1 10.0 5
lip to aboral ciliary wreath 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 Cp. Jin. 26 18 30 28 5.0 2.2 19.6 5
wreath to scopula 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.
Anim. Syst. Evol. Divers. Special Issue (9), 10-17 11
Ji Hye Kim, Mann Kyoon Shin
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, con-
tractile vacuoles; ED, epistomial disc; EM, epistomial membrane; GK, germinal kinety; HK, haplokinety; IF, infundibulum; MA, mac-
ronuclei; P1-3, infundibular polykinety 1-3; PK, polykinety; PL, peristomial lips; SP, spasmoneme; ST, stalk. Scale bars: A, C 50
μm, B 100 μm, F 500 μm.
=
= =
stalk diameter about 9 μm. Spasmoneme discontinuous on and one and a half additional turns on infundibular wall
each branching points (Figs. 1B, F, 2D). Zooids located dis- (Figs. 1D, 2E). Epistomial membrane fragmented, located
tal end of terminal stalk (Figs. 1F, 2A, B). near oral opening and consisted of approximately 10 serial
Zooids subconical to inverted bell-shape, length 100-140 kinetids (Fig. 1D). Germinal kinety parallel to haplokinety
μm in Jindo population and 51-82 μm in Yangsan popula- and length approximately half of infundibulum (Figs. 1D,
tion, width 60-80 μm in Jindo population and 31-46 μm in 2E). Three infundibular polykinety 1-3 (P1-3) consisted of
Yangsan population, zooids relatively symmetrical, some- three distinct rows, respectively (Fig. 1D). P1 spirally curved
times asymmetrical caused by movement or food vacuoles along wall of infundibulum and terminated at posterior half
(Table 1, Figs. 1A, C, 2C). Peristomial lip single-layered, of P3. P2 diverged from P1 near oral opening and terminated
diameter 49-95 μm, thickness approximately 8 μm (Table in between P1 and P3 (Figs. 1D, 2E). P3 commenced near
1, Figs. 1A-C, E, 2C). Epistomial disc flattened (Figs. 1A, posterior half of P2 and terminated at posterior end of P1
2C). Pellicle striped horizontally (Fig. 2F). (Fig. 1D). P1 and P3 adjoined abstomally and terminated
Cytoplasm predominantly colorless, sometimes brownish similar position (Fig. 1D). P2 terminated at the junction of
to grayish caused by food vacuolar color on low magnifica- P1 and P3 (Fig. 1D). Aboral ciliary wreath composed of din-
tion (Fig. 2A-C). Single contractile vacuole located ventral kinetids, indistinct in vivo, horizontally arranged and located
side of infundibulum (Figs. 1A, 2C). Macronucleus longitu- posteriad 3/4 of body length (Fig. 2E, F).
dinally arranged and forming J or S shape (Figs. 1A-C, E, Pellicular striations arranged horizontally and densely,
2E). number of striations on zooids 61-80 rows between peri-
Oral ciliature composed of parallel polykinety and hap- stomial lip and aboral ciliary wreath, 18-30 rows between
lokinety and turned one and a half times around peristome aboral ciliary wreath and scopula (Table 1, Fig. 2F).
12 Anim. Syst. Evol. Divers. Special Issue (9), 10-17
Two Vorticellid Species in Korea
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 500 μm, C 100 μm, D 40 μm.
= = =
Distribution. Austria, Brazil, Canada, China, Denmark, tribution. Gentekaki and Lynn (2010) assessed that C. polyp-
Germany, Japan, Spain, USA, and Korea (present study). inum consisted of three cryptic species at least, based on the
Remarks. Carchesium polypinum complex is common in criteria of mitochondrial and nuclear genes (cytochrome c
eutrophic freshwater environments and has worldwide dis- oxidase subunit I and small subunit ribosomal RNA genes),
Anim. Syst. Evol. Divers. Special Issue (9), 10-17 13
Ji Hye Kim, Mann Kyoon Shin
but major morphological differences could not be found al., 2010).
to differentiate them as distinct species. Consequently, C.
polypinum is now termed a “species complex.” Description Genus Vorticella Linnaeus, 1767
of the original population named Sertularia polypina was
done by Linnaeus (1758), with no illustrations but matches 2. ‌V‌orticella campanula Ehrenberg, 1831 (Table 1, ‌
the Korean populations according to their discontinuous Figs. 3, 4)
spasmoneme. Vorticella campanula Ehrenberg, 1831: 92; 1838: 272; No-
Two Korean populations of Carchesium polypinum were land and Finley, 1931: 105; Foissner and Schiffmann,
slightly different in the range of body size, respectively 1974: 500; Warren, 1986: 55; Foissner et al., 1992: 105;
(Table 1). Carchesium polypinum of Jindo population was Shi et al., 2003: 64; Qi and Shi, 2008: 9081.
larger than Yangsan population but the other characters were
same. The two Korean populations were similar to Austrian Description. Zooids subconical to inverted bell-shape, length
population in terms of branching pattern of colony, size and 58-85 μm with conspicuously wide peristomial lip, zooid
shape of zooid, and pattern of infundibular polykinety 1-3 width 45-66 μm, asymmetrical shaped. Peristomial lip single-
(Foissner et al., 1992). The Chinese (Wuhan) and Korean layered, diameter 73-104 μm, thickness approximately 6 μm
(Jindo) populations were silimilar in length of zooid (100- (Table 1, Figs. 3A-D, 4A-C). Epistomial disc conspicuous-
130 μm vs. 100-140 μm). However, the Chinese (Wuhan) ly protruded (Figs. 3A-D, 4A-C). Pellicle striped horizon-
and Korean (Yangsan) populations were different in the size tally but weak in live observation.
(100-130 μm vs. 51-82 μm) (Shi et al., 2001). The Chinese Cytoplasm predominantly colorless, colored dark, on low
population was also different to the two Korean popula- magnification, caused by orange to gray food vacuoles (Fig.
tions in the adjoined part of infundibular polykinety 1 and 4A-C). Single contractile vacuole located ventral side of in-
3 (shorter vs. longer) (Shi et al., 2001). The Brazilian (São fundibulum (Figs. 3A-D, 4C). Macronucleus longitudinally
Pedro stream) population was different to the two Korean arranged and forming J or S shape (Figs. 3A, 4E, F).
populations in the habitat (epizoic vs. benthic vs. benthic) Swarmer cylindrical shaped, length approximately 60 μm,
and the length of zooid (70-110 μm vs. 51-140 μm) (Dias et width approximately 40 μm (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, infundib-
ulum; MA, macronuclei; P1-3, infundibular polykinety 1-3; PK, polykinety; PL, peristomial lips; ST, stalk. Scale bar: A 30 μm.
=
14 Anim. Syst. Evol. Divers. Special Issue (9), 10-17
Two Vorticellid Species in Korea
Fig. 4. Microphotographs of Vorticella campanula Ehrenberg, 1831 in vivo (A-D), protargol impregnated (E, F) and silver nitrate im-
pregnated (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 200 μm, B,
C 30 μm, D 10 μm.
=
= =
er, swimming posteriad with cilia of aboral ciliary wreath. third of P2 and terminated at same level of P1 and row 1 of
Oral ciliature composed of polykinety and haplokinety P3 terminated at merging point between P1 and P3 (Figs.
parallelly and turned one and one-fourth around peristome 3E, 4E). Aboral ciliary wreath composed of dinkinetids, in-
and one and a half additional turns on infundibular wall distinct in vivo, horizontally arranged and located posteriad
(Figs. 3E, 4E, F). Epistomial membrane fragmented, located 3/4 of body length (Fig. 4G).
near oral opening and consisted of approximately serial 7-8 Pellicular striations arranged horizontally and densely,
kinetids (Figs. 3E, 4F). Germinal kinety parallel to haploki- number of striations on zooids 64-74 rows between peri-
nety and terminated on the same level of infundibular poly- stomial lip and aboral ciliary wreath, 27-41 rows between
kinety 2 (Fig. 3E). Three infundibular polykinety 1-3 (P1- aboral ciliary wreath and scopula (Table 1, Fig. 4G).
3) consisted of three distinct rows, respectively (Fig. 3E). P1 Distribution. Africa, Austria, China, England, Germany,
spirally curved along wall of infundibulum and terminated Netherland, USA, and Korea (present study).
at same level of P3 (Figs. 3E, 4E, F). P2 and P1 diverged Remarks. Vorticella campanula Ehrenberg, 1831 was main-
near oral opening, and P2 terminated at the junction of P1 ly characterized by broadly bulged peristomial lip rather
and P3 (Figs. 3E, 4E). P3 commenced near posterior one than body width. The two Korean populations of V. campan-
Anim. Syst. Evol. Divers. Special Issue (9), 10-17 15
Ji Hye Kim, Mann Kyoon Shin
ula where collected from Jindo and Busan were morpho- kalische Klasse, 1831:1-154.
logically same. The two Korean populations conspicuously Ehrenberg CG, 1838. Die Infusionsthierchen als Vollkommene
matched with the zooid shape of the original population Organismen. Ein Blick in das tiefere organische Leben der
(Ehrenberg, 1831). Noland and Finley (1931)’s population Naur. Verlag von Leopold Voss, Leipzig, pp. 1-548.
Esteban G, Fernández-Galiano D, 1989. Morphology and mor-
was similar to our Korean populations in its conspicuous
phogenesis in Carchesium polypinum (Ciliophora: Per-
oral opening, oval shaped body when strongly contracted,
itrichida). Transactions of the American Microscopic Soci-
and contractile vacuolar position. The German population
ety, 108:345-353.
was also morphologically well matched with the Korean
Foissner W, 1991. Basic light and scanning electron micro-
populations (Kahl, 1935).
scopic methods for taxonomic studies of ciliated protozoa.
The Korean and Austrian populations were slightly dif-
European Journal of Protistology, 27:313-330. https://doi.
ferent in the length of row 1 on infundibular polykinety 3 org/10.1016/S0932-4739(11)80248-8
(shorter vs. longer) (Foissner et al., 1992). The Korean popu- Foissner W, Berger H, Kohmann F, 1992. Taxonomische und
lations were same in every character to the Chinese popula- ökologische Revision der Ciliaten des Saprobiensystems
tion (Shi et al., 2003). The pattern of infundibular polykinety - Band II: Peritrichida, Heterotrichida, Odontostomtida.
in the swammer of other Chinese population was identical Informations berichte der Bayer. Landesamtes Wasser-
to that of Korean population (Qi and Shi, 2008). wirtschaft, 5:1-502.
Foissner W, Blake N, Wolf K, Breiner HW, Stoeck T, 2009.
Vorticella campanula is closely related to V. marginata
Morphological and molecular characterization of some
Stiller, 1931 but their main differences include macronu-
peritrichs (Ciliophora: Peritrichida) from tank bromeliads,
cleus shape (longitudinal J vs. horizontal U) and the mar-
including two new genera: Orborhabdostyla and Vorticel-
ginal side of its peristomial lip (flattened vs. inverted) (Kahl,
lides. Acta Protozoologica, 48:291-319.
1935; Warren, 1986; Foissner et al., 1992).
Foissner W, Schiffmann H, 1974. Vergleichende Studien an
argyrophilen Strukturen von vierzehn peritrichen Ciliaten.
Protistologica, 10:489-508.
ACKNOWLEDGMENTS
Gentekaki E, Lynn DH, 2010. Evidence of cryptic speciation in
Carchesium polypinum Linnaeus, 1758 (Ciliophora: Peritri-
This study was supported by the grants from the National chia) inferred from mitochondrial, nuclear, and molpholog-
Institute of Ecology, funded by the Ministry of Environ- ical markers. Journal of Eukaryotic Microbiology, 57:508-
ment of the Republic of Korea and the Basic Science Re- 519. https://doi.org/10.1111/j.1550-7408.2010.00505.x
search Program through the National Research Foundation Ji D, Kim JH, Shazib SUA, Sun P, Li L, Shin MK, 2015. Two
of Korea (NRF) funded by the Ministry of Education (NRF- new species of Zoothamnium (Ciliophora, Peritrichia) from
Korea, with new observations of Z. parahentscheli Sun et
2016R1D1A2B03933285, 2015R1D1A09058911).
al., 2009. Journal of Eukaryotic Microbiology, 62:505-518.
https://doi.org/10.1111/jeu.12205
Kahl A, 1935. Urtiere oder Protozoa I: Wimpertiere oder Cil-
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Received November 7, 2016
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Revised November 24, 2016
the three morphologically similar genera Carchesium, Epi- Accepted November 25, 2016
Anim. Syst. Evol. Divers. Special Issue (9), 10-17 17