Table Of ContentZOOSYSTEMATICA ROSSICA, 18(2): 184–190 25 DECEMBER 2009
Aspidisca beringiana sp. nov. and Simbiodisca subgen. nov.
(Ciliophora, Euplotida), a symbiont of terebellid polychaetes
in the Bering Sea
A.W. JANKOWSKI
A.W. Jankowski, Zoological Institute, Russian Academy of Sciences, Universitetskaya Emb. 1, St. Petersburg
199034, Russia. E-mail: [email protected]
Terebellids in tidal zone of the Bering Island bear three new symbionts – rhabdophryid sucto-
rians, peritrichs with small rosette-like colonies and aspidiscid hypotrich with a long peristome
parallel to left body margin. This is the main feature of a new subgenus of the genus Aspidisca,
named Simbiodisca. It may deserve the full generic rank if the use of protargol silvering method
will not reveal any upper left rudiment of the peristomal membranelles.
Key words: ciliate symbionts, terebellid polychaetes, Bering Sea, Ciliophora, Euplotida, Aspi-
disca, Simbiodisca, new species, new subgenus
INTRODUCTION wood borers) with marine invertebrates
may be facultative. A large genus Aspidisca
Euplotid ciliates are diverse and wide-
Ehrenberg, 1830 with world-wide distribu-
spread in all biotopes – soil, terrophyton
tion includes only free-living species.
(mosses, lichens, grass), in marshes, lakes,
While studying symbionts of marine
rivers, in brackish estuaries and lagoons,
invertebrates on the Bering Island shores
and in the sea, with endemics in Antarctic in 1973, I found an Aspidisca, which is de-
ice areas. Symbiosis in stichotrichid hy- scribed here as a new species and a new sub-
potrichs and in euplotids (Figs 1–4) is an genus, on almost each terebellid polychaete
exception – Kerona Müller, 1786 on Hydra worm collected at low tide near the village
Linnaeus, 1758, two species of Euplotes Eh- of Nikolskoye. Other common symbionts
renberg, 1831 (E. tuffraui Berger, 1965 and were a new genus of rhabdophryid vermi-
facultative E. balteatus (Dujardin, 1841) in genean suctorians for a species attached to
sea urchins, Euplotaspis Chatton & Seguela, host tentacles and new peritrichs, probably
1936 (Fig. 3) in tunicates (Chatton & Seg- Paravorticella Kahl, 1933, forming small ro-
uela, 1936; Burreson, 1973; Hill, 1979b), settes (one to four specimens on the baso-
Paraeuplotes Wichterman, 1942 (Fig. 4) on disc). However, the latter identification is
corals (Wichterman, 1942) and in actinians not certain for the type species of Paravor-
(Welch, 1977). ticella was not described in enough details
In my samples, Euplotaspis occurs in tu- in the literature. Local terebellids were ex-
nicates of the Barents and White seas and on amined later on the Barents Sea coast at the
shores of the southern Sakhalin Island. As- Dalniye Zelentsy Biostation. Aspidisca and
sociations of euplotids Diophrys Dujardin, suctorians were absent from this area and
1841, Uronychia Stein, 1859 (U. bivalvorum the examined worms bearid only commen-
Fenchel, 1965), Gastrocirrhus Lepsi, 1928 sal Urceolaria Stein, 1854, peritrichs with
(G. stentoreus Bullington, 1940 in sponges) another type of the fixon – true Paravorti-
and of several stichotrichs (like Holosticha cella terebellae (Faure-Fremiet, 1920), and
teredorum Tucolesco, 1962, in teredinid some parasitic intestinal astomes.
© 2009 Zoological Institute, Russian Academy of Scienсes
A.W. JANKOWSKI. NEW SPECIES AND NEW SUBGENUS OF EUPLOTID CILIATES 185
a e
aecolhella
cionxant
pis zoo
asc
Euplotmbioti
); sy
2(of
4) rt
6a
9p
uffrau, 1awings;
Tr
d
m: e
e
or
rh
ster (fn of tμm.
1); A. lyncacombinatioale bar: 10
au, 1964) (man, 1942; 5olet (). Sc
Tuffrhteryl-vi
m: Wiceth
yla (fro(from: ed by m
a polystugensis v., stain
Aspidiscotes tortsp. noa
c euplotids: 3); Paraeupla) beringian
bioti36) (odisc
m9bi
y1m
and suela, a (Si
5–. Free-living Chatton & Seg4d) (); Aspidisc
Figs1 (from: omitte
© 2009 Zoological Institute, Russian Academy of Scienсes, Zoosystematica Rossica 18(2): 184–190
186 A.W. JANKOWSKI. NEW SPECIES AND NEW SUBGENUS OF EUPLOTID CILIATES
MATERIAL AND METHODS to prevent cell swelling; after new washing
cells were stained in violet ink, differenti-
Terebellid worms were collected in tid-
ated by acetic acid and enclosed in drop of
al zone of Bering Island and neighbouring
glycerin or sugar solution for study under
Mednyy Island (Commandor Islands) in cover glass. Violet ink, available at sale, is
Summer 1973; each worm was individually made of 2 different stains, acid or basic; this
fixed in jars with 5–8% formalin or in half- may be determined by absence or presence
diluted Bouin’s fluid; both fixatives were of clear water halo surrounding drop of ink
diluted by sea water. Isolated symbionts on filter paper. Only basic stain (methyl vi-
(peritrichs, suctorians and a new species olet) may be used, because acid ink does not
of Aspidisca described in this article) were permit differentiation of overstained cells.
accumulated in drops of diluted sugar on The figures 5–7 are made from such cells
object glass, that was slowly drying (during stained with basic ink.
2–3 weeks).
In spite of crystallization, dry sugar per-
TAXONOMIC PART
fectly retains ciliates and this method is
commonly used by me for peritrichs and suc- Order EUPLOTIDA Jankowski, 1980
torians, for isolated cells or those intact on
This order is sometimes attributed to
their small hosts (hydroids, nematodes, co-
Small and Lynn (1985) but the author and
pepods, ostracods, mites). Stored cells may
date as given here are correct for the order
be liberated after adding a drop of water to
was described (Jankowski, 1980) in a valid
dry sugar. Before drying, sugar remains long
way (for comments see Jankowski, 2007:
time in dense colloid-like state and fixed
480).
material is gradually saturated with sugar of
raised concentration and thus persists crys-
Family ASPIDISCIDAE Ehrenberg, 1838
tallization. But now I prefer accumulation
and storage of isolated fixed cells in glyc-
Genus Aspidisca Ehrenberg, 1830
erin drops in Petri dishes, to prevent from
Aspidisca beringiana sp. nov.
dust, or on object slides, in pure glycerin or
(Figs 5–7)
in glycerin with hardener – smallest drop of
diluted polyethylene-glycol 4000.
Hapantotype. A slide, 2001-14 (30 for-
Only fixed material was studied in 2001,
mol-fixed unstained specimens enclosed
near 30 years after fixation of samples. At to drop of diluted sugar and then dried),
any fixation (less in diluted glutaraldehyde, deposited in the Laboratory of Protozool-
strongly in formalin) proteins are coagulat- ogy, Zoological Institute, Academy of Sci-
ed, transparency is lost, and study of small- ences, Saint Petersburg, Russia. The Ber-
est ciliates becomes difficult. Protargol ing Island shores at Nikolskoye, 1973, coll.
staining was not used; to reveal kinetome, A.W. Jankowski.
I have used my method (Jankowski, 2007: Diagnosis. Body clear, flat, elongate-
467) with few modifications. Although it ovoid, with narrow, somewhat pointed
was proposed for large hypotrichs only (like anterior part (anteron or apex); general
Oxytricha Bory de Saint Vincent, 1824, Sty- body shape resembles that of symbiotic
lonychia Ehrenberg, 1830 and Urostyla Eh- hypostome Allosphaerium Kidder & Sum-
renberg, 1830), I obtained good staining of mers, 1935, inhabiting talitrid amphipods
cirri in a species under study, except area of in the same region. Narrow hyaline margin
peristomal rudiments, too small and heavily or kiel surrounds entire body; body surface
granulated. Formol-fixed cells were isolat- with few folds; cytoplasm densely granu-
ed, washed in water and refixed in mixture lated (layer of mitochondria); food vacu-
of phosphotungstic acid with few glycerol, oles without refractile inclusions, such as
© 2009 Zoological Institute, Russian Academy of Scienсes, Zoosystematica Rossica 18(2): 184–190
A.W. JANKOWSKI. NEW SPECIES AND NEW SUBGENUS OF EUPLOTID CILIATES 187
-
s
u
d
e
al
e
v
e
r
t
o
n
s
e i
m
o
t
s
ri
e
p
e
h
t
of
t
n
e
m
g
a
r
r f
e
p
p
u
e
h
T
m.
μ
0
1
r:
a
b
e
al
c
S
t.
e
ol
vi
-
yl
h
t
e
m
y
b
d
e
n
ai
t
s
v.,
o
n
p.
s
a
n
a
gi
rinnt.
bese
) b
aa
cs
biodisor it i
md
a (Sietho
cm
disg
spinin
Aai
6, 7. his st
gs g t
Fin
i
© 2009 Zoological Institute, Russian Academy of Scienсes, Zoosystematica Rossica 18(2): 184–190
188 A.W. JANKOWSKI. NEW SPECIES AND NEW SUBGENUS OF EUPLOTID CILIATES
diatoms. Macronucleus inverse V-shaped, ous membranelles, but it retains rhomboid
usually with slightly unequal branches; mi- shape with sharp diminution of membranel-
cronucleus, possibly pale or small, was not lar width to the upper end (Deroux &Tuf-
detected after staining with acidified meth- frau, 1965; Li et al., 2008).
yl-green. Except this species, any modern descrip-
Body size “in fixo” (not contracted in tion of Aspidisca made by 4 procedures of sil-
balsam; measurements of 10 cells in forma- vering (methods of Klein, Chatton & Lwoff,
lin or sublimate at oil immersion, 10 × 90) Bodian and Fernandez-Galiano) may be
67–76 × 48–54 μm. used for comparison with a new symbiont,
As usually in euplotids, cilia compos- and all free-living species of Aspidisca are
ing cirri are separated at fixation and look different from A. beringiana in peristomal
like brushes or bundles, not as cones unlike shape and membranellar pattern. Some ex-
those in living ciliates. The ventral kinetome amples of this vast literature are publica-
includes 7 somatic cirri in 2 groups (4 + 3) tions of Tuffrau (1964), Hill (1979a), Foiss-
and 5–6 caudal cirri in diagonal row. The ner (1982), Dragesco & Dragesco-Kerneis
peristome is long, extends parallel to the (1986), Foissner et al. (1991), Augustin &
left body margin as a wide slightly curved Foissner (1992), Pang & Fu (1992), Song
cross-striated stripe with near 25–28 trans- (1995, 2003), Wang et al. (1997), Song &
versal membranelles; their bases are dimin- Wilbert (2002), Chen & Song (2002), Song
ished at size to both ends of a stripe, but & Warren (2009).
not so sharply as in other aspidiscids. The Any large genus must include sub-
absence of upper rudiment on the drawings groups – groups of species that may be
does not mean its absence in ciliates; it was recognized as subgenera by structural fea-
not distinctly revealed in fixed cells after tures of minute significance. Example in
long storage in formalin; this species must ciliates is Paramecium Müller, 1773 with 3
be restudied later with protargol silvering. subgenera based on body shape and degree
The argyrome and the dorsal setae were not of peristomal shift from cell apex. Attempt
revealed by the ink staining used. to distinguish subgenera in Aspidisca was
Hosts: terebellid polychetes (family Te- made by me (Jankowski, 1979, 2007: 489) –
re bellidae Malmgren, 1867) with dense subgenera Aspidisca Ehrenberg, 1830 s. str.,
crown of cephalic tentacles Neoamphi- Dimaspidisca Jankowski, 1979 and Netas-
trite figulus (Dalyell, 1853) and Thelepus pidisca Jankowski, 1979, were based, like
cincinnatus (Fabricius, 1780); additional those in Euplotes, on the pattern of dorsal
host – Cirratulus cirratus (Müller, 1776), argyrome. This alveolar net is difficult for
belonging to another family of polychaetes silvering and is rarely revealed in Aspidisca.
(Cirratulidae Ryckholt, 1851) with somatic Three groups of species distinguished
tentacles on somites. The site of sampling – in Aspidisca (Wu & Curds, 1979; Borror &
littoral at low tide near Nikolskoye, Bering Hill, 1995) are based on presence or absence
Island, and on Mednyj Island (Commandor of small additional cirri and, if present, on
Islands, Bering Sea). their location; these groups were not re-
garded as subgenera and have not received
Latin names. At present, subgeneric value of
DISCUSSION
dorsal argyrome pattern is denied in related
Almost all species of Aspidisca Ehren- genus Euplotes, and this genus was split into
berg, 1830 have small diagonal rhombic several genera with different cirral pattern
peristome with few membranelles (exam- (Borror & Hill, 1995). Thus separation of
ples: Figs 1, 2). Only A. orthopogon Deroux the above mentioned subgenera in Aspidisca
& Tuffrau, 1965 is an exception – it has based on differences in dorsal argyrome also
very long peristome composed of numer- is not acceptable, and instead only two dis-
© 2009 Zoological Institute, Russian Academy of Scienсes, Zoosystematica Rossica 18(2): 184–190
A.W. JANKOWSKI. NEW SPECIES AND NEW SUBGENUS OF EUPLOTID CILIATES 189
tinct groups of species (subgenera) may be mèdiaire entre les Euplotidae et les Aspidis-
distinguished – Aspidisca Ehrenberg, 1830 cidae: Euplotaspis cionaecola n. g., n. sp. Bul-
s. str. with small rhombic oblique peristome letin de la Sociètè Zoologique de France, 61:
332–340.
carrying few diagonal membranelles and
Chen, Z. & Song, W. 2002. Phylogenetic posi-
Simbiodisca subgen. nov. with a long peris-
tions of Aspidisca steini and Euplotes vannus
tome extending along almost the entire left
within the order Euplotida (Hypotrichia:
cell margin, and carrying a large number of
Ciliophora) inferred from complete small
transversal membranelles.
subunit ribosomal RNA gene sequences. Acta
Simbiodisca may be regarded as an inter- Protozoologica, 41: 1–9.
mediate form between ancestral euplotids, Deroux, G. & Tuffrau, M. 1965. Aspidisca ortho-
which possess a complete peristome typical pogon, n. sp. Rèvision de certains mècanismes
for the hypotrichs, with anterior and lateral de la morphogenèse a l’aide de une modifica-
zones, and Aspidisca s. str. with two rudi- tion de la tèchnique au protargol. Cahiers de
ments of the ancestral peristomal stripe. Biologie Marine, 6: 293–310.
Dragesco, J. & Dragesco-Kerneis, A. 1986. Ci-
liès libres de l’Afrique intertropicale. Faune
Simbiodisca subgen. nov.
Tropicale, 36: 1–559.
Foissner, W. 1982. Ökologie und Taxonomie der
Gender. Feminine.
Hypotrichida (Protozoa: Ciliophora) einiger
Etymology. Subgeneric name is a combi- Österreichischer Boden. Archiv für Protisten-
nation of a word “symbiosis” with a generic
kunde, 126: 19–143.
name Aspidisca. Foissner, W., Blatterer, H., Berger, H. & Koh-
Type species: Aspidisca beringiana sp. nov. mann, F. 1991. Taxonomische und ökologi-
Diagnosis. A long peristome; retention sche Revision der Ciliaten des Saprobiensy-
of a long membranellar stripe along the left stems. Band I. Cyrtophorida, Oligotrichida,
body margin. Other characters as described Hypotrichia, Colpodea. Informations-Be-
richte der Bayerischen Landesamtes für Was-
for the type species.
serwirtschaft, München, 1/91: 1–478.
Included species: type species.
Hill, B.F. 1979a. Reconsideration of cortical
Remark. If any anterior segment (rudi-
morphogenesis during cell division in Aspi-
ment) of a stripe is not revealed in the future
disca (Ciliophora, Hypotrichida). Transac-
by using silver protein or ammoniacal silver
tions of the American Microscopical Society,
staining methods (the methods of Bodian 98: 537–542.
and Fernandez-Galiano), this subgenus will Hill, B.F. 1979b. Structure and cortical morpho-
need to be raised to the generic level. genesis during cell division in Euplotaspis
cionaecola Chatton and Seguela, 1936 (Cil-
iophora, Hypotrichida). Journal of Protozool-
REFERENCES
ogy, 26, Supplement 3(1): 18.
Augustin, H. & Foissner, W. 1992. Morpholo- Jankowski, A.W. 1979. Taxonomy and phylog-
gie und Ökologie einiger Ciliaten (Protozoa: eny of the order Hypotrichida Stein, 1859
Ciliophora) aus dem Belebtschlamm. Archiv (Protozoa, Ciliophora). Proceedings of the
für Protistenkunde, 141: 243–283. Zoological Institute, Russian Academy of Sci-
Borror, A.Ch. & Hill, B. F.1995. The order Eup- ences, 85: 48–85. (In Russian).
lotida (Ciliophora): taxonomy, with division Jankowski, A.W. 1980. Conspectus of a new
of Euplotes into several genera. Journal of Eu- system of the phylum Ciliophora Doflein,
karyotic Microbiology, 42: 457–466. 1901. Proceedings of the Zoological Institute,
Burreson, E.M. 1973. Symbiotic ciliates from Russian Academy of Sciences, 94: 103–121.
solitary ascidians in the Pacific Northwest, (In Russian).
with a description of Parahypocoma rham- Jankowski, A.W. 2007. Phylum Ciliophora Do-
phisokarya n. sp. Transactions of the American flein, 1901. Review of taxa. In: Alimov, A.F.
Microscopical Society, 92: 517–522. (Ed.). Rukovodstvo po zoologii [Guide to Zo-
Chatton, E. & Seguela, J. 1936. Un hypotriche ology]. Protists, 2. Nauka, Saint Petersburg:
de la branchie de Ciona intestinalis L., inter- 415–993. (In Russian).
© 2009 Zoological Institute, Russian Academy of Scienсes, Zoosystematica Rossica 18(2): 184–190
190 A.W. JANKOWSKI. NEW SPECIES AND NEW SUBGENUS OF EUPLOTID CILIATES
Li, L., Shao, Ch., Yi, Zh., Song, W., Warren, Free-living ciliates in the Bohai and Yellow
A., Al-Rasheid, K.A.S., Al-Farraj, S.A., seas, China. Science Press, Beijing: 415–459.
Al-Quraishy, S. A., Zhang, Q.Q., Hu, X., Song, W. & Wilbert, N. 2002. Faunistic studies
Zhu, M., Ma, H. 2008. Redescriptions and on marine ciliates from the Antarctic benthic
SSrRNA gene sequence analyses of two ma- area, including descriptions of one epizoic
rine species of Aspidisca (Ciliophora, Eup- form, 6 new species, and 2 new genera (Pro-
lotida) with notes on morphogenesis in A. tozoa: Ciliophora). Acta Protozoologica, 41:
orthopogon. Acta Protozoologica, 47: 83–94. 23–61.
Pang, Y. & Fu, Z. 1992. The morphology and Tuffrau, M. 1964. La morphogenèse de biparti-
morphogenesis of Aspidisca costata. Journal tion et les structures neuromotrices dans le
of the East China Normal University, Supple- genre Aspidisca (ciliès hypotriches). Rèvue
ment 1992: 91–100. de quelques espèces. Cahiers de Biologie Ma-
Small, E.B. & Lynn, D.H. 1985. Phylum Cilio- rine, 5: 173–199.
phora Doflein, 1901. In: Lee, J.J., Hutner, Wang, M., Mu, Zh., Zhang, Sh. & Song, W.
S.H. & Bovee, E.C. (Ed.). An illustrated 1997. Morphogenesis of Aspidisca pulcher-
guide to the Protozoa. Society of Proto- rima (Protozoa: Ciliophora). Zoological Re-
zoologists, Allen Press, Lawrence, Kansas: search, 18: 185–188.
393–575. Welch, M.P. 1977. The apostome Foettingeria and
Song, W. 1995. Preliminary studies on the phy- other ciliate symbionts from the sea anemo-
logenetic relationship of genera within the ne Bunodosoma cavernata from Galveston
family Euplotidae (Ciliophora, Hypotrichi- Island, Texas. Transactions of the American
da). Oceanologica et Limnologica Sinica, 26: Microscopical Society, 96: 489–496.
Wichterman, R. 1942. A new ciliate from a coral
527–534.
of Tortugas and its symbiotic zooxanthellae.
Song, W. 2003.Reconsideration of the morpho-
Papers from the Tortugas Laboratory, Carnegie
genesis in the marine hypotrichous ciliate,
Institution of Washington, 524: 105–111.
Aspidisca leptaspis Fresenius, 1865 (Proto-
Wu, I.C.H. & Curds, C.R. 1979. A guide to the
zoa, Ciliophora). European Journal of Protis-
species of the genus Aspidisca. Bulletin of the
tology, 39: 53–61.
British Museum (Natural History), Zoology
Song, W. & Warren, A. 2009. Chapter 12. Pro-
Series, 36: 1–34.
tohypotrichs, discocephalids and euplotids.
In: Song, W., Warren, A. & Hu, X. (Ed.). Received 5 October 2009 / Accepted 20 November 2009
© 2009 Zoological Institute, Russian Academy of Scienсes, Zoosystematica Rossica 18(2): 184–190
