ARTICLE IN PRESS

European Journal of

PROTISTOLOGY

0932-4739/$ - se

doi:10.1016/j.ej

�CorrespondE-mail addr

European Journal of Protistology 43 (2007) 27–35

www.elsevier.de/ejop

Redescriptions of two marine planktonic ciliates from China, Parastrombi-dium faurei (Kahl, 1932) Maeda, 1986 and Strombidium capitatum (Lee-

gaard, 1915) Kahl, 1932 (Ciliophora, Oligotrichea)

Dapeng Xua, Weibo Songa,�, Alan Warrenb, Dave Robertsb, Xiaozhong Hua

aLaboratory of Protozoology, Ocean University of China, Qingdao 266003, ChinabDepartment of Zoology, Natural History Museum, Cromwell Road, London SW7 5BD, UK

Received 16 May 2006; received in revised form 6 September 2006; 26 September 2006

Accepted 27 September 2006

Abstract

The morphology and infraciliature of two marine planktonic ciliates, Parastrombidium faurei (Kahl, 1932) Maeda,1986 and Strombidium capitatum (Leegaard, 1915) Kahl, 1932, from coastal waters near Qingdao (Tsingtao), northernChina, were investigated based on live observation and protargol impregnation. This is the first time that these twospecies are reported from Yellow Sea/North Pacific. Emended diagnoses for the genus Parastrombidium and its singlespecies P. faurei are provided as they were not studied with modern methods before. The ciliary pattern and thestomatogenesis of Parastrombidium indicate that it belongs to the order Choreotrichida Small and Lynn, 1985, familyStrombidinopsidae Small and Lynn, 1985. An updated description for the ‘‘well-known’’ Strombidium capitatum is alsoincluded based on the Qingdao population.r 2006 Elsevier GmbH. All rights reserved.

Keywords: Choreotrichida; Morphology; Silverstain; Oligotrichida; Taxonomy

Introduction

Planktonic ciliates, especially oligotrichs, are animportant component in the marine microbial foodweb, part of which is referred to as the microbial loop(Azam et al. 1983), and they make substantial contribu-tions to trophic fluxes and nutrient cycling (Laybourn-Parry 1992; Pierce and Turner 1992). To date, about 200oligotrichids and aloricate choreotrichids have beenreported, of which �60% have been described, or

e front matter r 2006 Elsevier GmbH. All rights reserved.

op.2006.09.005

ing author.

ess: wsong@ouc.edu.cn (W. Song).

redescribed using modern methods. But there are stilllarge gaps in our knowledge of these taxa, and manyambiguities concerning the identification of taxa withinthis species-rich group need to be resolved.

During faunistic surveys on planktonic ciliates incoastal waters near Qingdao, northern China, manyoligotrich ciliates were found. Two species of those thatattracted our attention, Parastrombidium faurei (Kahl,1932) Maeda, 1986 and Strombidium capitatum (Lee-gaard, 1915) Kahl, 1932, were studied using modernmethods. Improved descriptions of these two species arepresented here and an updated diagnosis of the genusParastrombidium is supplied.

ARTICLE IN PRESSD. Xu et al. / European Journal of Protistology 43 (2007) 27–3528

Materials and methods

Sample collection: Samples were collected using 20 mmmesh plankton nets from coastal waters near Qingdao(Tsingtao, 361080N; 1201430E), China. Parastrombidium

faurei was isolated in May 2004 (salinity 27%, pH ca.7.9, water temperature ca. 17 1C). Strombidium capita-

tum was found in March 2005 (salinity 33%, pH ca. 8.2,water temperature ca. 12 1C).

Morphological investigations: The behaviour of bothspecies was observed in Petri dishes under a dissectingmicroscope. The morphology was investigated withdifferential interference contrast microscopy. The infra-ciliature was revealed by protargol impregnation (Wil-bert 1975) and the silver carbonate impregnationmethod (Ma et al. 2003). Counts, drawings (with helpof a camera lucida) and measurements were performedat a magnification of 1250� . Cell sizes were measuredboth in vivo (4–6 individuals) and on permanentpreparations, providing an estimate of shrinkage dueto fixation and staining.

Terminology: Terminology is mainly according toAgatha et al. (2005) and Montagnes and Lynn (1991).

Results and discussion

Parastrombidium Faure-Fremiet, 1924

Remarks: Faure-Fremiet (1924) established the genusParastrombidium based on an undetermined and insuffi-cently known species, Parastrombidium sp. Kahl (1932)considered Parastrombidium a synonym of Strobilidium

and established Strobilidium faurei for Faure-Fremiet’sspecimens. Maeda (1986) resurrected the genus withinthe family Halteriidae and affiliated Kahl’s species.

The ciliary pattern of Parastrombidium is unknown;hence, an improved diagnosis is provided based on boththe present study and Faure-Fremiet’s (1924) descrip-tion.

Improved diagnosis: Strombidinopsidae with slightlyopen adoral zone of membranelles. Some externalmembranelles elongated, extending from the buccalcavity across an inconspicuous peristomial rim, termi-nating posterior to the remaining external membra-nelles. Oral primordium develops hypoapokinetally in asubsurface pouch under the opening of the externalpolykinetid zone.

Type species: Strobilidium faurei (Kahl, 1932) Maeda,1986 (by monotype).

Comparison between Parastrombidium and similar

genera: In the Choreotrichida, some external membra-nelles are usually elongated proximally, extending intothe buccal cavity where buccal membranelles aresituated in most species. In Parastrombidium, however,

some membranelles are not only elongated proximallybut also distally, terminating distinctly posterior to theremaining external membranelles. Nevertheless, thearrangement of the adoral membranelles indicates anaffiliation of the genus to the Choreotrichida and thestructure of the somatic kinetids an assignment to theStrombidinopsidae.

Parastrombidium and Parastrombidinopsis Kim et al.,2005 share an open adoral zone and meridionaldikinetidal somatic kineties, but differ in distallyelongated membranelles (present vs. absent) and thearrangement of the somatic dikinetids in the posteriorcell portion (irregular vs. forming a suture) (Kim et al.2005).

Parastrombidium differs from Strombidinopsis Kent,1881 in the shape of the adoral zone of membranelles(slightly open vs. closed) and distally elongated mem-branelles (present vs. absent) (Kent 1880–1882).

Parastrombidium faurei (Kahl, 1932) Maeda, 1986(Figs. 1–3; Table 1)

Parastrombidium sp. Faure-Fremiet, 1924Strobilidium? (Parastrombidium) faurei Kahl, 1932Parastrombidium faurei (Kahl, 1932) Maeda, 1986Improved diagnosis: Large marine Parastrombidium,

about 95–155� 95–150 mm in vivo, and 112–144�100–140 mm after protargol staining, with truncatedsubspherical to obconical cell shape. About 52 externalpolykinetids form an incomplete circle. About 3–4external membranelles proximally and distally elon-gated, terminating posterior to the remaining 45–52external membranelles. Approximately 50 equallyspaced somatic kineties. Somatic dikinetids arrangedin longitudinal rows in anterior cell portion, irregular inposterior cell portion. About 7 globular macronuclearnodules.

Deposition of voucher slides: Two slides of protargol-impregnated specimens are deposited in the Laboratoryof Protozoology, Ocean University of China (registra-tion numbers: 04052401, 04052402). One slide isdeposited in the Natural History Museum, Londonwith registration number 2006:5:2:1. Relevant cells weremarked.

Description of the Qingdao population: Body size invivo 120–155� 110–145 mm, usually 140� 130 mm. Cellshape variable, i.e., subspherical to obconical and circularin cross-section, widest at oral region (Figs. 1A, 2A,H).Anterior cell portion transversely truncate, withoutperistomial collar or buccal cavity. In top view, protru-sion formed by the prolonged membranelles renders oralregion of cell asymmetrical (Figs. 1F, arrow; 2B arrow).Pellicle thin and delicate. Cortical granules about 0.5mmacross, scattered throughout cell (Fig. 2C). Endoplasmtransparent, usually with numerous small (2–4mm in size)glistening globules and large food vacuoles containingingested algae (8–10mm in diameter) which render cellsalmost dark grey at low magnification (Figs. 1A; 2A, E,

ARTICLE IN PRESS

Fig. 1. Parastrombidium faurei from life (A, C–F) and after protargol impregnation (B, G–J). A. A representative specimen. B. Fibre

systems. Two fibre bundles each originate at the distal end of an external polykinetid (arrows) and a bulge-like structure

(arrowheads). C. To show the resting cell with adoral membranelles forming typical flame-shape. D. Swimming trace, arrows mark

the positions of the cell when at rest. E. Specimen from type location (from Faure-Fremiet 1924). F, G. Apical views, to show the

prolonged polykinetids and the protrusion formed by them (arrows). H, I. Apical and posterior views of the same specimen, arrows

in (H) indicate the prolonged membranelles while arrowhead in (I) shows the base of the longest prolonged membranelle stretching

posteriorly. J. Left lateral view of ciliary pattern. B–bulge-like structure, CF–circular fibre, E–endoral membrane, EPk–external

polykinetid, Ma–macronuclear nodules, Prm–prolonged membranelles, SK–somatic kineties. Scale bars in (A, C, H, I, J)–70 mm.

D. Xu et al. / European Journal of Protistology 43 (2007) 27–35 29

arrowhead, G, H). No contractile vacuole, cytopyge orextrusomes detected. Macronuclear nodules horizontallylocated in anterior half of cell, variable in number, ca.20mm across, with several nucleoli ca. 1–4mm across(Figs. 1G, H; 3A). Micronucleus not detected.

Movement of cell very characteristic. Cell oftensuspended in the water with its membranelles packedtogether forming a typical flame-shape (Fig. 1C) orswimming smoothly, but when disturbed swims extre-mely fast with its membranelles stretched out in a wheel-like configuration when viewed apically (Fig. 1D, F).

Somatic kineties longitudinal, evenly distributed, com-mence posterior to adoral zone of membranelles andextend posteriorly, terminating near the posterior fifth ofcell where the arrangement of the kinetids becomesirregular, composed of widely spaced dikinetids (Figs. 1I,J; 3A, E); number roughly corresponds to that of externalmembranelles. Each somatic dikinetid possesses two3–6mm long cilia (Fig. 3F, arrows). Oral apparatus

occupies anterior end of cell. Adoral zone of membranellesforms an incomplete ring. External membranellescomposed of three basal body rows (Fig. 3G). Usually3–4 prolonged membranelles present, which are not onlyelongated proximally but also distally. The base of theright elongated polykinetid 1, is the longest at about 55mmlong, and terminates posterior to the common membra-nelles by about 20mm. Right elongated polykinetid 2, witha base about 28mm long, terminates posterior to thecommon membranelles by about 5mm (Fig. 1G, H,arrows). Left elongated polykinetids 1 and 2 (if present),positioned left of the cleft, are about 35mm and 30mmlong, respectively, terminate posterior to the commonmembranelles by 5mm. Fibre system beneath externalpolykinetid zone well developed: two fibre bundlesoriginate at distal end of each external polykinetid andextend anteriorly and posteriorly, merging into a circularfibre (Figs. 1B, arrows; 3D). Some bulge-like structuresalong inner portion of external polykinetid zone, recogniz-

ARTICLE IN PRESS

Fig. 2. Micrographs of Parastrombidium faurei from life (A–H) and after protargol impregnation (I). A. Lateral view of a typical

specimen. B. Apical view, arrow marks the protrusion formed by the prolonged membranelles. C. Detail of cortex, to show the

cortical granules. D. Detail of oral region, arrows indicate the bulge-like structures. E. Optical section through periphery of cell,

arrows show the short somatic cilia while arrowheads mark food vacuoles. F. Ventral portion of adoral zone of membranelle.

Arrows indicate the prolonged membranelles. G. Ventrolateral view of a typical specimen. H. A subspherical specimen

demonstrating the variability in the cell shape. I. Anterior cell portion of an early divider, arrow marks the oral primordium. Scale

bars in (A, B)–70 mm.

D. Xu et al. / European Journal of Protistology 43 (2007) 27–3530

able in live (Fig. 2D, arrows) and silver-impregnatedspecimens (Fig. 3B, arrows), each associated with two fibrebundles extending anteriorly and posteriorly (Figs. 1B,arrowheads; 3C, arrows). Endoral membrane extendsacross right side of peristomial field, composed of a singlerow of monokinetids, about 40–50mm long (Figs. 1J; 3C,arrowheads). Cytostome not detected.

One divider was found, viz., an early divider. The oralprimordium develops hypoapokinetally in a subsurfacepouch under the gap of the adoral zone of membranelles(Fig. 2I, arrow).

Comparison of Chinese population with type population

and with similar/related species: Our population corre-sponds well with the original description by Faure-Fremiet (1924; Fig. 1E), except for the cell size(120–155 mm vs. 95 mm). Since cell size varies consider-

ably in the Oligotrichea, it is reasonable to conclude aconspecificity of the two forms.

Our organism can be distinguished from Parastrom-

bidinopsis shimi by the cell shape (truncated subsphericalto obconical vs. elongated oval), 3–4 prolonged oralpolykinetids which are proximally and distally elongated(vs. several elongated membranelles are only proximallyelongated in Parastrombidinopsis shimi), and the ar-rangement of the somatic dikinetids in the posterior cellportion (irregular vs. forming a suture in Parastrombi-

dinopsis shimi) (Kim et al. 2005).

Strombidium capitatum (Leegaard, 1915) Kahl, 1932

Laboea capitata Leegaard, 1915Strombidium capitatum Kahl, 1932

ARTICLE IN PRESS

Fig. 3. Micrographs of Parastrombidium faurei after protargol (A–F) and silver carbonate impregnation (G). A. A typical specimen,

arrow marks the longest external polykinetid. B. Anterior (or) Top view, arrows indicate the bulge-like structures. C, D. Anterior

view, to show the endoral membrane (arrowheads in C) as well as the fibre bundles stretching from the bulge-like structure (arrows

in C) and the proximal end of external polykinetid (D). E. Lateral view, to show that the number of somatic kineties roughly

corresponds to that of external polykinetids. F. Detail of cell surface, arrows mark the dikinetids of the somatic kineties each of

which bear two cilia. G. External polykinetids, all of which are composed of three kinety rows. Scale bars in (A, B)–70mm.

Table 1. Morphometric data on Parastrombidium faurei

Characteristics Min Max Mean M SD n

Cell length 112 144 134 138 10.4 16

Cell width 100 140 123 122 17.2 16

Cell length: width, ratio 0.8 1.2 1.1 1 0.1 16

Macronuclear nodules, number 4 10 7.6 7 1.5 16

Macronuclear nodules diameter 12 22 21 20 5.4 16

External polykinetids, number 48 56 52 52 2.1 16

Elongated polykinetids, number 3 4 3.8 4 0.4 16

Endoral, length 40 55 46.6 45 5.7 16

Right elongated polykinetid 1, length 50 60 55.6 53 3.3 16

Right elongated polykinetid 2, length 25 35 28.4 27 2.5 16

Left elongated polykinetid 1, length 30 40 35.1 34 2.3 16

Left elongated polykinetid 2, length (if present) 28 32 30 31 3.1 16

Posterior cell end to elongated polykinetid 1, distance 45 70 52 50 6.0 16

Somatic kineties, number Somatic dikinetids, 43 54 48.9 49 3.0 16

number per 25mm 6 8 6.7 7 0.8 16

Data based on protargol-impregnated, randomly selected specimens. Measurements in mm. M–median, Max–maximum, Mean–arithmetic mean,

Min–minimum, n–number of specimens, SD–standard deviation.

D. Xu et al. / European Journal of Protistology 43 (2007) 27–35 31

ARTICLE IN PRESSD. Xu et al. / European Journal of Protistology 43 (2007) 27–3532

S. capitatum Maeda and Carey, 1985S. capitatum Montagnes et al., 1988S. capitatum Pettigrosso, 2003Remarks: The species diagnosis is improved because

additional distinguishing features were found, especiallyin live specimens.

Improved diagnosis: Size in vivo about 45–70�40–60 mm and 23–61� 30–55 mm after protargol stain-ing. Cell shape variable, truncated obconical to squatwith prominent transparent apical protrusion. Conspic-uous hemitheca composed of transparent polygonalcortical platelets covering posterior half of cell. Buccalcavity deep and wide, extending posteriorly to about 1/2of cell length. About 15–17 anterior and 16–20 ventralmembranelles. Girdle kinety horizontal, equatoriallyorientated, with small ventral gap, composed of about150 kinetids. Ventral kinety composed of about 5–12kinetids. Extrusomes attachment sites form continuousstripe anterior to girdle kinety. Single macronucleus,variable in shape but usually C-shaped.

Deposition of slides: Type material was previouslydeposited in the Ciliate Type Specimen Slide Collection,

Fig. 4. Strombidium capitatum from life (A, D–F) and after protar

indicate the extrusome girdle. B, C. Anterior and posterior views of th

of hemitheca showing the polygonal platelets. G. Macronucleus. H,

the girdle of extrusome attachment sites. J. Ventral view of an ea

AM–anterior membranelles, AP–apical protrusion, DC–distend

Ma–macronucleus, VK–ventral kinety, VM–ventral membranelles.

US Natural History Museum, Smithsonian Institution,Washington, DC, USA (registration number 39701).Voucher slides of the Qingdao specimens with relevantcells marked have been deposited in the Laboratory ofProtozoology, Ocean University of China (registrationnumbers: 05030902, 05030903) and at the NaturalHistory Museum, London (registration number2006:5:2:2).

Description of Qingdao population (Figs. 4 and 5;Table 2): Size in vivo 45–70� 40–60 mm, usually 55�50 mm. Body shape of Qingdao population is lessvariable, generally broadly obconical and circular incross-section, widest at shoulder region. Anterior of celltransversely truncated with prominent, hyaline, apicalprotrusion ca. 12 mm high (Figs. 4A; 5A, C, F, arrow-heads). Buccal cavity deep and wide, extending ob-liquely towards posterior half of right side of cell(Figs. 4A; 5A, C). Hemitheca covers cell portionposterior to girdle kinety, composed of polygonalplatelets �6 mm across (Figs. 4F; 5E). Cell surfacedistinctly distended posterior to girdle kinety in silver-impregnated cells (Fig. 4H, I). Extrusomes prominent,

gol impregnation (B, C, G–J). A. A typical specimen, arrows

e same specimen. D. Extrusomes. E. Swimming trace. F.Detail

I. Dorsal and ventral views of the same specimen, arrows mark

rly divider, arrow marks the newly formed oral primordium.

ed cell surface, E–endoral membrane, GK–girdle kinety,

Scale bars in (A)–930 mm, in (H–J)–20 mm, in (D)–10 mm.

ARTICLE IN PRESS

Fig. 5. Micrographs of Strombidium capitatum from life (A–C, E, F, H) and after protargol impregnation (D, G, I–L). A. A typical

specimen, to show the transparent apical protrusion (arrowhead) and the bulge formed by the extrusome attachment sites (arrows).

B. Dorsal view, to show the typical flame-shaped arrangement of the adoral membranelles when the cell is at rest and the extrusome

girdle (arrows). C. Lateral view, to show the apical protrusion (arrowhead). D. Dorsal view, to show the girdle kinety. E. Detail of

hemitheca, which is composed of polygonal platelets. F. Apical protrusion. G. Ventral view of an early divider, to show the newly

formed oral primordium beneath the girdle kinety, arrowhead indicates the gap in girdle kinety. H. To show the grouped

extrusomes. I. Posterior view, to show the ventral and girdle kinety. J. A middle divider, to show the oral primordium in a

subsurface tube and basal body proliferation within the girdle kinety. K. Ventral view, to show the anterior membranelles, ventral

membranelles, and the girdle kinety. L. To show the macronucleus. AM–anterior membranelles, GK–girdle kinety,

Ma–macronucleus, OP–oral primordium, VM–ventral membranelles. Scale bars in (A–C)–30 mm.

D. Xu et al. / European Journal of Protistology 43 (2007) 27–35 33

ARTICLE IN PRESS

Table 2. Morphometric data on Chinese population of Strombidium capitatum

Characteristics Min Max Mean M SD n

Cell lengtha 40 60 48 48 4.6 15

Cell widtha 35 50 43 44 3.9 15

Cell length: width, ratio 1.1 1.2 1.1 1.2 0.3 15

Apex to cytostome, distance 25 40 32 32 4.3 15

Apex to girdle kinety, distance 29 48 36 38 3.5 10

Apex to ventral kinety, distance 32 52 40 40 3.2 10

Macronucleus, number 1 1 1 1 0 25

Anterior membranelles, number 14 17 15 15 1.1 15

Ventral membranelles, number 16 23 20 20 2.6 15

Girdle kinety, number of kinetids 132 160 146 148 9.6 10

Ventral kinety, number of kinetids 10 12 11 11 0.9 10

Ventral kinety, length 6 8 7 8 0.8 10

Data based on protargol-impregnated, randomly selected specimens. Measurements in mm. M–median, Max–maximum, Mean–arithmetic mean,

Min–minimum, n–number of specimens, SD–standard deviation.aMeasured without distended cell surface.

D. Xu et al. / European Journal of Protistology 43 (2007) 27–3534

acicular, ca. 15 mm long and regularly grouped, eachgroup with about 6–8 extrusomes and closely spacedanterior to the girdle kinety (Figs. 4A, arrows, D; 5H).Extrusomes attachment sites form oblique, equidis-tantly-arranged rows of 6–8 organelles each, anteriorto girdle kinety, producing a granulated and slightlypunctated stripe on the cell surface in live specimens anda dotted stripe in protargol-impregnated cells (Figs. 4A,H, I, arrows; 5A, B, arrows). Cytoplasm transparent,contains numerous lipid-like droplets 2–4 mm across.Food vacuoles contain diatoms, flagellates etc. whosepresence can render cells often rather opaque or evendark at lower magnification (Fig. 5B), but produce acolourful appearance at higher magnification due toingested diatoms (Fig. 5A). Macronucleus variable inshape, typically elongate and C-shaped, usually containsmany small globular nucleoli about 2–5 mm across andpositioned longitudinally in the cell (Figs. 4C, G, H; 5L).Micronucleus, contractile vacuole and cytopyge werenot recognizable. Normally, cell moves quickly in widespirals by rotation about main cell axis, but whendisturbed it swims extremely fast in an almost straightline with anterior membranelles stretching anteriorly(Fig. 4E).

Oral apparatus consists of an endoral membrane oninner wall of buccal cavity and a conspicuous adoralzone of membranelles that surrounds the apical protru-sion. Endoral membrane composed of a single row ofmonokinetids (Fig. 4I). Adoral zone of membranelleswith distinct ventral opening and clearly divided intoanterior and ventral parts: anterior part comprises14–17 membranelles, ventral part comprises 16–23membranelles that lie in a deep, obliquely orientedventral groove (Figs. 4B, I; 5K). All membranellescomposed of three rows of basal bodies, except for the 3or 4 posteriormost ventral membranelles which com-prise only two rows. Cilia in anterior membranelles

about 35 mm long in vivo (Figs. 4A; 5A). Argentophilicfibres present between and parallel to anterior membra-nelles (Fig. 4B, H, I). Pharyngeal fibres are not recogni-zable.

Somatic cilia 2–3 mm long in vivo, arranged in a girdleand a ventral kinety (Figs. 4C, H, I; 5D, G, I, K). Girdlekinety horizontal, equatorially located, with small gapnear anterior end of ventral kinety (Fig. 5G, I, arrow-head), composed of densely packed kinetids, probablydikinetids of which only the ciliated basal bodyimpregnated (Fig. 4C, I). Ventral kinety extendsmeridionally on ventral side in furrow between girdlekinety and posterior end of cell, and comprises 10–12kinetids, probably dikinetids of which only the ciliatedbasal body impregnated (Figs. 4C; 5I).

Two division stages were found: an early divider withthe oral primordium posterior to the girdle and left ofthe ventral kinety (Figs. 4J; 5G) and a middle dividerwith oral primordium in the posterior cell half (Fig. 5J).

Occurrence and comparison of populations: Strombi-

dium capitatum has been reported from different placesworld-wide, i.e, in the North Atlantic (Leegaard 1915;Montagnes et al. 1988), the North Sea (Leegaard 1915),and the South Atlantic (Pettigrosso 2003). This is thefirst record from the North Pacific. Although theChinese population matches the populations studiedby Montagnes et al. (1988), except for the number ofkinetids in the ventral kinety (10–12 vs. 5–10 in USApopulations) and the course of the girdle kinety (withventral gap vs. ostensibly continuous). We considerthese differences to be only population-dependant.Strombidium capitatum was also found in the inner zoneof Bahıa Blanca Estuary, Argentina where the salinitywas 29–30% and temperature 12–21 1C (Pettigrosso2003). Considering the general morphology (cell shape,marine habitat, number of anterior and ventral mem-branelles etc.), the Argentina population corresponds

ARTICLE IN PRESSD. Xu et al. / European Journal of Protistology 43 (2007) 27–35 35

well with the USA and China populations although noinformation on its infraciliature was supplied. It is truethat cells of the Argentina population are smaller, withthe smallest specimens only 23 mm in length, but sincecell size varies considerably in the Oligotrichea, it isreasonable to conclude a conspecificity of the two forms.

Acknowledgements

This work was supported by ‘‘The National ScienceFoundation of China’’ (Project nos. 30430090,40376045) and Darwin Initiative Programme (Projectno. 14-015) which is funded by the UK Department forEnvironment, Food and Rural Affairs.

References

Agatha, S., Struder-Kypke, M.C., Beran, A., Lynn, D.H.,

2005. Pelagostrobilidium neptuni (Montagnes and Taylor,

1994) and Strombidium biarmatum nov. spec. (Ciliophora,

Oligotrichea): phylogenetic position inferred from mor-

phology, ontogenesis, and gene sequence data. Eur. J.

Protistol. 41, 65–83.

Azam, F., Fenchel, T., Field, J.G., Gray, J.S., Meyer-Reil,

L.A., Thingstad, F., 1983. The ecological role of water

column microbes in the sea. Mar. Ecol. Prog. Ser. 10,

257–263.

Faure-Fremiet, E., 1924. Contribution a la connaissance des

infusoires planktoniques. Bull. Biol. Fr. Belg. Suppl. 6,

1–171.

Kahl, A., 1932. Urtiere oder Protozoa I: Wimpertiere oder

Ciliata (Infusoria) 3. Spirotricha. Tierwelt Dtl. 25, 399–650.

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.

David Bogue, London.

Kim, J.S., Jeong, H.J., Struder-Kypke, M.C., Kim, S., Kim,

J.H., Lee, S.H., 2005. Parastrombidinopsis shimi n. gen., n.

sp. (Ciliophora: Choreotrichia) from the coastal waters of

Korea: morphology and small subunit ribosomal RNA

gene sequence. J. Eukaryot. Microbiol. 52, 1–9.

Laybourn-Parry, J., 1992. Protozoan Plankton Ecology.

Chapman & Hall, London, UK, 231pp.

Leegaard, C., 1915. Untersuchungen uber einige Planktonci-

liaten des Meers. Nyt Mag. f. Naturv. 53, 1–37.

Ma, H., Choi, J.K., Song, W., 2003. An improved silver

carbonate impregnation for marine ciliated protozoa. Acta.

Protozool. 42, 161–164.

Maeda, M., Carey, P.G., 1985. An illustrated guide to

the species of the family Strombidiidae (Oligotrichida,

Ciliophora), free swimming protozoa common in the

aquatic environment. Bull. Ocean Res. Inst., Univ. Tokyo

19, 1–68.

Maeda, M., 1986. An illustrated guide to the species of the

families Halteriidae and Strobilidiidae (Oligotrichida,

Ciliophora), free swimming protozoa common in the

aquatic environment. Bull. Ocean Res. Inst., Univ. Tokyo

21, 1–67.

Montagnes, D.J.S., Lynn, D.H., 1991. Taxonomy of choreo-

trichs, the major marine planktonic ciliates, with emphasis

on the aloricate forms. Mar. Microb. Food Webs 5, 59–74.

Montagnes, D.J.S., Lynn, D.H., Stoecker, D.K., Small, E.S.,

1988. Taxonomic descriptions of one new species and

redescription of four species in the family Strombidiidae

(Ciliophora, Oligotrichida). J. Protozool. 35, 189–197.

Pettigrosso, R.E., 2003. Planktonic ciliates Choreotrichida and

Strombidiida from the inner zone of Bahıa Blanca Estuary,

Argentina. Iheringia, Ser. Zool. 93, 117–126.

Pierce, R.W., Turner, J.T., 1992. Ecology of Planktonic ciliates

in marine food webs. Rev. Aquat. Sci. 6, 139–181.

Wilbert, N., 1975. Eine verbesserte Technik der Protargolim-

pragnation fur Ciliaten. Mikrokosmos 64, 171–179.