Oligotrichids and choreotrichids are ciliate taxa contributing to the multi-step microbial food web and episodically dominating the marine microzooplankton. The global diversity and distribution of aloricate Oligotrichea are unknown. Here, the geographic ranges of the 141 accepted species and their synonyms in marine and brackish sea water are analyzed, using hundreds of taxonomical and ecological studies; the quality of the records is simultaneously evaluated. The aloricate Oligotrichea match the moderate endemicity model, i.e., the majority (94) of morphospecies has a wide, occasionally cosmopolitan distribution, while 47 morphospecies show biogeographic patterns: they are restricted to single geographic regions and probably include 12 endemic morphospecies. These endemics are found in the Antarctic, North Pacific, and Black Sea, whereas the “flagship” species Strombidinopsis cercionis is confined to the Caribbean Sea. Concerning genera, again several geographic patterns are recognizable. The species richness is distinctly lower in the southern hemisphere than in the northern, ranging from nine morphospecies in the South Pacific to 95 in the North Atlantic; however, this pattern is probably caused by undersampling. Since the loss of species might affect higher trophical levels substantially, the aloricate Oligotrichea should not any longer be ignored in conservation issues. The ecophysiological diversity is considerably larger than the morphological, and even tops the richness of SSrRNA and ITS haplotypes, indicating that probably more than 83–89% of the diversity in aloricate Oligotrichea are unknown. The huge challenge to discover all these species can only be managed by combining the expertises of morphological taxonomists, molecular biologists, ecologists, and physiologists.
Citation: Agatha S (2011) Global Diversity of Aloricate Oligotrichea (Protista, Ciliophora, Spirotricha) in Marine and Brackish Sea Water. PLoS ONE 6(8): e22466. doi:10.1371/journal.pone.0022466
Editor: Brock Fenton, University of Western Ontario, Canada
Published: August 10, 2011
Copyright: © 2011 Sabine Agatha. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: The study was supported by the Austrian Science Foundation (FWF; Project P20461-B17), which had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
History of Discovery
Based on morphologic and ontogenetic features, the Oligotrichea Bütschli, 1887 unite the halteriids, oligotrichids, and choreotrichids (see ‘Classification and phylogeny’ and Table 1 for scientific and vernacular names). While the former two taxa contain exclusively aloricate (naked) species, the choreotrichids embrace naked species and the loricate (house-forming) tintinnids, which are not considered in the present compilation.
The first ciliate assigned to the oligotrichids was the marine species Strombidium sulcatum Claparède and Lachmann, 1859 . The freshwater species Strombidion caudatum Fromentel, 1876  is the first known aloricate choreotrichid ciliate, as it was transferred to the genus Strobilidium by Foissner . In 1773, Müller described the first halteriid, viz., the freshwater species Trichoda grandinella , which was affiliated with the genus Halteria by Dujardin .
In their revisions, Kent listed 21 species , Awerinzew 10 species , and Kahl 84 species ,, while the most recent monographs published in 1985 and 1986 ,  considered 127 species of aloricate Oligotrichea. The rate of discovery (Figure 1) reflects the introduction and improvement of light microscopy (period ~1860–1960) for the study of live and preserved specimens and the introduction of cytological staining methods (i.e., protargol and silver nitrate impregnation; period ~1980–present) to reveal the ciliary pattern and nuclear apparatus. The rate of discovery was also distinctly influenced by the trend to neotypify species rather than to establish new ones, assuming that the majority of species has a cosmopolitan distribution –. Accordingly, the intensity of taxonomic studies was much higher during the past thirty years than implied by Figure 1. Currently, species descriptions do not only comprise information from live observation, silver impregnation, and scanning electron microscopy, but often also sequence data of the small subunit ribosomal RNA gene (SSrRNA).
The published descriptions of new halteriid, oligotrichid, and aloricate choreotrichid species (including synonyms, nomina dubia, and nomina oblita) per year.
Ecology and Environments
Ciliates are highly developed unicellular eukaryotes, which propagate mainly asexually by transverse fission. The oligotrichids and choreotrichids are ciliate taxa episodically dominating the marine microzooplankton with maximum abundances of up to 1.2×106 individuals per litre in the upper water layers –. Such high cell densities (“blooms”) might cause water colourations , . The halteriids, however, occur only rarely and with low abundances in marine and brackish sea water. While the majority of Oligotrichea has a planktonic life style, 17 aloricate species are closely associated with the marine benthal, possessing special ciliary structures (thigmotactic membranelles) for a temporary attachment and/or migration on the substrate , , , and three species are endocommensals in sea urchins (see ‘Results’; –).
Most genera occur exclusively in marine and brackish sea water: the oligotrichid genera Apostrombidium, Cyrtostrombidium, Foissneridium, Laboea, Novistrombidium, Omegastrombidium, Opisthostrombidium, Parallelostrombidium, Paratontonia, Pseudotontonia, Spirostrombidium, Spirotontonia, Tontonia, and Varistrombidium, and the choreotrichid genera Leegaardiella, Lohmanniella, Lynnella, Parastrombidinopsis, Parastrombidium, and Strombidinopsis. The oligotrichid genus Strombidium, the choreotrichid genera Rimostrombidium and Pelagostrobilidium, and the halteriid genera Meseres and Pelagohalteria embrace both marine and freshwater species. The halteriid genus Halteria, the oligotrichid genera Limnostrombidium and Pelagostrombidium, and the choreotrichid genus Strobilidium are apparently restricted to freshwater, as the few records from brackish or marine environments are probably based on misidentifications (Table 1). All in all, there are 29 freshwater-specific species and six with a distribution only in saline inland waters or lakes (including the Caspian Sea), which are excluded from this compilation.
The Oligotrichea are members of the multi-step microbial food web. They mainly ingest bacteria as well as autotrophic and heterotrophic nanoplankton (2–20 µm) and are preyed upon by a wide variety of planktonic metazoans (e.g., copepods, fish larvae; –). Hence, they contribute to the energy flux of the conventional phytoplankton-based planktonic food web and may change the community composition of the bacterioplankton and nanoplankton through selective feeding . Most/many oligotrichids are mixotrophic, “farming” plastids of their ingested algal prey and benefiting from the photosynthetic products –.
Resting cysts, dormant stages formed during periods of adverse environmental conditions, are known in only a few marine species due to their rare occurrence, sedimentation, and difficult identification –. Apparently, open water species follow a seasonal encystment-excystment cycle , , , whereas the oligotrichid tide-pool ciliate Strombidium oculatum demonstrates a circatidal behaviour, encysting before high tide and excysting during low tide –, , –. The resting cysts are flask-shaped or spindle-shaped with a solid, hollow, or frothy plug closing the emergence pore. The surface of the cyst is smooth or may bear spines variable in number and length.
Ciliates have complex morphologies, which can be revealed by cytological staining techniques and electron microscopy (see ‘Morphology’). While fossils of tintinnids (loricate Oligotrichea) reach back to the Ordovician or possibly even Mesoproterozoic era , there are no remains of the probably older aloricate Oligotrichea. The number of reliable species in marine and brackish sea water amounts to 103 in the 15 oligotrichid genera, 36 in the eight aloricate choreotrichid genera, and two in the two halteriid genera (Table 1 and 1), based on my revision of the aloricate Oligotrichea in preparation.
Classification and Phylogeny
The Oligotrichea are separated from the closely related hypotrich and stichotrich spirotrichs (e.g., Euplotes, Stylonychia, Oxytricha) by several apomorphies: (i) a globular to obconical cell shape; (ii) a planktonic life style; (iii) an apically located adoral zone of membranelles (fan-like units composed of densely spaced cilia); (iv) a bipartition of the adoral zone in a collar portion with large membranelles and a buccal portion with small membranelles; (v) a lack of cirri (bristle-like complexes of somatic cilia); and (vi) an enantiotropic division mode (an inverse orientation of mother/proter and daughter/opisthe). According to cladistic analyses and phylogenies of the SSrRNA gene, the oligotrichids and choreotrichids are monophyletic , –. Concerning the position of the halteriids, however, the morphologic and genetic data are inconsistent, i.e., the morphology and pattern of cell division indicate a sister group relationship with a cluster formed by the oligotrichids and choreotrichids, whereas the halteriids are located among the stichotrichs (frequently as an adelphotaxon of Oxytricha granulifera) and thus distinctly apart from the oligotrichids and choreotrichids in the molecular trees , –.
The hypothesized evolution of the somatic ciliary patterns is one of the main feature complexes integrated into the cladistic analyses , , , . Agatha ,  assumed a convergent development of the ciliary patterns in the tailless oligotrichids and the tailed tontoniids, as the contractile tail is considered a strong synapomorphy due to its complex and unique ultrastructure. However, gene sequence analyses indicated that the sinistrally spiralled ciliary pattern is a synapomorphy of the tailed genus Spirotontonia and the secondarily tailless monotypic genus Laboea. Otherwise, the morphologic tree of the oligotrichids matches rather well the SSrRNA phylogenies . In both kind of trees, the aloricate choreotrichids are paraphyletic, but differ in the position of the genus Parastrombidinopsis. According to its morphology, it is an adelphotaxon of the genus Strombidinopsis at the base of the choreotrichids, whereas it represents a sister group to the more highly developed tintinnids in the molecular trees , .
In contrast to the majority of eukaryotes, ciliates are heterokaryotic, possessing two kinds of nuclei: one, rarely two or more diploid micronuclei involved into the sexual processes (conjugation) and usually one or several highly polyploid macronucleus nodules mainly controlling the metabolism. The aloricate Oligotrichea are globular, subspherical, ellipsoidal, obconical, or obovoidal and measure 15–260 µm. The somatic ciliature is often reduced, whereas the conspicuous adoral zone of membranelles at the apical cell end is used for locomotion and food collection by filter feeding .
Halteriids (Figures 2a, b). In the halteriids, the adoral zone of membranelles is C-shaped with a distinct ventral gap and consists of a collar portion with large membranelles and a buccal portion with small membranelles. On the inner wall of the buccal lip, a longitudinal row of occasionally ciliated basal bodies, the endoral membrane, extends into the eccentric buccal cavity. The few ciliated basal bodies on the outer cell surface at the level of the cytostome represent the paroral membrane. In the genus Meseres, the somatic ciliature is arranged in several longitudinal rows composed of dikinetids (paired basal bodies), each with a cilium associated only with the anterior basal body (Figure 2a). In Pelagohalteria, the short and equatorially arranged somatic kineties consist of a longitudinal anterior and a horizontal posterior portion (Figure 2b). Its somatic cilia are conspicuously long and form bristles. Usually, the specimens rotate on the spot, interrupted by long jumps.
Generalized ventral (a–c, f), dorsal (d, e), top (g), and posterior polar (h) views after protargol impregnation (a, after ; b, d, f, originals; c, e, after ; g, h, after ). a, b: The halteriid genera Meseres and Pelagohalteria. c: The oligotrichid genus Strombidium. d–h: The choreotrichid genera Strombidinopsis (d), Rimostrombidium (e), Lohmanniella (f), and Leegaardiella (g, h). B – bristle kineties, BM – buccal membranelles, CM – collar membranelles, E – endoral membrane, GK – girdle kinety, ICM – inner portion of collar membranelles, OCM – outer portion of collar membranelles, P – paroral membrane, SK – somatic kineties, VK – ventral kinety.
Oligotrichids (Figure 2c). In the oligotrichids, the adoral zone of membranelles is C-shaped with a distinct ventral gap and consists of a collar portion with large membranelles and a buccal portion with small membranelles. On the inner wall of the buccal lip, a longitudinal row of occasionally ciliated basal bodies, the endoral membrane, extends into the eccentric buccal cavity. The somatic ciliature typically comprises two ciliary rows: the girdle kinety and the ventral kinety. These kineties are composed of dikinetids, each with a stubby cilium associated only with the left or anterior basal body. Whereas the girdle kinety is arranged in several patterns, the ventral kinety generally extends longitudinally in the posterior cell portion. Rod-shaped or needle-shaped extrusomes (extrusive organelles) are usually attached to the cell membrane directly anteriorly to the girdle kinety and extend obliquely into the cytoplasm . The cell cortex posterior to the girdle kinety typically contains a layer of polygonal polysaccharide platelets , , –. The specimens usually swim in spirals by rotation about their main cell axis.
Choreotrichids (Figures 2d–h). In the choreotrichids, the adoral zone of membranelles forms a circle. The large collar membranelles insert on an elevated rim around the peristomial field. Some of them are elongated, extending into the eccentric buccal cavity, which also contains the small buccal membranelles. In the genera Lynnella, Parastrombidinopsis, and Parastrombidium, however, the adoral zone of membranelles opened secondarily, producing an indistinct ventral gap. The genus Leegaardiella is exceptional in its bipartited bases (polykinetids) of the collar membranelles, i.e., they consist of an outer portion with long cilia and an inner portion with short cilia (Figure 2g). While the structure of the somatic ciliature is rather uniform in the oligotrichids, the choreotrichids show a wide variety of patterns: (i) in the genera Pelagostrobilidium and Rimostrombidium, the stubby cilia are very densely arranged in a few longitudinal or curved monokinetidal (composed of single basal bodies) rows and bent leftwards by cytoplasmic flaps (kinetal lips) covering their bases (Figure 2e); (ii) in the genera Strombidinopsis, Parastrombidinopsis, and Parastrombidium, the somatic ciliature is well developed and comprises several longitudinal rows composed of dikinetids, each with two cilia (Figure 2d); (iii) in the genus Lohmanniella, the few kineties are short, extending in the posterior cell portion, and consist of dikinetids, each with a cilium associated only with the posterior basal body (Figure 2f); (iv) in the genus Leegaardiella, the few kineties are short, extending in the posterior cell portion, and consist of dikinetids, each with two cilia or one cilium associated only with the anterior basal body (Figure 2h); and (v) in the genus Lynnella, one kinety is monokinetidal, while the other consists of dikinetids, each with a cilium associated only with the posterior basal body. Many aloricate choreotrichids are able to jump.
Materials and Methods
While the biogeography of tintinnids (loricate Oligotrichea) is comparatively well studied –, a census and survey on the global distribution of aloricate Oligotrichea are not available. Even in recent estimations of marine species richness, ciliates are not considered or are subsumed under the protists , . A preliminary list of marine aloricate Oligotrichea merely exists for European sea regions .
The present compilation is based on hundreds of taxonomical and ecological studies, considering the accepted species mentioned (Table S1) and their synonyms; however, it cannot be excluded that some ecological papers might have been overlooked. The available records were classified according to their quality: (i) reliable records from the type or neotype locality accompanied by the original description or redescription; (ii) more or less reliable records supported by descriptions, measurements, and/or illustrations; and (iii) unsubstantiated records based on uncertain identifications.
The present analysis of the global distribution is not restricted to the pelagial, benthal, and sea ice of marine waters, but also includes all records from brackish sea waters in estuaries, fjords, coastal lagoons, the Baltic Sea, and the Black Sea. Finally, seven regions of the oceans were distinguished (Table S1), whose limits roughly correspond with the latitudinal-physical geographic zonation of water masses proposed by Van der Spoel and Heyman : the Arctic and Subarctic waters are pooled; the northern temperate, northern subtropical, and northern tropical waters are united each in the North Atlantic and North Pacific; the southern tropical, southern subtropical, and southern temperate waters are lumped each in the South Atlantic, South Pacific, and Indian Ocean; and the Subantarctic and Antarctic waters are amalgamated. Furthermore, the Mediterranean, Baltic, and Black Sea are considered. Even though almost all studies were performed in neritic waters, the recorded species are supposed to occur also in the affiliated oceanic regions.
In spite of the comprehensive literature research, the species inventories presented in Table S1are fragmentary and influenced by various limitations (see below) preventing detailed comparisons and ecological analyses.
The majority of aloricate Oligotrichea (94 morphospecies) has a wide, occasionally cosmopolitan distribution (occurring in all oceans and seas from the Arctic through the tropics to the Antarctic), while 47 morphospecies are restricted to single geographic regions and include, conservatively estimated, 12 endemic morphospecies. The choreotrichid Leegaardiella elbraechteri and the oligotrichids Spirostrombidium echini (possibly specific to its sea urchin host), Strombidium glaciale, S. kryale, S. syowaense nom. corr. (specific epithet emended, as the genus name is neuter gender), and Tontonia antarctica were only found in the Antarctic Sea. The choreotrichid Rimostrombidium sulcatum as well as the oligotrichids Strombidium costatum and S. opisthostomum are possibly confined to the Black Sea. The oligotrichids Strombidium foissneri and S. rapulum are restricted to the North Pacific, possibly due to the geographic ranges of their sea urchin hosts. Among the endemics, the choreotrichid Strombidinopsis cercionis represents a “flagship” species in the sense of Tyler . Because of its unique shape (pyriform with a posterior spine ~30 µm long) the species is so conspicuous that it would have probably been recorded if it indeed occurred outside the Caribbean Sea. However, it cannot be excluded that S. cercionis is a young species that not yet fully explored its potential range. So, endemic species occur within widely distributed genera of aloricate Oligotrichea, as in tintinnids . The oligotrichid Parallelostrombidium rhyticollare displays like the tintinnid Acanthostomella norvegica, the dinoflagellate Polarella glacialis, and some planktonic foraminifera a bipolar distribution, which possibly results from the glaciation during the Neogene , –. The other species recorded only in a certain region might actually have a wider distribution (see below).
The distribution of the genera presented here is like that of the species preliminary and necessitates more detailed studies. Several oversimplified geographic patterns are recognizable: (i) a cosmopolitan distribution in Laboea, Leegaardiella, Lohmanniella, Parallelostrombidium, Paratontonia, Pelagostrobilidium, Pseudotontonia, Rimostrombidium, Spirostrombidium, Strombidium, and Tontonia (Figure 3d–f, 4d, f, 5b–d, g); (ii) a worldwide distribution with the exception of the Antarctic Sea in Strombidinopsis (Figure 5f); (iii) a distribution roughly restricted to the northern hemisphere in Cyrtostrombidium and Foissneridium (Figure 3b, c); (iv) a distribution only in the northern hemisphere with the exception of the Arctic Sea in Novistrombidium, Omegastrombidium, Parastrombidium, Spirotontonia, and Varistrombidium (Figure 4b, c, e, 5e, h); (v) a distribution confined to the North Pacific in Apostrombidium, Lynnella, Opisthostrombidium, and Parastrombidinopsis (Figure 3a); (vi) a distribution limited to the North Atlantic, Black Sea, and probably Mediterranean in Pelagohalteria (Figure 5a); and (vii) a distribution restricted to the Black Sea in Meseres (Figure 4a), which mainly occurs in freshwater. The choreotrichid Lohmanniella oviformis and the oligotrichids Laboea strobila, Paratontonia gracillima, Strombidium conicum, S. dalum, and S. sulcatum have a worldwide range, although subtle morphologic differences indicate the presence of a species complex at least in Strombidium sulcatum.
Red colour marks the presumptive range in marine and brackish sea water (Table S1). Note that the distribution in freshwater and saline inland waters is not considered. a: Apostrombidium, Lynnella, Opisthostrombidium, and Parastrombidinopsis. b: Cyrtostrombidium. c: Foissneridium. d: Laboea. e: Leegaardiella. f: Lohmanniella and Rimostrombidium.
Red colour marks the presumptive range in marine and brackish sea water (Table S1). Note that the distribution in freshwater and saline inland waters is not considered. a: Meseres. b: Novistrombidium. c: Omegastrombidium. d: Parallelostrombidium. e: Parastrombidium. f: Paratontonia and Strombidium.
Red colour marks the presumptive range in marine and brackish sea water (Table S1). Note that the distribution in freshwater and saline inland waters is not considered. a: Pelagohalteria. b: Pelagostrobilidium. c: Pseudotontonia. d: Spirostrombidium. e: Spirotontonia. f: Strombidinopsis. g: Tontonia. h: Varistrombidium.
The number of accepted morphospecies ranges from nine for the South Pacific to 95 for the North Atlantic (Table S1). A high diversity of aloricate Oligotrichea is also found in the North Pacific (94 species), Mediterranean (48 species), and Black Sea (46 species). Generally, the recorded species richness is lower in the southern hemisphere than in the northern (see below).
The data on the biogeography and diversity of aloricate Oligotrichea are strongly influenced by taxonomy and investigation methods. Furthermore, the natural patterns have been disturbed by human impact.
- Taxonomy. The accurate circumscription of species is an essential requirement for biodiversity and biogeography assessments. Traditionally, morphological traits were used to define and identify ciliate species, viz., the morphospecies concept was employed. Taxonomic mistakes and uncertainties, e.g., the tendency to identify specimens from new regions with European species despite subtle differences  and unjustified synonymizations, affect the diversity and geographic ranges perceived: taxonomic separations that mainly concern sympatric populations cause a higher global and local species diversity, while separations of allopatric populations on species level result in a decreasing relative local species richness due to a higher proportion of endemics . Recent molecular and ecological studies showed that the morphospecies concept is too conservative in several groups of marine plankton protists, i.e., a tremendous genetic diversity indicating cryptic (no morphologic differences in cell and resting cyst) or pseudocryptic (subtle morphologic differences) species is frequently hidden within a morphospecies –. The discovery of these distinct (cut-off divergence of 1–2%) haplotypes underlying the morphospecies contributes to an increase of the perceived total taxonomic diversity. Simultaneously, the geographic ranges are probably reduced and endemic haplotypes/biological species might become evident .
- Investigation methods. Most species-specific features of the ciliates are recognizable in vivo and after cytological stainings (silver impregnation techniques). However, the application of both methods requires training by an expert. Since the Lugol-fixed material frequently used in ecological studies does not provide these characteristics, the discovery of new species and the identification of known ones is hardly feasible in such material. Furthermore, the fixation techniques are selective . Generally, a higher taxonomic resolution results in a higher species diversity and a lower relative local species richness . However, the species richness recorded in a certain region also depends on the spatial and temporal resolution of the sampling –. Hence, thorough studies are able to unveiled large portions of the otherwise cryptic diversity (organisms that are not detected as they are rare and/or patchily distributed) in marine protists, enhancing the species richness and influencing the number of endemics. Since ciliate taxonomists show a patchy distribution with “hot spots” of taxonomic excellence, comprehensive and reliable species lists are usually only available for the respective sampling regions.
- Human impact. The distribution patterns observed nowadays are the result of natural processes and anthropogenic influences, e.g., the more than thousand years of shipping with the transport of organisms by ballast water and the construction of canals connecting oceans and hence enabling the exchange of organisms –.
Biodiversity and Biogeography
The nature and extent of microbial biodiversity, biogeography, and community structure are controversially discussed: cosmopolitan vs. moderate endemicity model and niche-based vs. neutral theories , –.
Baas Becking postulated that in microorganisms, including ciliates, “everything is everywhere, but the environment selects” . According to the tenet of Finlay and colleagues, microorganisms have a high dispersal potential due to their small body size and huge abundance . Therefore, marine plankton ciliates should show a ubiquitous dispersal (random across all spatial scales), causing a cosmopolitan distribution wherever the required habitat is realized, a low allopatric speciation, a low global but high local diversity, and low extinction rates. The huge abundances are the fundamental drivers of the ubiquitous dispersal of encysted and active microorganisms . However, there are only few very abundant species of aloricate Oligotrichea in the plankton, while most species are only moderately abundant or even very rare , –. Additionally, the transport by ocean currents is non-random, resulting in an uneven distribution –, , . A ubiquitous dispersal is further hampered by the duration of the transport by ocean currents, i.e., a global circulation needs more than 1000 years ,  and even the transport by the Gulf Stream from the east coast of the USA to European coastal waters lasts about two years , . Active forms do not tolerate the uncomfortable conditions encountered during such long-distance dispersal (e.g., low temperatures and starvation in winter), and resting cysts are rarely formed by marine plankton ciliates, as indicated by molecular analyses comparing plankton and benthos samples from the same coastal sites . Since the cysts are also at risk to sediment (14.4 m d−1 in freshwater oligotrichids; , ) and the excystment ability decreases from ~60% to an incapability after some month at low temperatures ( = conditions met in deep water layers; , , ), a long-distance dispersal of the cysts and a subsequent population growth are thus apparently rare events. The isolation caused by distance , , patchiness  due to the heterogeneity of the oceans , , front systems, changes in the ocean circulation patterns, vicariance events, glacial-interglacial climate dynamics, and global extinction events might have fostered together with the short generation times ,  allopatric speciation in aloricate Oligotrichea. Furthermore, there is evidence for parapatric and sympatric speciation in some planktonic protists , –. Indeed, the statistical analyses of ciliate communities from the freshwater pelagial and marine benthal performed by Hillebrand and co-authors refuted the prediction that unicellular organisms generally have a higher relative local species diversity than metazoa ; thus, they must not necessarily be ubiquitous, but at least some species might possess a biogeography. Actually, geographic patterns are recognizable in many species or haplotypes of marine plankton protist (e.g., foraminifera, radiolaria, dinoflagellates, tintinnids, and aloricate Oligotrichea; [this study], [ 83], –, , –) as well as in many macrozooplankton species . The moderate endemicity model attenuates the “everything is everywhere” tenet, suggesting that (i) the abundances and thus the migration rates are low in ~90% of the species, (ii) the extinction rates are moderate, (iii) the proportion of the global species pool found locally is moderate, and (iv) ~30% of the species are endemics . Consistent with this model and the findings in the closely related tintinnids , the majority of aloricate Oligotrichea has a wide, possibly cosmopolitan distribution, while ~33% of the morphospecies are restricted to certain geographic regions, and at least ~9% of the morphospecies are endemic according to conservative estimations.
Molecular biogeography is still in its infancy in aloricate Oligotrichea. The few studies available focussed on the small subunit ribosomal RNA (SSrRNA) gene and/or the internal transcribed spacer (ITS) sequence from comparatively limited geographical samples. A gene flow was found between (i) the northwest Atlantic  and northwest Pacific , (ii) the Mediterranean  and northwest Pacific , , , and (iii) the Mediterranean ,  and northwest Atlantic , , . On the other hand, there are deviations in morphospecies from the northwest Pacific ,  and northwest Atlantic (five SSrRNA nucleotides; ) and from the Mediterranean  and northwest Pacific (1.2% in the SSrRNA gene and in morphologic details; ). In morphologically similar freshwater halteriids, the conspicuous genetic diversity registered by Katz and colleagues was correlated with differences in the resting cysts (cyst species; ) and minute deviations in the cell morphology  indicating biological species. Hence, the genetic diversity within a morphospecies might at least partially result from an insufficient taxonomic resolution, viz., haplotypes which are indistinguishable in live and Lugol-fixed material at low (400–600×) magnification might be differentiated by an experienced morphological taxonomist, using live observation, silver impregnation, and light microscopy at high (1000×) magnification. For example, the analyses of the ITS regions indicated a huge genetic diversity in similar-sized tide-pool oligotrichids identified with Strombidium oculatum due to their green sequestered plastids and the prominent eye-spot in the apical protrusion . It finally turned out that one haplotype had a >99% identity in the SSrRNA gene with Strombidium apolatum and one represents Strombidium rassoulzadegani , while it is still unknown whether one of the six further haplotypes really corresponds with Strombidium oculatum. So, the genetic diversity observed was mainly due to a lumping of species, which are morphologically distinct in live and silver-impregnated material (with or without a conspicuous posterior spine; girdle kinety continuous or with a distinct ventral gap; position of the extrusome girdle). This example is a plea for submitting molecular data of named species only after detailed morphological investigations of live and silver-impregnated specimens  and the deposition of permanent voucher slides in a recognized museum. Recent studies on a freshwater halteriid and aloricate choreotrichid suggested that the ecophysiological diversity is not only considerably larger than the morphological, but also tops that of the haplotypes , .
The high diversity of plankton organisms, especially, protists, raised the question of “how a number of species can coexist in a relatively isotropic or unstructured environment all competing for the same sorts of materials” (“paradox of the plankton”; ). Not only extrinsic (weather-driven) fluctuations, as suggested by Hutchinson , but also intrinsic mechanisms within the plankton communities can fuel non-equilibrium dynamics and result in a coexistence of many species on a handful resources –. A further explanation for the diversity of similar species is provided by Hubbell's “neutral community model” . The theory assumes that the interactions among species are equivalent on an individual ‘per capita’ basis. Since niche differentiation will, however, impact any of the basic processes of the neutral community model, Gravel and colleagues suggested the continuum hypothesis, reconciling both the niche-based and neutrality concepts . Additionally, Alonso and co-authors emphasized that different mechanisms, although strictly violating the equivalence assumption, can also generate patterns resembling neutrality . In aloricate Oligotrichea, the functional equivalence is limited, as they often show species-specific temperature optima for growth and threshold concentrations ,  as well as salinity preferences , food selectivity –, and different nutrition modes (see ‘Ecology and Environments’). Hence, the aloricate Oligotrichea are probably a physiologically quite heterogeneous group within the microbial food web. In tintinnids, the community structure was studied, using morphological approaches –, whereas the investigation of marine aloricate Oligotrichea was either based on molecular data ,  or morphological studies . The tintinnid abundances in the southeast tropical Pacific Ocean usually fitted a log-series distribution coherent with the neutral community theory . For Mediterranean tintinnids, the data are incoherent: while Sitran and colleagues found a log-normal distribution, indicating a strong impact of the environment , Dolan and co-workers observed a log-series distribution. A partition of the tintinnid assemblages revealed, however, a log-normal distribution in the core (numerical abundant) morphospecies and a log-series distribution in the occasional (rare) ones . Similar findings were obtained for the core and occasional haplotypes in aloricate Oligotrichea from the east coast of the USA , . Claessens and co-authors analyzed the ciliate community in the plankton of the Red Sea , . The species abundances (in total ~41% aloricate Oligotrichea, ~37% tintinnids, and ~22% other ciliate groups) most closely fitted the log-normal distribution mainly during mixing conditions and after onset of a stratification, while a log-series distribution was registered usually during the stratification. The authors concluded that the neutral community model did not explain the species diversity observed. Between-clone variation in the dominant cyanobacteria Synechococcus might be at least partially responsible for niche separation based on fine-scale food selectivity.
In general, the numbers of morphospecies found in the different geographic regions reflect rather the intensity of taxonomic research than the real diversity of aloricate Oligotrichea, viz., the North Atlantic, North Pacific, and Mediterranean harbour the largest numbers of accepted species (Table S1), which is consistent with the results of Bouchet . These findings are also influenced by various further factors (see ‘Limitations’). Even though molecular analyses are able to screen large water volumes, there is evidence of a cryptic diversity . Using a cut-off divergence of 1%, in sum 66 Oligotrichea haplotypes (including ~12 tintinnids) were found in 50–60 litres of sea water, each taken at three distantly located sites along the east coast of the USA in spring and autumn. An estimation of the total haplotype diversity yielded a maximum of 325 haplotypes for a spring sample. In samples of 200 ml Lugol-fixed material taken on the same occasions, up to 19 morphotypes could be discerned under the light microscope at a magnification of 400–600× . Due to the distinctly different volumes analyzed and the low taxonomic resolution provided by the Lugol-fixed material (see ‘Limitations’), the molecular and morphological data of this study are hardly comparable. In the Long Island Sound samples of this study, in sum 27 haplotypes of Oligotrichea (including at least three tintinnids) were found . In 12 further samples of each two litres of sea water taken at the same site in summer, 62 additional haplotypes (including eight tintinnids) were recorded, while only five haplotypes from the former study were rediscovered . This clearly shows the impact of the sampling effort on the diversity record. So, in total 89 Oligotrichea haplotypes (including tintinnids) were found in the Long Island Sound, which is similar to the number of morphologically identified species in the whole North Atlantic (95 without tintinnids; Table S1; , ). In total, 26 morphotypes of aloricate Oligotrichea were recorded in 6.6 litres formalin-fixed material taken at eleven stations in the Mediterranean at six different depths (1–100 m; ), whereas 48 morphospecies have been compiled for the whole region (Table S1). In the Arctic Sea, 38 morphologically identified species were recorded, but merely four oligotrichid sequences were found in 500–1000 ml of sea water, each taken in two depth, and a sediment sample at a single site near the west coast of Svalbard in summer (Table S1; ). Claessens and co-authors discovered 45 morphotypes of aloricate Oligotrichea in the Red Sea . Since half of the morphotypes could not be identified, merely 25 species from the Indian Ocean plus the Red Sea are assembled in Table S1.
At the present state of knowledge, a differentiation of longitudinal trends and undersampling effects (indicated by the low numbers of species descriptions and redescriptions; Table S1) is impossible in the aloricate Oligotrichea. In planktonic foraminifera and tintinnids, however, the number of taxa increases from high to low latitudes with two peaks near the Tropics of Cancer and Capricorn (20–30°N and S, respectively; –).
In contrast to the tintinnids, there are only few regional inventories about aloricate Oligotrichea. Hence, it is infeasible to apply the same statistical approaches as in soil ciliates . Nevertheless, the steady rate of species descriptions indicates a much higher total diversity. Foissner and colleagues concluded from habitat studies that the number of known ciliate species must be doubled . “Cyst species” increase the number further by 50%, and “genetic species” will again double the number. So, the authors argued that eventually 83–89% of the ciliate diversity are unknown. A similar percentage was estimated by Costello and co-workers with 70–80% in marine species  and by the Convention on Biological Diversity with about 95% in protists (~575,000 unknown species, as estimated from Figure 1 in ). Taking the conservative estimate of unknown species by Foissner and co-workers  and the data of the present study (Table S1), the number of biological species in aloricate Oligotrichea would amount to 560–860 for the North Atlantic and to 830–1280 worldwide.
Significance of Aloricate Oligotrichea
The aloricate Oligotrichea are occasionally important grazers on phytoplankton – and thus possibly influence (i) the ocean acidification via sequestration of anthropogenic CO2 by the phytoplankton and (ii) the climate by the release of DMS (dimethylsulfide) that can act as cloud condensation nuclei , . On the other hand, aloricate Oligotrichea supply the primary production of algae with inorganic nutrients through recycling . Some species feed on harmful and bloom-forming plankton algae – and hence might control these toxic organisms that contaminate seafood and/or kill marine organisms, e.g., fish. Neutral communities (see above) are characterized by high functional redundancy; thus, the extinction of a few species should have little effect on the functional integrity of the whole community or ecosystem . Even if (i) alternative nutritional strategies, such as mixotrophy, might have a stabilizing effect on ecosystem functioning and (ii) the rare species might compensate species loss due to dramatic shifts in the environmental conditions, the resulting changes in the community structure of aloricate Oligotrichea might affect higher trophical levels substantially , . Accordingly, the aloricate Oligotrichea should not any longer be ignored in conservation issues .
Although many governments, through the Convention on Biological Diversity, have acknowledged the shortage of trained taxonomists and the Global Taxonomic Initiative was established to overcome this problem (“Taxonomic impediment”; ), the number of ciliate taxonomists is still too low (i) to describe the conservatively estimated 690–1140 new species only in the aloricate Oligotrichea living in marine and brackish sea water, (ii) to investigate the southern hemisphere, the oceanic regions, and the deep sea, and (iii) to identify the huge amount of gene sequences yielded by environmental samples. Since the recognition of new morphospecies largely depends on the availability of reliable identification guides, the production of regularly updated comprehensive monographs should be a priority .
Molecular analyses, using SSrRNA and ITS sequences, have become an affordable and practical method that is increasingly applied in diversity studies. However, species identification merely by molecules cannot compensate the disappearing taxonomic expertise, as it is fraught with the same constraints and inconsistencies plaguing morphological judgments of species limits . A gene sequence that does not exactly match a previously sequenced and morphologically identified species cannot be assigned and thus determined, as a predictive rule about the degree of genetic divergence required for the recognition of distinct species is impossible , , . Further, gene sequences of misidentified species prevent correct interpretations of phylogenetic trees and geographic ranges. Accordingly, the identification of sequenced specimens should be based on detailed studies of live and silver-impregnated material by a morphological taxonomist, and permanent slides should be deposited , .
Future taxonomic studies will certainly (i) provide morphological data from additional populations that contribute to a better circumscription of the known species, (ii) identify further taxonomically significant features, and (iii) discover new species. Genetic analyses of environmental samples might assist in the detection of these new species, especially, the rare ones. The taxonomic investigations should use live observation, silver impregnation techniques, and electron microscopy as in  and should be complemented by molecular studies not only of the SSrRNA and ITS sequences, but also of the cytochrome oxidase I gene (COI), which might reveal biogeographic patterns even in organisms with identical SSrRNA and ITS genes . By means of systematic sampling, the species diversity and abundances from various distances and environmental conditions should be recorded to better distinguish between contemporary environmental and historical contingencies causing spatial variability . Likewise, the ecological and evolutionary processes of speciation and the mechanisms by which diversity is maintained in the pelagic realm require further investigations. In order to attain these objectives, synergistic approaches combining the expertises of morphological and molecular taxonomists, ecologists, and physiologists are indispensable.
Global distribution of halteriids (H), oligotrichids (O), and choreotrichids (C) in marine and brackish sea waters.
Thanks go to Steve Wickham and Wilhelm Foissner for constructive comments. The technical assistance of Anke Oertel is gratefully acknowledged.
Conceived and designed the experiments: SA. Performed the experiments: SA. Analyzed the data: SA. Contributed reagents/materials/analysis tools: SA. Wrote the paper: SA.
- 1. Claparède É, Lachmann J (1859) Études sur les infusoires et les rhizopodes. Mém Inst Natn Genev 6(year 1858): 261–482 + Plates 14–24.
- 2. Fromentel E de (1874–1876) Études sur les microzoaires ou infusoires proprement dits comprenant de nouvelles recherches sur leur organisation, leur classification et la description des espèces nouvelles ou peu connues (planches et notes descriptives des espèces par J. Jobard-Muteau). Paris: Masson G. pp i–viii + 364+. Plates 1–30 (1874: i–viii + 1–88; 1875: 89–192; 1876: 193–364).
- 3. Foissner W (1987) Miscellanea Nomenclatorica Ciliatea (Protozoa: Ciliophora). Arch Protistenk 133: 219–235 (in German with English summary).
- 4. Müller OF (1773) Vermium Terrestrium et Fluviatilium, seu Animalium Infusoriorum, Helminthicorum et Testaceorum, non Marinorum, Succincta Historia. Hauniae, Lipsiae: Heineck & Faber. 135 p.
- 5. Dujardin F (1841) Histoire naturelle des zoophytes. Infusoires, comprenant la physiologie et la classification de ces animaux, et la manière de les étudier a l'aide du microscope. Paris: Libraire Encyclopédique de Roret. 684 p. + 14 p. Explication des Planches + Plates 1–22.
- 6. Kent WS (1881–1882) 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. Vol. II. London: Bogue D. pp. 473–913 + Plates 25–51.
- 7. Awerinzew S (1901) Zur Morphologie und Systematik der Familie Halterina Clap. et Lachm. Trudy Imp S-Peterb Obshch Estest 31: 1–63 (in Russian with German summary).
- 8. Kahl A (1932) Urtiere oder Protozoa I: Wimpertiere oder Ciliata (Infusoria) 3. Spirotricha. Tierwelt Dtl 25: 399–650.
- 9. Kahl A (1935) Urtiere oder Protozoa I: Wimpertiere oder Ciliata (Infusoria) 4. Peritricha und Chonotricha. Tierwelt Dtl 30: 651–886.
- 10. Maeda M, Carey PG (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.
- 11. 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.
- 12. Corliss JO (2003) Comments on the neotypification of protists, especially ciliates (Protozoa, Ciliophora). Bull Zool Nom 60: 48.
- 13. Foissner W (2002) Neotypification of protists, especially ciliates (Protozoa, Ciliophora). Bull Zool Nom 59: 165–169.
- 14. Foissner W, Agatha S, Berger H (2002) Soil ciliates (Protozoa, Ciliophora) from Namibia (Southwest Africa), with emphasis on two contrasting environments, the Etosha region and the Namib Desert. Part I: Text and line drawings. Part II: Photographs. Denisia 5: 1–1459.
- 15. Dale T, Dahl E (1987) Mass occurrence of planktonic oligotrichous ciliates in a bay in southern Norway. J Plankton Res 9: 871–879.
- 16. Edwards ES, Burkill PH (1995) Abundance, biomass and distribution of microzooplankton in the Irish Sea. J Plankton Res 17: 771–782.
- 17. Jonsson PR (1989) Vertical distribution of planktonic ciliates - an experimental analysis of swimming behaviour. Mar Ecol Prog Ser 52: 39–53.
- 18. Tanaka T, Rassoulzadegan F (2002) Full-depth profile (0–2000 m) of bacteria, heterotrophic nanoflagellates and ciliates in the NW Mediterranean Sea: vertical partitioning of microbial trophic structures. Deep-Sea Res II 49: 2093–2107.
- 19. Montagnes DJS, Humphrey E (1998) A description of occurrence and morphology of a new species of red-water forming Strombidium (Spirotrichea, Oligotrichia). J Eukaryot Microbiol 45: 502–506.
- 20. Fauré-Fremiet E (1910) La fixation chez les infusoires ciliés. Bull Scient Fr Belg 45: 27–50.
- 21. Fauré-Fremiet E (1950) Écologie des ciliés psammophiles littoraux. Bull Biol Fr Belg 84: 35–75.
- 22. Song W, Wilbert N, Hill BF (1994) Description of three endocommensal ciliates from sea urchins in the Weddell Sea, Antarctica (Protozoa, Ciliophora). Antarctic Res (Chin Ed) 6: 53–61 . (in Chinese with English summary; content almost identical to  in the supporting information Table S1).
- 23. Xu D, Sun P, Song W, Warren A (2008) Studies on a new endocommensal ciliate, Strombidium foissneri nov. sp. (Ciliophora, Oligotrichida), from the intestine of the sea urchin Hemicentrotus pulcherrimus (Camarodonta, Echinoida). Denisia 23: 273–278.
- 24. Xu D, Song W, Sun P, Chen X (2006) Morphology and infraciliature of the oligotrich ciliate Strombidium rapulum (Yagiu, 1933) Kahl, 1934 (Protozoa, Ciliophora, Oligotrichida) from the intestine of sea urchin Hemicentrotus pulcherrimus Agassiz. Zootaxa 1113: 33–40.
- 25. Azam F, Fenchel T, Field JG, Gray JS, Meyer-Reil LA, et al. (1983) The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser 10: 257–263.
- 26. Pierce RW, Turner JT (1992) Ecology of planktonic ciliates in marine food webs. Rev Aquat Sci 6: 139–181.
- 27. Fenchel T (2008) The microbial loop – 25 years later. J Exp Mar Biol Ecol 366: 99–103.
- 28. Strom SL, Loukos H (1998) Selective feeding by protozoa: model and experimental behaviors and their consequences for population stability. J Plankton Res 20: 831–846.
- 29. Blackbourn DJ, Taylor FJR, Blackbourn J (1973) Foreign organelle retention by ciliates. J Protozool 20: 286–288.
- 30. Laval-Peuto M, Febvre M (1983) Ultrastructure of Tontonia appendiculariformis (Ciliophora, Oligotrichida, Oligotrichina). Europ Conf Ciliate Biol 5:
- 31. Laval-Peuto M, Salvano P, Gayol P, Greuet C (1986) Mixotrophy in marine planktonic ciliates: ultrastructural study of Tontonia appendiculariformis (Ciliophora, Oligotrichina). Mar Microb Food Webs 1: 81–104.
- 32. Stoecker DK, Silver MW (1987) Chloroplast retention by marine planktonic ciliates. Ann NY Acad Sci 503: 562–565.
- 33. Stoecker DK, Silver MW (1990) Replacement and aging of chloroplasts in Strombidium capitatum (Ciliophora: Oligotrichida). Mar Biol 107: 491–502.
- 34. Stoecker DK, Michaels AE, Davis LH (1987) Large proportion of marine planktonic ciliates found to contain functional chloroplasts. Nature 326: 790–792.
- 35. Stoecker DK, Silver MW, Michaels AE, Davis LH (1988) Obligate mixotrophy in Laboea strobila, a ciliate which retains chloroplasts. Mar Biol 99: 415–423.
- 36. Stoecker DK, Silver MW, Michaels AE, Davis LH (1989) Enslavement of algal chloroplasts by four Strombidium spp. (Ciliophora, Oligotrichida). Mar Microb Food Webs 3(year 1988/1989): 79–100.
- 37. Agatha S, Strüder-Kypke MC, Beran A, Lynn DH (2005) Pelagostrobilidium neptuni (Montagnes and Taylor, 1994) and Strombidium biarmatum nov. spec. (Ciliophora, Oligotrichea): phylogenetic position inferred from morphology, ontogenesis, and gene sequence data. Eur J Protistol 41: 65–83.
- 38. Ichinomiya M, Nakamachi M, Taniguchi A (2004) A practical method for enumerating cysts of ciliates in natural marine sediments. Aquat Microb Ecol 37: 305–310.
- 39. Kim Y-O, Taniguchi A (1995) Excystment of the oligotrich ciliate Strombidium conicum. Aquat Microb Ecol 9: 149–156.
- 40. Kim Y-O, Suzuki T, Taniguchi A (2002) A new species in the genus Cyrtostrombidium (Ciliophora, Oligotrichia, Oligotrichida): its morphology, seasonal cycle and resting stage. J Eukaryot Microbiol 49: 338–343.
- 41. Kim Y-O, Ha S, Taniguchi A (2008) Morphology and in situ sedimentation of the cysts of a planktonic oligotrich ciliate, Strombidium capitatum. Aquat Microb Ecol 53: 173–179.
- 42. Fauré-Fremiet E (1948) Le rythme de marée du Strombidium oculatum Gruber. Bull Biol Fr Belg 82: 3–23.
- 43. Fauré-Fremiet E (1948) The ecology of some infusorian communities of intertidal pools. J Anim Ecol 17: 127–130.
- 44. Jonsson PR (1994) Tidal rhythm of cyst formation in the rock pool ciliate Strombidium oculatum Gruber (Ciliophora, Oligotrichida): a description of the functional biology and an analysis of the tidal synchronization of encystment. J Exp Mar Biol Ecol 175: 77–103.
- 45. McManus GB, Xu D, Costas BA, Katz LA (2010) Genetic identities of cryptic species in the Strombidium stylifer/apolatum/oculatum cluster, including a description of Strombidium rassoulzadegani n. sp. J Eukaryot Microbiol 57: 369–378.
- 46. Montagnes DJS, Lowe CD, Poulton A, Jonsson PR (2002) Redescription of Strombidium oculatum Gruber 1884 (Ciliophora, Oligotrichia). J Eukaryot Microbiol 49: 329–337.
- 47. Reid PC (1987) Mass encystment of a planktonic oligotrich ciliate. Mar Biol 95: 221–230.
- 48. Kim Y-O, Taniguchi A (1997) Seasonal variation of excystment pattern of the planktonic oligotrich ciliate Strombidium conicum. Mar Biol 128: 207–212.
- 49. Lowe CD, Montagnes DJS (2001) Population growth strategies of a rock pool ciliate. Br Ecol Soc Bull 32: 24–25.
- 50. Montagnes DJS, Wilson D (1998) Population dynamics of a rock-pool ciliate, a model system. Br Ecol Soc Bull 29: 25.
- 51. Montagnes DJS, Wilson D, Brooks SJ, Lowe C, Campey M (2002) Cyclical behaviour of the tide-pool ciliate Strombidium oculatum. Aquat Microb Ecol 28: 55–68.
- 52. Li Y-X, Zhang S-X, Zhang J (2009) Mesoproterozoic Calymmian tintinnids from Central China. Open Paleontol J 2: 10–13.
- 53. Agatha S (2004) A cladistic approach for the classification of oligotrichid ciliates (Ciliophora: Spirotricha). Acta Protozool 43: 201–217.
- 54. Agatha S, Strüder-Kypke MC (2007) Phylogeny of the order Choreotrichida (Ciliophora, Spirotricha, Oligotrichea) as inferred from morphology, ultrastructure, ontogenesis, and SSrRNA gene sequences. Eur J Protistol 43: 37–63.
- 55. Agatha S, Strüder-Kypke MC, Beran A (2004) Morphologic and genetic variability in the marine planktonic ciliate Laboea strobila Lohmann, 1908 (Ciliophora, Oligotrichia), with notes on its ontogenesis. J Eukaryot Microbiol 51: 267–281.
- 56. Gao S, Gong J, Lynn D, Lin X, Song W (2009) An updated phylogeny of oligotrich and choreotrich ciliates (Protozoa, Ciliophora, Spirotrichea) with representative taxa collected from Chinese coastal waters. Syst Biodiv 7: 235–242.
- 57. Gao S, Gong J, Lynn D, Lin X, Song W (2009) An updated phylogeny of oligotrich and choreotrich ciliates (Protozoa, Ciliophora, Spirotrichea) with representative taxa collected from Chinese coastal waters – Corrigendum. Syst Biodiv 7: 347.
- 58. Kim JS, Jeong HJ, Strüeder-Kypke MC, Lynn DH, Kim S, et al. (2005) Parastrombidinopsis shimi n. gen., n. sp. (Ciliophora: Choreotrichia) from the coastal waters of Korea: morphology and small subunit ribosomal DNA sequence. J Eukaryot Microbiol 52: 514–522.
- 59. Kim Y-O, Kim SY, Lee W-J, Choi JK (2010) New observations on the choreotrich ciliate Strombidinopsis acuminata Fauré-Fremiet 1924, and comparison with Strombidinopsis jeokjo Jeong et al., 2004. J Eukaryot Microbiol 57: 48–55.
- 60. Modeo L, Petroni G, Rosati G, Montagnes DJS (2003) A multidisciplinary approach to describe protists: redescriptions of Novistrombidium testaceum Anigstein 1914 and Strombidium inclinatum Montagnes, Taylor, and Lynn 1990 (Ciliophora, Oligotrichia). J Eukaryot Microbiol 50: 175–189.
- 61. Snoeyenbos-West OLO, Salcedo T, McManus GB, Katz LA (2002) Insights into the diversity of choreotrich and oligotrich ciliates (Class: Spirotrichea) based on genealogical analyses of multiple loci. Int J Syst Evol Microbiol 52: 1901–1913.
- 62. Strüder-Kypke MC, Lynn DH (2003) Sequence analyses of the small subunit rRNA gene confirm the paraphyly of oligotrich ciliates sensu lato and support the monophyly of the subclasses Oligotrichia and Choreotrichia (Ciliophora, Spirotrichea). J Zool Lond 260: 87–97.
- 63. Strüder-Kypke MC, Lynn DH (2008) Morphological versus molecular data – phylogeny of tintinnid ciliates (Ciliophora, Choreotrichia) inferred from small subunit rRNA gene sequences. Denisia 23: 417–424.
- 64. Tsai S-F, Xu D, Chung C-C, Chiang K-P (2008) Parastrombidinopsis minima n. sp. (Ciliophora: Oligotrichia) from the coastal waters of northeastern Taiwan: morphology and small subunit ribosomal DNA sequence. J Eukaryot Microbiol 55: 567–573.
- 65. Agatha S, Foissner W (2009) Conjugation in the spirotrich ciliate Halteria grandinella (Müller, 1773) Dujardin, 1841 (Protozoa, Ciliophora) and its phylogenetic implications. Eur J Protistol 45: 51–63.
- 66. Foissner W, Müller H, Agatha S (2007) A comparative fine structural and phylogenetic analysis of resting cysts in oligotrich and hypotrich Spirotrichea (Ciliophora). Eur J Protistol 43: 295–314.
- 67. Shin MK, Hwang UW, Kim W, Wright A-DG, Krawczyk C, et al. (2000) Phylogenetic position of the ciliates Phacodinium (order Phacodiniida) and Protocruzia (subclass Protocruziidia) and systematics of the spirotrich ciliates examined by small subunit ribosomal RNA gene sequences. Eur J Protistol 36: 293–302.
- 68. Agatha S (2004) Evolution of ciliary patterns in the Oligotrichida (Ciliophora, Spirotricha) and its taxonomic implications. Zoology 107: 153–168.
- 69. Agatha S (2011) Updated hypothesis on the evolution of oligotrichid ciliates (Ciliophora, Spirotricha, Oligotrichida) based on somatic ciliary patterns and ontogenetic data. Eur J Protistol 47: 51–56.
- 70. Fenchel T (1986) Protozoan filter feeding. Progr Protistol 1: 65–113.
- 71. Modeo L, Petroni G, Bonaldi M, Rosati G (2001) Trichites of Strombidium (Ciliophora, Oligotrichida) are extrusomes. J Eukaryot Microbiol 48: 95–101.
- 72. Fauré-Fremiet E, Ganier M-C (1970) Structure fine du Strombidium sulcatum Cl. et L. (Ciliata Oligotrichida). Protistologica 6: 207–223.
- 73. Laval-Peuto M, Febvre M (1986) On plastid symbiosis in Tontonia appendiculariformis (Ciliophora, Oligotrichina). Biosystems 19: 137–158.
- 74. Laval-Peuto M, Gayol P, Salvano P, Greuet C (1985) Ultrastructure et cytochimie de la pellicule de Tontonia appendiculariformis, Ciliophora, Oligotrichida. J Protozool 32: 40A.
- 75. Pierce RW, Turner JT (1993) Global biogeography of marine tintinnids. Mar Ecol Prog Ser 94: 11–26.
- 76. Zeitzschel B (1966) Die Verbreitung der Tintinnen im Nordatlantik. Veröff Inst Meeresforsch Bremerh Sonderbd 2: 293–300.
- 77. Zeitzschel B (1969) Tintinnen des westlichen Arabischen Meeres, ihre Bedeutung als Indikatoren für Wasserkörper und Glied der Nahrungskette. “Meteor” Forschungsergeb (D) 4: 47–101.
- 78. Zeitzschel B (1982) Zoogeography of pelagic marine protozoa. Annls Inst Océanogr, Paris 58,: Suppl91–116.
- 79. Zeitzschel B (1990) Zoogeography of marine protozoa: an overview emphasizing distribution of planktonic forms. In: Capriulo GM, editor. Ecology of Marine Protozoa. New York: Oxford Univ Press. pp. 139–185.
- 80. Bouchet P (2006) The magnitude of marine biodiversity. In: Duarte CM, editor. The Exploration of Marine Biodiversity: Scientific and Technological Challenges. Madrid: Fundación BBVA. pp. 31–64.
- 81. Costello MJ, Coll M, Danovaro R, Halpin P, Ojaveer H, et al. (2010) A census of marine biodiversity knowledge, resources, and future challenges. PLoS ONE 5: e12110. doi:10.1371/journal.pone.0012110.
- 82. Agatha S Costello MJ, Emblow C, White R, editors. (2001) Oligotrichea (aloricate species). European Register of Marine Species. A Check-list of the Marine Species in Europe and a Bibliography of Guides to Their Identification. Patrimoines naturels 50: 42–44.
- 83. Van der Spoel S, Heyman RP (1983) A Comparative Atlas of Zooplankton. Biological Patterns in the Oceans. Berlin, Heidelberg, New York, Tokyo: Springer-Verlag. 186 p.
- 84. Tyler PA (1996) Endemism in freshwater algae with special reference to the Australian region. Hydrobiologia 336: 127–135.
- 85. Darling KF, Wade CM, Stewart IA, Kroon D, Dingle R, et al. (2000) Molecular evidence for genetic mixing of Arctic and Antarctic subpolar populations of planktonic foraminifers. Nature 405: 43–47.
- 86. Lazarus D (1983) Speciation in pelagic Protista and its study in the planktonic microfossil record: a review. Paleobiol 9: 327–340.
- 87. Montresor M, Lovejoy C, Orsini L, Procaccini G, Roy S (2003) Bipolar distribution of the cyst-forming dinoflagellate Polarella glacialis. Polar Biol 26: 186–194.
- 88. Fenchel T (1987) Ecology of Protozoa: the Biology of Free-living Phagotrophic Protists. In: Brock TD, editor. Berlin: Brock/Springer Series in Contemporary Bioscience. pp i–x + 197.
- 89. Hillebrand H, Watermann F, Karez R, Berninger U-G (2001) Differences in species richness patterns between unicellular and multicellular organisms. Oecologia 126: 114–124.
- 90. Weisse T (2008) Distribution and diversity of aquatic protists: an evolutionary and ecological perspective. Biodivers Conserv 17: 243–259.
- 91. Aurahs R, Grimm GW, Hemleben V, Hemleben C, Kucera M (2009) Geographical distribution of cryptic genetic types in the planktonic foraminifer Globigerinoides ruber. Mol Ecol 18: 1692–1706.
- 92. Simon N, Cras A-L, Foulon E, Lemée R (2009) Diversity and evolution of marine phytoplankton. C R Biologies 332: 159–170.
- 93. De Vargas C, Norris R, Zaninetti L, Gibb SW, Pawlowski J (1999) Molecular evidence of cryptic speciation in planktonic foraminifers and their relation to oceanic provinces. Proc Natl Acad Sci USA 96: 2864–2868.
- 94. Sáez AG, Probert I, Geisen M, Quinn P, Young JR, et al. (2003) Pseudo-cryptic speciation in coccolithophores. Proc Natl Acad Sci USA 100: 7163–7168.
- 95. Morard R, Quillévéré F, Escarguel G, Ujiie Y, De Garidel-Thoron T, et al. (2009) Morphological recognition of cryptic species in the planktonic foraminifer Orbulina universa. Mar Micropaleontol 71: 148–165.
- 96. Palumbi SR (1994) Genetic divergence, reproductive isolation, and marine speciation. Annu Rev Ecol Syst 25: 547–572.
- 97. Agapow P-M, Bininda-Emonds ORP, Crandall KA, Gittleman JL, Mace GM, et al. (2004) The impact of species concept on biodiversity studies. Q Rev Biol 79: 161–179.
- 98. Modigh M, Castaldo S (2005) Effects of fixatives on ciliates as related to cell size. J Plankton Res 27: 845–849.
- 99. Green J, Bohannan BJM (2006) Spatial scaling of microbial biodiversity. Trends Ecol Evol 21: 501–507.
- 100. Chao A, Li PC, Agatha S, Foissner W (2006) A statistical approach to estimate soil ciliate diversity and distribution based on data from five continents. Oikos 114: 479–493.
- 101. Nolte V, Pandey RV, Jost S, Medinger R, Ottenwälder B, et al. (2010) Contrasting seasonal niche separation between rare and abundant taxa conceals the extend of protist diversity. Mol Ecol 19: 2908–2915.
- 102. Foissner W (2006) Biogeography and dispersal of micro-organisms: a review emphasizing protists. Acta Protozool 45: 111–136.
- 103. Pierce RW, Carlton JT, Carlton DA, Geller JB (1997) Ballast water as a vector for tintinnid transport. Mar Ecol Prog Ser 149: 295–297.
- 104. Kaluza P, Kölzsch A, Gastner MT, Blasius B (2010) The complex network of global cargo ship movements. J R Soc Interface 7: 1093–1103.
- 105. Finlay BJ, Esteban GF, Fenchel T (2004) Protist diversity is different? Protist 155: 15–22.
- 106. Foissner W (1999) Protist diversity: estimates of the near-imponderable. Protist 150: 363–368.
- 107. Hughes Martiny JB, Bohannan BJM, Brown JH, Colwell RK, Fuhrman JA, et al. (2006) Microbial biogeography: putting microorganisms on the map. Nature Rev 4: 102–112.
- 108. Hubbell SP (2001) The Unified Neutral Theory of Biodiversity and Biogeography. Monographs in Population Biology 32. Princeton, NJ: Princeton Univ Press. 448 p.
- 109. Ricklefs RE (2003) A comment on Hubbell's zero-sum ecological drift model. Oikos 100: 185–192.
- 110. Baas Becking LGM (1934) Geobiologie of inleiding tot de milieukunde. The Hague: Van Stockum WP & Zoon. 263 p. (in Dutch).
- 111. Finlay BJ (2002) Global dispersal of free-living microbial eukaryote species. Science 296: 1061–1063.
- 112. Dolan JR, Ritchie ME, Ras J (2007) The “neutral” community structure of planktonic herbivores, tintinnid ciliates of the microzooplankton, across the SE Tropical Pacific Ocean. Biogeosci 4: 297–310.
- 113. Dolan JR, Ritchie ME, Tunin-Ley A, Pizay M-D (2009) Dynamics of core and occasional species in the marine plankton: tintinnid ciliates in the north-west Mediterranean Sea. J Biogeogr 36: 887–895.
- 114. Sitran R, Bergamasco A, Decembrini F, Guglielmo L (2009) Microzooplankton (tintinnid ciliates) diversity: coastal community structure and driving mechanisms in the southern Tyrrhenian Sea (Western Mediterranean). J Plankton Res 31: 153–170.
- 115. Doherty M, Costas BA, McManus GB, Katz LA (2007) Culture-independent assessment of planktonic ciliate diversity in coastal northwest Atlantic waters. Aquat Microb Ecol 48: 141–154.
- 116. Doherty M, Tamura M, Costas BA, Ritchie ME, McManus GB, et al. (2010) Ciliate diversity and distribution across an environmental and depth gradient in Long Island Sound, USA. Environ Microbiol 12: 886–898.
- 117. Foissner W (2008) Protist diversity and distribution: some basic considerations. Biodivers Conserv 17: 235–242.
- 118. Magurran AE, Henderson PA (2003) Explaining the excess of rare species in natural species abundance distributions. Nature 422: 714–716.
- 119. Kato S, Taniguchi A (1993) Tintinnid ciliates as indicator species of different water masses in the western North Pacific Polar Front. Fish Oceanogr 2: 166–174.
- 120. Holzer M, Primeau FW (2006) The diffusive ocean conveyor. Geophys Res Lett 33, L14618: 1–5.
- 121. Bonhommeau S, Le Pape O, Gascuel D, Blanke B, Tréguier A-M, et al. (2009) Estimates of the mortality and the duration of the trans-Atlantic migration of European eel Anguilla anguilla leptocephali using a particle tracking model. J Fish Biol 74: 1891–1914.
- 122. Kettle AJ, Haines K (2006) How does the European eel (Anguilla anguilla) retain its population structure during its larval migration across the North Atlantic Ocean? Can J Fish Aquat Sci 63: 90–106.
- 123. Rubino F, Moscatello S, Saracino OD, Fanelli G, Belmonte G, et al. (2002) Plankton-derived resting stages in marine coastal sediments along the Salento Peninsula (Apulia, South-Eastern Italy). PSZN, Mar Ecol 23,: Suppl 1329–339.
- 124. Müller H, Stadler P, Weisse T (2002) Seasonal dynamics of cyst formation of strombidiid ciliates in alpine Lake Mondsee, Austria. Aquat Microb Ecol 29: 181–188.
- 125. Foissner W (2007) Dispersal and biogeography of protists: recent advances. Jpn J Protozool 40: 1–16.
- 126. Helbig AJ (2005) A ring of species. Heredity 95: 113–114.
- 127. Montagnes DJS, Poulton AJ, Shammon TM (1999) Mesoscale, finescale and microscale distribution of micro- and nanoplankton in the Irish Sea, with emphasis on ciliates and their prey. Mar Biol 134: 167–179.
- 128. Pinel-Alloul B, Ghadouani A (2007) Spatial heterogeneity of planktonic microorganisms in aquatic systems. In: Franklin RB, Mills AL, editors. The Spatial Distribution of Microbes in the Environment. Dordrecht: Springer. pp. 203–310.
- 129. Tittensor DP, Mora C, Jetz W, Lotze HK, Ricard D, et al. (2010) Global patterns and predictors of marine biodiversity across taxa. Nature 466: 1098–1101 + Supplementary Information.
- 130. Benton MJ, Pearson PN (2001) Speciation in the fossil record. Trends Ecol Evol 16: 405–411.
- 131. Koester JA, Swalwell JE, von Dassow P, Armbrust EV (2010) Genome size differentiates co-occurring populations of the planktonic diatom Ditylum brightwellii (Bacillariophyta). BMC Evol Biol 10: 1. doi:10.1186/1471-2148-10-1.
- 132. Palenik B, Grimwood J, Aerts A, Rouzé P, Salamov A, et al. (2007) The tiny eukaryote Ostreococcus provides genomic insights into the paradox of plankton speciation. Proc Natl Acad Sci USA 104: 7705–7710.
- 133. Pearson PN, Shackleton NJ, Hall MA (1997) Stable isotopic evidence for the sympatric divergence of Globigerinoides trilobus and Orbulina universa (planktonic foraminifera). J Geol Soc, Lond 154: 295–302.
- 134. Sexton PF, Norris RD (2008) Dispersal and biogeography of marine plankton: long-distance dispersal of the foraminifer Truncorotalia truncatulinoides. Geology 36: 899–902.
- 135. Bass D, Richards TA, Matthai L, Marsh V, Cavalier-Smith T (2007) DNA evidence for global dispersal and probable endemicity of protozoa. BMC Evol Biol 7: 162. doi:10.1186/1471-2148-7-162.
- 136. Casteleyn G, Leliaert F, Backeljau T, Debeer A-E, Kotaki Y, et al. (2010) Limits to gene flow in a cosmopolitan marine planktonic diatom. Proc Natl Acad Sci USA 107: 12952–12957.
- 137. Darling KF, Wade CM (2008) The genetic diversity of planktic foraminifera and the global distribution of ribosomal RNA genotypes. Mar Micropaleontol 67: 216–238.
- 138. Darling KF, Kucera M, Pudsey CJ, Wade CM (2004) Molecular evidence links cryptic diversification in polar planktonic protists to Quaternary climate dynamics. Proc Natl Acad Sci USA 101: 7657–7662.
- 139. De Vargas C, Bonzon M, Rees NW, Pawlowski J, Zaninetti L (2002) A molecular approach to biodiversity and biogeography in the planktonic foraminifer Globigerinella siphonifera (d'Orbigny). Mar Micropaleontol 45: 101–116.
- 140. Taylor FJR, Hoppenrath M, Saldarriaga JF (2008) Dinoflagellate diversity and distribution. Biodivers Conserv 17: 407–418.
- 141. Jeong HJ, Kim JS, Kim S, Song JY, Lee I, et al. (2004) Strombidinopsis jeokjo n. sp. (Ciliophora: Choreotrichida) from the coastal waters off western Korea: morphology and small subunit ribosomal DNA gene sequence. J Eukaryot Microbiol 51: 451–455.
- 142. Zhang Q, Yi Z, Xu D, Al-Rasheid KAS, Gong J, et al. (2010) Molecular phylogeny of oligotrich genera Omegastrombidium and Novistrombidium (Protozoa, Ciliophora) for the systematical relationships within Family Strombidiidae. Chin J Oceanol Limnol 28: 769–777.
- 143. Foissner W, Chao A, Katz LA (2008) Diversity and geographic distribution of ciliates (Protista: Ciliophora). Biodivers Conserv 17: 345–363.
- 144. Katz LA, McManus GB, Snoeyenbos-West OLO, Griffin A, Pirog K, et al. (2005) Reframing the ‘everything is everywhere’ debate: evidence for high gene flow and diversity in ciliate morphospecies. Aquat Microb Ecol 41: 55–65.
- 145. McManus GB, Katz LA (2009) Molecular and morphological methods for identifying plankton: what makes a successful marriage? J Plankton Res 31: 1119–1129.
- 146. Weisse T, Strüder-Kypke MC, Berger H, Foissner W (2008) Genetic, morphological, and ecological diversity of spatially separated clones of Meseres corlissi Petz & Foissner, 1992 (Ciliophora, Spirotrichea). J Eukaryot Microbiol 55: 257–270.
- 147. Weisse T, Rammer S (2006) Pronounced ecophysiological clonal differences of two common freshwater ciliates, Coleps spetai (Prostomatida) and Rimostrombidium lacustris (Oligotrichida), challenge the morphospecies concept. J Plankton Res 28: 55–63.
- 148. Hutchinson GE (1961) The paradox of the plankton. Amer Nat 95: 137–145.
- 149. Huisman J, Weissing FJ (1999) Biodiversity of plankton by species oscillations and chaos. Nature 402: 407–410.
- 150. Fox JW, Barreto C (2006) Surprising competitive coexistence in a classic model system. Commun Ecol 7: 143–154.
- 151. Scheffer M, Van Nes EH (2006) Self-organized similarity, the evolutionary emergence of groups of similar species. Proc Natl Acad Sci USA 103: 6230–6235.
- 152. Gravel D, Canham CD, Beaudet M, Messier C (2006) Reconciling niche and neutrality: the continuum hypothesis. Ecol Lett 9: 399–409.
- 153. Alonso D, Etienne RS, McKane AJ (2006) The merits of neutral theory. Trends Ecol Evol 21: 451–457.
- 154. Gismervik I (2005) Numerical and functional responses of choreo- and oligotrich planktonic ciliates. Aquat Microb Ecol 40: 163–173.
- 155. Montagnes DJS (1996) Growth responses of planktonic ciliates in the genera Strobilidium and Strombidium. Mar Ecol Prog Ser 130: 241–254.
- 156. Agatha S, Riedel-Lorjé JC (1997) Morphology, infraciliature, and ecology of halteriids and strombidiids (Ciliophora, Oligotrichea) from coastal brackish water basins. Arch Protistenk 148: 445–459.
- 157. Christaki U, Dolan JR, Pelegri S, Rassoulzadegan F (1998) Consumption of picoplankton-size particles by marine ciliates: effects of physiological state of the ciliate and particle quality. Limnol Oceanogr 43: 458–464.
- 158. Gonzalez JM, Sherr EB, Sherr BF (1990) Size-selective grazing on bacteria by natural assemblages of estuarine flagellates and ciliates. Appl Environ Microbiol 56: 583–589.
- 159. Jonsson PR (1986) Particle size selection, feeding rates and growth dynamics of marine planktonic oligotrichous ciliates (Ciliophora: Oligotrichina). Mar Ecol Prog Ser 33: 265–277.
- 160. Claessens M, Wickham SA, Post AF, Reuter M (2008) Ciliate community in the oligotrophic Gulf of Aqaba, Red Sea. Aquat Microb Ecol 53: 181–190.
- 161. Claessens M, Wickham SA, Post AF, Reuter M (2010) A paradox of the ciliates? High ciliate diversity in a resource-poor environment. Mar Biol 157: 483–494.
- 162. Countway PD, Gast RJ, Savai P, Caron DA (2005) Protistan diversity estimates based on 18S rDNA from seawater incubations in the western North Atlantic. J Eukaryot Microbiol 52: 95–106.
- 163. Pitta P, Giannakourou A (2000) Planktonic ciliates in the oligotrophic Eastern Mediterranean: vertical, spatial distribution and mixotrophy. Mar Ecol Prog Ser 194: 269–282.
- 164. Luo W, Li H, Cai M, He J (2009) Diversity of microbial eukaryotes in Kongsfjorden, Svalbard. Hydrobiologia 636: 233–248.
- 165. Brayard A, Escarguel G, Bucher H (2005) Latitudinal gradient of taxonomic richness: combined outcome of temperature and geographic mid-domains effects? J Zool Syst Evol Res 43: 178–188.
- 166. Rutherford S, D'Hondt S, Prell W (1999) Environmental controls on the geographic distribution of zooplankton diversity. Nature 400: 749–753.
- 167. Dolan JR, Lemée R, Gasparini S, Mousseau L, Heyndrickx C (2006) Probing diversity in the plankton: using patterns in tintinnids (planktonic marine ciliates) to identify mechanisms. Hydrobiologia 555: 143–157.
- 168. Secretariat of the Convention on Biological Diversity (2008) Guide to the Global Taxonomy Initiative. 105 p. CBD Technical Series 30.
- 169. Rassoulzadegan F, Laval-Peuto M, Sheldon RW (1988) Partitioning of the food ration of marine ciliates between pico- and nanoplankton. Hydrobiologia 159: 75–88.
- 170. Strom SL, Postel JR, Booth BC (1993) Abundance, variability, and potential grazing impact of planktonic ciliates in the open subarctic Pacific Ocean. Prog Oceanogr 32: 185–203.
- 171. Verity PG (1986) Grazing of phototrophic nanoplankton by microzooplankton in Narragansett Bay. Mar Ecol Prog Ser 29: 195–115.
- 172. Belviso S, Kim S-K, Rassoulzadegan F, Krajka B, Nguyen BC, et al. (1990) Production of dimethylsulfonium propionate (DMSP) and dimethylsulfide (DMS) by a microbial food web. Limnol Oceanogr 35: 1810–1821.
- 173. Christaki U, Belviso S, Dolan JR, Corn M (1996) Assessment of the role of copepods and ciliates in the release to solution of particulate DMSP. Mar Ecol Prog Ser 141: 119–127.
- 174. Dolan JR (1997) Phosphorus and ammonia excretion by planktonic protists. Mar Geol 139: 109–122.
- 175. Clough J, Strom S (2005) Effects of Heterosigma akashiwo (Raphidophyceae) on protist grazers: laboratory experiments with ciliates and heterotrophic dinoflagellates. Aquat Microb Ecol 39: 121–134.
- 176. Fileman ES, Cummings DG, Llewellyn CA (2002) Microplankton community structure and the impact of microzooplankton grazing during an Emiliania huxleyi bloom, off the Devon coast. J Mar Biol Ass UK 82: 359–368.
- 177. Graham SL, Strom SL (2010) Growth and grazing of microzooplankton in response to the harmful alga Heterosigma akashiwo in prey mixtures. Aquat Microb Ecol 59: 111–124.
- 178. Jeong HJ, Shim JH, Lee CW, Kim JS, Koh SM (1999) Growth and grazing rates of the marine planktonic ciliate Strombidinopsis sp. on red-tide and toxic dinoflagellates. J Eukaryot Microbiol 46: 69–76.
- 179. Jeong HJ, Kim JS, Song JY, Kim JH, Kim TH, et al. (2007) Feeding by protists and copepods on the heterotrophic dinoflagellates Pfiesteria piscicida, Stoeckeria algicida, and Luciella masanensis. Mar Ecol Prog Ser 349: 199–211.
- 180. Johnson MD, Rome M, Stoecker DK (2003) Microzooplankton grazing on Prorocentrum minimum and Karlodinium micrum in Chesapeake Bay. Limnol Oceanogr 48: 238–248.
- 181. Rosetta CH, McManus GB (2003) Feeding by ciliates on two harmful algal bloom species, Prymnesium parvum and Prorocentrum minimum. Harmful Algae 2: 109–126.
- 182. Ptacnik R, Moorthi SD, Hillebrand H (2010) Hutchinson reversed, or why there need to be so many species. Adv Ecol Res 43: 1–43.
- 183. Caron DA, Countway PD (2009) Hypotheses on the role of the protistan rare biosphere in a changing world. Aquat Microb Ecol 57: 227–238.
- 184. Cotterill FPD, Al-Rasheid K, Foissner W (2008) Conservation of protists: is it needed at all? Biodivers Conserv 17: 427–443.
- 185. Secretariat of the Convention on Biological Diversity (2005) Handbook of the Convention on Biological Diversity Including its Cartagena Protocol on Biosafety, 3rd edition. Montreal, Canada: pp i–xl + 1493.
- 186. Will KW, Rubinoff D (2004) Myth of the molecule: DNA barcodes for species cannot replace morphology for identification and classification. Cladistics 20: 47–55.
- 187. Ferguson JWH (2002) On the use of genetic divergence for identifying species. Biol J Linnean Soc 75: 509–516.
- 188. Knapp S, Bateman RM, Chalmers NR, Humphries CJ, Rainbow PS, et al. (2002) Taxonomy needs evolution, not revolution. Nature 419: 559.
- 189. Seberg O, Humphries CJ, Knapp S, Stevenson DW, Petersen G, et al. (2003) Shortcuts in systematics? A commentary on DNA-based taxonomy. Trends Ecol Evol 18: 63–65.
- 190. Petz W, Foissner W (1992) Morphology and morphogenesis of Strobilidium caudatum (Fromentel), Meseres corlissi n. sp., Halteria grandinella (Müller), and Strombidium rehwaldi n. sp., and a proposed phylogenetic system for oligotrich ciliates (Protozoa, Ciliophora). J Protozool 39: 159–176.
- 191. Barth D, Krenek S, Fokin SI, Berendonk TU (2006) Intraspecific genetic variation in Paramecium revealed by mitochondrial cytochrome c oxidase I sequences. J Eukaryot Microbiol 53: 20–25.
- 192. Lynn DH, Montagnes DJS (1988) Taxonomic descriptions of some conspicuous species of strobilidiine ciliates (Ciliophora: Choreotrichida) from the Isles of Shoals, Gulf of Maine. J Mar Biol Ass UK 68: 639–658.