Reconciling Cladistic and Genetic Analyses in Choreotrichid Ciliates (Ciliophora, Spirotricha, Oligotrichea)

Reconciling Cladistic and Genetic Analyses in Choreotrichid Ciliates (Ciliophora,Spirotricha, Oligotrichea)

SABINE AGATHAaand MICHAELA C. STRUDER-KYPKE

b

aDepartment of Organismic Biology, University of Salzburg, Hellbrunnerstraße 34, A-5020 Salzburg, Austria, andbDepartment of Molecular and Cellular Biology, University of Guelph, Guelph, ON, N1G 2W1, Canada

ABSTRACT. Fifty-six features of halteriid, oligotrichid, and choreotrichid ciliates are cladistically analysed, including an updatedhypothesis about the evolution of the somatic ciliary patterns. Based on its morphology, Lynnella clusters with Parastrombidinop-sis, Parastrombidium, and Strombidinopsis, while it is basal to the other choreotrichids in the molecular phylogenies. The two clus-ters of Favella species in small subunit rRNA gene trees are supported by morphological features, justifying a separation at genusand family level. The genus Favella has a smooth lorica surface and a somatic ciliary pattern comprising a left and lateral ciliaryfield as well as two dorsal kineties and a monokinetidal ventral kinety abutting on the right ciliary field. The new genus Schmidin-gerella n. gen., established for the second Favella cluster, groups with Metacylis and Rhabdonella in the molecular trees. It differsfrom Favella in (i) a lorica wall with reticulate surface ridges and minute openings and (ii) a ventral kinety that is distinctly apartfrom the right ciliary field and composed of a monokinetidal anterior and a dikinetidal posterior portion. The genera Codonaria,Codonella, and Codonellopsis are affiliated with the family Dictyocystidae, whose diagnosis is improved to include the lorica sac.

Key Words. Lorica, morphology, new genus, phylogeny, revised classification, somatic ciliary pattern, strobilidiids, taxonomy,tintinnids.

T HE phylogenies of the small subunit ribosomal RNA(SSU rRNA) genes reveal a non-monophyly of the tintin-

nid genera Tintinnopsis Stein, 1867 and Favella Jorgensen,1924 and place the aloricate genus Lynnella Liu et al., 2011 atthe base of the choreotrichids (Gao et al. 2009; Kim S. Y.et al. 2010; Kim Y.-O. et al. 2010; Li et al. 2009; Liu et al.2011; Snoeyenbos-West et al. 2002; Struder-Kypke and Lynn2003, 2008). Specifically, the genus Favella shows great dis-crepancies between the current classification and the molecularphylogenies. Despite a supposedly well-defined lorica morphol-ogy, species of the genus Favella group in two separate clus-ters in the phylogenetic trees. The type genera of the familiesCodonellidae Kent, 1881; Codonellopsidae Kofoid and Camp-bell, 1929; and Dictyocystidae Haeckel, 1873 have loricae ofdifferent structures, being agglomerated in Codonella Haeckel,1873; entirely hyaline in some species of Dictyocysta Ehren-berg, 1854, and composed of hyaline collars and agglomeratedbowls in Codonellopsis Jorgensen, 1924 and some Dictyocystaspecies. Nevertheless, the gene trees indicate a close relation-ship of these latter three genera, as they consistently grouptogether in a well-supported branch.

By molecular analyses of five new SSU rRNA genesequences and cladistic analyses of 56 partially new or newlyinterpreted features of halteriids, oligotrichids, and choreotri-chids, we try to reconcile the morphologic and moleculartrees. The evolutionary hypothesis of the somatic ciliary pat-terns suggested by Agatha and Struder-Kypke (2007) for thechoreotrichid ciliates is revised based on new and recently rec-ognized patterns and included into our analyses as one of themain feature complexes.

MATERIALS AND METHODS

Data acquisition. The consideration of the halteriids andoligotrichids in the present cladistic analysis of the choreotri-chids allows not only the reconstruction of the last commonancestor, which entered the pelagial, but also the detection ofconvergences and adaptations to the planktonic life style.Besides the data already analysed by Agatha and Struder-Kypke (2007), recent findings from live and silver-impregnated

specimens and electron microscopic studies are included (Aga-tha 2008, 2010a, b, 2011; Agatha and Foissner 2009; Agathaand Tsai 2008; Foissner et al. 2007; Kim and Taniguchi 2007;Kim Y.-O. et al. 2008, 2010; Kim S. Y. et al. 2010; Liu et al.2009, 2011; McManus et al. 2010; Muller 2007; Tsai et al.2008, 2010; Xu et al. 2007, 2008, 2009; Zhang et al. 2010).

Favella panamensis Kofoid and Campbell, 1929 was collectedin the Indian River (Florida; FeFL10-9) and the ChesapeakeBay (FeMD10-52) as well as at the Atlantic coast of Maryland(FeMD10-46) in 2010. Favella arcuata (Brandt, 1906) Jorgen-sen, 1924 was collected at the Atlantic coast of Maryland in2009 (SaMD09) and 2010 (SaMD10); further protargol-impreg-nated material of both species was provided by Wayne Coats(Smithsonian Environmental Research Center, Maryland).Gene sequence analyses, live observations, protargol impregna-tions, and scanning electron microscopic studies were per-formed. The definitions of the terms epilorica, paralorica, andprotolorica follow Laval-Peuto and Brownlee (1986). The sti-chotrichs are chosen as outgroup as previous genetic genealo-gies invariably revealed a sister-group relationship with theoligotrichids sensu lato (s. l.), i.e., oligotrichids sensu stricto (s.str.) and choreotrichids (Agatha and Struder-Kypke 2007; Aga-tha et al. 2005; Gao et al. 2009; Kim et al. 2005; Kim S. Y.et al. 2010; Kim Y.-O. et al. 2010; Li et al. 2009; Liu et al.2011; Modeo et al. 2003; Snoeyenbos-West et al. 2002; Struder-Kypke and Lynn 2003, 2008; Zhang et al. 2010). The presenceof a perilemma corroborates these genetic findings and is usedby Berger (2008) as the main feature of a new taxon, the Peri-lemmaphora, that unites the stichotrichs, halteriids, and oligo-trichids s. l.

Concerning the position of the halteriids, the genetic andmorphologic data are inconsistent: the halteriids are locatedwithin the stichotrich outgroup and thus distinctly apart fromthe oligotrichids and choreotrichids in the molecular trees (Shinet al. 2000; Snoeyenbos-West et al. 2002; Weisse et al. 2008),whereas the morphology and pattern of cell division indicate asister-group relationship with a cluster formed by the oligotri-chids and choreotrichids (Agatha 2004b; Agatha and Foissner2009; Foissner et al. 2007; Petz and Foissner 1992).

Cladistic analyses. The phylogenetic relationships amongthe choreotrichids were elucidated by applying Hennig’s argu-mentation method (Table 1; Hennig 1966, 1982) as well as thecomputer programs PAUP* ver. 4.0b10 (Swofford 2002)and Hennig86 (Table 2). The computed parsimony treesused ordered states (Wagner/Farris optimization), except for

Corresponding Author: S. Agatha, Department of OrganismicBiology, University of Salzburg, Hellbrunnerstraße 34, A-5020Salzburg, Austria—Telephone number: + 43 650 310 6550; FAXnumber: + 43 662 8044 5698; e-mail: [email protected]

J. Eukaryot. Microbiol., 0(0), 2012 pp. 1–26© 2012 The Author(s)Journal of Eukaryotic Microbiology © 2012 International Society of ProtistologistsDOI: 10.1111/j.1550-7408.2012.00623.x

1

Published bythe International Society of ProtistologistsEukaryotic Microbiology

The Journal of

Characters 13, 14, 16, 17, 20, 28, 29, 31, 33, 34, 38, 48, and 53(Table 1). The Characters 8, 18, 26, and 41 were translatedinto character state trees by additive binary coding (Lipscomb1992; Table 2). Several characters were double-weighted toreceive a better resolution (see “Results”): the shape of theadoral zone of membranelles (Character 4), the cyrtos-likepharyngeal fibres (Character 11), the orientation of the oligo-trichid ventral kinety (Character 17), the pattern of the oligo-

trichid girdle kinety (Character 18), the somatic ciliarypatterns in tintinnids (Characters 20–25), the contractile pos-terior cell portion (Character 33), the lorica sac (Character39), and the mode of stomatogenesis (Character 41). The poly-morphic characters cell shape (Character 1), position of theadoral zone of membranelles (Character 3), number ofsomatic kineties (Character 14), nuclear apparatus (Character28), and polysaccharide cortical platelets (Character 35) were

Table 1. Character numbers, character states, and coding used for the construction of the traditional cladogram (Fig. 17). The coding ismainly based on the outgroup comparison with the stichotrichs. If not stated otherwise, the characters are additive (ordered; Wagner/Farrisoptimization).

No. Characters

Apomorphic state Plesiomorphic state

1 Cell shape globular to obconical (coded 1) Cell shape distinctly dorsoventrally flattened (coded 0)2 Usually planktonic (coded 1) Usually benthic (coded 0)3 Adoral zone of membranelles mainly apical (coded 1) Adoral zone of membranelles mainly ventral (coded 0)4 Adoral zone of membranelles circular (coded 1) or secondarily with

minute ventral gap (coded 2)Adoral zone of membranelles C-shaped (coded 0)

5 30–50% (coded 1) or 0% (coded 2) of adoral polykinetids composedof four rows of basal bodies

> 90% of adoral polykinetids composed of four rows of basalbodies (coded 0)

6 Postciliary and transverse microtubules absent in adoral membranelles(coded 1)

Postciliary and transverse microtubules present in adoralmembranelles (coded 0)

7 Collar polykinetids bipartite (coded 1) Collar polykinetids continuous (coded 0)8b Adoral zone bipartite in buccal membranelles with small polykinetids

and short cilia and collar membranelles with broad polykinetids andlong cilia (coded 1; coded 1000), buccal membranelles absent (coded 2;coded 1100), last collar membranelles proximally elongated (coded 3;coded 1010), last collar membranelles proximally and distallyelongated (coded 4; coded 1011)

Polykinetids and cilia of adoral membranelles graduallydecrease in size towards the cytostome (coded 0; coded 0000)

9 Undulating membrane(s) often diplostichomonad or polystichomonad(coded 1)

Undulating membrane(s) monostichomonad (coded 0)

10 Paroral membrane absent (coded 1), paroral and endoral membranesabsent (coded 2)

Usually endoral and paroral membranes present (coded 0)

11 Cyrtos-like pharyngeal fibres (coded 1) Common pharyngeal fibres (coded 0)12 Cirri absent (coded 1) Cirri present (coded 0)13a Somatic kinetids unciliated (coded 1) or with clavate cilia (coded 2) Somatic kinetids with rod-shaped or fusiform cilia (coded 0)14a One or two somatic kineties (coded 1), ten or more somatic kineties

(coded 2)3–9 somatic kineties (coded 0)

15 � 40% of unspecialized somatic kineties shortened or entirely reduced(coded 1)

Unspecialized somatic kineties extend from adoral zone ofmembranelles to posterior cell end (coded 0)

16a Some unspecialized somatic kineties distinctly curved (coded 1) orforming a posterior spiral (coded 2)

Unspecialized somatic kineties longitudinal (coded 0)

17a Oligotrichid ventral kinety erected (coded 1), usually indistinct or absent(coded 2)

Oligotrichid ventral kinety dextrally spiralled (coded 0)

18b Oligotrichid girdle kinety (coding follows hypothesis of Agatha 2011):dextrally spiralled with posterior end inversely orientated (coded 1;coded 100000000); horizontally orientated with oral primordiumposteriorly (coded 2; coded 010000000); sinistrally spiralled (coded 3;coded 011000000); horizontally orientated with dorsal gap (coded 4;coded 010100000); horizontally orientated with oral primordiumanteriorly (coded 5; coded 010010000); O-shaped with oralprimordium posteriorly (coded 6; coded 010001000); O-shaped withoral primordium anteriorly (coded 7; coded 000000100); in twoinverted U-shaped fragments (coded 8; coded 000000110); in severalmostly clockwise inclined fragments (coded 9; coded 000000101)

Oligotrichid girdle kinety dextrally spiralled (coded 0;coded 000000000)

19 Somatic kineties arranged in a right and left ciliary field (coded 1) Somatic kineties more or less equidistantly arranged (coded 0)20a Two ventral organelles (coded 1) or one specialized tintinnid ventral

kinety present (coded 2)Ventral organelles or specialized tintinnid ventral kinety absent(coded 0)

21 Tintinnid ventral kinety composed of a monokinetidal anterior anddikinetidal posterior portion (coded 1)

Tintinnid ventral kinety monokinetidal (coded 0)

22 Right ciliary field and tintinnid ventral kinety separated by a broadunciliated stripe (coded 1)

Right ciliary field abuts on tintinnid ventral kinety (coded 0)

23 Two specialized dorsal kineties (coded 1) or one dorsal kinety (coded 2) Specialized dorsal kineties absent (coded 0)24 Specialized posterior kinety present (coded 1) Specialized posterior kinety absent (coded 0)

(continued)

2 J. EUKARYOT. MICROBIOL., 0, NO. 0, APRIL 2012

Table 1. (continued)

No. Characters

Apomorphic state Plesiomorphic state

25 Lateral ciliary field present (coded 1) Lateral ciliary field absent (coded 0)26b Unspecialized somatic kineties: some dikinetids with cilia only at the

anterior basal bodies, other dikinetids with two cilia (coded 1; coded10000000); all dikinetids with two cilia (coded 2; coded 11000000);most dikinetids with cilia only at the posterior basal bodies, fewdikinetids with two cilia (coded 3; coded 11100000); all dikinetids withcilia only at the posterior basal bodies (coded 4; coded 11110000);some dikinetids with cilia only at the posterior basal bodies, someciliated monokinetids (coded 5; coded 11111000); ciliatedmonokinetids (coded 6; coded 11111100); mostly ciliatedmonokinetids, some dikinetids with two cilia, some dikinetids withcilia only at the posterior basal bodies (coded 7; coded 11100010);mostly ciliated monokinetids, some dikinetids with two cilia (coded 8;coded 11100011)

Unspecialized somatic kineties composed of dikinetids, eachwith a cilium only at the anterior basal body (coded 0;coded 00000000)

27 Somatic kinetids condensed (coded 1) Somatic kinetids distinctly separate (coded 0)28a One ellipsoidal macronucleus nodule (coded 1), one C-shaped

macronucleus (coded 2), or more than two macronucleus nodules(coded 3)

Two macronucleus nodules (coded 0)

29a Tintinnid extrusomes (capsules) and/or structures usually associatedwith tintinnid extrusomes (coded 1) or oligotrichid extrusomes(trichites; coded 2) present

Extrusomes absent (coded 0)

30 Stripe of extrusome attachment sites distinctly apart from theoligotrichid girdle kinety (coded 1)

Stripe of extrusome attachment sites directly anterior to theoligotrichid girdle kinety (coded 0)

31a Capsule Type I (coded 1) or Type II (coded 2) present Capsules absent (coded 0)32 Tintinnid mucocyst Type A present (coded 1) Mucocysts absent or different (coded 0)33a Contractility of peduncle (coded 1) or tail (coded 2) Posterior cell portion acontractile (coded 0)34a Anterior cell portion with contractile tentacles (coded 1) or tentaculoids

(coded 2)Anterior cell portion without cytoplasmic appendages (coded 0)

35 Polysaccharide cortical platelets present (coded 1) Cortical platelets absent (coded 0)36 Kinetal lips covering the bases of the somatic cilia present (coded 1) Kinetal lips covering the bases of the somatic cilia absent

(coded 0)37 Vesicular reticulum present (coded 1) Vesicular reticulum absent (coded o)38a Lorica: soft, agglomerated (coded 1); soft, agglomerated, and with

subterminal membrane (coded 2); hard, agglomerated (coded 3);posterior portion agglomerated, anterior hyaline (coded 4); entirelyhyaline (coded 5)

Lorica absent (coded 0)

39 Lorica sac and closing apparatus present (coded 1) Lorica sac and closing apparatus absent (coded 0)40 Enantiotropy (coded 1) Homeotropy (coded 0)41b Stomatogenesis hypoapokinetal in transient tube (coded 1; coded 100),

permanent tube (coded 2; coded 110), or transient pouch (coded 3;coded 101)

Stomatogenesis epiapokinetal (coded 0; coded 000)

42 Undulating membranes originate de novo (coded 1) Undulating membranes originate from oral primordium orcirral anlagen (coded 0)

43 Unspecialized somatic kineties originate de novo (coded 1) Unspecialized somatic kineties originate usually by intrakinetalproliferation of basal bodies (coded 0)

44 Reorganization of somatic kineties present (coded 1) Reorganization of somatic kineties absent (coded 0)45 Preformed emergence pore closed with a plug (coded 1) Preformed emergence pore and plug absent (coded 0)46 Ectocyst bipartite and granular (coded 1) Ectocyst comprises a single microfibrillar or membranous layer

(coded 0)47 Wall of resting cyst with inorganic layers (coded 1) Wall of resting cyst without inorganic layers (coded 0)48a Lepidosomes: with tubular fine structure (coded 1); with fibrous fine

structure and conical/spine-like shape (coded 2); with fibrous finestructure and globular shape (coded 3)

Lepidosomes absent (coded 0)

49 Cytoplasm of resting cyst with “curious structures” (coded 1) Cytoplasm of resting cyst without “curious structures” (coded 0)50 Cyst wall precursors of halteriid type (coded 1) Cyst wall precursors of stichotrich type (coded 0)51 Inner cyst membrane absent (coded 1) Inner cyst membrane present (coded 0)52 Pycnosis of vegetative macronucleus without fragmentation (coded 1) Pycnosis of vegetative macronucleus after fragmentation

(coded 0)53a Interlocking (coded 1) or oblique (coded 2) arrangement of conjugants Parallel arrangement of conjugants (coded 0)54 Transient dimorphism of conjugants (coded 1) Isomorphic conjugants (coded 0)55 Conjugants share membranelles (coded 1) Conjugants do not share membranelles (coded 0)56 Single derivative of first maturation division performs second division

(coded 1)All derivatives of first maturation division participate in seconddivision (coded 0)

aNonadditive (unordered) characters.bBinary coding of character state trees (first code for Hennigian argumentation scheme; second code for computer analyses).

AGATHA & STRUDER-KYPKE—EVOLUTION OF CHOREOTRICHIDS 3

Table

2.Distributionofcharacter

statesover

thetaxacladisticallyanalysedwiththecomputerprogramsPAUP*andHennig86(Fig.18).

Note

thatthecharacter

state

treesof

Character

8(bipartitionofadoralzoneofmem

branelles),Character

18(oligotrichid

girdle

kinety),

Character

26(structure

ofsomatickinetids),andCharacter

41(stomatogenesis)

wereconvertedinto

additivebinary

coding(Table

1).

Shades

ofgreymark

themost

commoncharacter

state

inapolymorphic

taxonandthepresumed

character

state

ofataxon

adoptedfrom

thestate

initsclosest

relatives.


considered, as they contribute important phylogenetic infor-mation and thus increase the accuracy of the analyses (Poeand Wiens 2000). Therefore, the “majority method” wasapplied, which codes a polymorphic taxon as having the traitthat is most common among the taxa considered (Wiens2000). Characters with unknown states in some taxa wereincluded into the analyses as such data also significantlyincrease the phylogenetic accuracy (Poe and Wiens 2000). Insome characters concerning ultrastructure, ontogenesis, restingcysts, and conjugation (Characters 9, 37, 40–45, 47, 48 and52–56), the scattered data were also assigned to the closestrelatives in the cladistic analyses.

With Hennig86, the most parsimonious tree was found by aheuristic analysis, and a strict consensus tree was calculated.Using the computer program PAUP*, the 50% majority-ruleconsensus tree was found by the heuristic analyses of 10,000trees optimized by the application of the accelerated transfor-mation (ACCTRAN). The bootstrap method with heuristicsearch included 10 replicates and used the establishment of thestarting tree/s by stepwise addition, a random addition of fur-ther taxa, and the tree-bisection-reconnection (TBR) branch-swapping algorithm. One tree was held at each step duringstepwise addition. The resulting tree was imported into Tree-View (Page 1996).

Molecular methods. One to thirty individually picked cellswere placed in a microcentrifuge tube. Cells were fixed in 80%ethanol or 180 ll of Animal Tissue Lysis (ATL) buffer wasadded to the cells. All samples were stored at � 20 °C untilDNA extraction was performed with the DNeasy Blood andTissue kit (Qiagen, Mississauga, Canada), following the manu-facturer’s protocol, with the exception that only 100 ll of elu-tion buffer was used. In general, 4–5 ll of the extracted DNAsample were amplified by PCR, following standard protocolsand using the SSU rDNA forward primer A (5′-AACCTGGTTGATCCTGCCAGT-3′) and the reverse primerB (5′-TGATCCTTCTGCAGGTTCACCTAC-3′; Medlin et al.1988). Finally, the amplified DNA was purified with theMinElute gel purification kit (Qiagen). The samples weresequenced in both directions with a 3730 DNA Analyser(Applied Biosystems Inc., Foster City, CA), using the ABIPRISM BigDye Terminator (ver. 3.1) and the Cycle Sequenc-ing Ready Reaction kit. Sequencing primers were the amplifi-cation primers and the internal primers 690F and 690R(Elwood et al. 1985).

Phylogenetic analyses. The sequences of F. panamensis andF. arcuata were imported into Sequencher ver. 4.0.5 (GeneCodes Corp., Ann Arbor, MI), trimmed at the ends, andassembled into contigs. The new SSU rRNA gene sequenceswere imported into MEGA ver. 4.0 (Tamura et al. 2007) andaligned to other tintinnid sequences available from the Gen-Bank database. The stichotrich species Laurentiella strenua,Oxytricha granulifera, Tetmemena pustulata, and Styxophryaquadricornuta, as well as the halteriids Halteria grandinella andMeseres corlissi, were used as outgroup in the phylogeneticanalyses. We excluded clonal and identical sequences from thefinal dataset, which comprised 69 species and 1,789 positions.Highly variable regions were not considered in the analyses.Four analyses were performed to construct a phylogenetictree: maximum likelihood (ML; PhyML; Guindon et al. 2010),Bayesian inference (BI; MrBayes; Ronquist and Huelsenbeck2003), maximum parsimony (MP; PAUP ver. 4.0b10; Swof-ford 2002), and neighbour joining (NJ; PHYLIP ver. 3.69;Felsenstein 2005). MODELTEST ver. 3.0 (Posada and Cran-dall 1998) was employed to find the model of DNA substitu-tion that best fits our data. The general-time-reversible (GTR)model for nucleotide substitution with gamma distributed sub-

Table2(con

inued)


stitution rates and invariable sites was determined as bestmodel. We included these parameters in PhyML and MrBa-yes. DNADIST was employed to calculate the genetic dis-tances with the Kimura 2-parameter model (Kimura 1980),and the distance trees were constructed with NEIGHBOUR

(NJ; Saitou and Nei 1987). The data were re-sampled 500(PhyML) and 1,000 (MP, NJ) times, respectively. The MPanalysis was performed, using 438 parsimony-informativecharacters and a random addition (n = 5) of the species withthe TBR branch-swapping algorithm in effect.

Fig. 1–7. Kinetal maps showing the early evolution of the choreotrichid somatic ciliary patterns (originals; protargol impregnation).1. Ancestor’s dorsal side with 3–9 longitudinal somatic kineties composed of dikinetids, each having a distinct cilium associated only with theanterior basal body. This pattern is still found in recent stichotrich and hypotrich ciliates (e.g. Fig. 4b in Berger 2011 and Fig. 54b in Petz et al.1995). 2. In a “dorsalization” process, the ancestor’s ventral side was reduced and the dorsal side extended across the whole posterior cell por-tion. The posterior dikinetidal basal bodies became ciliated, producing the pattern of Strombidinopsis and Leegaardiella sol (inferred from Fig. 1,13, 14 in Agatha et al. 2003 and Fig. 8D in Lynn and Montagnes 1988). 3. Hypothetical tintinnid ancestor with a right and left ciliary field.The anterior cilia of the dikinetids were reduced in the posterior kinety portions. 4. Lohmanniellidae Montagnes and Lynn, 1991. The anteriorcilia of all dikinetids were reduced. The pattern was inferred from the neotype material of Lohmanniella oviformis Leegaard, 1915 kindly pro-vided by D. H. Lynn (Dept. Zoology, Univ. British Columbia, Vancouver, Canada). 5. Strobilidiidae Kahl in Doflein and Reichenow, 1929.The unciliated anterior basal bodies of the dikinetids were lost, and the resulting monokinetids condensed (inferred from Fig. 19 in Foissneret al. 1988). 6. Parastrombidinopsis and Parastrombidium (inferred from Fig. 1 in Kim et al. 2005 and Fig. 1J in Xu et al. 2007). The genera dif-fer from Strombidinopsis in the secondarily slightly opened adoral zone of membranelles. 7. Lynnella. The anterior dikinetidal cilia were reducedin one kinety, while the second kinety apparently consists of ciliated monokinetids (inferred from Fig. 9, 10 in Liu et al. 2011). BM, buccalmembranelle; CM, collar membranelles; LF, left ciliary field; RF, right ciliary field; SK, somatic kineties.


RESULTS

Ancestor. The last common ancestor of the stichotrichs,halteriids, and oligotrichids s. l. was presumably characterizedby (i) a benthic life style, (ii) a dorsoventrally flattened cellshape, (iii) a C-shaped adoral zone of membranelles mainly

extending on the ventral side, (iv) 3–9 dorsal somatic kinetiescomposed of dikinetids, each having a distinct cilium associatedonly with the anterior basal body (Fig. 1; Agatha 2004a, b),(v) ventral cirri, (vi) an adoral zone composed of paramembran-elles with postciliary and transverse microtubules (Foissner andAl-Rasheid 2006; Grain 1972; Grim 1987; Lynn 2008), (vii)

Fig. 8–11. Kinetal maps showing the evolution of the somatic ciliary patterns in tintinnids with a ventral kinety (8, original; 9, modifiedfrom Fig. 4 in Snyder and Brownlee 1991; 10; modified from Fig. 3c in Choi et al. 1992; 11; modified from Fig. 13 in Kim S. Y. et al. 2010;protargol impregnation). 8. Hypothetical tintinnid ancestor. 9. Nolaclusilis. A ventral kinety was created and the dikinetids, except for the ante-riormost ones, transformed into monokinetids. 10. Eutintinnus. Dorsal kineties developed. 11. Favella ehrenbergii. A monokinetidal lateral ciliaryfield was introduced. BM, buccal membranelle; CM, collar membranelles; DK, dorsal kineties; LA, lateral ciliary field; LF, left ciliary field; OP,oral primordium; RF, right ciliary field; VK, ventral kinety.


monostichomonad endoral and paroral membranes (Agatha2004a), (viii) a perilemma (Berger 2008), (ix) a subepiplasmicmicrotubule basket (Faure-Fremiet and Ganier 1970; Fleuryet al. 1992; Foissner 2005; Grain 1972; Grim 1987; Laval 1972),(x) an intrakinetal proliferation of kinetids in the dorsal somatickineties, (xi) a ventral reorganization of the somatic ciliature(Agatha 2004a), (xii) an apokinetal development of the oral cil-iature (Agatha 2004a; Foissner 1996), (xiii) gene-sized frag-ments in the macronucleus (Riley and Katz 2001), (xiv) amacronuclear replication band, (xv) probably kinetosome-re-sorbing or partial-kinetosome-resorbing resting cysts (Foissner2005; Foissner et al. 2007; Gutierrez et al. 2003), and (xvi) aninner cyst membrane (Muller 2007).

Evolution of somatic ciliary patterns. The evolution of thesomatic ciliary pattern in the aloricate choreotrichids was pro-posed by Agatha and Struder-Kypke (2007), except for thegenera Lynnella and Parastrombidium Faure-Fremiet, 1924,which were only recently described (Liu et al. 2011) and rede-scribed (Xu et al. 2007), respectively.

The diciliated dikinetidal pattern found in StrombidinopsisKent, 1881 (Fig. 2) and Leegaardiella sol Lynn and Montag-nes, 1988 could have given rise not only to the pattern of thetintinnid ancestor (Fig. 3) and the pattern of LohmanniellaLeegaard, 1915 (Fig. 4), but also to the pattern of Para-strombidinopsis Kim et al., 2005 and Parastrombidium (Fig. 6;both genera with secondarily slightly opened adoral zone),

Fig. 12–13. Tintinnids with ventral kineties, lateral ciliary fields, and dorsal kineties (12, original; 13, modified from Fig. 46 in Agatha2010b; protargol impregnation). 12. Favella arcuata has an unciliated stripe between the right ciliary field and the ventral kinety, which is com-posed of a monokinetidal anterior and a dikinetidal posterior portion. 13. The most complex ciliary pattern comprising a posterior kinety. BM,buccal membranelle; CM, collar membranelles; DK, dorsal kinety; LA, lateral ciliary field; LF, left ciliary field; OP, oral primordium; PK, pos-terior kinety; RF, right ciliary field; VK, ventral kinety.


from which the Lynnella pattern (Fig. 7) evolved. The strobili-diid pattern (Fig. 5) with condensed monokinetids againdeveloped from the Lohmanniella pattern (Agatha and Stru-der-Kypke 2007).

Descending from the tintinnid ancestor with a right and leftciliary field and reduced anterior cilia in the posterior dikinet-ids (Fig. 8), Agatha and Struder-Kypke (2007) hypothesizedtwo evolutionary lineages based on the introduction of twoventral organelles and a ventral kinety (Fig. 9), respectively.The evolution in the majority of freshwater tintinnids with thetwo de novo-originating ventral organelles was described indetail by Agatha and Struder-Kypke (2007), while new dataon Favella ehrenbergii (Claparede and Lachmann, 1858)Jorgensen, 1924 provided by Kim S. Y. et al. (2010), F. pan-amensis (this study), and F. arcuata (this study) necessitate anupdate of the evolutionary hypothesis on tintinnids with aventral kinety. In these tintinnids, the dikinetids of the rightand left ciliary fields, except for the anteriormost ones, trans-formed into ciliated monokinetids, producing the pattern ofNolaclusilis Snyder and Brownlee, 1991 (Fig. 9). Next, twodorsal kineties evolved, creating the pattern of EutintinnusKofoid and Campbell, 1939 (Fig. 10). Subsequently, a lateralciliary field was introduced, generating the pattern of F. ehren-bergii (Fig. 11) and F. panamensis (Fig. 28, 29).

Then, one dorsal kinety was partially or completelyreduced. Small kinety fragments occurring in about one-fourthof the specimens in F. arcuata indicate that the left of the twodorsal kineties is usually completely reduced (Fig. 44; thisstudy). In the remaining tintinnids analysed, one dorsal kinetyis invariably lost (Agatha 2008, 2010b; Agatha and Riedel-Lorje 2006; Agatha and Tsai 2008; Cai et al. 2006; Foissnerand O’Donoghue 1990; Foissner and Wilbert 1979; Petz et al.1995; Wasik and Mikołajczyk 1994).

By the loss of one dorsal kinety, the pattern of Tintinnopsisbrasiliensis Kofoid and Campbell, 1929 was produced. Theventral kinety developed a dikinetidal posterior portion andseparated from the right ciliary field in F. arcuata (Fig. 12, 32,37–43; see below), while the most complex tintinnid ciliarypattern so far known was created by the introduction of aposterior kinety (Fig. 13). It occurs with minute deviations inCodonella and the remaining Tintinnopsis species with agglom-erated loricae, Codonellopsis and Stenosemella Jorgensen, 1924whose loricae are composed of agglomerated bowls and hya-

line collars, and Cymatocylis Laackmann, 1910 with hyalineloricae. Thus, this kinety pattern (Fig. 13) is associated withdifferent lorica structures. All these species are marine, withthe exception of the freshwater species Codonella cratera (Lei-dy, 1877) Imhof, 1885 and Stenosemella lacustris Foissner andO’Donoghue, 1990, whose generic affiliations are doubtful(Agatha 2010a; Agatha and Tsai 2008).

Morphological characters and character states. The cladisticinferences of the halteriids and oligotrichids s. l. are based on11 groups of characters: cell shape (Character 1), life style(Character 2), morphology of the oral apparatus (Characters3–11), somatic ciliature (Characters 12–27), nuclear apparatus(Character 28), special organelles and cell structures (Charac-ters 29–34), features of the cell cortex (Characters 35–37), fea-tures of the lorica (Characters 38 and 39), ontogeneticparticulars (Characters 40–44), the structure of the resting cyst(Characters 45–51), and particulars of conjugation (Characters52–56). The characters and their states are summarized inTable 1, and their distribution among the taxa is shown inTable 2. As Agatha and Struder-Kypke (2007), Foissner et al.(2007), and Agatha and Foissner (2009) already discussedmany of the characters analysed, only the new or newly codedfeatures for choreotrichid ciliates are described here.

Although the generic affiliation of the freshwater species C.cratera is questionable (Agatha 2010a), its features were sub-sumed under the genus Codonella in the present analyses.

Character 6. Fibrillar associates of adoral membranelles.In contrast to the stichotrichs, Halteria Dujardin, 1841, andthe aloricate choreotrichid Strobilidium Schewiakoff, 1892,the infraciliature of tintinnid polykinetids lacks postciliaryand transverse microtubules (Grain 1972; Grim 1987; Laval-Peuto and Brownlee 1986; Lynn 2008). Although data arenot available, the most parsimonious assumption is the pres-ence of postciliary and transverse microtubules in oligotri-chids s. str.; otherwise, the loss of these structures wouldhave happened twice independently: in the tintinnids and oli-gotrichids s. str.

Character 8. Bipartition of adoral zone of membranelles. Ingeneral, the polykinetids of the adoral membranelles graduallydecrease in width towards the cytostome in stichotrichs (Foiss-ner et al. 1991). In halteriids and oligotrichids s. l., smallerand shorter buccal membranelles can usually be distinguishedfrom larger and longer collar membranelles; in the oligotrichid

Fig. 14–16. Anterior cell portions of Codonellopsis schabi (14), Favella arcuata (15), and a marine Tintinnidium species (16) from life (origi-nals). Clavate or pin-shaped tentaculoids (arrowheads) insert between the collar membranelles. CM, collar membranelles; L, lorica. Scale bars10 lm (Fig. 14), 30 lm (Fig. 15), and 20 lm (Fig. 16).


Fig. 17. Monophyletic branch of the choreotrichid ciliates in the maximum parsimony tree of the Oligotrichea generated by the Hennigianargumentation method. For character coding, see Table 1 and section on character states. Black squares mark apomorphies. Asterisks denotehomoplasies. Semitintinnidium, subgenus Semitintinnidium Agatha and Struder-Kypke, 2007 of genus Tintinnidium with T. semiciliatum (Sterki,1879) Kent, 1881; Tintinnidium, subgenus Tintinnidium with T. fluviatile (Stein, 1863) Kent, 1881 and T. pusillum Entz, 1909.


Cyrtostrombidium Lynn and Gilron, 1993 and a few choreotri-chids, buccal membranelles are absent. Although the collarmembranelles are usually similar-sized in halteriids and oligo-trichids s. str., the polykinetids of the proximal-most mem-branelles are elongated, extending into the buccal cavity inchoreotrichids. In the aloricate choreotrichid Parastrombidium,also the outer ends of the proximal-most collar polykinetidsare elongated, terminating posteriorly to the polykinetids ofthe other collar membranelles on the ventral cell side (Xuet al. 2007).

Character 14. Number of somatic kineties. Assuming a“dorsalization” process, the ancestor of the halteriids and oli-gotrichids s. l. had probably few (dorsal) somatic kineties(Foissner et al. 2004), as 3–9 ciliary rows are usually found inthe hypotrichs (Curds and Wu 1983) and stichotrichs (Berger2006, 2008, 2011). In general, seven kineties occur in halteri-ids, four to six in aloricate choreotrichids, and one or two inoligotrichids s. str. (Agatha 2004a, 2011; Agatha and Struder-Kypke 2007). In Strombidinopsis, Parastrombidinopsis, Para-strombidium, and tintinnids, however, the somatic ciliatureusually comprises more than 10 kineties.

Character 21. Structure of tintinnid ventral kinety. The tin-tinnid ventral kineties are monokinetidal, except for those ofF. arcuata (Fig. 12, 37–43) and Favella sp. (Fig. 72 in Laval-Peuto 1994), which comprise a monokinetidal anterior and adikinetidal posterior portion (for details, see “Taxonomicimplications”).

Character 22. Unciliated ventral stripe. Usually, the distancebetween the ventral kinety and the right ciliary field is similarto that found between kineties of the right and left ciliaryfields; only in F. arcuata (Fig. 12, 32, 37, 39–42) and Favellasp. (Fig. 72 in Laval-Peuto 1994), both structures are sepa-rated by a conspicuous unciliated stripe. Possibly, this featureis connected with the extraordinary structure of the ventralkinety (Character 21).

Character 23. Dorsal differentiations. First, two usually di-kinetidal dorsal ciliary rows were generated, of which one waslater partially reduced in F. arcuata or completely reduced inCodonella, Codonellopsis, Cymatocylis, Stenosemella, and thoseTintinnopsis species with a ventral kinety.

Character 24. Posterior kinety. The introduction of a usu-ally dikinetidal kinety posterior to the left or lateral ciliaryfield is considered the derived state (Agatha and Struder-Ky-pke 2007). Based on the published data, the posterior kinetyevolved after the reduction of one dorsal kinety in tintinnidswith a monokinetidal ventral kinety close to the right ciliaryfield (Fig. 13, 17, 18). However, Brownlee (1982) described inhis unpublished PhD Thesis a Favella species that is similar toF. arcuata in having an extraordinary ventral kinety (Charac-ter 21) separated from the right ciliary field by an unciliatedstripe (Character 22), but possesses additionally a posteriorkinety. If these observations were correct, a posterior kinetywould have already been present in the ancestor of F. arcuata-like tintinnids (Fig. 12) and those with the most complex cili-

Fig. 18. The monophyletic branch of the choreotrichid ciliates in the maximum parsimony tree of the Oligotrichea computed with Hen-nig86. For character coding, see Table 2. The tree is the 50% majority-rule consent of 100 trees (Length = 164, Consistency index = 75, Reten-tion index = 93). Numbers on the branches are the bootstrap values (percentage out of 10 replicates) for the congruent internal nodes calculatedwith PAUP* ver. 4.0b10 (Swofford 2002). Black squares mark the main apomorphies.


ary pattern (Fig. 13), and F. arcuata would have later lost theposterior kinety. Further investigations are needed to properlydetermine where the posterior kinety appeared.

Character 31. Capsule types. Ultrastructural studies on tin-tinnids revealed five types of capsules (Laval-Peuto and Barrıade Cao 1987), which are assumed to be always associated withstriae, accessory combs, and/or tentaculoids. One or more ofthese organelles were found in Climacocylis Jorgensen, 1924(Type III), Codonaria Kofoid and Campbell, 1939, Codonella,Codonellopsis (Fig. 14), Dictyocysta, and Stenosemella (TypeII), Cyttarocylis Fol, 1881, Petalotricha Kent, 1881, Rhabdo-nella Brandt, 1906, and Xystonella Brandt, 1906 (Type IV),Cymatocylis (Wasik and Mikołajczyk 1992), Dadayiella Kof-oid and Campbell, 1929 (Entz 1884), Eutintinnus (Daday 1887;Entz 1909; Faure-Fremiet 1924; Schweyer 1909), F. arcuataand its relatives (see below; Fig. 15; Hedin 1975), Nolaclusilis(Sniezek et al. 1991; Snyder and Brownlee 1991), ParafavellaKofoid and Campbell, 1929 (Type III), Proplectella Kofoidand Campbell, 1929, and Undella Daday, 1887 (Type V),Ptychocylis Brandt, 1896 (Hedin 1976; Schweyer 1909), Tintin-nidium Kent, 1881 (Fig. 16; Entz 1885; Foissner and Wilbert1979; Hofker 1931), Tintinnopsis (Type I), and TintinnusSchrank, 1803 (Entz 1909; Schweyer 1909). In the species anal-ysed here, only Types I and II occasionally occur. Observa-tions concerning the presence of capsules, striae, accessorycombs, and tentaculoids are occasionally contradictory, possi-bly because their occurrence is correlated with food availabil-ity (Capriulo et al. 1986; Entz 1909).

Character 32. Mucocyst types. Laval-Peuto and Barrıa deCao (1987) found three types of mucocysts in tintinnid ciliates.The description of the mucocysts considered the size and theappearance in the transmission electron microscope, while theshape of the organelles was neither described nor illustrated.Type A is 1.5–2 9 0.5–0.75 lm in size, is very dense, and hasa slightly fibrous centre and a finely granulated periphery. Itoccurs in Codonaria, Codonella, Codonellopsis, Dictyocysta,and Stenosemella. Type B is 400–500 9 150–180 nm in size,ovoidal, and dense, except for an eccentric granule and theanterior portion, which distinctly projects towards the cellmembrane. It was found in Cyttarocylis, Petalotricha, Rhabdo-nella, and Xystonella. Type C is 200–500 nm in size, is slightlybilobed, and has a very dense, homogenous, paracrystallinestructure. It occurs in Proplectella and Undella. In the speciesanalysed here, only Type A is occasionally found.

Although the homology of the different types of tintinnidmucocysts and the cortical granules in some stichotrichs (Ber-ger 2006, 2008, 2011) is speculative, such organelles were notreported from halteriids and oligotrichids s. str. Likewise, thevast majority of aloricate choreotrichids do not possess muco-cysts: only six strobilidiids show argyrophilic granules ofunknown function (Agatha and Riedel-Lorje 1998; Agathaet al. 2005; Foissner et al. 1999; Krainer 1995; Kuppers et al.2006; Lynn and Montagnes 1988; Montagnes and Taylor1994). Therefore, the presence of a certain type of mucocystsis regarded as the apomorphic state occurring in sometintinnids.

Character 34. Cytoplasmic appendages at anterior cell por-tion. In the tontoniid Pseudotontonia cornuta (Leegaard, 1915)Agatha, 2004, contractile tentacles with plastids in their swol-len distal portions insert directly posteriorly to the collarmembranelles (Skovgaard and Legrand 2005). In tintinnids,potentially contractile cytoplasmic extensions, the tentaculoidscontaining capsules (Character 31), were found in marineCodonella species (Haeckel 1873; Schweyer 1909), Codonellop-sis schabi (Brandt, 1906) Kofoid and Campbell, 1929 (Fig. 14),Dictyocysta lepida Ehrenberg, 1854 (see pin-shaped structures

in Fig. 23 in Agatha 2010a), Eutintinnus species (Schweyer1909), F. arcuata (Fig. 15), Rhabdonella species (Schweyer1909), Stenosemella pacifica Kofoid and Campbell, 1929 (Aga-tha and Tsai 2008), marine Tintinnidium species (Fig. 16), andmarine Tintinnopsis species (Agatha 2010b; Haeckel 1873;Schweyer 1909), while they are at least temporarily absent insome other tintinnids, e.g. in F. ehrenbergii (not mentioned byKim S. Y. et al. 2010) and F. panamensis (Agatha S., pers.observ.). As the alternative is less parsimonious, the tentaclesand the tentaculoids are regarded as homoplasious apomor-phies.

Character 37. Vesicular reticulum. The cell cortex of Cyttar-ocylis brandti Kofoid and Campbell, 1929, Parafavella denticu-lata (Ehrenberg, 1840) Kofoid and Campbell, 1929, andPetalotricha ampulla (Fol, 1881) Kent, 1882 comprises a vesic-ular reticulum (i.e. cavities that communicate with each otherand the pericellular space underneath the perilemma; Laval1972; Laval-Peuto 1975; Sokolova and Gerassimova 1984; So-kolova et al. 1986). The vesicular reticulum was regarded as aspecial structure of tintinnids by Sokolova and Gerassimova(1984). It seems less likely that it represents a preparationartefact, as the vesicular reticulum was observed in speciesfrom three different families (i.e. Cyttarocylididae Kofoid andCampbell, 1929; Xystonellidae Kofoid and Campbell, 1929;Petalotrichidae Kofoid and Campbell, 1929) and after twokinds of preservation (i.e. glutaraldehyde in cacodylate bufferplus postfixation with osmium tetroxide or merely osmiumtetroxide in cacodylate buffer).

Character 39. Lorica sac and closing apparatus. A membra-nous closing apparatus shuts the lorica opening in disturbedtintinnids of six genera belonging to four families. Morpholog-ical and functional similarities indicate that the foldable clos-ing apparatus is a synapomorphy of the genera Codonaria,Codonella, Codonellopsis, and Dictyocysta (Agatha 2010a; seebelow). In Codonaria, Codonella, and Dictyocysta, the appara-tuses were found to merge posteriorly into membranous loricasacs. Probably, the diaphragm-like apparatuses in the generaSalpingacantha Kofoid and Campbell, 1929 and SalpingellaJorgensen, 1924 are not homologous to the foldable ones inthe genera mentioned above (Agatha 2010a).

As cell division, resting cysts, and conjugation were studiedin only a few genera, the data in Characters 40–45, 47, 48,and 52–56 are also applied to their closest relatives.

Character 45. Emergence pore and plug. The preformedemergence pore of resting cysts is closed by a plug in oligotri-chids s. str., the aloricate choreotrichids Rimostrombidium Jan-kowski, 1978 and Strombidinopsis spp. (Agatha S., pers.observ. of cysts kindly provided by A. Saage, University ofKiel, Germany; Ichinomiya et al. 2004), and tintinnids similarto F. arcuata (see below; Fenchel 1987; Margalef and Duran1953; McManus and Katz 2009; Meunier 1919; Reid and John1978; Van Breemen 1905). Cysts of hypotrichs, stichotrichs,and the halteriids Meseres Schewiakoff, 1892 and Halteria,however, lack a preformed emergence site; thus, the cyst is leftthrough rupture of the wall (Foissner et al. 2005, 2007). Theellipsoidal inclusions found in loricae of HelicostomellaJorgensen, 1924 (Laackmann 1908; Meunier 1919; Paranjape1980), Leprotintinnus Jørgensen, 1900 (Meunier 1910; Reidand John 1978), and Parundella Jorgensen, 1924 (Paranjape1980) are probably resting cysts that lack plugs. Globular rest-ing cysts apparently without plugs were found in Acantho-stomella Jorgensen, 1927 (Davis 1985), Coxliella Brandt, 1906(Laackmann 1908), Parafavella (Busch 1920; Reid and John1978), and marine Tintinnopsis species (Biernacka 1952; Meu-nier 1919). Claparede and Lachmann (1858) observed astalked structure, possibly a resting cyst, in loricae of Ampho-


rides amphora (Claparede and Lachmann, 1858) Strand, 1928(reported as Amphorella amphora). The cyst plug might repre-sent a synapomorphy of the oligotrichids and choreotrichidsthat has been lost in some tintinnids.

Character 51. Inner cyst membrane. In stichotrichs, the hal-teriid Meseres corlissi Petz and Foissner, 1992, and several dis-tantly related taxa (e.g. Nassula ornata and Didiniumnasutum), the ciliates emerging from the outer cyst wall arestill enclosed with a thin and flexible membrane that mightrepresent the endocyst (Muller 2007). In oligotrichids s. str.,however, such a membrane is apparently absent (Faure-Fremi-et 1948; Kim and Taniguchi 1995; Montagnes et al. 2002),while data on the excystment of choreotrichids are not avail-able. The presence of an inner cyst membrane might be inver-sely correlated with the presence of an emergence pore closedwith a plug (Character 45).

Morphology of Favella panamensis. In scanning electronmicrographs, the lorica is 170–260 lm long (�x = 222 lm;n = 80) and often has a spiralled or annulated epilorica 2.5–11 lm long (�x = 5.5 lm; n = 80; Fig. 23). The opening mea-sures 60–100 lm (�x = 81 lm; n = 104) in diameter. The pos-terior process is 20–90 lm long (�x = 57 lm; n = 80) and hasdextrally spiralled ribs (Fig. 23, 25, 26). The lorica wall ismonolaminar with alveoli and has a smooth surface (Fig. 21,23, 24). The paralorica has a spiralled structure and a broadlyrounded posterior end; a posterior process is absent (Fig. 27).The somatic ciliary pattern comprises a right, left, and lateralciliary field, as well as two dikinetidal dorsal kineties and amonokinetidal ventral kinety abutting on the right ciliary field(Fig. 22, 28, 29). The ciliary rows of the right and left ciliaryfields are composed of monokinetids and one anterior dikine-tid. The lateral ciliary field is composed of densely spacedmonokinetids. Tentaculoids, striae, and accessory combs werenot recognisable.

Morphology of Favella arcuata. In scanning electron micro-graphs, the lorica is 150–200 lm long (�x = 182 lm; n = 43)and has a ring-shaped subapical bulge and often a spiralled orannulated epilorica 3–10.5 lm long (�x = 6 lm; n = 37;Fig. 30, 31). The opening measures 55–75 lm (�x = 67 lm;n = 46) in diameter. The posterior process is 20–50 lm long(�x = 35 lm; n = 43) and lacks ribs (Fig. 31, 35). The loricawall is monolaminar with alveoli, pores, and occasionallysome subapical windows; its outer surface has reticulate ridges(Fig. 31–35). The paralorica has a spiralled structure and abroadly rounded posterior end; a posterior process is absent(Fig. 36). The somatic ciliature comprises a dikinetidal dorsalkinety occasionally plus some kinety fragments, a left and lat-eral ciliary field, and a right ciliary field separated by a con-spicuous unciliated stripe from the ventral kinety, which iscomposed of a monokinetidal anterior and a dikinetidal pos-terior portion (Fig. 12, 32, 37–45). The ciliary rows of theright and left ciliary fields are composed of monokinetids andone anterior dikinetid. The lateral ciliary field is composed ofdensely spaced monokinetids. Tentaculoids insert between thecollar membranelles on the peristomial rim (Fig. 15).

Cladistic analyses. In the cladogram based on the Hennigianargumentation method, the Leegaardiellidae Lynn and Mon-tagnes, 1988 are the most basal choreotrichid taxon followedby the cluster of Strombidinopsis, Parastrombidium, Para-strombidinopsis, and Lynnella and a cluster of the Lohmanniel-lidae and Strobilidiidae (Fig. 17). Although the tintinnids aremonophyletic mainly based on characters 19-1 and 38-1(Table 1), the suborder Strobilidiina comprising the aloricatechoreotrichids is paraphyletic. Here, we follow Mayr and Bock(2002) and Horandl and Stuessy (2010) in recognizing the para-phyletic suborder Strobilidiina. Within the tintinnids, those

with two ventral organelles and those having a ventral kinetyform distinct branches; the different structure and origin of theventral organelles and the ventral kinety indicate that they arenot homologous (dikinetidal and originating de novo vs. usu-ally monokinetidal and originating by intrakinetal proliferationof basal bodies and a subsequent split of the ciliary row; Petzand Foissner 1993; Fig. 44, 45). The structure of the cladogramroughly follows the evolution of somatic ciliary patterns withits increasing complexity in mostly marine tintinnids. Somebranches are not supported by apomorphies, possibly due tobudding processes (i.e. the parental branch continues essen-tially unchanged; Mayr and Bock 2002) or unknown derivedcharacters.

Of the 76 characters used in the Hennig86 and PAUP*computer analyses (Table 2), 61 were parsimony informative.The trees created by Hennig86 are shorter (L = 164) andhave lower consistency (Ci = 75) and retention indices(Ri = 93) than those established with PAUP* (L = 205,Ci = 80, Ri = 97), but the consensus tree (Fig. 18) has morepolytomies than that calculated by PAUP* (not shown).

In contrast to the Hennigian argumentation scheme(Fig. 17), the Leegaardiellidae do not form a monophylumbased on their bipartite collar membranelles in the computedtrees (Fig. 18). While the secondarily opened adoral zone ofmembranelles represents the synapomorphy of Lynnella, Para-strombidinopsis, and Parastrombidium in the Hennig86 andhand-made trees (Fig. 17, 18), Lynnella falls into a clusterformed by Lohmanniella and the Strobilidiidae (Pelagostrobili-dium Petz et al. 1995; Strobilidium; Rimostrombidium) in thePAUP* analysis.

A clear separation of tintinnids with two ventral organellesfrom those with a ventral kinety as revealed by the argumen-tation scheme (Fig. 17) is not recognizable in the consensustrees (Fig. 18). The synapomorphic character of the extrusometypes (Characters 31, 32) for Codonella, Codonellopsis, andStenosemella (excluding S. lacustris with doubtful generic affili-ation) is not shown by the PAUP* and Hennig86 analyses,while the introduction of a lorica sac (Character 39) in Codo-nella and Codonellopsis is at least recognizable in the hand-made and Hennig86 trees (Fig. 17, 18).

In all trees, the most highly derived tintinnids share themost complex ciliary pattern (Fig. 13) composed of a right,left, and lateral ciliary field as well as a ventral, dorsal, andposterior kinety. The genera Codonella, Codonellopsis, Cymat-ocylis, Stenosemella, and Tintinnopsis demonstrate this patternwith the exceptions of T. brasiliensis studied by Cai et al.(2006), whose pattern is similar to that of F. ehrenbergii, andT. cylindrata Kofoid and Campbell, 1929 studied by Foissnerand Wilbert (1979), which has a Tintinnidium pattern. Notethat the generic affiliation of C. cratera with the genus Codo-nella is questionable due to the lack of a lorica sac and closingapparatus (Agatha 2010a).

Without selective character weighting, the species of Lee-gaardiella Lynn and Montagnes, 1988 successively branch,Lynnella clusters with the Strobilidiidae, the tintinnids withtwo ventral organelles successively branch, and Codonella,Codonellopsis, Cymatocylis, Favella arcuata, Stenosemella, andthose Tintinnopsis species with a ventral kinety form an unre-solved cluster in Hennig86. As we believe that these cladesrepresent true natural lineages, we favour the use of selectiveweighting to demonstrate these relationships.

New sequences. The GenBank accession number, length,and GC content of the new SSU rRNA gene sequences are asfollows: Favella panamensis (FeFL10-9)—JQ837817, 1,758 nu-cleotides, GC 47.0%; F. panamensis (FeMD10-46)—JQ837818,1,748 nucleotides, GC 46.9%; F. panamensis (FeMD10-52)—


Fig. 19. Maximum likelihood tree inferred from SSU rRNA gene sequences, computed with PhyML (Guindon et al. 2010), based on thegeneral-time-reversible (GTR) model with gamma distribution and an estimate of invariable sites. The first numbers at the nodes represent thebootstrap supports (of 500 replicates) for PhyML (ML), whereas the second numbers represent posterior probability values of the Bayesiananalysis (BI), and the third and fourth numbers represent bootstrap values (of 1,000 replicates) for maximum parsimony (MP) and neighbourjoining (NJ), respectively. An asterisk represents full support in all analyses and dashes indicate bootstrap values of less than 20%. The scalebar represents 10 substitutions per 100 nucleotides. New sequences appear in boldface.


JQ837819, 1,729 nucleotides, GC 46.9%; Favella arcuata(SaMD09; Schmidingerella arcuata 2009)—JQ837815, 1,761nucleotides, GC 47.1%; F. arcuata (SaMD10; Schmidingerellaarcuata 2010)—JQ837816, 1,736 nucleotides, GC 47.0%.

Phylogenetic trees and signature nucleotides. All phyloge-netic analyses result in trees with comparable topologies(Fig. 19). As in previous analyses, the aloricate choreotrichidsare not monophyletic and are basal to the loricate tintinnids.Within the monophyletic tintinnids, the families TintinnidiidaeKofoid and Campbell, 1929 and Tintinnidae Claparede andLachmann, 1858 branch successively, followed by a well-sup-ported cluster of Favella species, which comprises the KoreanF. ehrenbergii sensu Kim S. Y. et al. (2010), F. campanulasequenced by Gao et al. (2009), F. panamensis analysed byStruder-Kypke and Lynn (2003), and F. panamensis from thepresent study (see below; Fig. 21–29). This group of Favellaspecies has a relatively long branch, indicating many nucleo-tide changes and a high mutation rate. Actually, many signa-ture positions exist that separate this cluster from the othertintinnid taxa (Fig. 20).

The topology of the remaining sequences, however, is muchless consistent and resolved, as most branches are not or onlyweakly supported, except for two groups: (i) a cluster of Codo-nella, Codonellopsis, Dictyocysta, and Stenosemella (94% ML,1.0 BI, 79% MP, 99% NJ), (ii) a branch comprising MetacylisJorgensen, 1924, Rhabdonella, and again Favella (with full sup-port), including F. ehrenbergii sensu Snoeyenbos-West et al.

(2002; LAK-2008; Fehr99ssu_1), F. taraikaensis Hada, 1932sequenced by Li et al. (2009), and F. arcuata from this study(see below; Fig. 30–45). The average genetic divergence betweenthe two Favella clusters is 6.88%. Within both groups, the inter-specific genetic divergence is relatively low (0.11–2.34%), andthe intraspecific divergence in F. arcuata and F. panamensis isvery low (0.06% and 0.0%, respectively). The sequences ofMetacylis sp. and M. angulata Lackey and Balech, 1966 analy-sed by Struder-Kypke and Lynn (2003) do not group together,but with Rhabdonella and Favella, respectively. Actually, sev-eral signature nucleotides support the division of the genusMetacylis (Fig. 20). The Rhabdonella species differ from Meta-cylis sp. in the presence of three signature nucleotides (Fig. 20).The analysis of further sequences is required to determine thelevel of sequence variation within those three genera and toresolve the generic assignment of the two Metacylis species.

Within the cluster of Codonella, Codonellopsis, Dictyocysta,and Stenosemella, the genetic divergences range between0.65% for Codonellopsis americana Kofoid and Campbell,1929 and C. nipponica Hada, 1964 and 2.55% for Stenosemellanivalis (Meunier, 1910) Kofoid and Campbell, 1929 and S.ventricosa (Claparede and Lachmann, 1858) Jorgensen, 1924.The four genera form two well-supported groups, each withsome signature nucleotides (Fig. 19, 20): one comprises Dicty-ocysta and Codonella (97% ML, 1.0 BI, 90% MP, 98% NJ),the other Codonellopsis and S. nivalis (with full support).Stenosemella ventricosa and Tintinnopsis fimbriata Meunier,

Fig. 20. Signature nucleotide positions of supported tintinnid clusters. (a) Families Rhabdonellidae Kofoid and Campbell, 1929 and Ptych-ocylididae Kofoid and Campbell, 1929. (b) Families Dictyocystidae and Rhabdonellidae and various Tintinnopsis species. Numbers above thenucleotides refer to the positions in the original alignment. Background in different grey tints defines the distinguishing nucleotides; in caseswhere several signature nucleotides are present at the same position, darker and lighter tints are used for differentiation. Shading does not relateto any evolutionary state. Horizontal lines separate the supported clusters of the phylogenetic tree. Dots represent missing data. Species abbrevi-ations: Cpsamer, Codonellopsis americana; Cpsnipp, Codonellopsis nipponica; Codapic, Codonella apicata; Dicreti, Dictyocysta reticulata;Fav_FNB, Favella sp. (FNB99; Struder-Kypke and Lynn 2008); Fav_LAK, Favella ehrenbergii (Fehr99ssu_1; Snoeyenbos-West et al. 2002);Favarcu, Favella arcuata (this study); Favcamp, Favella campanula (Gao et al. 2009); Favehre, Favella ehrenbergii (Kim S. Y. et al. 2010); Fav-pan2, Favella panamensis (FeMD10–46; this study); Favpana, Favella panamensis (Struder-Kypke and Lynn 2003); Favtara, Favella taraikaensis(Li et al. 2009); Met_MNB, Metacylis sp. (MNB99; Struder-Kypke and Lynn 2003); Metangu, Metacylis angulata (Struder-Kypke and Lynn2003); Rhabran, Rhabdonella brandti (MSK., unpubl. data); Rhahebe, Rhabdonella hebe; Steniva, Stenosemella nivalis; Stevent, Stenosemella ven-tricosa; Tpscyli, Tintinnopsis cylindrica; Tpsdada, Tintinnopsis dadayi; Tpslohm, Tintinnopsis lohmanni; Tpsradi, Tintinnopsis radix; Tpssuba, Tin-tinnopsis subacuta; Tpstoca, Tintinnopsis tocantinensis; Tpstubu, Tintinnopsis tubulosoides; Tpsurug, Tintinnopsis uruguayensis.


Fig. 21–27. Favella panamensis (originals; 21, 22, 24, 25, from life; 23, 26, 27, scanning electron micrographs). 21. Longitudinal optical sec-tion. 22. Anterior ventral cell portion. Kinety 2, the first row of the right ciliary field, abuts on the ventral kinety. 23. Lateral view of lorica. 24.Alveolar structure of lorica wall. 25, 26. Posterior lorica processes showing dextrally spiralled ribs. 27. Coxlielliform lorica. Note the smoothsurface of the whorls. K2, first kinety of right ciliary field; L, lorica; LA, lateral ciliary field; P, peduncle; VK, ventral kinety. Scale bars 100 lm(Fig. 21), 50 lm (Fig. 23, 27), 20 lm (Fig. 22, 25, 26), and 10 lm (Fig. 24).


1919 analysed by Struder-Kypke and Lynn (2003) branchbasally to these two groups.

DISCUSSION

Comparison of cladistic analysis with SSU rRNAphylogeny. The following comparison cannot be very detailed,as only seven genera have been analysed, using both morphol-ogy and gene sequences. In general, the morphologic andmolecular trees match rather well in showing (i) the non-monophyly of the aloricate choreotrichids, (ii) the monophylyof the tintinnids, and (iii) the early branching of Tintinnidiumfollowed by Eutintinnus, F. ehrenbergii sensu Kim S. Y. et al.(2010), and a diverse group of highly developed tintinnids. Inaddition, the character-based and gene-based trees reveal anonmonophyly of the genera Tintinnopsis and Favella and agrouping of the genera with a lorica sac and closing apparatus(Character 39; Gao et al. 2009; Kim S. Y. et al. 2010; Li et al.2009; Struder-Kypke and Lynn 2008).

Thus, there are morphologic features that support the twoFavella clusters, necessitating a split of the genus and the estab-lishment of a new one (see below). The interpretation of the lor-ica sac and its closing apparatus as synapomorphy ofCodonaria, Codonella, Codonellopsis, and Dictyocysta results ina far-reaching revision of the families Codonellidae, Codonel-lopsidae, and Dictyocystidae (see below). On the other hand, areasonable split of the genus Tintinnopsis cannot be performed,as the cell morphology of its type species, Tintinnopsis beroideaStein, 1867, is not known (Agatha and Riedel-Lorje 2006).

The main difference between the cladistic and genetic analy-ses is the position of the aloricate choreotrichid Lynnella. Thecladistic analyses based on Hennigian argumentation andHennig86 show a sister-group relationship between Strombi-dinopsis and a cluster formed by Parastrombidinopsis, Para-strombidium, and Lynnella. In the gene trees, however,Lynnella branches basally to all other choreotrichids. But, thisposition might change when the aloricate choreotrichids Leeg-aardiella, Lohmanniella, and Parastrombidium have beensequenced.

Taxonomic implications. Agatha (2010a) improved the diag-noses of Codonaria, Codonella, and Dictyocysta, noting thepresence of a lorica sac and its closing apparatus (Character39), which was regarded as synapomorphy of these genera.Although it is unknown whether the type species of Codonell-opsis possesses a lorica sac, closing apparatuses were found inat least two of its congeners. Furthermore, the genus is similarto the other three genera in the ultrastructure of the capsulesand mucocysts (Characters 31, 32) and its SSU rRNA genesequence (see “Results”; Kim Y.-O et al. 2010; Liu et al.2011). Struder-Kypke and Lynn (2008) already discussed thatthe families Codonellidae and Codonellopsidae are probablyinterrelated and in need of a revision. The combination of thefour genera in the oldest family, the Dictyocystidae Haeckel,1873, has far-reaching consequences (see below), as three ofthem are types of the families Codonellidae Kent, 1881, Codo-nellopsidae Kofoid and Campbell, 1929, and Dictyocystidae.Upon the transfers of the type genera, the families Codonelli-dae and Codonellopsidae are removed.

Fig. 28, 29. Favella panamensis (originals; protargol impregnation). Micrographs of several focal planes were stacked, using the computerprogram CombineZP from Alan Hadley. 28. Ventral view showing the monokinetidal ventral kinety abutting on the right ciliary field. 29. Dor-sal view showing two dorsal kineties. CM, collar membranelles; DK, dorsal kineties; L, lorica; LA, lateral ciliary field; LF, left ciliary field; MA,macronucleus; RF, right ciliary field; VK, ventral kinety. Scale bars 50 lm.


Accordingly, three genera lost their homes in the familyCodonellidae after the transfer of the type genus Codonellato the family Dictyocystidae: Codonopsis Kofoid and Camp-bell, 1939; Poroecus Cleve, 1902; and Tintinnopsis Stein,1867. No alternative family name exists for these taxa. Asmerely the lorica features of the type species are known,which have a low significance for a natural tintinnid classifi-cation (Agatha 2010a), no new family is established and thethree genera remain for the present as incertae sedis in thetintinnids.

After the transfer of the type genus Codonellopsis to thefamily Dictyocystidae, only two recent genera of the formerfamily Codonellopsidae are left: Stenosemella Jorgensen, 1924and Laackmanniella Kofoid and Campbell, 1929. The diagnosisof Stenosemella was recently improved by Agatha and Tsai(2008). It is the type genus of the Stenosemellinae establishedby Campbell (1954), as inferred from the subfamily’s stem(International Commission on Zoological Nomenclature[ICZN] 1999; Article 11.7). The subfamily is raised to familyrank here, becoming the Stenosemellidae Campbell, 1954 nov.

Fig. 30–35. Schmidingerella arcuata n. gen., n. comb. (originals; 30, 33, from life; 31, 32, 34, 35, scanning electron micrographs). 30, 31.Longitudinal optical section and lateral view of loricae. Arrowheads mark subapical bulge. 32. Anterior ventral cell portion of a middle dividershowing an unciliated stripe (arrowhead) separating the right ciliary field and the ventral kinety (cf. Fig. 37, 39–42). 33. Two kinds of reticula-tion are recognizable in the lorica wall: one caused by the small alveoli in the wall, the other caused by the ridges on the outer surface. 34. Outerlorica surface showing reticulate ridges and pores. 35. Posterior lorica process showing a reticulate surface. L, lorica; LA, lateral ciliary field;OP, oral primordium; P, peduncle; RF, right ciliary field; VK, ventral kinety. Scale bars 100 lm (Fig. 30), 50 lm (Fig. 31), 20 lm (Fig. 33),10 lm (Fig. 32, 35), and 5 lm (Fig. 34).


stat. It contains the single recent genus Stenosemella, while theaffiliation of the many fossil genera of the family Codonel-lopsidae mentioned by Lynn (2008) is questionable. Laack-manniella neither matches the diagnoses of theStenosemellidae nor Dictyocystidae (see below), as it has along lorica collar and a lorica sac is unknown. However, thegenus is placed incertae sedis in the Dictyocystidae due to thesimilarity in lorica morphology to Codonellopsis.

The genus Wangiella Nie, 1934 remains affiliated with theDictyocystidae, but as incertae sedis because it is unknown

whether its inner collar with flaps corresponds to a closingapparatus (Nie 1934).

Family Dictyocystidae Haeckel, 1873.1873 Dictyocystida—Haeckel, Jen. Z. Med. Naturwiss., 7 (year1871):562.1881 Codonellidae, Kent, A Manual of the Infusoria:615 (proparte).1929 Codonellopsidae Kofoid and Campbell, Univ. Calif. Publ.Zool., 34:67 (pro parte).

Fig. 36–41. Schmidingerella arcuata n. gen., n. comb. (originals; 36, scanning electron micrograph; 37–41, micrographs of protargol-impreg-nated cells at several focal planes stacked by the computer program CombineZP (Alan Hadley). 36. Coxlielliform lorica with reticulate ridgeson the surface of the whorls. 37, 39–41. Ventral (37, 40, 41) and ventrolateral (39) views of early dividers showing the genus-specific features,viz., the unciliated stripe (arrowheads) between the ventral kinety and the right ciliary field and the dikinetidal posterior portion of the ventralkinety. The dikinetids have cilia about 10 lm long only at each posterior basal body. 38. Dorsal view showing the dorsal kinety. CM, collarmembranelles; DK, dorsal kinety; LA, lateral ciliary field; LF, left ciliary field; MA, macronucleus nodules; OP, oral primordium; RF, right cili-ary field; VK, ventral kinety. Scale bars 50 lm.


Fig. 42–45. Schmidingerella arcuata n. gen., n. comb. (originals; after protargol impregnation). 42, 43. Ventral and dorsal views of samemorphostatic specimen. The ventral kinety is separated by an unciliated stripe (arrowhead) from the right ciliary field and composed of a mono-kinetidal anterior and a dikinetidal posterior portion. 44, 45. Ventrolateral and dorsolateral views of same late divider. The ventral kinety isbetween an unciliated stripe (arrow) and the oral primordium and shows a single split. Thus, the dikinetidal posterior portion does not representa posterior kinety abutting on a monokinetidal ventral kinety as otherwise one split each in the monokinetidal and the dikinetidal portionswould be recognizable. The arrowhead marks a fragment of a possibly strongly reduced second dorsal kinety, which occurs in about one-fourthof the specimens investigated. BM, buccal membranelle; CM, collar membranelles; DK, dorsal kinety; LA, (proter’s) lateral ciliary field; LA′,opisthe’s lateral ciliary field; LF, (proter’s) left ciliary field; LF′, opisthe’s left ciliary field; MA, macronucleus nodules; OP, oral primordium;RF, (proter’s) right ciliary field; RF′, opisthe’s right ciliary field; VK, (proter’s) ventral kinety; VK′, opisthe’s ventral kinety. Scale bars 50 lm(Fig. 42, 43) and 100 lm (44, 45).


Improved diagnosis. Lorica hard, agglomerated, hyaline, orcomposed of an agglomerated bowl and hyaline collar. Withlorica sac (i.e. a membranous envelope that lines the loricabowl and merges anteriorly into a foldable closingapparatus).

Type genus. Dictyocysta Ehrenberg, 1854.Remarks. The most complex somatic ciliary pattern is not

included into the family diagnosis, as it was found in Codo-nellopsis glacialis (Laackmann, 1907) Kofoid and Campbell,1929 by Petz et al. (1995), while the pattern is unknown in thetype genus Dictyocysta.

Family Stenosemellidae Campbell, 1954 nov. stat.Diagnosis. Lorica hard, composed of an agglomerated bowl

and a small hyaline collar. Somatic ciliature comprises a ven-tral, dorsal, and posterior kinety as well as a lateral, right,and left ciliary field.

Type genus. Stenosemella Jorgensen, 1924.In our SSU rRNA gene trees, the genus Favella is not

monophyletic and a similar topology is found in our clado-grams. Hence, the question arises—which of the two branchesrepresents the “true” genus Favella Jorgensen, 1924? Toanswer this question, the history of the type species is recon-structed.

Jorgensen (1924) established the genus, ambiguously sug-gesting F. serrata (Mobius, 1887) Jorgensen, 1924 as type spe-cies (“may be considered the type species”; p. 25), which doesnot represent a valid designation (International Commissionon Zoological Nomenclature [ICZN] 1999; Article 67.5). Ko-foid and Campbell (1929) selected F. ehrenbergii (Claparedeand Lachmann, 1858) Jorgensen, 1924, the oldest originallyincluded species of the genus (International Commission onZoological Nomenclature [ICZN] 1999; Article 67.2).

According to the short original description of the type speciesby Claparede and Lachmann (1858), the lorica wall has smallalveoli, producing a fine granulation at 300X magnification.The first redescription of specimens from the type locality, thecoastal waters of Norway, was performed by Jørgensen (1900).As he did not provide illustrations, the description by Brandt(1906, 1907) again of Norwegian loricae is regarded as authori-tative. These loricae were characterized by a monolaminar wallwith alveoli (primary structure; Brandt 1907). The outer loricasurface was more or less smooth and the posterior process waslarge and solid (i.e. lacked a central canal) and had three dis-tinct ribs.

Recently, Kim S. Y. et al. (2010) redescribed F. ehrenbergiifrom Korean coastal waters. These authors investigated forthe first time the somatic ciliary pattern, but did not mentionthe lorica ultrastructure (texture) and omitted to discuss thespecies identification in detail. Favella panamensis collected byus in the North Atlantic matches the Korean specimens in theciliary pattern (cf. Fig. 22, 28, 29 with Fig. 11) and both havea genetic similarity of 99.89%. As they are thus at least cong-eners, we transfer our observations of the monolaminar loricawall and the posterior process to the Korean specimens. Ourfindings agree with the original and authoritative loricadescriptions (Fig. 21, 23–26; Brandt 1906, 1907; Claparedeand Lachmann 1858). Since the Korean and Norwegianspecimens also have similar lorica dimensions (length: 94–330 lm vs. 230–290 lm; opening diameter: 88–94 lm vs. 83–104 lm; Brandt 1906, 1907), the identification by Kim S. Y.et al. (2010) seems to be correct. Their redescription of thetype species F. ehrenbergii and the SSU rRNA gene sequenceprovided are thus regarded as authoritative. Accordingly, thediagnosis of the genus Favella is improved by including thedescriptions by Brandt (1906, 1907) and Kim S. Y. et al.(2010) as well as our own data from F. panamensis (Fig. 21–

29). For the morphologically and genetically deviating Favellaspecies clustering with Metacylis and Rhabdonella, a newgenus is established (see below).

The authoritative SSU rRNA gene sequence of F. ehrenber-gii (Kim S. Y. et al. 2010) diverges by 0.11% from that of F.panamensis identified and analysed by Struder-Kypke andLynn (2003) and in this study. This deviation corresponds totwo nucleotide differences, which may result from (i) errorsduring the amplification or sequencing process, (ii) a variationin one of the internal primers, (iii) the geographical distance,as in Meseres corlissi (Weisse et al. 2008), or (iv) the occur-rence of different species, as in Stylonychia lemnae and S. my-tilus (Schmidt et al. 2006). In contrast to Kim S. Y. et al.(2010), we refrain from a synonymization of F. panamensiswith F. ehrenbergii as the reason for the genetic deviation isunknown. A detailed morphologic study of F. panamensis hasto show whether there are differences that might support thegenetic distance. Perhaps, some minute morphologic devia-tions might support the genetic distance. Compared with othertintinnids, F. panamensis apparently has a variable loricaopening diameter, ranging from 63–103 lm in the specimensstudied in the scanning electron microscope (Agatha S., pers.observ.). However, the opening tends to collapse in preparations,impeding correct measurements.

Laval-Peuto (1977, 1981) studied the lorica variability dur-ing the cell cycle in a Favella species and discovered a hugephenotypic plasticity. While the generic affiliation seems to becorrect due to the apparently smooth lorica surface (Fig. 29 inLaval-Peuto 1981), the identification with F. ehrenbergii isquestionable as the posterior process is more slender andapparently lacks ribs (Fig. 2, 11, 30–32 in Laval-Peuto 1981).The population produced not only typical Favella loricae, butalso loricae that were identified with Coxliella annulata (Da-day, 1887) Brandt, 1907 and Coxliella decipiens Jorgensen,1924. Likewise, Kim S. Y. et al. (2010) found Coxliella loricaein their monoclonal cultures, but omitted to identify them(lorica length: 60–231 lm; opening diameter: 80–90 lm;~0.84–1.07 whorls per 10 lm of length, as estimated from themicrographs provided). Probably, they are conspecific withCoxliella multispiralis Strelkow, 1953 (lorica length: 133–265 lm; opening diameter: 77–82 lm; ~0.87–1.23 whorls per10 lm of length, as estimated from illustrations and measure-ments provided by Strelkow 1953). The four Coxliella loricaefound in scanning electron micrographs of our samples fromthe Chesapeake Bay and the Atlantic coast of Maryland wereidentical to the co-occurring F. panamensis in the monolami-nar lorica wall and the smooth outer surface (cf. Fig. 27 withFig. 23); however, the opening diameter could be measuredonly in a single specimen, as the loricae usually collapsed.Hence, identification was impossible. Several further Coxliellaspecies will probably be affiliated in the future.

Favella adriatica (Imhof, 1886) Jorgensen, 1924; Favellacampanula (Schmidt, 1901) Jorgensen, 1924; Favella elongataRoxas, 1941; Favella markusovszkyi (Daday, 1887) Jorgensen,1924; Favella philippinensis Roxas, 1941; and Favella septentri-onalis Campbell, 1942 probably belong to the genus Favelladue to the structure of their lorica walls. The affiliation of F.campanula is supported by its SSU rRNA gene sequence(Fig. 19; Gao et al. 2009). The assignment of Favella amoyen-sis Wang and Nie, 1932; Favella gracilicauda Strelkow, 1953;and Favella hainanensis Nie and Ch’eng, 1947 is, however,uncertain. Favella panamensis illustrated by Small and Lynn(1985) and Lynn and Small (2002) apparently differs from ourspecimens in the presence of a posterior kinety and thus mightrepresent a further distinct genus. According to unpublishedscanning electron micrographs, these specimens have a smooth


outer lorica surface, but a larger opening diameter than thetype population [86–123 lm vs. 68–80 lm; Kofoid and Camp-bell 1929; Brownlee’s (1977) unpublished Master Thesis].

The tintinnid genus Favella Jorgensen, 1924 has a juniorhomonym, the ostracod genus Favella Coryell and Fields,1937, which thus got the replacement name Puriana by Coryelland Fields in Puri (1953). Several ostracod species were affili-ated with that genus: Favella pijpersi Van den Bold, 1946;Favella puella Coryell and Fields, 1937; Favella rugipunctata(Ulrich and Bassler, 1904) Edwards, 1944; and Favella mesa-costalis Edwards, 1944.

Genus Favella Jorgensen, 1924.1906 Untergattung Coxliella—Brandt, Ergebn. Plankton-Ex-ped. Humboldt-Stiftung, 3 La:7 (pro parte).1907 Untergattung Coxliella n.—Brandt, Ergebn. Plankton-Exped. Humboldt-Stiftung, 3 La:259 (pro parte).1924 Favella n. gen.—Jorgensen, Mediterranean Tintinni-dae:25.1929 Favella Jorgensen emended—Kofoid and Campbell,Univ. Calif. Publ. Zool., 34:147.1939 Favella Jorgensen emended Kofoid and Campbell—Kof-oid and Campbell, Bull. Mus. Comp. Zool., 84:122.1968 Favella Jorgensen, 1924—Loeblich and Tappan, J. Proto-zool., 15:187.2001 Favella Jorgensen 1924—Aescht, Denisia, 1:72.

Non Favella Coryell and Fields, 1937, Amer. Mus. Nat.Hist., Novitates, 956:8 (now ostracod genus Puriana Coryelland Fields, 1953).

Improved diagnosis. Ptychocylididae with two types of cam-panulate or cylindroidal loricae with smooth or irregular open-ing rims and broadly rounded to obconical posterior portions:(i) protolorica often with spiralled or annulated epilorica, pos-terior portion usually with a process; (ii) paralorica coxlielli-form, posterior portion with or without process. Lorica wallmonolaminar with alveoli; outer surface smooth. Adoral zoneof membranelles horizontally orientated in contracted speci-mens. Somatic ciliature comprises two dorsal kineties occasion-ally plus some kinety fragments, a monokinetidal ventral kinetyas well as a lateral, right, and left ciliary field.

Type species. Tintinnus ehrenbergii Claparede and Lach-mann, 1858.

In SSU rRNA gene trees, F. ehrenbergii (LAK-2008;Fehr99ssu_1) sensu Snoeyenbos-West et al. (2002), F. tarai-kaensis, Favella sp. (McManus and Katz 2009), and F. arcu-ata from this study form a cluster with Metacylis andRhabdonella distinctly apart from the Favella species men-tioned above (Gao et al. 2009; Kim S. Y. et al. 2010; Liet al. 2009; McManus and Katz 2009; Struder-Kypke andLynn 2003, 2008). Differences in the somatic ciliary pattern(cf. Fig. 12, 32, 37–43 in this study and Fig. 72 in Laval-Pe-uto 1994 with Fig. 11, 22, 28, 29 in this study and Fig. 15,16 in Kim S. Y. et al. 2010) and lorica ultrastructure (cf.Fig. 30–35 with Fig. 23–26) support the separation of F.arcuata from the “true” Favella cluster (see above). Thesemorphologic and genetic discrepancies justify the establish-ment of a new genus with Favella arcuata (Brandt, 1906)Jorgensen, 1924 as type, becoming Schmidingerella arcuata(Brandt, 1906) n. gen., n. comb.

At first glance, it seems that a dikinetidal posterior kinetyabuts on the posterior end of the monokinetidal ventral kinetyin S. arcuata (Fig. 12, 37–43) and Favella sp. (Fig. 72 in La-val-Peuto 1994). During ontogenesis, individual divisions ofthe monokinetidal and dikinetidal ciliary rows associated withsubstantial migration processes are thus expected. However,

only a single break occurs (Fig. 44, 45; Fig. 72 in Laval-Peuto1994), indicating a single kinety with a monokinetidal anteriorand dikinetidal posterior portion. This assumption is sup-ported by unpublished observations of Brownlee (1982) on aFavella species, showing besides such an extraordinary ventralkinety a dikinetidal posterior kinety. Furthermore, the posi-tion of this ciliary row right of the oral primordium is typicalof a ventral kinety, while posterior kineties extend on the leftof the oral primordia.

Schmidingerella n. gen. matches the characterization of thefamily Rhabdonellidae Kofoid and Campbell, 1929 given byLynn (2008), especially, in the ultrastructure of the lorica wall(i.e. alveoli enclosed by an inner and outer layer, low surfaceridges, and pores). The surface ridges probably cause the whit-ish appearance of S. arcuata in the light microscope at lowmagnification, and these are not visible in F. panamensis withits smooth lorica surface (cf. Fig. 30, 31, 34 with Fig. 21, 23,26). The affiliation of Schmidingerella with the Rhabdonellidaeis not only supported by ultrastructural studies on Rhabdonel-la spiralis (Fol, 1881) Brandt, 1906 (Agatha S., unpubl.observ.), but also by the rather close relationship of the twogenera in the SSU rRNA phylogenies (Fig. 19; Gao et al.2009; Kim S. Y. et al. 2010; Li et al. 2009; Struder-Kypke andLynn 2003, 2008) and the shared signature nucleotides(Fig. 20). Metacylis angulata falls into the same cluster. Thespecimens sequenced by Struder-Kypke and Lynn (2003) werecollected from Buzzards Bay, Massachusetts, which is ratherclose to the type locality of Great South Bay, Long Island,New York, at the east coast of the USA. The lorica wall ofM. angulata is composed of alveoli and has “many small,irregular, and very faint fenestrae” and several “small roundedelevations or plicae” in the anterior portion of the bowl(Lackey and Balech 1966). Hence, the clustering of M. angula-ta with Rhabdonella and Schmidingerella is supported by thelorica ultrastructure; cell features cannot be compared as theyare unknown in the former two genera.

Obconical loricae with and without a spiralled wall structurewere found in live samples and in scanning electron micrographsfrom material collected at the east coast of the USA (Fig. 36).As they match S. arcuata in the wall structure (i.e. the reticulatesurface and pores), they probably belong to its cell cycle.

Genus Schmidingerella nov. gen.Diagnosis. Rhabdonellidae with two types of campanulate,

cylindroidal, or obconical loricae with broadly rounded to ob-conical posterior portions: (i) protolorica often with some api-cal spirals or annuli (possibly an epilorica) and a subapicalbulge, opening rim smooth or denticulate, posterior portionusually with a process, (ii) paralorica coxlielliform, openingrim smooth or irregular. Lorica wall monolaminar with alve-oli, pores, and occasionally some subapical windows; outersurface with ridges. Adoral zone of membranelles horizontallyorientated in contracted specimens. Somatic ciliature com-prises a dorsal kinety occasionally plus some kinety fragments,a left and lateral ciliary field, and a right ciliary field separatedby a conspicuous unciliated stripe from the ventral kinetycomposed of a monokinetidal anterior and a dikinetidal pos-terior portion.

Type species. Cyttarocylis arcuata Brandt, 1906.Etymology. The genus is dedicated to Prof. Dr. Heinrich

Schmidinger, Rector of the University of Salzburg, Austria,who greatly supports protozoological research. Feminine gen-der due to the Latin suffix -ella.

Remarks. Very likely, several Favella species are congenersof Schmidingerella arcuata due to ridges on the lorica surfaceand/or a similar somatic ciliary pattern and SSU rRNA genesequence: Schmidingerella mexicana (Osorio-Tafall, 1941) n.


comb. (basionym: Favella mexicana); Schmidingerella meunieri(Kofoid and Campbell, 1929) n. comb. (basionym: Favella me-unieri; Meunier 1919); Schmidingerella quequenensis (Balech,1945) n. comb. (basionym: Favella quequenense); Schmidinge-rella serrata (Mobius, 1887) n. comb. (basionym: Tintinnusserratus; Balech 1959; Brandt 1906, 1907); Schmidingerellataraikaensis (Hada, 1932) n. comb. (basionym: Favellataraikaensis; Hada 1932; Li et al. 2009); Favella sp. (Fig. 72 inLaval-Peuto 1994; McManus and Katz 2009); and Favellaehrenbergii sensu Hedin (1975) and Snoeyenbos-West et al.(2002).

The specimens sequenced by Li et al. (2009) and identifiedwith F. taraikaensis have a genetic dissimilarity of 0.17% withS. arcuata. As morphologic data are lacking for the Chineseciliates, the correctness of the determination cannot be verifiedand we thus refrain from a synonymization of S. taraikaensiswith S. arcuata at the present state of knowledge. As in F.ehrenbergii (see above), the similarity of the gene sequencesincreases with the proximity of the sampling sites: thesequences of the specimens collected in this study at differentsites along the coast of Maryland (USA) and in different yearsare more similar to each other (i.e. 0.058% genetic divergence)than to the SSU rRNA gene sequences of the Chinese speci-mens (i.e. 0.171–0.173% genetic divergence).

The subapical lorica bulge found in S. arcuata is shared by S.taraikaensis (Hada 1932; Li et al. 2009) and Favella ehrenbergiisensu Fenchel (1987) and sensu Snoeyenbos-West et al. (2002).Favella sp. sequenced by McManus and Katz (2009) forms curi-ous campanulate resting cysts with an emergence pore and plug.Such cysts also occur in S. meunieri (Meunier 1919), S. serrata(Margalef and Duran 1953; Reid and John 1978; Van Breemen1905), and F. ehrenbergii sensu Fenchel (1987).

Our assignment of species to the revised genus Favella andthe new genus Schmidingerella leaves the following Favellaspecies as insufficiently known and thus without proper affilia-tion: Favella attingata Kofoid and Campbell, 1929; Favellaazorica (Cleve, 1900) Jorgensen, 1924; Favella brevis Kofoidand Campbell, 1929; Favella composita Jorgensen, 1924;Favella confessa Kofoid and Campbell, 1929; Favella cylindricaWang, 1936; Favella ecaudata Strelkow, 1953; Favella fistuli-cauda Jorgensen, 1924; Favella franciscana Kofoid and Camp-bell, 1929; Favella gilmartinniana Rodriguez de Tazan, 1966;Favella helgolandica (Brandt, 1906) Jorgensen, 1924; Favellainfundibulum Kofoid and Campbell, 1929; Favella jorgensisAthanassopoulos, 1930; Favella shintsuenensis Nie and Ch’eng,1947; Favella simplex Roxas, 1941; Favella thori Kofoid andCampbell, 1939; Favella truncata Athanassopoulos, 1930; andFavella undulata Wang and Nie, 1932. In the BIOSIS data-bank, several new Favella species are attributed to Stepanowa(1937): Favella conica, Favella grandis, Favella edentatiformis,Favella orientalis, and Favella pulchella. However, they wereestablished merely as variations of F. denticulata (reported asF. dentata, which is probably an incorrect spelling).

ACKNOWLEDGMENTS

The cladistic analyses and the taxonomic work of SAwere supported by the Austrian Science Fund (FWF; Pro-ject P20461-B17). The molecular work of MSK was finan-cially supported by a Discovery Grant of the NationalScience and Engineering Research Council (NSERC)awarded to Denis H. Lynn. Collection and processing ofthe samples were made possible through the hospitality ofWayne Coats (Smithsonian Environmental Research Center,Maryland, USA). Thanks go also to Andrea Saage for pro-viding resting cysts of Rimostrombidium. The technical assis-

tance of Johannes Rattey, University of Salzburg, is greatlyacknowledged.

LITERATURE CITED

Aescht, E. 2001. Catalogue of the generic names of ciliates (Protozoa,Ciliophora). Denisia, 1:1–350.

Agatha, S. 2003. Redescription of Strombidinopsis minima (Gruber,1884) Lynn et al., 1991 (Protozoa, Ciliophora), with notes on itsontogenesis and distribution. Eur. J. Protistol., 39:233–244.

Agatha, S. 2004a. Evolution of ciliary patterns in the Oligotrichida(Ciliophora, Spirotricha) and its taxonomic implications. Zoology,107:153–168.

Agatha, S. 2004b. A cladistic approach for the classification of oligotri-chid ciliates (Ciliophora: Spirotricha). Acta Protozool., 43:201–217.

Agatha, S. 2008. Redescription of the tintinnid ciliate Tintinnopsis fim-briata Meunier, 1919 (Spirotricha, Choreotrichida) from coastalwaters of Northern Germany. Denisia, 23:261–272.

Agatha, S. 2010a. A light and scanning electron microscopic study ofthe closing apparatus in tintinnid ciliates (Ciliophora, Spirotricha,Tintinnina): a forgotten synapomorphy. J. Eukaryot. Microbiol.,57:297–307.

Agatha, S. 2010b. Redescription of Tintinnopsis parvula Jorgensen,1912 (Ciliophora: Spirotrichea: Tintinnina), including a novel loricamatrix. Acta Protozool., 49:213–234.

Agatha, S. 2011. Updated hypothesis on the evolution of oligotrichidciliates (Ciliophora, Spirotricha, Oligotrichida) based on somaticciliary patterns and ontogenetic data. Eur. J. Protistol., 47:51–56.

Agatha, S. & Foissner, W. 2009. Conjugation in the spirotrich ciliateHalteria grandinella (Muller, 1773) Dujardin, 1841 (Protozoa, Cilio-phora) and its phylogenetic implications. Eur. J. Protistol., 45:51–63.

Agatha, S. & Riedel-Lorje, J. C. 1998. Morphology, infraciliature, andecology of some strobilidiine ciliates (Ciliophora, Oligotrichea) fromcoastal brackish water basins of Germany. Eur. J. Protistol., 34:10–17.

Agatha, S. & Riedel-Lorje, J. C. 2006. Redescription of Tintinnopsiscylindrica Daday, 1887 (Ciliophora, Spirotricha) and unification oftintinnid terminology. Acta Protozool., 45:137–151.

Agatha, S. & Struder-Kypke, M. C. 2007. Phylogeny of the orderChoreotrichida (Ciliophora, Spirotricha, Oligotrichea) as inferredfrom morphology, ultrastructure, ontogenesis, and SSrRNA genesequences. Eur. J. Protistol., 43:37–63.

Agatha, S. & Tsai, S.-F. 2008. Redescription of the tintinnid Steno-semella pacifica Kofoid and Campbell, 1929 (Ciliophora, Spirotri-cha) based on live observation, protargol impregnation, andscanning electron microscopy. J. Eukaryot. Microbiol., 55:75–85.

Agatha, S., Struder-Kypke, M. C., Beran, A. & Lynn, D. H. 2005.Pelagostrobilidium neptuni (Montagnes and Taylor, 1994) andStrombidium biarmatum nov. spec. (Ciliophora, Oligotrichea): phy-logenetic position inferred from morphology, ontogenesis, and genesequence data. Eur. J. Protistol., 41:65–83.

Balech, E. 1959. Tintinnoinea del Mediterraneo. Trab. Inst. esp. Ocea-nogr., 28:1–88.

Berger, H. 2006. Monograph of the Urostyloidea (Ciliophora, Hypo-tricha). Monographiae Biologicae, Springer, Dordrecht, Nether-lands. 85. i–xv + 1–1303 p.

Berger, H. 2008. Monograph of the Amphisiellidae and Trachelostyli-dae (Ciliophora, Hypotricha). Monographiae Biologicae, Springer,Dordrecht, Netherlands. 88. i–xvi + 1–737 p.

Berger, H. 2011. Monograph of the Gonostomatidae and Kahliellidae(Ciliophora, Hypotricha). Monographiae Biologicae, Springer, Dor-drecht, Netherlands. 90. i–xiv + 1–741 p.

Biernacka, I. 1952. Studia nad rozrodem nicktorych gatunkow rodzajuTintinnopsis Stein. (Studies on the reproduction of some species ofthe genus Tintinnopsis Stein). Ann Univ. Mariae Curie-Sklodowska,Sec. C, 6:211–247. (with Russian and English summaries)

Brandt, K. 1906. Die Tintinnodeen der Plankton-Expedition. Tafel-erklarungen nebst kurzer Diagnose der neuen Arten. In: Hensen, V.(ed.), Ergebn. Plankton-Exped. Humboldt-Stiftung. Lipsius and Ti-scher, Kiel, Leipzig. 3 La: p. 1–33 + Plates 1–70.

Brandt, K. 1907. Die Tintinnodeen der Plankton-Expedition. Systema-tischer Teil. In: Hensen, V. (ed.), Ergebn. Plankton-Exped. Hum-boldt-Stiftung. Lipsius and Tischer, Kiel, Leipzig. 3 La: p. 1–488.


Brownlee, D. C. 1977. The significance of cytological characteristicsas revealed by protargol silver staining in evaluating the systematicsof the Tintinnina. Master Thesis. University of Maryland, Mary-land, USA. i–ix + 146 p.

Brownlee, D. C. 1982. Measuring the secondary production of marineplanktonic tintinnine ciliates. Dissertation. University of Maryland,Maryland, USA. i–vi + 202 p.

Busch, W. 1920. Dauercysten bei Cyttarocylis edentata var. parumden-tata Brandt. Arch. Hydrobiol., 12:756–758.

Cai, S., Song, W., Xu, D. & Chiang, K. 2006. Morphological studieson the infraciliature of a planktonic ciliate, Tintinnopsis brasiliensis(Ciliophora: Tintinina). J. Ocean Univ. China, 5:55–57.

Campbell, A. S. 1954. Tintinnina. In: Campbell, A. S. & Moor, R. C.(ed.), Protista 3: Protozoa (Chiefly Radiolaria and Tintinnina). In:Moor, R. C. (ed.), Treatise on Invertebrate Paleontology. Geologi-cal Society of America and University of Kansas Press, Lawrence.p. D166–D180.

Capriulo, G. M., Taveras, J. & Gold, K. 1986. Ciliate feeding: effectof food presence or absence on occurrence of striae in tintinnids.Mar. Ecol. Prog. Ser., 30:145–158.

Choi, J. K., Coats, D. W., Brownlee, D. C. & Small, E. B. 1992.Morphology and infraciliature of three species of Eutintinnus (Cilio-phora; Tintinnina) with guidelines for interpreting protargol-stainedtintinnine ciliates. J. Protozool., 39:80–92.

Claparede, E. & Lachmann, J. 1858. Etudes sur les infusoires et les rhizo-podes.Mem. Inst. Natn. Genev., 5 (year 1857):1–260+Plates 1–13.

Coryell, H. N. & Fields, S. 1937. A Gatun ostracode fauna from Cati-va, Panama. Amer. Mus. Nat. Hist., Novitates, 956:1–18.

Curds, C. R. & Wu, I. C. H. 1983. A review of the Euplotidae (Hypo-trichida, Ciliophora). Bull. Br. Mus. Nat. Hist. (Zool.), 44:191–247.

Daday, E. von 1887. Monographie der Familie der Tintinnodeen.Mitt. Zool. Stn Neapel, 7:473–591 + Plates 18–21.

Davis, C. C. 1985. Acanthostomella norvegica (Daday) in Insular New-foundland waters, Canada (Protozoa: Tintinnina). Int. Revue ges.Hydrobiol., 70:21–26.

Elwood, H. J., Olsen, G. J. & Sogin, M. L. 1985. The small-subunitribosomal RNA gene sequences from the hypotrichous ciliates Oxy-tricha nova and Stylonychia pustulata. Mol. Biol. Evol., 2:399–410.

Entz, G. Sr. 1884. Uber Infusorien des Golfes von Neapel. Mitt. Zool.Stn Neapel, 5:289–444 + Plates 20–25.

Entz, G. Sr. 1885. Zur naheren Kenntnis der Tintinnoden. Mitt. Zool.Stn Neapel, 6:185–216.

Entz, G. Jr. 1909. Studien uber Organisation und Biologie der Tin-tinniden. Arch. Protistenk., 15:93–226 + Plates 8–21.

Faure-Fremiet, E. 1924. Contribution a la connaissance des infusoiresplanktoniques. Bull. Biol. Fr. Belg. Suppl., 6:1–171.

Faure-Fremiet, E. 1948. Le rythme de maree du Strombidium ocula-tum Gruber. Bull. Biol. Fr. Belg., 82:3–23.

Faure-Fremiet, E. & Ganier, M.-Cl. 1970. Structure fine du Strombid-ium sulcatum Cl. et L. (Ciliata Oligotrichida). Protistologica, 6:207–223. (with English summary)

Felsenstein, J. 2005. PHYLIP (Phylogeny Interference Package) Ver-sion 3.6. distributed by the author, Department of Genetics, Uni-versity of Washington, Seattle, Washington.

Fenchel, T. 1987. Ecology of Protozoa: The Biology of Free-LivingPhagotrophic Protists. Brock/Springer Series in Contemporary Bio-science, Berlin. i–x + 1–197 p.

Fleury, A., Delgado, P., Iftode, F. & Adoutte, A. 1992. Molecularphylogeny of ciliates: what does it tell us about the evolution of thecytoskeleton and of developmental strategies? Develop. Genet.,13:247–254.

Foissner, W. 1996. Ontogenesis in ciliated protozoa, with emphasis onstomatogenesis. In: Hausmann, K. & Bradbury, P. C. (ed.), Cili-ates: Cells as Organisms. G. Fischer, Stuttgart. p. 95–177.

Foissner, W. 2005. The unusual, lepidosome-coated resting cyst ofMeseres corlissi (Ciliophora: Oligotrichea): transmission electronmicroscopy and phylogeny. Acta Protozool., 44:217–230.

Foissner, W. & Al-Rasheid, K. A. S. 2006. A unified organization ofthe stichotrichine oral apparatus, including a description of thebuccal seal (Ciliophora: Spirotrichea). Acta Protozool., 45:1–16.

Foissner, W. & O’Donoghue, P. J. 1990. Morphology and infracilia-ture of some freshwater ciliates (Protozoa: Ciliophora) from Wes-tern and South Australia. Invertebr. Taxon., 3:661–696.

Foissner, W. & Wilbert, N. 1979. Morphologie, Infraciliatur undOkologie der limnischen Tintinnina: Tintinnidium fluviatile Stein,Tintinnidium pusillum Entz, Tintinnopsis cylindrata Daday undCodonella cratera (Leidy) (Ciliophora, Polyhymenophora). J. Proto-zool., 26:90–103. (with English summary)

Foissner, W., Berger, H. & Schaumburg, J. 1999. Identification andecology of limnetic plankton ciliates. Informationsberichte desBayer. Landesamtes fur Wasserwirtschaft, 3/99:1–793.

Foissner, W., Muller, H. & Agatha, S. 2007. A comparative fine struc-tural and phylogenetic analysis of resting cysts in oligotrich andhypotrich Spirotrichea (Ciliophora). Eur. J. Protistol., 43:295–314.

Foissner, W., Muller, H. & Weisse, T. 2005. The unusual, lepido-some-coated resting cyst of Meseres corlissi (Ciliophora: Oligotri-chea): light and scanning electron microscopy, cytochemistry. ActaProtozool., 44:201–215.

Foissner, W., Skogstad, A. & Pratt, J. R. 1988. Morphology and in-fraciliature of Trochiliopsis australis n. sp., Pelagohalteria viridis(Fromentel, 1876) n. g., n. comb., and Strobilidium lacustris n. sp.(Protozoa, Ciliophora). J. Protozool., 35:489–497.

Foissner, W., Blatterer, H., Berger, H. & Kohmann, F. 1991. Taxonomi-sche und okologische Revision der Ciliaten des Saprobiensystems –Band I: Cyrtophorida, Oligotrichida, Hypotrichia, Colpodea. Infor-mationsberichte des Bayer. Landesamtes furWasserwirtschaft, 1/91:1–478.

Foissner, W., Moon-van der Staay, S. Y., van der Staay, G. W. M.,Hackstein, J. H. P., Krautgartner, W.-D. & Berger, H. 2004. Rec-onciling classical and molecular phylogenies in the stichotrichines(Ciliophora, Spirotrichea), including new sequences from some rarespecies. Eur. J. Protistol., 40:265–281.

Gao, S., Gong, J., Lynn, D., Lin, X. & Song, W. 2009. An updatedphylogeny of oligotrich and choreotrich ciliates (Protozoa, Cilio-phora, Spirotrichea) with representative taxa collected from Chi-nese coastal waters. Syst. Biodivers., 7:235–242.

Grain, J. 1972. Etude ultrastructurale d’Halteria grandinella O.F.M.,(Cilie Oligotriche) et considerations phylogenetiques. Protistologica,8:179–197. (with English summary)

Grim, J. N. 1987. The kinetid structures of the choreotrichous ciliateStrobilidium velox and an assessment of its evolutionary lineage. J.Protozool., 34:117–123.

Guindon, S., Dufayard, J. F., Lefort, V., Anisimova, M., Hordijk, W.& Gascuel, O. 2010. New algorithms and methods to estimate max-imum-likelihood phylogenies: assessing the performance of PhyML3.0. Syst. Biol., 59:307–321.

Gutierrez, J. C., Dıaz, S., Ortega, R. & Martın-Gonzalez, A. 2003.Ciliate resting cyst walls: a comparative review. Recent Res. Dev.Microbiol., 7:361–379.

Hada, Y. 1932. The Tintinnoinea from the Sea of Okhotsk and itsneighborhood. J. Fac. Sci. Hokkaido Univ., 2:37–59.

Haeckel, E. 1873. Ueber einige neue pelagische Infusorien. Jen. Z.Med. Naturwiss., 7 (year 1871):561–568 + Plates 27, 28.

Hedin, H. 1975. On the ultrastructure of Favella ehrenbergii (Cla-parede & Lachmann) and Parafavella gigantea (Brandt), Protozoa,Ciliata, Tintinnida. Zoon, 3:11–18.

Hedin, H. 1976. Microtubules and microfilaments in the tintinnid cili-ate Ptychocylis minor Jorgensen. Zoon, 4:3–10.

Hennig, W. 1966. Phylogenetic Systematics. University of IllinoisPress, Urbana, Chicago, London. p. i–iii + 1–263.

Hennig, W. 1982. Phylogenetische Systematik. Pareys Studientexte 34,Berlin, Hamburg. 1–246 p.

Hofker, J.1931.Studien uberTintinnoidea.Arch.Protistenk.,75:315–402.Horandl, E. & Stuessy, T. F. 2010. Paraphyletic groups as natural

units of biological classification. Taxon, 59:1641–1653.Ichinomiya, M., Nakamachi, M. & Taniguchi, A. 2004. A practical

method for enumerating cysts of ciliates in natural marine sedi-ments. Aquat. Microb. Ecol., 37:305–310.

International Commission on Zoological Nomenclature [ICZN]. 1999.International Code of Zoological Nomenclature. Fourth EditionAdopted by the International Union of Biological Sciences.International Trust for Zoological Nomenclature 1999, London. Ti-pografia La Garangola, Padova. 1–306 p.

Jørgensen, E. 1900. Ueber die Tintinnodeen der norwegischen West-kuste. Bergens Mus. Aarb., 2 (year 1899):1–48 + Plates 1–3.

Jorgensen, E. 1924. Mediterranean Tintinnidae. Rep. Danish Ocean.Exped., 1908–1910, Mediterr. Seas, Vol. II (Biol.), J3:1–110.


Kent, W. S. 1880–1882. A Manual of the Infusoria: Including aDescription of all Known Flagellate, Ciliate, and TentaculiferousProtozoa, British and Foreign, and an Account of the Organizationand Affinities of the Sponges. David Bogue, London. p. i–x + 1–913 + Plates 1–51 (1880: p. i–x + 1–472 + Plates 1–23; 1881:473–720 + Plates 24–40; 1882: 721–913 + Plates 41–51).

Kim, J. S., Jeong, H. J., Strueder-Kypke, M. C., Lynn, D. H., Kim,S., Kim, J. H. & Lee, S. H. 2005. Parastrombidinopsis shimi n. gen.,n. sp. (Ciliophora: Choreotrichia) from the coastal waters ofKorea: morphology and small subunit ribosomal DNA sequence.J. Eukaryot. Microbiol., 52:514–522.

Kim, S. Y., Yang, E. J., Gong, J. & Choi, J. K. 2010. Redescriptionof Favella ehrenbergii (Claparede and Lachmann, 1858) Jorgensen,1924 (Ciliophora: Choreotrichia), with phylogenetic analyses basedon small subunit rRNA gene sequences. J. Eukaryot. Microbiol.,57:460–467.

Kim, Y.-O. & Taniguchi, A. 1995. Excystment of the oligotrich ciliateStrombidium conicum. Aquat. Microb. Ecol., 9:149–156.

Kim, Y.-O. & Taniguchi, A. 2007. Cyst morphology and encystmentof the planktonic oligotrich ciliate Strombidium capitatum. Protis-tology, 5:41.

Kim, Y.-O., Ha, S. & Taniguchi, A. 2008. Morphology and in situsedimentation of the cysts of a planktonic oligotrich ciliate, Strom-bidium capitatum. Aquat. Microb. Ecol., 53:173–179.

Kim, Y.-O., Kim, S. Y., Lee, W.-J. & Choi, J. K. 2010. New observa-tions on the choreotrich ciliate Strombidinopsis acuminata Faure-Fremiet 1924, and comparison with Strombidinopsis jeokjo Jeonget al., 2004. J. Eukaryot. Microbiol., 57:48–55.

Kimura, M. 1980. A simple model for estimating evolutionary ratesof base substitutions through comparative studies of nucleotidesequences. J. Mol. Evol., 16:111–120.

Kofoid, C. A. & Campbell, A. S. 1929. A conspectus of the marineand fresh-water Ciliata belonging to the suborder Tintinnoinea,with descriptions of new species principally from the Agassiz Expe-dition to the eastern tropical Pacific 1904–1905. Univ. Calif. Publ.Zool., 34:1–403.

Kofoid, C. A. & Campbell, A. S. 1939. Reports on the scientificresults of the expedition to the eastern tropical Pacific, in charge ofAlexander Agassiz, by the U.S. Fish Commission Steamer “Alba-tross,” from October, 1904, to March, 1905, Lieut.-Commander L.N. Garrett, U.S.N., Commanding. 37. The Ciliata: the Tintinnoi-nea. Bull. Mus. Comp. Zool., 84:1–473 + Plates 1–36.

Krainer, K.-H. 1995. Taxonomische Untersuchungen an neuen undwenig bekannten planktischen Ciliaten (Protozoa: Ciliophora) ausBaggerseen in Osterreich. Lauterbornia, 21:39–68. (with Englishsummary)

Kuppers, G. C., Lopretto, E. C. & Claps, M. C. 2006. Morphologicalaspects and seasonal changes of some planktonic ciliates (Protozoa)from a temporary pond in Buenos Aires Province, Argentina.PANAMJAS, 1:74–90. (with Portuguese summary)

Laackmann, H. 1908. Ungeschlechtliche und geschlechtliche Fort-pflanzung der Tintinnen. Wiss. Meeresunters., Abt. Kiel, 10:13–38+ Plates 1–3.

Lackey, J. B. & Balech, E. 1966. A new marine tintinnid. Trans. Am.Microsc. Soc., 85:575–578.

Laval, M. 1972. Ultrastructure de Petalotricha ampulla (Fol). Com-paraison avec d’autres tintinnides et avec les autres ordres de cilies.Protistologica, 8:369–386. (with English summary)

Laval-Peuto, M. 1975. Cortex, perilemme et reticulum vesiculeux deCyttarocylis brandti (cilie Tintinnide). Les cilies a perilemme. Protis-tologica, 11:83–98. (with English summary)

Laval-Peuto, M. 1977. Reconstruction d’une lorica de forme Coxliellapar le trophonte nu de Favella ehrenbergii (Ciliata, Tintinnina). C.r. Hebd. Seanc. Acad. Sci., Paris, Serie D, 284:547–550.

Laval-Peuto, M. 1981. Construction of the lorica in Ciliata Tintin-nina. In vivo study of Favella ehrenbergii: variability of the pheno-types during the cycle, biology, statistics, biometry. Protistologica,17:249–272. (with French summary)

Laval-Peuto, M. 1994. Classe des Oligotrichea Butschli, 1887. Ordredes Tintinnida Kofoid et Campbell, 1929. In: Puytorac, P. de (ed.),Traite de Zoologie. Anatomie, Systematique, Biologie. II. InfusoiresCilies. 2. Systematique. Masson, Paris, Milano, Barcelona. p. 181–219.

Laval-Peuto, M. & Barrıa de Cao, M. S. 1987. Les capsules, extru-somes caracteristiques des Tintinnina (Ciliophora), permettent uneclassification evolutive des genres et des familles du sous-ordre. IleReun. Scientif. GRECO 88, Trav. C.R.M., 8:53–59.

Laval-Peuto, M. & Brownlee, D. C. 1986. Identification and systemat-ics of the Tintinnina (Ciliophora): evaluation and suggestion forimprovement. Ann Inst. Oceanogr., Paris, 62:69–84. (with Frenchsummary)

Li, Z., Yi, Z., Yang, J., Gong, J., Clamp, J. C., Al-Rasheid, K. A. S.,Al-Arifi, S., Al-Khedhairy, A. A. & Song, W. 2009. Phylogeneticinvestigation on five genera of tintinnid ciliates (Ciliophora, Cho-reotrichia), based on the small subunit ribosomal RNA genesequences. Prog. Nat. Sci., 19:1097–1101.

Lipscomb, D. L. 1992. Parsimony, homology and the analysis of mul-tistate characters. Cladistics, 8:45–65.

Liu, W., Xu, D., Lin, X., Li, J., Gong, J., Al-Rasheid, K. A. S. &Song, W. 2009. Novistrombidium sinicum n. sp. and Novistrombidi-um orientale n. sp. (Protozoa: Ciliophora): two new oligotrich cili-ates from a mangrove wetland, South China. J. Eukaryot.Microbiol., 56:459–465.

Liu, W., Yi, Z., Lin, X. & Al-Rasheid, K. A. S. 2011. Morphologicand molecular data suggest that Lynnella semiglobulosa n. g, n. sp.represents a new family within the subclass Choreotrichia (Cilio-phora, Spirotrichea). J. Eukaryot. Microbiol., 58:43–49.

Loeblich, A. R. & Tappan, H. 1968. Annotated index to genera, sub-genera and suprageneric taxa of the ciliate order Tintinnida. J. Pro-tozool., 15:185–192.

Lynn, D. H. 2008. The Ciliated Protozoa. Characterization, Classifi-cation and Guide to the Literature. 3rd ed. Springer, Dordrecht,Netherlands. p. i–xxxiii + 1–605.

Lynn, D. H. & Montagnes, D. J. S. 1988. Taxonomic descriptions ofsome conspicuous species of strobilidiine ciliates (Ciliophora: Cho-reotrichida) from the Isles of Shoals, Gulf of Maine. J. mar. Biol.Assoc. U.K., 68:639–658.

Lynn, D. H. & Small, E. B. 2002. Phylum Ciliophora Doflein, 1901.In: Lee, J. J., Leedale, G. F. & Bradbury, P. (ed.), An IllustratedGuide to the Protozoa. 2nd Edition. Organisms TraditionallyReferred to as Protozoa, or Newly Discovered Groups. Societyof Protozoologists, Year 2000. Allen Press, Lawrence, KS, USA.p. 371–656.

Margalef, R. & Duran, M. 1953. Microplancton de Vigo, de octubre de1951 a septiembre de 1952. P. Inst. Biol. Apl., 13:5–78 + Table 1.

Mayr, E. & Bock, W. J. 2002. Classifications and other ordering sys-tems. J. Zool. Syst. Evol. Res., 40:169–194.

McManus, G. B. & Katz, L. A. 2009. Molecular and morphologicalmethods for identifying plankton: what makes a successful mar-riage? J. Plankton Res., 31:1119–1129.

McManus, G. B., Xu, D., Costas, B. A. & Katz, L. A. 2010. Geneticidentities of cryptic species in the Strombidium stylifer/apolatum/oc-ulatum cluster, including a description of Strombidium rassoulzade-gani n. sp. J. Eukaryot. Microbiol., 57:369–378.

Medlin, L. K., Elwood, H. J., Stickel, S. & Sogin, M. L. 1988. Thecharacterization of enzymatically amplified eukaryotic 16S-likerRNA-coding regions. Gene, 71:491–499.

Meunier, A. 1910. Campagne Arctique de 1907. Microplankton desMers de Barents et de Kara. Bulens, Bruxelles. p. i–xviii + 1–355+ Plates 1–37.

Meunier, A. 1919. Microplankton de la mer Flamande: Les Tintinnideset caetera. Mem. Mus. R. Hist. Nat. Belg., 8:1–59 + Plates 22, 23.

Modeo, L., Petroni, G., Rosati, G. & Montagnes, D. J. S. 2003. Amultidisciplinary approach to describe protists: redescriptions ofNovistrombidium testaceum Anigstein 1914 and Strombidium inclina-tum Montagnes, Taylor, and Lynn 1990 (Ciliophora, Oligotrichia).J. Eukaryot. Microbiol., 50:175–189.

Montagnes, D. J. S. & Taylor, F. J. R. 1994. The salient features offive marine ciliates in the class Spirotrichea (Oligotrichia), withnotes on their culturing and behaviour. J. Eukaryot. Microbiol.,41:569–586.

Montagnes, D. J. S., Lowe, C. D., Poulton, A. & Jonsson, P. R.2002. Redescription of Strombidium oculatum Gruber 1884 (Cilio-phora, Oligotrichia). J. Eukaryot. Microbiol., 49:329–337.

Muller, H. 2007. Live observation of excystment in the spirotrich cili-ate Meseres corlissi. Eur. J. Protistol., 43:95–100.


Nie, D. 1934. Notes on Tintinnoinea from the Bay of Amoy. Rep.mar. Biol. Ass. China, 3:71–80.

Page, R. D. M. 1996. TREEVIEW: an application to display phyloge-netic trees on personal computers.Comput. Appl. Biosci., 12:357–358.

Paranjape, M. A. 1980. Occurrence and significance of resting cysts ina hyaline tintinnid, Helicostomella subulata (Ehre.) Jorgensen. J.Exp. Mar. Biol. Ecol., 48:23–33.

Petz, W. & Foissner, W. 1992. Morphology and morphogenesis ofStrobilidium caudatum (Fromentel), Meseres corlissi n. sp., Halteriagrandinella (Muller), and Strombidium rehwaldi n. sp., and a pro-posed phylogenetic system for oligotrich ciliates (Protozoa, Cilio-phora). J. Protozool., 39:159–176.

Petz, W. & Foissner, W. 1993. Morphogenesis in some freshwater tin-tinnids (Ciliophora, Oligotrichida). Eur. J. Protistol., 29:106–120.

Petz, W., Song, W. & Wilbert, N. 1995. Taxonomy and ecology ofthe ciliate fauna (Protozoa, Ciliophora) in the endopagial and pela-gial of the Weddell Sea, Antarctica. Stapfia, 40:1–223.

Poe, S. & Wiens, J. J. 2000. Character selection and the methodologyof morphological phylogenetics. In: Wiens, J. J. (ed.), PhylogeneticAnalysis of Morphological Data. Smithsonian Institution Press,Washington, London. p. 20–36.

Posada, D. & Crandall, K. A. 1998. MODELTEST: testing the modelof DNA substitution. Bioinformatics, 14:817–818.

Puri, H. S. 1953. Taxonomic comment on: “Ostracoda from Wells inNorth Carolina Part I: Cenozoic Ostracoda” by F. M. Swain. J.Paleontol., 27:750–752.

Reid, P. C. & John, A. W. G. 1978. Tintinnid cysts. J. mar. Biol. Ass.U.K., 58:551–557 + Plate 1.

Riley, J. L.&Katz, L.A. 2001.Widespread distribution of extensive chro-mosomal fragmentation in ciliates.Mol. Biol. Evol., 18:1372–1377.

Ronquist, F. & Huelsenbeck, J. 2003. MrBayes 3: Bayesian phylo-genetic inference under mixed models. Bioinformatics, 19:1572–1574.

Saitou, N. & Nei, M. 1987. The neighbor-joining method: a newmethod for reconstructing phylogenetic trees. Mol. Biol. Evol.,4:406–425.

Schmidt, S. L., Bernhard, D., Schlegel, M. & Fried, J. 2006. Fluores-cence in situ hybridization with specific oligonucleotide rRNAprobes distinguishes the sibling species Stylonychia lemnae and Styl-onychia mytilus (Ciliophora, Spirotrichea). Protist, 157:21–30.

Schweyer, A. 1909. Zur Kenntnis des Tintinnodeenweichkorpers,nebst einleitenden Worten uber die Hulsenstruktur und die Hulsen-bildung. Arch. Protistenk., 18:134–189 + Plates 10, 11.

Shin, M. K., Hwang, U. W., Kim, W., Wright, A.-D. G., Krawczyk,C. & Lynn, D. H. 2000. Phylogenetic position of the ciliates Pha-codinium (order Phacodiniida) and Protocruzia (subclass Proto-cruziidia) and systematics of the spirotrich ciliates examined bysmall subunit ribosomal RNA gene sequences. Eur. J. Protistol.,36:293–302.

Skovgaard, A. & Legrand, C. 2005. Observation of live specimens ofPseudotontonia cornuta (Ciliophora: Oligotrichida) reveals new dis-tinctive characters. J. mar. Biol. Ass. U.K., 85:783–786.

Small, E. B. & Lynn, D. H. 1985. Phylum Ciliophora Doflein, 1901.In: Lee, J. J., Hutner, S. H. & Bovee, E. C. (ed.), An IllustratedGuide to the Protozoa. Society of Protozoologists. Allen Press,Lawrence, Kansas. p. 393–575.

Sniezek, J. H., Capriulo, G. M., Small, E. B. & Russo, A. 1991. Nola-clusilis hudsonicus n. sp. (Nolaclusiliidae n. fam.) a bilaterally sym-metrical tintinnine ciliate from the lower Hudson River estuary. J.Protozool., 38:589–594.

Snoeyenbos-West, O. L. O., Salcedo, T., McManus, G. B. & Katz, L.A. 2002. Insights into the diversity of choreotrich and oligotrich cil-iates (Class: Spirotrichea) based on genealogical analyses of multi-ple loci. Int. J. Syst. Evol. Microbiol., 52:1901–1913.

Snyder, R. A. & Brownlee, D. C. 1991. Nolaclusilis bicornis n. g., n.sp. (Tintinnina: Tintinnidiidae): a tintinnine ciliate with novel loricaand cell morphology from the Chesapeake Bay estuary. J. Protozo-ol., 38:583–589.

Sokolova, Y. Y. & Gerassimova, Z. P. 1984. The ultrastructure of theciliates Parafavella denticulata Ehrenberg, 1840. Tsitologiya,26:1237–1245 + Plates 1–3. (in Russian with English summary)

Sokolova, Y. Y., Seravin, L. N. & Gerassimova, Z. P. 1986. Mem-brane structures and their supposed involvement in the digestiveevents with the ciliate Parafavella denticulata Ehrenberg, 1890 (Tin-tinnina). Tsitologiya, 28:220–224. (in Russian with English sum-mary)

Stepanowa, W. 1937. Biologische Zeichnungen der Stromungen imnordlichen Teil des Berings- und im sudlichen Teil des Tschukt-schen Meeres. Explor. Mers U.R.S.S., 25:175–216. (in Russian withGerman summary)

Strelkow, A. A. 1953. New species of pelagic Tintinnoinea of far eastwaters. Trav. Inst. Zool. Acad. Sci. U.R.S.S., 13:57–68.

Struder-Kypke, M. C. & Lynn, D. H. 2003. Sequence analyses of thesmall subunit rRNA gene confirm the paraphyly of oligotrich cili-ates sensu lato and support the monophyly of the subclasses Oligo-trichia and Choreotrichia (Ciliophora, Spirotrichea). J. Zool. Lond.,260:87–97.

Struder-Kypke, M. C. & Lynn, D. H. 2008. Morphological versusmolecular data – phylogeny of tintinnid ciliates (Ciliophora, Cho-reotrichia) inferred from small subunit rRNA gene sequences. Deni-sia, 23:417–424.

Swofford, D. L. 2002. PAUP*. Phylogenetic Analysis Using Parsi-mony (* and Other Methods). Version 4.0b10. Sinauer Ass., Sun-derland, Massachusetts.

Tamura, K., Dudley, J., Nei, M. & Kumar, S. 2007. MEGA4: Molec-ular Evolutionary Genetics Analysis (MEGA) software version 4.0.Mol. Biol. Evol., 24:1596–1599.

Tsai, S.-F., Chen, J.-Y. & Chiang, K.-P. 2010. Spirotontonia taiwanican. sp. (Ciliophora: Oligotrichida) from the coastal waters of north-eastern Taiwan: morphology and nuclear small subunit rDNAsequence. J. Eukaryot. Microbiol., 57:429–434.

Tsai, S.-F., Xu, D., Chung, C.-C. & Chiang, K.-P. 2008. Para-strombidinopsis minima n. sp. (Ciliophora: Oligotrichia) from thecoastal waters of northeastern Taiwan: morphology and small sub-unit ribosomal DNA sequence. J. Eukaryot. Microbiol., 55:567–573.

Van Breemen, P. J. 1905. Plankton van Noordzee en Zuiderzee. Dis-sertation. University of Amsterdam, Netherlands. 180 p. + Plates1, 2.

Wasik, A. & Mikołajczyk, E. 1992. The morphology and ultrastruc-ture of the Antarctic ciliate, Cymatocylis convallaria (Tintinnina).Acta Protozool., 31:233–239.

Wasik, A. & Mikołajczyk, E. 1994. Infraciliature of Cymatocylis affi-nis/convallaria (Tintinnina). Acta Protozool., 33:79–85.

Weisse, T., Struder-Kypke, M. C., Berger, H. & Foissner, W. 2008.Genetic, morphological, and ecological diversity of spatially sepa-rated clones of Meseres corlissi Petz & Foissner, 1992 (Ciliophora,Spirotrichea). J. Eukaryot. Microbiol., 55:257–270.

Wiens, J. J. 2000. Coding morphological variation within species andhigher taxa for phylogenetic analysis. In: Wiens, J. J. (ed.), Phylo-genetic Analysis of Morphological Data. Smithsonian InstitutionPress, Washington, London. p. 115–145.

Xu, D., Warren, A. & Song, W. 2009. Oligotrichs. In: Song, W., War-ren, A. & Hu, X. (ed.), Free-Living Ciliates in the Bohai and Yel-low Seas, China. Science Press, Beijing. p. 307–351.

Xu, D., Sun, P., Song, W. & Warren, A. 2008. Studies on a new en-docommensal ciliate, Strombidium foissneri nov. sp. (Ciliophora,Oligotrichida), from the intestine of the sea urchin Hemicentrotuspulcherrimus (Camarodonta, Echinoida). Denisia, 23:273–278.

Xu, D., Song, W., Warren, A., Roberts, D. & Hu, X. 2007. Rede-scriptions of two marine planktonic ciliates from China, Parastrom-bidium faurei (Kahl, 1932) Maeda, 1986 and Strombidium capitatum(Leegaard, 1915) Kahl, 1932 (Ciliophora, Oligotrichea). Eur. J.Protistol., 43:27–35.

Zhang, Q., Yi, Z., Xu, D., Al-Rasheid, K. A. S., Gong, J. & Song,W. 2010. Molecular phylogeny of oligotrich genera Omegastrombid-ium and Novistrombidium (Protozoa, Ciliophora) for the systemati-cal relationships within Family Strombidiidae. Chin. J. Oceanol.Limnol., 28:769–777.

Received: 09/27/2011, 02/16/11, 02/22/12; accepted: 02/23/2012


Documents

Reconciling Cladistic and Genetic Analyses in Choreotrichid Ciliates (Ciliophora, Spirotricha, Oligotrichea)