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89
 Abstract The ciliated protozoa are a distinct group of 
protists characterized by (1) the presence of cilia de-
rived from kinetosomes with three fi brillar associates; 
(2) nuclear dimorphism; and (3) conjugation as a 
sexual process. They are exceedingly diverse in 
shape and size, and may have evolved over 2 billion 
years ago. The ciliate body form likely evolved from 
a fl agellate that proliferated kinetids near its oral 
apparatus, and these kinetids became fi rst the ciliate 
paroral, which itself replicated to provide somatic 
kineties and fi nally the adoral kinetids. Ciliates are 
now divided into two subphyla and 11 classes based 
on features of nuclear division and the pattern of 
fi brillar associates in their somatic kinetids. They 
are found in a diversity of microhabitats, with the 
majority of species likely cosmopolitan. However, 
endemism appears to be characteristic of perhaps as 
many as 30% of the species. Ciliates are important 
components of the microbial loop, often responsible 
for consuming the majority of primary production 
and bacterial production in certain habitats. 
 Their development is complex since the kinetid 
patterns of the somatic and oral cortex are them-
selves complex. This complexity has made them 
useful models for developmental biologists while 
the systematists have used these patterns to relate 
different taxa to each other. The life cycles of cili-
ates are also complex and clearly separate sexual 
processes from asexual reproduction. Sexual proc-
ess, conjugation, occurs in the context of a breeding
strategy, ranging from an inbreeding one to an 
outbreeding one. A new macronucleus typically 
develops at each conjugation cycle through a com-
plicated set of processes of DNA fragmentation, 
diminution, and replication. However, this process 
likely occurs at each cell cycle in karyorelictean 
ciliates whose macronuclei do not divide. 
 Keywords Cytotaxis, structural guidance, extru-
some, metachrony, alveoli 
 The ciliates, without doubt, are a most homo-
geneous group, which have long been separated 
from other protists. They are briefly distinguished 
by three major features: (1) by their cilia, variable 
in number and arrangement, distributed over the 
body surface and derived from kinetosomes with 
three typical fibrillar associates – the kinetodesmal 
fibril , the postciliary microtubular ribbon , and the 
 transverse microtubular ribbon ; (2) by their two 
kinds of nuclei – a macronucleus and a micro-
nucleus , the former controlling the physiological 
and biochemical functions of the cell and the latter 
as a germ-line reserve; and (3) by conjugation , 
a sexual process in which partners typically fuse 
temporarily to exchange gametic nuclei. All cili-
ates are heterotrophic and most possess a mouth, 
although some are mouthless (e.g., the astomes ) 
and others could be called polystomic (e.g., sucto-
rians with their tentacles). 
 Ciliates vary in shape and size. There are 
stalked and colonial species that have unusual 
forms, but generally the shapes are simple geo-
metric ones – spheres, cones, oblate spheroids, 
and cylinders, which may be flattened dorsoven-
trally in substrate-oriented species. Body form is 
relatively permanent since the cortex is supported 
by a complex microtubular and microfilamentous 
cytoskeleton. Ciliates range in size from 10 µm in 
very small spheroid forms to 4,500 µm in highly 
 Chapter 4 
 Phylum CILIOPHORA – Conjugating, 
Ciliated Protists with Nuclear Dualism 
90 4. Phylum CILIOPHORA – Conjugating, Ciliated Protists with Nuclear Dualism
elongate and contractile ones. Biovolume ranges 
give another impression of size: in the Class 
 COLPODEA , cell volume ranges from 10 2 µm 3 for 
Nivaliella to 10 8 µm 3 for Bursaria ; and in the Class 
 OLIGOHYMENOPHOREA , cell volumes range 
from 10 3 µm 3 for some Cyclidium species to >10 9
µm3 for the trophonts of Ichthyophthirius (Lynn & 
Corliss, 1991). 
 Ciliates were first observed microscopically 
by van Leeuwenhoek (1674), the founder of pro-
tozoology (Corliss, 1975b). Ciliates were visible 
as blooms or colored waters in both marine and 
freshwater habitats, probably thousands of years 
before van Leeuwenhoek’s discoveries. Their for-
mal nomenclatural history begins in 1767 with the 
establishment of Vorticella by Linnaeus (Aescht, 
2001). They were named the INFUSORIA through-
out the 19th century, a name that was replaced in 
the early 20th century by the present name of the 
phylum – CILIOPHORA . The ciliates were an 
isolated group until 1991 when it was proposed 
that the membrane-bound sacs underlying their 
plasma membrane, the alveoli , were a synapo-
morphy or shared-derived character for a major 
clade of protists, the ALVEOLATA , which initially 
included dinoflagellates , apicomplexans , and cili-
ates (Cavalier-Smith, 1991; Wolters, 1991). This 
clade was reaffirmed in the revised classification of 
the protists proposed by Adl et al. (2005). Based on 
strong molecular evidence, this clade now includes 
these three major groups, along with the aber-
rant “ dinoflagellate ” Oxyrrhis and the perkinsids 
associated with the dinoflagellate clade and several 
flagellates, such as Colpodella , associated with the 
base of the apicomplexan clade. Dinoflagellates 
and apicomplexans are strongly supported as sister 
taxa, leaving the ciliates as a separate lineage 
(Leander & Keeling, 2003). When and how the cil-
iates diverged from the alveolate common ancestor 
are still open questions, but we have some ideas. 
 With regard to when, ciliates probably arose 
in the Precambrian era . While there are no fos-
sils from this time, Wright and Lynn (1997c) 
argued that the phylum could be over 2 billion 
years old, based on the rate of evolution of the 
small subunit rRNA molecular clock (Fig. 4.1). 
While this estimate can be challenged as it makes 
some strong assumptions on the constancy of the 
 molecular clock , there is no dispute over fossils 
of the loricate tintinnines , which stretch from the 
 Ordovician period of the Paleozoic era , some 400–450 
million years before present (myBP) into the 
 Pleistocene , about 1 myBP. Tintinnine fossils are 
most abundant in the sediments of the Jurassic and 
 Cretaceous periods of the Mesozoic era (see Bonet, 
1956; Colom, 1965; Tappan & Loeblich, 1968, 
1973). Fossils of other loricate forms have also 
been found: Deflandre and Deunff (1957) reported 
a fossil folliculinid heterotrich while Weitschat 
and Guhl (1994) described several fossil loricate 
peritrichs from the Lower Triassic period . Even 
more recently, extremely well-preserved ciliates, a 
Paramecium species and several colpodeans, have 
been described from amber derived from southern 
Germany in amber-bearing sandstone deposits 
(Schönborn, Dörfelt, Foissner, Krientiz, & Schäfer, 
1999), which have now been assigned to the Late 
Cretaceous , some 90 million years ago (Schmidt, 
von Eynatten, & Wagreich, 2001). However, these 
fossil forms can generally be placed in contempo-
rary families and even genera, so they provide little 
insight into the origin of the ciliates. Nevertheless, 
this has not deterred some speculation on how 
ciliates diverged. Given the molecular phylogenies, 
there is no doubt that the ciliates evolved from a 
flagellate ancestor. Two major features of ciliates 
– their complex cortex and their nuclear dualism 
– have preoccupied those who have speculated on 
how a flagellate ancestor might have evolved into 
the ancestral ciliate. 
 The complex ciliate cortex undoubtedly evolved 
from a simpler flagellate dikinetid. Earlier evolu-
tionary schemes of Orias (1976) and Small (1984) 
argued that the dikinetids of the flagellate ances-
tor replicated to form first a “torsionless chain”, 
similar to the polynergid dinoflagellate Polykrikos , 
and then a ribbon-like form with multiple somatic 
kineties . Orias imagined that the ribbon-likeform 
rolled up to ultimately form an ancestral prostomial 
form, while Small imagined that the ribbon-like 
form might have been very similar to the contem-
porary karyorelictean Kentrophoros , with an elon-
gate, flattened “ventral” surface, which it used for 
ingestion. Both these schema suggested that oral 
ciliature derived from somatic ciliature. 
 Eisler (1992) proposed a contrary model in which
the paroral dikinetids of ciliates represent the first 
ciliature of the ancestral ciliate and that the somatic 
kinetids derived from this. This model, most 
recently summarized by Schlegel and Eisler (1996), 
begins with a similar polyenergid stage as above. 
However, this “first” kinety is interpreted to be a 
 paroral , lying adjacent to a tube-like cytopharyngeal
apparatus supported by microtubules, as is found 
in some dinoflagellates (Fig. 4.2). At this stage, the 
paroral dikinetids are considered to lie orthogonal to 
the longitudinal axis of the cell and their postciliary 
microtubular ribbons extended to support the 
 cytopharynx . In the second stage, somatic Kinety 1 
(K1, Fig. 4.2) was derived from these paroral 
dikinetids by separation and rightward migration 
of the anterior or rightmost kinetosome of each 
paroral dikinetid (Step a, Fig. 4.2). Replication of 
these kinetosomes followed to reconstitute the 
ancestral dikinetid state (Lynn & Small, 1981). 
Eisler suggested that multiple repetitions of this 
process could give rise to multiple somatic kineties 
(Step b, Fig. 4.2). Alternatively, one could invoke the
processes of either torsion and fragmentation (see 
Small, 1984) or elineation to increase the number 
of somatic kineties . In a final stage, the adoral or 
“lefthand” oral structures are imagined to derive 
from the differentiation of somatic kinetids to the 
left of the oral region (Step c, Fig. 4.2). To support 
this, Schlegel and Eisler (1996) noted that the adoral 
ciliature is derived from a somatically-derived 
anlage in many contemporary ciliates. The paroral 
model has the advantage that, from the beginning, 
the ciliate ancestor, like many contemporary 
 dinoflagellates , has a cytopharynx supported by 
microtubules derived from the “paroral” dikinetids: 
there is no need to invoke an independent evolution 
Fig. 4.1. A phylogeny of the ciliates demonstrating the estimated time of divergence of some major lineages as 
 estimated by the divergence rate of small subunit rRNA gene sequences . The upper limit of 1% divergence per 80 
million years was used to determine the lengths of the branches on the tree. (from Wright & Lynn, 1997c.)
4. Phylum CILIOPHORA – Conjugating, Ciliated Protists with Nuclear Dualism 91
92 4. Phylum CILIOPHORA – Conjugating, Ciliated Protists with Nuclear Dualism
of the oral apparatus as in the competing models 
(see Orias, 1976; Small). Stomatogenesis and mor-
phogenesis of the progeny cell or opisthe would 
have been of a buccokinetal type. 
 Speculations on the evolution of another major 
feature distinguishing ciliates – nuclear dualism 
– are intriguing. Orias (1991b) used the life cycle 
of heterokaryotic foraminifera as an analogue to 
provide a rationale for how a heterophasic life cycle 
of a ciliate, ancestral to the karyorelicteans , might 
have evolved. This heterophasic life cycle had an 
alternation of haploid and diploid generations. 
From this, Orias developed the possible steps to the 
evolution of a karyorelictean cell cycle in which 
 nuclear dualism occurs but with divisionless macro-
nuclei differentiated at every cell cycle. While we 
now know that ciliates and foraminiferans are not 
closely related (Nikolaev et al., 2004), it is still 
possible that a heterophasic kind of life cycle might 
have been an intermediate stage in the evolution of 
ciliate nuclear dualism . 
 Orias (1991a) argued further that macronuclear 
division must have originated de novo within the 
ciliates. He noted that macronuclei in most cili-
ates fail to divide during the first postzygotic cell 
cycle following conjugation : more macronuclei are 
differentiated than is typical and these “excess” 
macronuclei are segregated without macronuclear 
division during postconjugation fissions , reminiscent
of the phenomenon that occurs at every cell cycle
in karyorelicteans . Macronuclear “dividers” may 
have had selective advantages: the division process 
is much faster than the nuclear differentiation proc-
ess and so “dividers” would outcompete “non-
dividers”; and dividing macronuclei may have 
increased the capability to assort intraclonally the 
genetic diversity of the parents and so increase the 
probability of generating more fit variants (Orias, 
1991a). Why do karyorelicteans still persist? Orias 
suggested that they may still be more fit in the 
“refugial” relict environments in which they are 
often found, and that many karyorelicteans may 
have compensated for macronuclear polyploidy by 
increasing the number of macronuclei, so support-
ing their increased cell size. 
 As additional evidence that macronuclear divi-
sion originated within the ciliates, Orias (1991a) 
noted that diversity in the modes of karyokinesis 
suggested at least two independent origins of 
 macronuclear division – heterotrichs use extrama-
cronuclear microtubules and other ciliates use 
intramacronuclear microtubules . Herrick (1994) 
argued that macronuclear division may have evolved 
independently perhaps three or more times, given 
the diversity of molecular mechanisms underlying 
 macronuclear differentiation . However, Katz (2001) 
has used current molecular phylogenies of ciliates 
to argue for a single origin of a differentiating 
Fig. 4.2. Scheme of evolution of the ancestral ciliate oral and somatic cortex as proposed by Eisler (1992). Step a
– an ancestral flagellate with a cytostome (c) and paroral of dikinetids separates the rightmost kinetosome of each 
dikinetid (arrowhead) to form somatic Kinety 1 (K1). Step b – this process is repeated (arrow) a number of times until 
the entire somatic cortex is covered by somatic kineties (Kn). Step c – adoral structures derive from the differentiation 
of somatic kinetids to the left of the cytostome. (Modified from Schlegel & Eisler, 1996.)
mechanism relying on trans -acting factors that 
emanate from the parental macronucleus to influ-
ence the differentiation of the developing macro-
nuclei. This epigenetic mechanism is conceived to 
be plastic enough to have generated the molecular 
genomic diversity that we see in contemporary 
ciliates.
 Nevertheless, the number of origins of macronu-
clear division is still unsettled. Two models have 
been proposed. For Model 1, the ancestral ciliate 
had a dividing macronucleus that lost its capacity 
to divide in the karyorelicteans . For Model 2, there 
were two independent origins of macronuclear 
division from a “non-dividing” ancestor – one 
with extramacronuclear microtubules in the het-
erotrich lineage and one with intramacronuclear
 microtubules in the intramacronucleate lineage 
(Hammerschmidt et al., 1996; Lynn, 1996a). We 
currently favor Model 2, which is consistent with 
the evidence presented by Orias (1991a, 1991b). 
For it, the macronucleus of intramacronucleate 
ciliates would “regain” the capacity to use intranu-
clear microtubules that continued to be used by the 
micronucleus during its mitoses while the hetero-
trich lineage would have “re-invented” the use of 
 extranuclear microtubules to divide their macronuclei,
an invention used also by some dinoflagellates 
(Perret, Albert, Bordes, & Soyer-Gobillard, 1991). 
 In summary, what would our ancestral ciliate 
look like? It would have had a pellicle with alveoli 
underlying the plasma membrane. If the paroral 
model is used for cortical evolution, the ances-
tral ciliate would have possessed a paroral , would 
have had a ventral oral region , would have had a 
 cytopharynxsupported by postciliary microtubu-
lar ribbons , and would have undergone buccoki-
netal stomatogenesis (Schlegel & Eisler, 1996). 
Its micronucleus would have divided by using an 
intranuclear spindle of microtubules and kineto-
chores and its macronucleus would have been non-
dividing and paradiploid. 
 4.1 Taxonomic Structure 
 The ciliates are among the top five groups of pro-
tists in terms of numbers of species (Corliss, 2004). 
There are likely at least 8,000 species; this includes 
about 200 fossil forms and close to 3,000 symbiotic
species, but there is some dispute over these numbers
(see below: Life History and Ecology ). As noted 
in Chapter 1 , the ciliates are now regarded as 
a phylum divided into two major subphyla and 
eleven classes. Among the classes, the classes 
 SPIROTRICHEA , PHYLLOPHARYNGEA , and 
 OLIGOHYMENOPHOREA have over two-thirds 
of the described species. 
 Lynn (1996a) argued for the establishment of 
two subphyla based primarily on data emerg-
ing from molecular phylogenetic studies, which 
showed a strongly supported bifurcation in the 
phylogenies of ciliates based on the small subunit 
rRNA gene (e.g., Hammerschmidt et al., 1996; 
Hirt et al., 1995). This bifurcation separated post-
ciliodesmatophoran ciliates, which are placed in 
the Subphylum Postciliodesmatophora and are dis-
tinguished from all other ciliates by their somatic 
kinetids with postciliodesmata (Table 4.1). While 
the other clade is strongly supported by a variety 
of genes (see Chapter 16 ), the only morphological 
feature uniting this clade appears to be division of 
the macronucleus by intramacronuclear microtu-
bules , hence the Subphylum Intramacronucleata 
(Table 4.1) (Lynn, 1996a). The history of the macro-
system presented in the following chapters was 
developed in Chapter 1 and the distribution of sig-
nificant characters on molecular phylogenies will 
be presented in Chapter 16 . In the remainder of 
this section, we briefly characterize the 11 classes 
that are now recognized. 
 To begin with, the primary characters used to dis-
tinguish ciliate taxa reside in the cortex, although 
some non-cortical characters, such as nuclear 
features, are also important. The cortex, which is 
the main interface between the organism and its 
environment, can be divided into a somatic region 
and an oral region . The somatic region functions 
in locomotion, provides protective coverings and 
defensive responses, and enables attachment to the 
substrate. The oral region functions in the acquisi-
tion and ingestion of nutrients. Features of both 
regions, and particularly the kinds and arrange-
ments of ciliary structures, are important in the 
characterization of the major groups of ciliates. 
 The subphylum Postciliodesmatophora is 
divided into the Classes KARYORELICTEA and 
 HETEROTRICHEA (Table 4.1). Karyorelicteans , 
like Loxodes (Fig. 4.3), have non-dividing macro-
nuclei and somatic kinetids with postcilio desmata 
(Fig. 4.7) in which the postciliary microtubular 
4.1 Taxonomic Structure 93
94 4. Phylum CILIOPHORA – Conjugating, Ciliated Protists with Nuclear Dualism
Table 4.1. Classification of the Phylum Ciliophora. 
 Phylum CILIOPHORA Doflein, 1901 
 Subphylum POSTCILIODESMATOPHORA Gerassimova & 
Seravin, 1976 
 Class KARYORELICTEA Corliss, 1974 
 Order Protostomatida Small & Lynn, 1985 
 Order Loxodida Jankowski, 1980 
 Order Protoheterotrichida Nouzarède, 1977 
 Class HETEROTRICHEA Stein, 1859 
 Order Heterotrichida Stein, 1859 
 Subphylum INTRAMACRONUCLEATA Lynn, 1996 
 Class SPIROTRICHEA Bütschli, 1889 
 Subclass Protocruziidia de Puytorac, Grain, & Mignot, 1987 
 Order Protocruziida Jankowski, 1980 
 Subclass Phacodiniidia Small & Lynn, 1985 
 Order Phacodiniida Small & Lynn, 1985 
 Subclass Licnophoria Corliss, 1957 
 Order Licnophorida Corliss, 1957 
 Subclass Hypotrichia Stein, 1859 
 Order Kiitrichida Nozawa, 1941 
 Order Euplotida Small & Lynn, 1985 
 Suborder Discocephalina Wicklow, 1982 
 Suborder Euplotina Small & Lynn, 1985 
 Subclass Choreotrichia Small & Lynn, 1985 
 Order Tintinnida Kofoid & Campbell, 1929 
 Order Choreotrichida Small & Lynn, 1985 
 Suborder Leegaardiellina Laval-Peuto, Grain, & Deroux, 
 1994 
 Suborder Lohmanniellina Laval-Peuto, Grain, & Deroux, 
 1994 
 Suborder Strobilidiina Small & Lynn, 1985 
 Suborder Strombidinopsina Small & Lynn, 1985 
 Subclass Stichotrichia Small & Lynn, 1985 
 Order Stichotrichida Fauré-Fremiet, 1961 
 Order Sporadotrichida Fauré-Fremiet, 1961 
 Order Urostylida Jankowski, 1979 
 Subclass Oligotrichia Bütschli, 1887/1889 
 Order Strombidiida Petz & Foissner, 1992 
 Class ARMOPHOREA Lynn, 2004 
 Order Armophorida Jankowski, 1964 a
 Order Clevelandellida de Puytorac & Grain, 1976 
 Class LITOSTOMATEA Small & Lynn, 1981 
 Subclass Haptoria Corliss, 1974 
 Order Haptorida Corliss, 1974 
 Order Pleurostomatida Schewiakoff, 1896 
 Order Cyclotrichiida Jankowski, 1980 incertae sedis
 Subclass Trichostomatia Bütschli, 1889 
 Order Vestibuliferida de Puytorac et al., 1974 
 Order Entodiniomorphida Reichenow in Doflein & 
 Reichenow, 1929 
 Suborder Archistomatina de Puytorac et al., 1974 
 Suborder Blepharocorythina Wolska, 1971 
 Suborder Entodiniomorphina Reichenow in Doflein & 
 Reichenow, 1929 
 Order Macropodiniida order nov. a
 Class PHYLLOPHARYNGEA de Puytorac et al., 1974 
 Subclass Cyrtophoria Fauré-Fremiet in Corliss, 1956 
 Order Chlamydodontida Deroux, 1976 
 Order Dysteriida Deroux, 1976 
 Subclass Chonotrichia Wallengren, 1895 
 Order Exogemmida Jankowski, 1972 
 Order Cryptogemmida Jankowski, 1975 
 Subclass Rhynchodia Chatton & Lwoff, 1939 
 Order Hypocomatida Deroux, 1976 
 Order Rhynchodida Chatton & Lwoff, 1939 
 Subclass Suctoria Claparède & Lachmann, 1858 
 Order Exogenida Collin, 1912 
 Order Endogenida Collin, 1912 
 Order Evaginogenida Jankowski, 1978 
 Class NASSOPHOREA Small & Lynn, 1981 
 Order Synhymeniida de Puytorac et al., 1974 
 Order Nassulida Jankowski, 1967 
 Order Microthoracida Jankowski, 1967 
 Order Colpodidiida Foissner, Agatha & Berger, 2002 
 incertae sedis 
 Class COLPODEA Small & Lynn, 1981 
 Order Bryometopida Foissner, 1985 
 Order Bryophryida de Puytorac, Perez-Paniagua, & 
 Perez-Silva, 1979 
 Order Bursariomorphida Fernández-Galiano, 1978 
 Order Colpodida de Puytorac et al., 1974 
 Order Cyrtolophosidida Foissner, 1978 
 Order Sorogenida Foissner, 1985 
 Class PROSTOMATEA Schewiakoff, 1896 
 Order Prostomatida Schewiakoff, 1896 
 Order Prorodontida Corliss, 1974 
 Class PLAGIOPYLEA Small & Lynn, 1985 a
 Order Plagiopylida Jankowski, 1978 
 Order Odontostomatida Sawaya, 1940 incertae sedis 
 Class OLIGOHYMENOPHOREA de Puytorac 
 et al., 1974
 Subclass Peniculia Fauré-Fremiet in Corliss, 1956 
 Order Peniculida Fauré-Fremiet in Corliss, 1956 
 Order Urocentrida Jankowski, 1980 
 Subclass Scuticociliatia Small, 1967 
 Order Philasterida Small, 1967 
 Order Pleuronematida Fauré-Fremiet in Corliss, 1956 
 Order Thigmotrichida Chatton & Lwoff, 1922 
 Subclass Hymenostomatia Delage & Hérouard, 1896 
 Order Tetrahymenida Fauré-Fremiet in Corliss, 1956 
 Order Ophryoglenida Canella, 1964 
 Subclass Apostomatia Chatton & Lwoff, 1928 
 Order Apostomatida Chatton & Lwoff, 1928 
 Order Astomatophorida Jankowski, 1966 
 Order Pilisuctorida Jankowski, 1966 
 Subclass Peritrichia Stein, 1859 
 Order Sessilida Kahl, 1933 
 Order Mobilida Kahl, 1933 
 Subclass Astomatia Schewiakoff, 1896 
 Order Astomatida Schewiakoff, 1896 
a
 A taxon based on molecular phylogenetics, but still lacking a 
morphological synapomorphy. 
ribbons are separated by 1 + 2 microtubules 
(see Chapter 5 ). Heterotricheans , like Stentor , 
Blepharisma , and Fabrea (Figs. 4.3, 4.4), have 
macronuclei that divide by extramacro nuclear
 microtubulesand somatic kinetids with postcilio-
desmata (Fig. 4.7) in which the postciliary micro-
tubular ribbons are separated by only a single 
microtubule (see Chapter 6 ). Oral structures in 
the karyorelicteans are quite variable, ranging 
from prostomial with simple circumoral ciliature 
to ventrostomial with developed paroral and adoral 
 ciliature . Heterotricheans , like Stentor , are virtually 
all bearers of a paroral and an elaborately developed 
adoral zone of polykinetids (Figs. 4.3, 4.4). 
 The Subphylum Intramacronucleata includes 
the remaining nine classes, each of which will 
Fig. 4.3. Stylized drawings of genera representative of each class in the Phylum Ciliophora: Loxodes – Class 
 KARYORELICTEA ; Stentor – Class HETEROTRICHEA ; Protocruzia , Euplotes – Class SPIROTRICHEA ; Metopus
– Class ARMOPHOREA ; Didinium – Class LITOSTOMATEA ; Chilodonella – Class PHYLLOPHARYNGEA ;
Obertrumia – Class NASSOPHOREA ; Colpoda – Class COLPODEA ; Plagiopyla – Class PLAGIOPYLEA ; 
Holophrya – Class PROSTOMATEA ; and Tetrahymena – Class OLIGOHYMENOPHOREA 
4.1 Taxonomic Structure 95
96 4. Phylum CILIOPHORA – Conjugating, Ciliated Protists with Nuclear Dualism
Fig. 4.4. Scanning electron micrographs of ciliate diversity. A–C Class HETEROTRICHEA . Blepharisma ( A ), Fabrea
( B ), and Stentor ( C ). D–I Class SPIROTRICHEA . The oligotrich Strombidium ( D ), the tintinnids Dictyocysta ( E ) and 
Tintinnopsis ( F ), the stichotrich Stylonychia ( G ), and the hypotrichs Euplotes ( H ) and Uronychia ( I). (Micrographs 
courtesy of E. B. Small and M. Schlegel.)
be briefly characterized here (Table 4.1). Lynn 
(2004) has noted that four of the classes – the 
 LITOSTOMATEA , PHYLLOPHARYNGEA , 
 NASSOPHOREA , and COLPODEA – are 
strongly supported by both molecular and 
morpholo gical characteristics. The remaining five 
classes – the SPIROTRICHEA , ARMOPHOREA , 
 PLAGIOPYLEA , PROSTOMATEA , and 
 OLIGOHYMENOPHOREA – have less strong 
support from molecules and morphology. Two 
of these latter five, the ARMOPHOREA and 
 PLAGIOPYLEA , are only supported by molecules,
and hence called “riboclasses” (Lynn, 2004). 
 Spirotricheans , like Protocruzia , Euplotes , 
Strombidium , Dictyocysta , Tintinnopsis , Stylonychia , 
and Uronychia (Figs. 4.3, 4.4, Table 4.1), are a 
diverse group, typically having a paroral and 
a well-developed adoral zone of polykinetids . 
The class is rarely strongly supported as a clade by 
molecular phylogenetics. Most of the taxa exhibit 
somatic dikinetids with a poorly developed kineto-
desmal fibril (Fig. 4.7) and two of the included 
subclasses, the Hypotrichia and Stichotrichia , have 
compound ciliary organellar complexes called cirri 
(Figs. 4.3, 4.4, 4.7). The strongest morphological 
synapomorphy for the class is the replication band 
that occurs during macronuclear DNA S-phase 
(see Chapter 7 ). The replication band has been 
confirmed in members of all subclasses except 
the two monotypic Subclasses Protocruziidia and 
 Phacodiniidia . The phacodiniids are undoubtedly 
 spirotrichs by their placement well within the 
spirotrichean clade using the small subunit rRNA 
( SSUrRNA ) molecule (Shin et al., 2000). The situ-
ation for Protocruzia , also the only member of its 
subclass, is more uncertain as it is typically placed 
as the basal lineage in the spirotrich branch. We 
have placed protocruziids in this class because they 
are tenuously associated with it by SSUrRNA gene 
sequences (see Chapter 16 ). However, they may 
warrant separate class status in the future because 
their histone sequences are divergent from other 
spirotrichs (Bernhard & Schlegel, 1998), and they 
exhibit a unique mode of macronuclear division 
(Ammermann, 1968; Ruthmann & Hauser, 1974). 
 Armophoreans , like the armophorid Metopus
and the related clevelandellid Nyctotherus (Figs. 
4.3, 4.5, Table 4.1), are strongly supported only 
by SSUrRNA gene sequences (van Hoek et al., 
2000b). The somatic kinetids of the two subclasses 
within this class are quite different (Fig. 4.7; and see 
 Chapter 8 ). However, Villeneuve-Brachon (1940) 
speculated that these ciliates might be related to 
each other, a view later endorsed by Jankowski 
(1968b) and Albaret (1975). Both free-living and 
endosymbiotic armophoreans are found in anoxic or 
close to anoxic environments and all are presumed 
to have hydrogenosomes . Future research on armo-
phorean hydrogenosomes may reveal synapomor-
phies in their anaerobic metabolism that may more 
strongly confirm this class. 
 Litostomateans , like the haptorians Didinium
and Dileptus and the trichostomes Isotricha , 
Entodinium , and Ophryoscolex (Figs. 4.3, 4.5, Table
4.1) are strongly supported by both SSUrRNA 
gene sequences and by features of the somatic 
kinetid , which is a monokinetid with two trans-
verse ribbons (Fig. 4.7; and see Chapter 9 ). The 
two included subclasses may not be mono phyletic: 
it now appears the haptorians may be a para-
phyletic group (Strüder-Kypke, Wright, Foissner, 
Chatzinotas, & Lynn, 2006). 
 Phyllopharyngeans , like the cyrtophorians 
Chilodonella and Trithigmostoma and the suctorian
Podophrya (Figs. 4.3, 4.6, Table 4.1), form a diverse 
group, strongly supported by both SSUrRNA gene 
sequences and by features of the somatic kinetid , 
which is a somatic monokinetid that has a laterally-
directed kinetodesmal fibril and whose kineto-
somes are underlain by subkinetal micro tubules 
(Fig. 4.7; and see Chapter 10 ). A significant 
feature of the phyllopharyngean oral apparatus is a 
set of radial ribbons of microtubules that support the 
cytopharynx, the phyllae . 
 Nassophoreans , like Obertrumia (Fig. 4.3, Table 
4.1), are also strongly supported by both SSUrRNA 
gene sequences and by features of the somatic 
kinetids, which are monokinetids that can be 
linked as dikinetids by filaments near the base of 
the transverse microtubular ribbon (Fig. 4.7; and 
see Chapter 11 ). In addition, the cytopharyngeal 
basket or nasse of these ciliates exhibits a suite of 
characters not found together in any other class. 
 Colpodeans , like Colpoda (Figs. 4.3, 4.5, 
Table 4.1), are typically well supported by both 
SSUrRNA gene sequences and by features of the 
somatic kinetids, which are dikinetids whose pos-
terior kinetosomes have well-developed transverse 
microtubular ribbons extending posteriorly along 
the kinety, forming the transversodesma or LKm 
fibre (Fig. 4.7; and see Chapter 12 ). 
 Prostomateans , like Holophrya and Coleps (Figs. 
4.3, 4.5, Table 4.1), are not strongly supported by 
molecular signals, but this may in part be due to the 
low taxon sampling for this group. Their somatic 
kinetids show similarities to those of the next three 
classes (Fig. 4.7), and it is only in the details of 
their oral structures and stomatogenesis that the 
group may be distinguished (see Chapter 13 ). 
 Plagiopyleans , like Plagiopyla (Fig. 4.3, Table 
4.1), are strongly supported by SSUrRNA gene 
sequences even though the taxon sampling is low. 
Nevertheless, this is the second “ riboclass ” within 
the phylum because there is no strong synapo-
morphy for the group. The somatic kinetids are 
similar to those of the Classes PROSTOMATEA 
and OLIGOHYMENOPHOREA , showing a well-
developed anteriorly-directed kinetodesmal fibril 
and a radially-oriented transverse microtubular 
ribbon (Fig. 4.7). A remarkable recent discovery 
4.1 Taxonomic Structure 97
98 4. Phylum CILIOPHORA – Conjugating, Ciliated Protists with Nuclear Dualism
is the indication that odontostomatids , represented 
by Epalxella , may form a third clade within 
this class (Stoeck, Foissner, & Lynn, 2007) (see 
Chapter 14 ). 
 Oligohymenophoreans , like the peniculines 
Paramecium and Lembadion , the hymenostomes 
Tetrahymena and Glaucoma , and the peritrichsRhabdostyla , Vorticella , and Trichodina (Figs. 4.3, 
4.6, Table 4.1), are a speciose assemblage that is 
not strongly supported by molecular phylogenies. 
The somatic kinetids are generally similar to those 
of the previous two classes. However, the somatic 
kinetids of the subclass Peniculia are more similar 
to those of other groups, like the hypotrichs , and 
the somatic kinetids of the trochal girdle of the 
subclass Peritrichia are highly divergent (Fig. 4.7; 
see Chapter 15 ). It is really only the paroral and 
the three adoral polykinetids that all these genera 
share, affirming the 20th century view that oral features
are indeed indicative of common ancestry! 
Fig. 4.5. Scanning electron micrographs of ciliate diversity. A–B Class ARMOPHOREA . Metopus ( A ) and 
Nyctotherus ( B). C–G Class LITOSTOMATEA . The haptorians Didinium ( C ) and Dileptus ( D ) and the trichostomes 
Isotricha ( E ), Entodinium ( F ), and Ophryoscolex ( G ). H Class COLPODEA . Colpoda . I Class PROSTOMATEA . 
Coleps . (Micrographs courtesy of E. B. Small.)
 4.2 Life History and Ecology 
 The life history of a typical ciliate would include 
an asexual or vegetative cycle during which growth 
and cell division occur, a sexual cycle during which 
the exchange of genetic material occurs between 
 conjugants , and a cryptobiotic cycle during which 
the organism would typically form a resting cyst 
(Fig. 4.8). These life histories, however, are diverse 
and undoubtedly adaptive. The cyst forms are 
diverse, stimulated by a variety of conditions to 
both encyst and excyst (Bussers, 1984; Corliss 
& Esser, 1974), and a complex set of physiological
changes, for example, “switched on” by gene 
expression, accompany the development of the 
 cryptobiotic state (Gutiérrez, Martín-González, & 
Matsusaka, 1990). One adaptive variation involves 
the presence or absence of the cryptobiotic cycle 
Fig. 4.6. Scanning electron micrographs of ciliate diversity. A , B , D , E , G–I Class OLIGOHYMENOPHOREA . 
The peritrichs Rhabdostyla ( A ), Vorticella with its helically contracted stalk ( B ), and Trichodina with its suction 
disk ( D , E). The peniculines Paramecium ( G , ventral on left and dorsal on right) and Lembadion ( H ). The hymenos-
tome Glaucoma ( I ). C , F Class PHYLLOPHARYNGEA . The cyrtophorian Trithigmostoma ( C ) and the suctorian
Podophrya ( F ). (Micrographs courtesy of E. B. Small, A. H. Hofmann, and C. F. Bardele.)
4.2 Life History and Ecology 99
100 4. Phylum CILIOPHORA – Conjugating, Ciliated Protists with Nuclear Dualism
and, related to this, differences in the survivability 
of the non-encysted stages (Jackson & Berger, 
1985a, 1985b). Often, the starving trophont trans-
forms into a highly motile form, the theront, 
which may be adapted both for dispersal and very 
long survival (Fig. 4.8) (Fenchel, 1990; Nelsen & 
DeBault, 1978). 
 A common adaptive variation is the differentiation 
of macrostome cannibal forms – ciliates that differ-
entiate a new oral apparatus large enough to ingest 
their microstomatous siblings (de Puytorac, 1984b) 
(Fig. 4.8). This transformation is often induced by 
starvation, like the theront transformation mentioned 
above. More dramatic examples of adaptation are 
found in symbiotic forms, especially parasitic ones 
(Bradbury, 1996). Ichthyophthirius , the parasite of 
fish gills and epithelium, apparently lacks a typical 
resting cyst stage. Instead, it grows to a consider-
able size as a trophont on the fish host, then drops 
off the host and becomes a tomont in a reproductive 
cyst. The tomont divides to produce thousands of 
tomites , which may reside for some time within 
the cyst before breaking out to find the next host. 
Finally, hyperparasites or hyperpredators can be 
Fig. 4.7. Schematics of somatic kinetids of genera representative of each class in the Phylum Ciliophora. ( a ) Loxodes
– Class KARYORELICTEA ; ( b ) Blepharisma – Class HETEROTRICHEA ; ( c , d ) Protocruzia ( c ), Euplotes ( d ) 
– Class SPIROTRICHEA ; ( e ) Metopus – Class ARMOPHOREA ; ( f ) Balantidium – Class LITOSTOMATEA ; ( g)
Chilodonella – Class PHYLLOPHARYNGEA ; ( h ) Obertrumia – Class NASSOPHOREA ; ( i) Colpoda – Class 
 COLPODEA ; ( j ) Plagiopyla – Class PLAGIOPYLEA ; ( k ) Holophrya – Class PROSTOMATEA ; ( l) Tetrahymena
– Class OLIGOHYMENOPHOREA ; ( m ) Plagiotoma – Class SPIROTRICHEA . Kd – kinetodesmal fibril; Pc – post-
ciliary microtubular ribbon; T – transverse microtubular ribbon (from Lynn, 1981, 1991)
found among the apostome oligohymenophoreans : 
Phtorophrya insidiosa is an apostome that attacks 
other apostomes, which are themselves symbionts 
on the cuticle of crustaceans (see Fig. 3.1). 
 Ciliates are heterotrophic, exhibiting a wide 
range of feeding behaviours, and occupying a 
diversity of ecological niches (Dragesco, 1984b; 
Finlay & Fenchel, 1996). As noted above, some 
can transform to feed on their siblings, which in 
the vast majority of cases are suspension feeders 
(Fenchel, 1980a, 1980b). The “particles” removed 
from suspension can be very small, like viruses
and bacteria , moderately-sized, like various kinds 
of unicellular algae, and relatively large, like other 
ciliates. The varieties of specific prey chosen by 
ciliates in the different classes are detailed in 
Fig. 4.8. Life cycle stages of ciliates. A microstome trophont , typically feeding on bacteria, grows from the tomite
stage until it roughly doubles in size to become a dividing tomont . This vegetative or asexual cycle can repeat itself 
as long as food is present. If food becomes limiting the ciliate may transform to a macrostome trophont , which is 
a cannibal form that can eat tomites and smaller microstome trophonts or other ciliates. If food is limiting or other 
stressful environmental circumstances prevail, the ciliate may form a cyst or may transform into a theront , a rapidly 
swimming dispersal stage. If the theront does not find food, it too may encyst . In unusual circumstances, when food 
is depleted and a complementary mating type is present, the ciliates may fuse together as conjugants and undergo the 
sexual process of conjugation
4.2 Life History and Ecology 101
102 4. Phylum CILIOPHORA – Conjugating, Ciliated Protists with Nuclear Dualism
the following chapters. Bacterivorous ciliates are 
 particularly important in maintaining the “quality” of 
effluent from sewage treatment plants as they can 
reduce bacterial densities ten-fold by their feeding 
(Curds & Cockburn, 1970a, 1970b; Foissner, 
1988a; Madoni, 2003) and may even consume 
viruses (Pinheiro et al., 2007). 
 In addition to being symbionts in other organisms 
(Bradbury, 1996; Fernández-Leborans & Tato-
Porto, 2000a, 2000c; Levine, 1972; Song, 2003), a 
variety of other organisms can use ciliates as their 
host (Ball, 1969). These endosymbionts of ciliates 
can range from bacteria living in the micronucleus 
(Görtz, 1983, 1996; Hovasse, 1984b) to various spe-
cies of algae (Hovasse, 1984a; Lobban et al., 2002; 
Reisser, 1986). 
 Ciliates are distributed globally in a diversity of 
habitats where they function as important trophic 
links in a variety of food webs (Adl, 2003; Finlay 
& Fenchel, 1996; Foissner, 1987; Pierce & Turner, 
1992; Sanders & Wickham, 1993). They are found 
in the world’s oceans, in the plankton (Edwards & 
Burkhill, 1995; Lynn & Montagnes, 1991; Pierce 
& Turner, 1993; Strom, Postel, & Booth, 1993), on 
ocean shores (Agamaliev, 1971; Al-Rasheid, 1999d; 
Dragesco, 1965; Kovaleva & Golemansky, 1979), 
in ocean depths (Fenchel et al., 1995; Hausmann, 
Hülsmann, Polianski, Schade, & Weitere, 2002; 
Silver, Gowing, Brownlee, & Corliss, 1984), and 
associated with sea ice (Lee & Fenchel, 1972; Song 
& Wilbert, 2000b). They are found in a variety of 
“land-locked” waters, including freshwater bodies, 
suchas lakes (Beaver & Crisman, 1982, 1989a; 
Esteban, Finlay, Olmo, & Tyler, 2000; Taylor 
& Heynen, 1987), freshwater ponds (Finlay & 
Maberly, 2000; Taylor & Berger, 1976), rivers 
(Balazi & Matis, 2002; El Serehy & Sleigh, 1993; 
Foissner, 1997b), and streams (Madoni & Ghetti, 
1980; Taylor, 1983a), and hypersaline lagoons and 
lakes (García & Niell, 1993; Post, Borowitzka, 
Borowitzka, Mackay, & Moulton, 1983; Yasindi, 
Lynn, & Taylor, 2002). Ciliates are also recorded 
from terrestrial habitats,primarily soils and mosses 
(Buitkamp, 1977; Foissner, 1998a; Ryan et al., 
1989). Along with their association with mosses, 
ciliates can also be found in the liquid in pitcher 
plants leaves (Addicott, 1974; Rojo-Herguedas & 
Olmo, 1999) and in the axils of tropical plants, such 
as bromeliads (Foissner, Strüder-Kypke, van der 
Staay, Moon-van der Staay, & Hackstein, 2003). 
The species composition and diversity of ciliates 
have been used as bioindicators of the state of eco-
systems (e.g., Foissner, 1988a, 1997b, 1997e). 
 How have ciliates come to be distributed as 
we now see them? Bamforth (1981) reviewed the 
 factors that, in his view, explained the biogeography 
of both free-living and symbiotic species. For 
free-living species, these included characteristics 
of the autecology of the species and environmental 
conditions, such as wind patterns and ocean currents. 
For example, a variety of species are distributed by 
wind currents (Maguire, 1963b). The distribution 
of tintinnids in the Adriatic Sea , for example, is 
strongly influenced by ocean currents: still certain 
 tintinnid species, despite the absence of vertical bar-
riers to migration, can be characterized as surface, 
mesopelagic, or deep-sea forms (Krsinic & Grbec, 
2006). Symbiotic ciliates have a biogeography that 
is influenced by the historical biogeography of 
their hosts. However, even species that we do not nor-
mally imagine as symbiotic, such as Paramecium , 
can be transported in tropical snails from flower to 
flower (Maguire & Belk, 1967)! Humans may have 
also played a role in dispersing species as a variety 
of taxa has been observed in the ballast tanks of 
ocean-going vessels (Galil & Hülsmann, 1997). 
 Nevertheless, the opinions on how the diversity 
of free-living ciliates is geographically distributed 
have become polarized into two major views. On one 
hand, ciliates are considered ubiquitous and cosmo-
politan , and on the other, many ciliates are considered 
moderately endemic . Some of the controversy cent-
ers around semantics. Finlay, Esteban, and Fenchel 
(2004) have offered the following definitions to 
focus debate. They suggested that ubiquitous refer 
to the process of continuous, worldwide dispersal 
of organisms while cosmopolitan should refer to 
species that thrive wherever their habitat is found 
worldwide. Endemic refers to organisms of low 
dispersal ability and restricted distribution. Many 
years ago, Beijerinck (1913) made the argument 
for bacterial species that “everything is everywhere, 
the environment selects”. Finlay and Clarke (1999) 
and Finlay and Fenchel (1999) have taken up this 
argument for protists, emphasizing that the typically 
small size and extremely high abundances of protist 
species, including most ciliates, should permit them 
to defy barriers to migration, making allopatric 
speciation almost impossible. While it is undoubt-
edly impossible that everything be everywhere, 
 cosmopolitan species, as defined above, have been 
observed. For example, similar freshwater species 
assemblages have been found in the northern and 
southern hemispheres (Esteban et al., 2000); marine 
ciliates have been recorded in inland saline envi-
ronments (Esteban & Finlay, 2004); and allegedly 
endemic “flagship” ciliates may be more broadly 
distributed than previously thought (Esteban, Finlay, 
Charubhun, & Charubhun, 2001). Moreover, there 
is now genetic evidence to suggest that the effec-
tive population sizes of ciliates might be quite large 
(Snoke, Berendon, Barth, & Lynch, 2006), although 
there is debate on how large (Katz, Snoeyenbos-
West, & Doerder, 2006). 
 On the other side, Foissner (1999c) takes the 
view that many species show limited geographical 
distributions and low dispersal abilities. For exam-
ple, the large tropical peniculine Neobursaridium 
gigas , a “ flagship ” tropical freshwater species , was 
described over 60 years ago in Africa, and yet it has 
only been recorded in the Southern Hemisphere des-
pite intensive sampling of Northern Hemisphere 
habitats. Foissner (2005a) has described two large, 
scaled trachelophyllid haptorians that he describes 
as new “flagship” species from the Southern 
Hemisphere , to which can be added large-bodied 
species of the nassophorean Frontonia and the 
 stichotrichian Gigantothrix (Foissner, 2006). Thus, 
he argued that endemism and a biogeography may 
be properties of a much larger subset of species 
than currently reported, perhaps up to one-third. 
This proportion has been supported by a more 
extensive analysis of over 300 soil samples from 
five continents (Chao, Li, Agatha, & Foissner, 
2006), but a contrary view was provided by Finlay, 
Esteban, Clarke, and Olmo (2001) who found 
no evidence for geographic restriction of species 
across local and global scales. 
 The debate has important implications, as pointed 
out by Mitchell and Meisterfeld (2005). If species 
have global distributions, then overall diversity will 
be low; if species have more restricted distributions, 
not just due to narrow niche breadths, then overall 
diversity will be high. For ciliates, Finlay, Corliss, 
Esteban, and Fenchel (1996) concluded that there 
may only be 3,000 morphospecies of free-living 
ciliates. On the other hand, Foissner (1999c) argued 
that the number could be considerably higher, per-
haps two or three times as many, since up to 80% 
of the morphospecies at some sites were new in 
his global studies of soil ciliate species diversity. 
New species are being discovered even in regions 
of Central Europe , which have been intensively 
investigated (Foissner, Berger, Xu, & Zechmeister-
Boltenstern, 2005b). Of crucial importance to this 
debate is one’s conception of a species: “splitters” 
might conclude that there are high rates of ende-
mism while “lumpers” might conclude just the 
opposite (Mitchell & Meisterfeld). 
 Finlay et al. (1996) concluded that a pragmatic 
approach to ciliate biodiversity should be to recognize 
the “morphospecies” as the operational unit for ana-
lyses of biodiversity. They defined a morphospecies 
as “a collection of forms that all fit into a defined 
range of morphological variation – forms that, so far 
as we can tell, occupy the same ecological niche” 
(p. 232, Finlay et al.; see also Esteban & Finlay, 
2004). Given the broad physicochemical tolerances 
of many ciliates species, they suggested that niche 
breadths are probably broad, and so morphospe-
cies provide us a reasonable understanding of the 
functional role of ciliate biodiversity in ecosystems. 
There are certainly a number of studies that suggest that
subunits of morphospecies, such as sibling species 
and particular genotypes, are not geographically 
restricted (e.g., Ammerman, Schlegel, & Hellmer, 
1989; Bowers, Kroll, & Pratt, 1998; Przybos & 
Fokin, 2000; Stoeck, Przybos, & Schmidt, 1998; 
Stoeck, Przybos, Kusch, & Schmidt, 2000a). 
 In contrast, however, there is preliminary 
 evidence that some genotypes may have restricted 
ranges (Stoeck et al., 1998) or appear at particular 
seasons of the year (Doerder, Gates, Eberhardt, 
& Arslanyolu, 1995; Doerder et al., 1996). Katz 
et al. (2005) have presented convincing evidence 
that gene flow was high and diversity was low in 
planktonic spirotrichs that inhabit open coastal 
waters (e.g., Laboea ), while gene flow was high 
and diversity was also high in oligotrichs that 
inhabit ephemeralhabitats (e.g., Halteria , Meseres ). 
Furthermore, there are ecologically significant 
differences in growth rates and responses to tem-
perature between geographically distant isolates 
of species of Uronema (Pérez-Uz, 1995) and 
Urotricha (Weisse & Montagnes, 1998; Weisse 
et al., 2001), and even among clones of planktonic 
Coleps and Rimostrombidium species (Weisse & 
Rammer, 2006). Dini and Nyberg (1999) have 
shown that ecological differentiation of genotypes 
occurs at all levels among species of Euplotes – at 
4.2 Life History and Ecology 103
104 4. Phylum CILIOPHORA – Conjugating, Ciliated Protists with Nuclear Dualism
the morphospecies level, breeding system level, 
 breeding group level, and stock level. Thus, we 
must put pragmatism aside if we are to advance 
our understanding of the interactions between 
the ecological factors and the evolutionary forces 
 shaping ciliate diversity , and we must also move 
beyond the concept of morphospecies. A major 
first step would be to consider models for specia-
tion other than the allopatric one, which is clearly 
inappropriate in its classical interpretation. 
 4.3 Somatic Structures 
 The surface of ciliates is covered by a plasma 
membrane underlain by cortical alveoli (Figs. 4.9B, 
4.10A, 4.10B). In some nassophoreans, the alveoli 
can extend into the cortex as the so-called alveolo-
cysts (Fig. 4.10G). The plasma membrane is char-
acterized by a variety of intramembranous particles 
(Allen, 1978; Bardele, 1983; Hufnagel, 1992). The 
surface membranes are sites of ion channels that 
enable ciliates to sense mechanical, chemical, and 
temperature stimuli (Machemer & Teunis, 1996). 
The alveoli can be the sites of Ca 2+ ion storage 
in some ciliates, thus playing a role in modulat-
ing locomotion (Mohamed et al., 2003; Plattner, 
Diehl, Husser, & Hentschel, 2006; Stelly, Halpern, 
Nicolas, Fragu, & Adoutte, 1995). All these inputs 
to the cell are “translated” into complex behavioral 
sequences that Ricci (1990, 1996) has described 
as an ethogram – a quantitative description of the 
behavioral repertoire of a species. 
 At various points on the cell surface, typically 
associated with the emergence of cilia, parasomal
sacs or coated pits extend into the cytoplasm (Fig. 
4.10E). These sacs can be the sites of pinocytosis 
(Nilsson & Van Deurs, 1983). The membranous 
junctions of neighboring alveoli or fibrous compo-
nents associated with these boundaries (Fig. 4.10E) 
form characteristic patterned networks that are 
revealed upon silver-staining – the so-called argy-
rome (Foissner & Simonsberger, 1975a, 1975b). 
Underlying the alveoli is a fibrous or filamentous 
layer called the epiplasm , which is constructed, 
in part, by specific proteins called epiplasmins 
and articulins (Figs. 4.9B, 4.9C, 4.10B) (Coffe, 
Le Caer, Lima, & Adoutte, 1996; Huttenlauch & 
Stick, 2003; Huttenlauch, Peck, Plessmann, Weber, 
& Stick, 1998b; de Puytorac, 1984a). Genetic 
interference with some of these “cortical” genes 
can influence cell shape (Williams, 2004). 
 The most prominent features of the somatic 
surface of the vast majority of ciliates are the cilia . 
Membranous particles are also distributed in cili-
ary membranes, and undoubtedly function in the 
movement of Ca 2+ ions influencing the ciliary beat 
pattern (Machemer & Teunis, 1996; Plattner, 1975; 
Plattner et al., 2006), and these patterns of intram-
embranous particles on the cilia may characterize 
different groups of ciliates (Bardele, 1981). The 
cilia beat with a straight effective stroke and a 
curved recovery stroke, typically moving the cili-
ate through the medium, whether it be the water of 
an ocean or pond or the digestive contents of the 
intestine of a sea urchin (Sleigh & Barlow, 1982). 
The often thousands of cilia on the cell surface 
are coordinated by a hydrodynamic coupling that 
is manifested in the metachronal waves observed 
passing along the cell’s surface (Guirao & Joanny, 
2007; Sleigh, 1984, 1989). 
 The ciliary axoneme with its 9 + 2 arrangement 
of microtubules underlies the ciliary membrane. 
The major force for the ciliary beat derives from 
active sliding of the nine peripheral doublet micro-
tubules driven by dynein motors and ATP (Satir & 
Barkalow, 1996). The central pair of microtubules 
may rotate in a counterclockwise direction, viewed 
from the outside of the cell, making a complete 
rotation with every beat cycle (Omoto & Kung, 
1980). Furthermore, this defined directional rota-
tion, if true, means that when a patch of cortex is 
rotated, as sometimes happens following conjuga-
tion of Paramecium when the two cells separate, 
the cilia on the reversed patch beat in the opposite 
direction to the surrounding cortex that has a normal 
polarity (Tamm, Sonneborn, & Dippell, 1975). The 
central-pair microtubules are anchored in the axo-
some , which lies in a region of extreme complexity 
– the transition zone – between the ciliary axoneme 
and the basal body or kinetosome (Dute & Kung, 
1978). In reviews, Fokin (1994, 1995) has demon-
strated a considerable diversity in transition zone 
structures in ciliates, and suggested that transition-
zone types may characterize some of the major 
clades of ciliates. 
 The axonemal microtubules arise out of the 
 kinetosome , which is composed in most ciliates of 
nine sets of microtubular triplets. Associated with 
the ciliate kinetosome are three fibrillar associates 
– the striated kinetodesmal fibril , the transverse 
microtubular ribbon , and the postciliary microtubu-
lar ribbon (Fig. 4.10C, 4.10F, 4.10H–K). All these 
elements together – cilium, kinetosome, fibrillar 
associates – form the kinetid . Theoretical calcula-
tions support the notion that these fibrous struc-
tures function as anchors for the kinetid (Sleigh 
& Silvester, 1983). These fibrillar systems have 
 diversified in form and pattern as ciliate lineages 
have evolved, providing a variety of patterns that 
have proved useful in characterizing major clades 
(Fig. 4.7; see Taxonomic Structure above). The 
fibrillar associates extend in a various directions, 
depending upon the ciliate, and form an elaborate 
cortical cytoskeleton (Figs. 4.10D, 4.11). This 
 cytoskeleton functions both to “passively” support 
the cortex, since disassembly of the microtubules 
changes the form of the cell (Lynn & Zimmerman, 
1981), and to “actively” change cell shape, since 
active sliding of postciliary microtubular ribbons in 
the heterotrich Stentor extends the body after con-
traction (Huang & Pitelka, 1973). Electron micro-
Fig. 4.9. Ultrastructural features of ciliates. A Longitudinal section of the colpodean Colpoda steinii . Note the anterior 
 oral cavity ( OC ), macronucleus ( MA ) with its large nucleolus ( N ), and food vacuoles ( FV ) filled with bacteria ( B ).
B Section through two cortical alveoli ( A ) of the colpodean Colpoda cavicola . Note the thin epiplasmic layer (arrow) 
in this small ciliate. C Section through the pellicle of the colpodean Colpoda magna . Note the much thicker epiplas-
mic layer (arrow) in this large colpodid and the mitochondrion ( M ) with tubular cristae. D A mucocyst in the cortex 
of the colpodean Bresslaua insidiatrix
4.3 Somatic Structures 105
Fig. 4.10. Ultrastructural features of the somatic cortex of ciliates. A Section through a cortical alveolus (A) of the colpo-
dean Colpoda cavicola . Note the epiplasm underlain by overlapping ribbons of cortical microtubules. B Section through 
the pellicle of the colpodean Colpoda magna showing microtubules underlying the thicker epiplasm ( Ep ). C Cross-section 
of the somatic dikinetid of the heterotrichean Climacostomum virens , showing the transverse microtubular ribbon ( T), 
 kinetodesmal fibril ( Kd ), and postciliary microtubular ribbon ( Pc ) (from Peck, Pelvat, Bolivar, & Haller, 1975). D Section 
throughtwo cortical ridges of the oligohymenophorean Colpidium campylum . Note the longitudinal microtubules ( L ) above 
the epiplasm and the postciliary microtubules ( Pc ) underlying the epiplasm (from Lynn & Didier, 1978). E Freeze-fracture 
replica of the external faces of the inner alveolar membranes of the nassophorean Nassula citrea . Note the cilium ( C ) emerg-
ing between two alveoli , the parasomal sac ( PS ) anterior to the cilium, and in-pocketings of the alveolocysts (arrows) (see 
Fig. 4−10G) (from Eisler & Bardele, 1983). F Cross-section of the somatic dikinetid of the colpodean Colpoda magna . Note 
the single postciliary microtubule (arrow) associated with the anterior kinetosome. G Section through two adjacent alveoli 
(A ) in the cortex of the nassophorean Furgasonia blochmanni . Note that the alveoli extend into the cell in the form of alveo-
locysts ( Ac ). M – mitochondrion (from Eisler & Bardele, 1983). H Cross-section of the somatic monokinetid of the phyl-
lopharyngean Trithigmostoma steini (from Hofmann & Bardele, 1987). I Cross-section of the somatic monokinetid of the 
 oligohymenophorean Colpidium campylum (from Lynn & Didier, 1978). J Cross-section of the somatic monokinetid of the 
 prostomatean Coleps bicuspis . K Cross-section of the somatic kinetid of the litostomatean Lepidotrachelophyllum fornicis
scopy has demonstrated that several silver-staining 
methods are highly specific for these fibrillar com-
ponents (Foissner & Simonsberger, 1975a; Tellez, 
Small, Corliss, & Maugel, 1982; Zagon, 1970). 
Thus, the patterns observed after such staining pro-
cedures are grounded in the cytoskeletal structures 
of the cells, further confirming their essential use-
fulness as tools for systematists . 
 How this 9 + 2 structure evolved is still open to 
speculation. Hartman (1993) imagined its gradual 
evolution from a 3 + 0 structure, still found in some 
parasitic gregarines , like Diplauxis , by additions of 
“nucleating three’s” – from a 6 + 0 to a 9 + 0 structure 
also found in some gregarines , like Stylocephalus
(Kuriyama, Besse, Gèze, Omoto, & Schrével, 2005; 
but see Mitchell, 2004). 
 In addition to the kinetosomal fibrillar associates, 
there is a variety of other fibrous and filamentous 
components in the cortex, which also function to 
maintain or change cell shape (Adoutte & Fleury, 
1996; Allen, 1971; Garreau de Loubresse, Keryer, 
Viguès, & Beisson, 1988; de Haller, 1984a, 1984b; 
Huang & Pitelka, 1973). 
 The somatic cortex is also differentiated in many 
species to provide a means of attachment to the 
substrate. These differentiations range from special 
 thigmotactic cilia to complex attachment struc-
tures, like stalks and hooks (Fauré-Fremiet, 1984). 
Undoubtedly the most complex attachment structure 
exhibited by any ciliate is the attachment disc of 
the mobiline peritrichs , underlain by a complex set 
of fibres and denticles to form a “suction cup-like” 
structure (Fig. 4.6E) (Favard, Carasso, & Fauré-
Fremict, 1963; Hausmann & Hausmann, 1981b). 
 More details on the somatic cortex can be 
found in later chapters and in reviews by Adoutte 
and Fleury (1996), Grain (1984), Lynn (1981), 
Lynn and Corliss (1991), Paulin (1996), and de 
Puytorac (1984a). 
 4.4 Oral Structures 
 The oral region shows great diversity among 
ciliates, a reflection of the ecological diversity 
within the phylum (Figs. 4.3–4.6, 4.12). If we use 
Eisler’s model (Eisler, 1992), we assume that the 
simplest and earliest oral ciliature was a set of 
dikinetids extending along the righthand side of the 
oral region (Fig. 4.2). The oral dikinetids typically 
bear a single postciliary microtubular ribbon 
(Fig. 4.13). These microtubules often extend 
towards the cytopharynx , directing the movement 
of precursor or disc-shaped vesicles to the food 
vacuole -forming region where they fuse with the 
plasma membrane to provide membrane for the 
forming food vacuole (Allen, 1984). A typical 
oral organization has a set of adoral polykinetids 
or membranelles on the lefthand side of the oral 
region (Figs. 4.2, 4.3). These oral polykinetids are 
often initially constructed of dikinetids that assemble 
side-by-side into the organellar complexes to form 
Fig. 4.11. Schematic drawing of the somatic cortex of a ciliate illustrating the interrelationships of the various structures
4.4 Oral Structures 107
108 4. Phylum CILIOPHORA – Conjugating, Ciliated Protists with Nuclear Dualism
two rows to which a third and fourth rows may 
be added by additional kinetosomal replication 
(Fig. 4.14) (Frankel, 1989; Jerka-Dziadosz, 
1981a). The complexity and diversity of these 
 adoral polykinetids has given rise to a prolifera-
tion of terms that help to classify this diversity 
– cirromembranelle , membranelle , membranoid , 
 heteromembranelle , paramembranelle , peniculus , 
 polykinety , and quadrulus (see Chapter 2. 
Glossary for details). Further details of each of 
these structures and references to the primary 
literature are provided in the following chapters 
describing the features of each class. 
 Oral dikinetids are also found in prostomial 
forms (Fig. 4.12). In the Class PROSTOMATEA , 
ultrastructural evidence suggests that these develop 
from a paroral primordium that migrates and encircles
the cytostomial region (Huttenlauch & Bardele, 
1987). However, in the Class LITOSTOMATEA , 
Foissner and Foissner (1985, 1988) have proposed
that the “original” oral ciliature has been lost 
and the oral dikinetids that we now see have 
been derived secondarily from the “oralization” of 
somatic kinetids. This is certainly consistent with 
the orientation of these oral dikinetids, which are 
not rotated and/or inverted like those of the paroral. 
Instead, the transverse or “anterior” microtubular 
ribbons of litostome oral dikinetids extend directly 
to support the cytopharynx (Fig. 4.13). Another 
novel hypothesis has been proposed for the oral 
structures of the Class PHYLLOPHARYNGEA .
Bardele and Kurth (2001) proposed that the ances-
tral phyllopharyngean , now extinct, had also lost 
its primary oral ciliature, and had instead a sucto-
rial oral apparatus , possibly similar to present−day 
 rhynchodines . Therefore, the complex oral ciliature 
of cyrtophorine phyllopharyngeans was derived 
later from “oralization” of somatic kinetids during 
stomatogenesis. This formation of oralized somatic 
kinetosomes in litostomes and phyllopharyngeans 
has been called deuterostomisation (Bardele & 
Kurth, 2001). 
 Acquiring food can be a simple process of 
encountering edible food particles and then ingest-
ing them, a behavior that is typical of prostomial 
forms and those with simpler arrangements of oral 
Fig. 4.12. Schematic drawings illustrating the diversity of kinds of oral regions in the Phylum Ciliophora
ciliature (Fig. 4.12) (Peck, 1985; Tucker, 1968; 
Wessenberg & Antipa, 1970). Ciliates with a paro-
ral and adoral polykinetids are characterized as 
 suspension feeders . The polykinetidal cilia can be 
used to both create the current and filter particles 
out of the suspension – the so-called upstream filter 
feeders – or the current can be created by these cilia 
and the particles filtered by the cilia of the paroral 
– the so-called downstream filter feeders (Fig. 4.15)
(Fenchel, 1980a). Suspension feeding ciliates are 
typically considered to be non-selective feeders, 
“discriminating” among particles primarily on the 
basis of size (Fenchel, 1980b, 1980c). However, 
ciliates with filter-feeding oral apparati do dem-
onstrate some selectivity, so feeding and ingestion 
may be more complicated than a simple mechanical 
process (Sanders, 1988; Stoecker, 1988; Stoecker, 
Gallager, Langdon, & Davis, 1995). 
 Food or food particles are sequestered in a food 
vacuole or phagosome . The food vacuole membrane
is constructed when hundredsof disc-shaped vesicles 
fuse with the cytopharyngeal plasma membrane. 
Digestion occurs by processes typical of most 
eukaryotes, although in Paramecium an unusual set 
Fig. 4.13. Cross-sections of the paroral dikinetids of genera representative of classes in the Phylum Ciliophora. ( a ) 
Eufolliculina – Class HETEROTRICHEA . ( b ) Lepidotrachelophyllum – Class LITOSTOMATEA . ( c ) Chilodonella
– Class PHYLLOPHARYNGEA . ( d ) Woodruffia – Class COLPODEA . ( e ) Furgasonia – Class NASSOPHOREA . 
(f ) Paramecium – Class OLIGOHYMENOPHOREA . ( g ) Cyclidium – Class OLIGOHYMENOPHOREA . ( h ) 
Colpidium – Class OLIGOHYMENOPHOREA (from Lynn, 1981, 1991) 
4.4 Oral Structures 109
Fig. 4.14. Ultrastructure of the oral polykinetids of ciliates. A A square-packed oral polykinetid of the nassopho-
rean Nassula citrea with the posterior row of kinetosomes bearing postciliary microtubular ribbons ( Pc ) (from Eisler & 
Bardele, 1986). B A hexagonally-packed oral polykinetid of the oligohymenophorean Colpidium campylum . Note the 
 parasomal sacs ( Ps ) lying on either side of the three rows of kinetosomes (from Lynn & Didier, 1978). C Cross-sec-
tion through the oral cavity of C. campylum shows the three oral polykinetids separated by two cortical ridges ( R ) 
underlain by alveoli . The polykinetids are connected by filamentous connectives ( FC ) (from Lynn & Didier, 1978). 
D A rhomboid-packed oral polykinetid of the oligohymenophorean Thuricola folliculata (from Eperon & Grain, 
1983). E A slightly off square-packed oral polykinetid of the colpodean Woodruffia metabolica
of vesicles, called acidosomes , fuse with the phago-
some to first acidify the phagosomal compartment 
prior to fusion of lysosomes (Allen, 1984; Allen & 
Fok, 2000). The old food vacuoles ultimately arrive 
in the region of the cytoproct where their contents 
are expelled to the outside. Excess food vacuole 
membrane is then recycled to the cytopharyngeal 
region as disc-shaped vesicles (Allen; Allen & Fok; 
Allen & Wolf, 1974). 
 More details on the oral region and its function 
can be found in later chapters and in reviews by 
Grain (1984), de Haller (1984c), Lynn (1981), Lynn 
and Corliss (1991), Paulin (1996), de Puytorac 
(1984a), de Puytorac and Grain (1976), and Radek 
and Hausmann (1996). 
 4.5 Division and Morphogenesis 
 Ciliates can be studied as cells, and like all cells 
during the interphase period of the cell cycle, they 
can be expected to faithfully duplicate all their 
component parts (Berger, 2001; Méténier, 1984a). 
This is what is called balanced growth . Following 
this duplication, ciliates as unicellular organisms 
reproduce by cell division . Unlike animals, this 
reproductive process in ciliates is separate from 
sexual processes (see below, Nuclei, Sexuality, and 
Life Cycle ) so that months to years of asexual repro-
duction can take place between sexual events. 
 Ciliates typically divide by binary fission , in 
which the parental cell divides into two filial products, 
offspring, or progeny (Fig. 4.8). The anterior 
“daughter” cell is termed the proter and the poste-
rior “daughter” cell is called the opisthe (Chatton 
& Lwoff, 1935b). This binary fission is usually 
equal or isotomic , that is both filial products are 
the same size, but it can be unequal or anisotomic . 
 Budding is a common type of anisotomy , which is 
found especially in sessile taxa, such as suctorians 
and chonotrichs (see Chapter 10 ). Ciliate fission 
is also termed homothetogenic in the vast majority 
of cases, meaning that the cell axes of proter and 
opisthe have the same orientation or polarity: 
typically the posterior end of the proter is in 
contact with the anterior end of the opisthe. This 
is modified in two main ways. Some spirotrichs , 
especially oligotrichs and choreotrichs , undergo a 
modified division mode called enantiotropic divi-
sion : the axes of proter and opisthe of these plank-
tonic ciliates shift during cell division so that 
they have an almost opposite polarity. The second 
Fig. 4.15. Filter feeding ciliates can use their oral structures to function as a downstream filter feeder , which 
creates a current with the cilia of the oral polykinetids and captures particles in the cilia of the paroral, or as an 
 upstream filter feeder , which both creates the current and captures the particles using the cilia of the oral polykinetids .
(Redrawn after Fenchel, 1980a.)
4.5 Division and Morphogenesis 111
112 4. Phylum CILIOPHORA – Conjugating, Ciliated Protists with Nuclear Dualism
modification is found in peritrichs whose sessile 
life style is accompanied by a seemingly parallel 
type of cell division: the proter and opisthe appear 
to develop “alongside” each other with the 
fission furrow separating them “longitudinally”. 
However, Lom (1994) has argued that this may 
just be a highly modified form of homothetogenic 
fission , easily re-interpreted by assuming that the 
stalk of peritrichs arises out of the dorsal surface, 
and is not the posterior end of the cell. 
 In some ciliates, binary fission may not occur 
when the ciliate doubles all its components. For 
example, the parasitic ciliate Ichthyophthirius
may grow several orders of magnitude as a 
parasite in the epithelium of its fish host before 
dropping off, encysting, and dividing up to eight 
times sequentially to yield over 1,000 offspring. 
Even free-living ciliates, which may undergo a 
period of starvation as they disperse from one 
food patch to another, may undergo a period of 
 “unbalanced” growth , presumably as they replen-
ish and “balance” cell constituents that were dif-
ferentially more exhausted during the starvation 
period. Upon refeeding, these free-living ciliates, 
like Tetrahymena , may grow larger than the typi-
cal size during balanced growth and then, undergo 
several sequential cell divisions without interven-
ing growth (Lynn, 1975; Lynn & Tucker, 1976; 
Lynn, Montagnes, & Riggs, 1987). The process 
of multiple divisions without intervening growth 
is termed palintomy . It can occur sequentially in 
a cyst , as it does in Ichthyophthirius and some 
 colpodean ciliates, or it may occur in a linear 
fashion in highly elongate ciliates, as it does in 
some astomes. In the latter case, it can also be 
called catenulation or strobilation . 
 Cell division can be thought of as being com-
posed of two processes: division of the cytoplasm 
or cytokinesis and division of the nucleus or karyo-
kinesis , often called mitosis . Cytokinesis is most 
obvious in its last stages where a fission furrow 
appears near the equator in ciliates undergoing 
 isotomy . The furrow develops in some ciliates by 
assembly and then contraction of special kinds 
of microfilaments (Yasuda, Numata, Ohnishi, & 
Watanabe, 1980). Prior to furrow formation, special 
microtubules may appear in the cortical ridges, 
above the epiplasm, the so-called cytospindle of 
Paramecium (Sundararaman & Hanson, 1976). As 
the isthmus between the cells narrows further, the 
twisting and pulling movements of the progeny 
achieve the final separation. 
 Karyokinesis is more complicated in ciliates, 
since they have two nuclei. The typically globular 
or ellipsoid micronucleus undergoes a eukaryotic 
cell mitosis except that the nuclear membrane does 
not break down. Spindle microtubules assemble 
within the nuclear envelope and are used to separate
the sister chromatids (LaFountain & Davidson, 1980).
Raikov (1982) categorized the ciliate micro nuclear 
mitosis as a closed intranuclear orthomitosis . The 
 macronuclei of ciliates may take a variety of 
shapes and may be subdivided into apparently 
disconnected nodules. Prior to division, these 
macronuclear nodules often condense so that the 
many nodes, for example, may ultimately comprise 
a single ellipsoid body. The macronucleus then 
divides in two phases –an elongation phase and a 
constriction phase (Raikov). The elongation phase 
is likely driven by both the assembly and slid-
ing of microtubules, which may assemble inside 
the macronuclear envelope (e.g., Tucker, Beisson, 
Roche, & Cohen, 1980; Williams & Williams, 
1976) or outside the macronuclear envelope (e.g., 
Diener, Burchill, & Burton, 1983). 
 While duplication of all cell constituents occurs 
during the cell cycle, developmental biologists 
and systematists have been particularly fasci-
nated by the duplication of the cortical compo-
nents. Lynn and Corliss (1991) have separated 
this development into cortical somatogenesis and 
cortical stomatogenesis : the replication of the com-
ponents of the somatic cortex and the oral cortex, 
respectively, which are often highly co-ordinated 
 processes. Frankel (1989) has provided a detailed 
review of these processes from the perspective of 
a developmental biologist. In particular, ciliate 
 systematists have long been fascinated with the 
 ontogeny of the oral apparatus (see Chapter 1 ; 
Corliss, 1968; Fauré-Fremiet, 1950a, 1950b). 
Foissner (1996b) has provided a detailed discus-
sion of the comparative stomatogenesis of ciliates, 
but see also Tuffrau (1984). 
 Briefly, the conspicuous elements of cortical 
 somatogenesis that have attracted attention are 
the kinetosomes , contractile vacuole pores , and 
 cytoproct . Ciliates were one of the first groups 
of organisms to be investigated for replication of 
kinetosomes, demonstrating that the “daughter” 
kinetosome developed in close proximity to and in 
a well-defined relationship with the parental kine-
tosome (Allen, 1969; Dippell, 1968). This proc-
ess, now called cytotaxis or structural guidance ,
is responsible for the precise positioning of new 
cortical units (Aufderheide, Frankel, & Williams, 
1980; Frankel, 1989). Kinetosomal replication can 
occur throughout the cell cycle or be confined to 
a period close to the time of cytokinesis and be 
highly correlated with cortical stomatogenesis. 
Initiation of kinetosomal replication undoubtedly 
involves participation of gene products that diffuse 
through the cytoplasm: for example, the product 
of one such gene, sm19+ , appears to be involved 
in kinetosomal replication in Paramecium (Ruiz, 
Garreau de Loubresse, & Beisson, 1987). New 
 contractile vacuole pores (CVPs) are typically 
replicated at cell division, although in some cili-
ates with large numbers of contractile vacuoles the 
replication process may be uncoupled from cell 
division. In Tetrahymena , the proter develops new 
CVPs adjacent to somatic kineties in a predictable 
location in its posterior right quadrant, defined 
by the “ central angle ”. This angle is a manifesta-
tion of a mechanism that places the new pores in 
a roughly proportional fashion in relation to the 
total number of somatic kineties (Frankel; Nanney, 
1980; Nanney, Nyberg, Chen, & Meyer, 1980b). In 
Chilodonella species, a proportioning mechanism 
may also exist, but in this case the many contrac-
tile vacuole pores , which are distributed over the 
ventral surface, are newly placed in both proter and 
opisthe, apparently in relation to major features 
of the cortex, such as somatic kineties, the oral 
region, and the boundaries of the ventral surface. 
During this somatogenesis in Chilodonella , the old 
contractile vacuoles and their pores dedifferentiate 
and disappear (Kaczanowska, 1981; Kaczanowska, 
Wychowaniec, & Ostrowski, 1982). The old cyto-
proct , since it is typically in the posterior end of 
the cell, is inherited by the opisthe, and a new 
cytoproct develops in the appropriate position in 
the proter, presumably positioned by mechanisms 
similar to those specifying the position of CVPs. 
 In addition to these conspicuous cortical ele-
ments, we should remember that all other organelles 
are typically duplicated during each interfission 
period – mitochondria , extrusomes , Golgi apparati , 
 ribosomes , lysosomes , and all the smaller molecu-
lar constituents not visible as discrete entities by 
the microscopist. 
 Cortical stomatogenesis is literally the forma-
tion of a mouth. This process is usually the most 
conspicuous cortical ontogenetic event, since the 
oral region is generally the most obvious corti-
cal differentiation. Since the oral apparatus was 
historically considered highly significant as a taxo-
nomic feature, its development in different taxa has 
preoccupied ciliate systematists . In the chapters 
that follow, stomatogenesis of each of the classes 
is briefly characterized, based on the primary lit-
erature and the comprehensive review of Foissner 
(1996b). Stomatogenic patterns are now divided 
into five major types with subtypes – apokinetal , 
 parakinetal , buccokinetal , telokinetal , and mixoki-
netal (Corliss, 1979; Foissner, 1996b). However, all 
subtypes within a pattern of stomatogenesis should 
not be regarded as diversifying from an ancestral 
type: they should not be considered as homologous . 
Rather, the several kinds of telokinetal stomatogen-
esis probably have evolved independently in dif-
ferent classes as the morphology of these ciliates 
diversified. For example, cyrtophorids , prostomate-
ans , colpodeans , and litostomateans all exhibit dif-
ferent kinds of telokinetal stomatogenesis (Foissner, 
1996b), but molecular phylogenetic analyses clearly 
demonstrate that these classes are not closely 
related. Thus, typifying stomatogenesis using this 
classification system should be viewed only as a 
descriptive approach, enabling a systematic charac-
terization of the existing diversity. It may be of phy-
logenetic significance in relating groups within the 
classes. More complete definitions of these kinds of 
 stomatogenesis can be found in the Glossary (see 
Chapter 2 ) and in Foissner (1996b). 
 The conspicuousness of stomatogenesis has also 
attracted the attention of developmental biologists 
who have investigated a variety of its aspects. The 
primordium or anlage for the new oral apparatus 
may be positioned by mechanisms that are influ-
enced by the global properties of the cell, ensuring 
that the new oral apparatus is placed in some pro-
portional manner in relation to the whole (Frankel, 
1989; Lynn, 1977b). However, the assembly of the 
oral apparatus adds a level complexity to cortical 
developmental processes as it encompasses at least 
three levels of biological organization – organelles 
(e.g., kinetosomes ), organellar complexes (e.g., 
 membranelles , polykinetids ), and organellar systems
(e.g., the entire apparatus itself). There is a complex 
interplay of controls at these levels and different 
4.5 Division and Morphogenesis 113
114 4. Phylum CILIOPHORA – Conjugating, Ciliated Protists with Nuclear Dualism
processes that coordinate assembly at each level 
(Frankel, 1989). Furthermore, this development 
takes place in the context of the cell, so that the 
entire apparatus, both in terms of the size of each 
oral polykinetid, for example, and sometimes the 
numbers of oral polykinetids are strongly related, 
for example, to cell size (Bakowska & Jerka-
Dziadosz, 1980; Bakowska, Nelsen, & Frankel, 
1982a; Jacobson & Lynn, 1992). Thus, systema-
tists must be aware of all of these potential con-
straints on oral development when they consider 
which aspects of the process and which features 
of the differentiated oral apparatus are significant 
from a systematic perspective. For example, are the 
differences in number and size of oral polykinetids 
in two isolates of a genus evidence of different 
species or of the phenotypic plasticity of these 
components in a single species as it varies in cell 
size? Even somatic structures, such as numbers of 
somatic kineties, can be strongly correlated with 
 cell size (Lynn & Berger, 1972, 1973). 
 Finally, once the cells have separated, there are 
often significant morphogenetic processes