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175
Abstract The Class ARMOPHOREA represents 
a new assemblage of ciliates, and one of the two 
“ riboclasses” as their establishment is completely 
dependent upon small subunit rRNA gene sequences 
that showed affi nities of the two included orders 
– Armophorida and Clevelandellida. The ciliates in 
this class occupy anoxic habitats. Armophorids are 
typical of sapropelic habitats, but can be benthic or 
planktonic, while clevelandellids are endosymbi-
onts in the digestive systems of a wide variety of 
invertebrates, particularly insects, and some verte-
brates, particularly amphibians. While their somatic
dikinetids are quite different, armophoreans are all 
characterized by having their mitochondria trans-
formed to hydrogenosomes, organelles that provide 
hydrogen to the methanogenic bacterial symbionts 
of these ciliates. The oral structures of the two orders
are also divergent: membranelle-like in armophorids
and heteromembranelles in clevelandellids. Stomato-
genesis is pleurotelokinetal. The macronucleus is 
of simple form, but polytene chromosomes develop 
after conjugation and the macronuclear DNA ulti-
mately differentiates into gene-sized pieces. Armo-
phorids, because of their habitat preferences, are 
particularly good bioindicators of anoxic aquatic 
environments. 
Keywords Endosymbiont, cathetodesmal fi bril, 
 sulfureta, secant system 
 The ciliates included in this class are typically small 
to medium-sized cells. Armophoreans are free-
swimming and typically holotrichously ciliated. 
However, their body ciliation can vary from many, 
densely ciliated kineties in some clevelandellids 
to only anterior and posterior cirrus-like tufts 
in some armophorids. All species have multiple 
adoral polykinetids, ranging from around a dozen 
in some armophorids to several dozens in some 
 clevelandellids . These ciliates are very restricted 
in their distribution. Although world-wide, they 
are confined to sediments, both aquatic (Fenchel, 
1993) and terrestrial (Foissner, 1987), and the 
water column (Fenchel et al., 1995), where oxygen 
tensions are extremely reduced to absent. They are 
also found as endocommensal symbionts in the 
digestive tracts of a variety of metazoans, rang-
ing from selected invertebrates (Albaret, 1970b; 
Hackstein & Stumm, 1994) through to amphibians 
(Affa’a, Ndongo, & Granosik, 1995). Interest has 
increased in the group recently because they harbor 
endosymbiotic methanogenic bacteria , which can 
themselves produce the greenhouse gas, methane . 
There can be thousands of methanogenic bacteria 
per ciliate (van Bruggen, Stumm, & Vogels, 1983), 
producing significant quantities of methane , which 
is then liberated into the environment (Fenchel & 
Finlay, 1992; Hackstein & Stumm, 1994). 
 The name of the class, ARMOPHOREA , is 
derived from the subordinal name originally pro-
posed by Jankowski (1964a, 1964b) to include 
only the caenomorphid heterotrichs, which he 
argued derived from a Metopus -like ancestor. It 
derives from the Latin arma , meaning weapons (or 
it derives from the Latin armus meaning shoulder), 
and refers to the fact that caenomorphids have the 
appearance of military helmets (or the caenomor-
phid body is twisted to give the appearance of a 
shoulder). Although not highly similar, a number 
 Chapter 8 
 Subphylum 2. 
INTRAMACRONUCLEATA: Class 2. 
ARMOPHOREA – Sapropelibionts that 
Once Were Heterotrichs 
176 8. Subphylum 2. INTRAMACRONUCLEATA: Class 2. ARMOPHOREA
of clevelandellids have conspicuous polysaccha-
ride “skeletal” elements in their cortex, an “armor” 
of a different sort (see Albaret, 1970a). 
 Like the Class SPIROTRICHEA , there is no 
conspicuous synapomorphy for members of this 
class. They are united by the following three fea-
tures. First, they are restricted to anaerobic habitats 
and are typically dependent upon methanogenic 
symbionts . Although this is not a unique feature 
for the Class ARMOPHOREA (see particularly 
Chapter 12. Class PLAGIOPYLEA ), we predict 
that the metabolic dependence on hydrogenases 
in this class will be shown to have a common 
phylogenetic origin. Second, clevelandellids and 
 armophorids share pleurotelokinetal stomatogen-
esis of the adoral polykinetids , a feature shown 
by members of other classes (Foissner & Agatha, 
1999). Finally, they show strong similarities in the 
sequences of their small subunit rRNA (SSUrRNA) 
genes (Embley et al., 1995; Hackstein, Van Hoek, 
Leunissen, & Huynen, 2001; van Hoek, van Alen, 
Sprakel, Hackstein, & Vogels, 1998). This class 
could be called the first “ riboclass ” of ciliates, 
since its monophyly is predicted by sequence 
analyses of the SSUrRNA genes. However, we do 
not yet have a signature sequence that would char-
acterize the class. 
 8.1 Taxonomic Structure 
 The two major groups – the clevelandellids and 
 armophorids – included in this class have long 
been considered heterotrichs because of their pos-
session of multiple adoral polykinetids (Fig. 8.1). 
Corliss (1979) considered them to be suborders 
within the Order Heterotrichida . However, early 
ultrastructural analysis demonstrated clear differ-
ences between the somatic and oral structures of 
 clevelandellids and their presumed “ heterotrich ” 
relatives. The somatic dikinetids do not give rise to 
 postciliodesmata , their kinetodesmal fibril is differ-
ently shaped, and there is a prominent left-directed 
striated cathetodesmal fibril arising adjacent to the 
anterior kinetosome (Paulin, 1967; de Puytorac & 
Grain, 1969, 1976). Although there is still no pub-
lished account devoted solely to the ultrastructure 
of armophorids , Schrenk and Bardele (1991) have 
indicated differences between the somatic kinetid 
of the armophorid Metopus and those of cleve-
landellids . It does appear that Metopus may have 
 cathetodesmal-like fibrils , which do not appear 
striated. Little research has been done on members 
of this class, outside the recent interest in their 
symbiotic methanogens (see below Life History 
and Ecology ). 
 We place armophorids and clevelandellids in the 
Class ARMOPHOREA primarily based on their 
strong association derived from sequence simi-
larities of the SSUrRNA gene: the clevelandellids 
Nyctotherus and Nyctotheroides strongly group 
with the armophorids Metopus and Caenomorpha
(Embley et al., 1995; van Hoek et al., 1998). Both 
Jankowski (1968b) and Albaret (1975) have sug-
gested that clevelandellids may have derived from 
metopids through transformation of the cortical 
patterning, following a suggestion by Villeneuve-
Brachon (1940). Therefore, we place these two 
groups together and elevate them to ordinal status, 
as others have done (Lynn & Small, 1997, 2002; 
de Puytorac, 1994a; Small & Lynn, 1985). 
Following Jankowski (1964a, 1964b, 1968b) and 
Albaret (1975), we assume that the free-living 
armophorids represent the descendants of the 
ancestral group from which the endosymbiotic cleve-
landellids evolved. 
 The Order Armophorida includes two fami-
lies: the Family Metopidae and the Family 
 Caenomorphidae (Fig. 8.1). In most forms, there 
is a slight twist left to the anterior end of the 
body, which is covered by up to five perizonal or 
epistomial kineties (e.g., Fernández-Galiano & 
Fernández-Leborans, 1980; Jankowski, 1968b). 
This twist becomes pronounced in derived forms 
and in all caenomorphids (Fig. 8.1). Caenomorphids 
are not typically holotrichous, but rather may have 
the somatic ciliation restricted to anterior and pos-
terior cirrus-like tufts. 
 The Order Clevelandellida has not changed in 
composition since Corliss (1979). It contains five 
families: the Family Nyctotheridae , the Family 
 Sicuophoridae , the Family Clevelandellidae , 
the Family Inferostomatidae , and the Family 
 Nathellidae . The latter two families are mono-
typic. Clevelandellids are densely ciliated, often 
laterally compressed ciliates with many