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Handbook of Zoology Online

Handbook of Zoology/Handbuch der Zoologie
Editor-in-Chief: Schmidt-Rhaesa, Andreas

Ed. by Beutel, Rolf G. / Kristensen, Niels Peder / Leschen, Richard / Purschke, Günter / Westheide, Wilfried / Zachos, Frank

Handbook of Zoology

A Natural History of the Phyla of the Animal Kingdom

Annelida: Polychaetes

Editor(s): Wilfried Westheide, Günter Purschke

Ctenodrilidae Kennel, 1882

Harlan K. Dean, James A. Blake

Introduction

Ctenodrilidae are small polychaetes found from the intertidal zone to depths of 4.000 m. There are two subfamilies, the Ctenodrilinae with short bodies and no branchial
filaments, and the Raphidrilinae with more elongate bodies and branchial filaments dorsal to the notochaetal bundles (Hartmann-Schröder 1971, Petersen & George 1991).
Ctenodrilinae includes Ctenodrilus Claparède, 1863, with two species, and Aphropharynx Wilfert, 1974 with a single species. Raphidrilinae consists of two genera,
Raphidrilus Monticelli, 1910a and Raricirrus Hartman, 1961, each with three described species. Due to the lack of parapodia and the presence of simple chaetae emerging
directly from the body wall, Ctenodrilidae are similar to Cirratulidae and also share morphological characters with Parergodrilidae. All ctenodrilids, except Ctenodrilus,
possess simple capillaries which may be accompanied by pectinate or coarsely serrate hooks and stout spines.

Fauchald & Jumars (1979) characterized the ctenodrilids as surface deposit feeders; they have often been found associated with organically enriched sediments perhaps
feeding on diatoms and organic detritus. They may be hermaphroditic or gonochoric and may also reproduce asexually. Asexual reproduction by paratomy has been
reported in Ctenodrilis and asexual fragmentation followed by regeneration has been noted for some species of the Raphidrilinae. Viviparity by release of 7-chaetiger
swimming embryos from the female has been reported in Ctenodrilus serratus (Schmidt, 1857) (see Schmidt 1857, Rouse & Pleijel 2001) and larval development in jelly
masses has been described in what was identified as Raphidrilus nemasoma (see below) from western Canada (Qian & Chia 1989). Additionally, both sexual and asexual
dispersive forms (and epitokes) have been reported in the genus Raricirrus (see Petersen & George 1991, Dean 1995).

Morphology
External morphology

Ctenodrilids are relatively small worms with a cylindrical body not divided into regions, a rounded to conical prostomium, and without projecting parapodial lobes.
Ctenodrilus and Aphropharynx (Ctenodrilinae) are smaller with 7–12 chaetigers, a reported length of 1.5 to 8 mm and width of 0.1–3 mm. Species of Raricirrus and
Raphidrilus (Raphidrilinae) are larger with 4–35 chaetigers, a length of 1–17 mm, and a width of 0.25–0.5 mm.

The short, conical or rounded prostomium lacks antennae, palps and pigmented eyespots. A pair of dorso-lateral nuchal organs is present posteriorly on the prostomium;
those of Raricirrus maculatus were reported by Petersen & George (1991) as anterolateral patches of cilia which may have been the result of an eversion of the nuchal
organs. The peristomium is a complete ring, sometimes indistinguishable from the prostomium (and perhaps the first chaetiger) in the genera Aphropharynx and
Ctenodrilus, although Salazar-Vallejo & Rincon (1983) and Bastida-Zavala (1994) show a clear separation between these two segments in specimens of Ctenodrilus
serratus from Mexico. In these two genera, the first chaetigerous segment lies immediately behind the peristomium. In the genus Raphidrilus there are one or two
achaetous segments between the peristomium and the first chaetigerous segment, whereas in the genus Raricirrus the prostomium, peristomium, and the first chaetiger
are united dorsally.

A ciliary field has been reported ventrally on the prostomium on either side of a groove anterior to the mouth ( Rouse & Pleijel 2001, Fig. 54.2 b, c) and from the
peristomium to the end of the second chaetiger in Ctenodrilus serratus (see Wilfert 1973, Westheide 1981, Scharff 1887). Raricirrus beryli Petersen & George, 1991 has a
pair of ciliated bands extending ventrally posterior to the nuchal organs and uniting on the ventrum to form a single ciliated band on the peristomium and the first few
chaetigers (Petersen & George 1991). A ventral ciliated band is absent in R. maculatus Hartman, 1961 and R. variabilis Dean 1995 (Petersen & George 1991, Dean 1995).
Aphropharynx heterochaeta Wilfert, 1974 possesses a small ciliated field restricted to the ventrum of the prostomium anterior to the mouth opening (Wilfert 1974). A ventral
ciliated field was reported for Raphidrilus nemasoma by Qian & Chia (1989) but Petersen & George (1991) indicate that their species had a ciliated ventral field, “normal”
capillaries, and serrated multidentate chaetae. These are all characters noted for Raricirrus but not seen in Raphidrilus thus Petersen & George (1991) regard Qian & Chia’s
material as an undescribed species. There are no reported ciliated fields on the ventral side of the body for any of the described species of Raphidrilus.

There is little differentiation of chaetigerous segments along the body and the noto- and neurochaetae emerge directly from the body wall (Fig. 7.15.5.1A, B). Dorsal
branchiae occur postero-dorsal to the notochaetal bundles in the subfamily Raphidrilinae (Raphidrilus and Raricirrus); branchiae are absent in the sub-family Ctenodrilinae
(Ctenodrilus and Aphropharynx ). The posterior body is unmodified in the genera Aphropharynx, Ctenodrilus and Raphidrilus with the pygidium consisting of a simple lobe
lacking cirri and with a terminal or dorso-terminal anus. Salazar-Vallejo & Rincon (1983) mentioned a ring of cilia around the anus in specimens of Ctenodrilus serratus from
Mexico. The last 6–14 chaetigers are widened, shorter, and crowded relative to other chaetigers in species of Raricirrus (Fig. 7.15.5.1B). The simple-lobed pygidium lacks

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cirri and the terminal anus is dorsal. The wide posterior region of R. variabilis has a ventral opening (interpreted as a gonopore) with one and perhaps two pairs of
associated large reproductive spines (Dean 1995; Fig. 7.15.5.2A). There is also a pair of enlarged spines present in the wide posterior region of R. maculatus but no
gonopore was noted by Petersen & George (1991). The pygidium is simple with no associated appendages and a terminal or dorso-terminal anus.

Fig. 7.15.5.1.

A. Ctenodrilus serratus from South Africa, lateral view. B. Raricirrus variabilis from the Gulf of Mexico, lateral view. C. R. variabilis from the Gulf of Mexico, epitoke/dispersal phase (HB =
heart body, NC = natatory chaetae). Scale bars = 500 μm.

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Fig. 7.15.5.2.

A. Raricirrus variabilis from Tongue of the Ocean, Virgin Islands, reproductive stylet, ventral view (CS= coarsely serrate chaetae, PC = pectinate chaetae, RS = reproductive stylet). B. R.
variabilis from the Gulf of Mexico, pectinate chaetiger. C. R. variabilis from the Gulf of Mexico, coarsely serrate chaetae. D. Ctenodrilus serratus from South Africa, multidentate acicular
spines. Scale bars A = 50 μm, B-D = 10 μm.

Chaetae are entirely serrate capillaries in the genus Raphidrilus. Those of Raricirrus include capillaries as well as pectinate and coarsely serrate chaetae in the notochaetal
and neurochaetal bundles (Fig. 7.15.5.2A, B, C). In the genus Ctenodrilus all chaetae are stout, multidentate acicular spines (Fig. 7.15.5.2D). The chaetae of Aphropharynx
heterochaeta include capillaries in a few anterior noto- and neurochaetal bundles and acicular spines bearing several large dentations in the remaining chaetigers. Elongate
natatory setae occur in epitokous or dispersive forms of Raricirrus (Petersen & George 1991, Dean 1995).

The most obvious sensory structures in the Ctenodrilidae are the paired, oval nuchal organs located posteriorly on the prostomium adjacent to the peristomial region. Those
of Raricirrus beryli and Raphidrilus nemasoma are described as pits surrounded by cilia (Petersen & George, 1991) whereas those of Raricirrus variabilis (Dean, 1995) and
all other species of Raphidrilus (see Sokolow 1911, Magalhães et al. 2011) are described as ciliated pits. It is possible that these organs may be capable of eversion thus
explaining these differences in structure. Qian & Chia (1989) noted the presence of sensory tufts of cilia on the surface of the prostomium and postero-dorsal to the
notochaetae of juveniles of their undescribed species of Raphidrilus from British Columbia, Canada. Similar sensory tufts may also be seen on the surface of the
prostomium of a species of Ctenodrilus from Nahant, Massachusetts, USA (Rouse & Pleijel 2001, Fig. 54.2 b, c). Wilfert (1974) also described fine, short “taste hairs” on
the prostomium of Aphropharynx heterochaeta. Qian & Chia (1989) also reported the presence of pigment spots (“eyes”) on the rear of the prostomium of their undescribed
species of Raphidrilus but such eyespots are unknown in other species of Ctenodrilidae.

Internal anatomy

A pair of segmental organs, or nephridia, was reported in Ctenodrilus serratus within the first chaetiger and opening on the peristomium (Galvagni 1905, Wilfert 1973). In
Raphidrilus nemasoma the segmental organs occurred in the single achaetous segment and opened anteriorly, perhaps on the peristomium (Monticelli 1910b).

A closed circulatory system along with a dorsal heart body occurs in Ctenodrilidae. In Ctenodrilus and Aphropharynx the heart body begins in chaetiger 1 and is weakly
developed. In the genus Raphidrilus the heart body begins in chaetiger 4 (Magalhães et al. 2011) and extends for a number of chaetigers from 1–5. In Raricirrus there is
great variation in the development of the heart body from chaetigers 8–9 in R. maculatus and R. beryli and extending posteriorly for 6–15 chaetigers to R. variabilis the
heart body begins in chaetiger 4–6 and extends posteriorly for 4–11 chaetigers in the benthic forms and 8–16 in epitokous forms (Dean 1995; Fig. 7.15.5.2).

The coelom of Ctenodrilus serratus was found to be only partially covered by peritoneum with the muscles of the outer body wall and the parapodial muscle bundles
uncovered by epithelial cells but with flat extensions of cytoplasm from the outer muscle cells (Franzen 1980).

The gut of ctenodrilids is a straight tube which is somewhat widened in midbody segments with an anterior soft pharyngeal structure. Using transmission electron
microscopy, Purschke (1988) found that the pharynx of Ctenodrilus serratus consists of a bulbous muscle with a tongue-like structure made up of lateral folds. Based upon
light microscopy, this type of bulbous muscle system is believed to be homologous to those of other Ctenodrilidae, Terebellidae, Cirratulidae, Orbiniidae, Flabelligeridae,
Poecilochaetidae, Spionidae and Poeobiidae. This type of pharyngeal structure is believed to be used in the scraping of food particles from the substrate (Purschke 1988).

Gelder & Palmer (1976) analyzed the nervous system of Ctenodrilus serratus and found it to consist of central, stomatogastric and peripheral segments. The central

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system consists of a cerebral ganglion (brain), a circumesophageal loop, and two ventral nerve cords. The stomatogastric portion consists of a small stomodeal loop, which
sends branches to form a nerve plexus along the gut, and a loop around the eversible pharynx. The peripheral nervous system consists of four pairs of nerves per segment
emerging from the ventral nerve cords, these join to a pair of longitudinal epidermal nerve cords dorsally, and there is also a small nephridial plexus. These authors pointed
out the similarities of this nervous system with those described for Cirratulus and Dodecaceria in Cirratulidae as evidence of the affinities between these two families.

Habitat and geographic distribution

Ctenodrilids range from the intertidal to the deep sea; many species appear to be opportunistic and often associated with organically enriched sediments. Raricirrus beryli
was originally described from upper slope sediments near oil rigs at depths of 200–500 m in the North Sea (Petersen & George 1991), later on the Norwegian continental
shelf (Ugland et al. 2008), and more recently as a colonizer on organically enriched sediments in experiments near mud volcanos in the Bay of Cádiz ( Cunha et al. 2013).
R. variabilis is known from an experimental wood island placed at 4.000 m off St Croix in the Caribbean Sea and more recently from soft continental slope sediments, ca.
800 m, in the Gulf of Mexico near an operating oil and gas platform off Louisiana (Blake, unpublished data; Fig. 7.15.5.1). Raricirrus maculatus is known from organically
enriched sediments off the California (USA) coast. Aphropharynx heterochaeta has only been collected from a museum aquarium in Germany and Ctenodrilus serratus has
often been collected from aquaria and running seawater tables of marine laboratories (Wilfert 1973, Hartmann-Schröder 1996). Ctenodrilus serratus has also been reported
to occur as a commensal on sea urchins (Fauchald & Jumars 1979, Bastida-Zavala 1994). The undescribed species of Raphidrilus of Qian & Chia (1989) was collected
from decaying Zostera roots on Vancouver Island, Canada. Ctenodrilus paucidentatus Ben-Eliahu, 1979 has only been reported from the Gulf of Aqaba (Gulf of Elat), Israel
(Ben-Eliahu 1979). Raphidrilus nemasoma is known from the Italian Mediterranean and Adriatic Seas, Raphidrilus harperi Magalhães et al., 2011 from Florida, and
Raphidrilus hawaiiensis Magalhães et al., 2011 from Hawaii, USA (Magalhães et al., 2011).

Ctenodrilus serratus has been considered a cosmopolitan species (Salazar-Vallejo & Rincon 1983), thought to perhaps be the result of its abilities for asexual reproduction.
Westheide et al. (2003) analyzed internal transcribed spacers (ITS) and 5.8S DNA and found that there were no significant molecular differences between populations from
northern Europe and the eastern United States perhaps indicating a significant transatlantic exchange of genetic material. These authors did note some differences in ITS
sequences in a population from Bermuda perhaps due to the geographic isolation of that site.

Biology and ecology

Feeding

Ctenodrilids were characterized as motile herbivores and surface deposit feeders by Fauchald & Jumars (1979), Jumars et al. (2015), updated this by classifying
ctenodrilids as highly selective feeders on microbial films and rich organic debris. Wilfert (1973) maintained laboratory populations of Ctenodrilus serratus feeding on the
diatom Dunaliella sp. and his observations indicated that they used their lower lip (and perhaps tongue-like organ) to feed on benthic diatoms and detritus in the field
(Wilfert 1973), Purschke (1988) described the pharyngeal apparatus of C. serratus as consisting of a muscular bulb with associated glandular cells and an overlying
laterally attached tongue-like organ. Feeding is believed to occur by extrusion of the tongue-like organ and bulb followed by intake of detritus or algal cells. Moore (1991)
analyzed the gut contents of Raricirrus beryli in the North Sea and found the median grain size of ingested material to be greater than that of the surrounding sediments
indicating they were feeding selectively on sediment grains and suggested they were utilizing the associated organic material on these particles. Based on Moore’s
observations, Jumars et al. (2015) suspected that R. beryli was highly selective for organic coatings, possibly diatoms found on grains of sediment at the sediment-water
interface. Petersen et al. (2012) collected specimens of R. beryli from a whale fall in the Kosterfjord, Sweden and found sulfur-oxidizing chemosynthetic bacteria, similar to
those found in bathymodiolin mussels from hydrothermal vents and cold seeps in the surface mucous layer of the worms. The association between these bacteria and the
ctenodrilid is unclear but it is possible that there is a symbiotic association between these organisms in high organic habitats.

Environmental aspects

Most of the ctenodrilids are associated with sediments having high organic content (Petersen & George 1991, Dean 1995, Magalhães et al. 2011). Ctenodrilus serratus has
been used as a laboratory test organism for metals, petrochemicals and polluted sediments and indicated that this species was relatively more tolerant of chromium,
cadmium and zinc in terms of the suppression of reproduction Moore (1991) (Reish & Gerlinger 1997). found dense populations of Raricirrus beryli present in sediments
contaminated by hydrocarbons in the North Sea and suggested that this species could be used as a pollution indicator. Ugland et al. (2008) later included this species as
an indicator species in an environmental stress index for the oilfields of the Norwegian continental shelf. The heart body (Fig. 7.15.5.2) has been thought to perhaps be a
site of blood cell production. However, Vovelle et al. (1994) analyzed the heart body of specimens of R. beryli from the North Sea and found levels of iron (among other
metals) correlated with proximity to offshore oil platforms. Perhaps the heart body may be involved in the detoxification of pollutants such as iron rather than hematopoiesis
thus explaining its ability to thrive in these polluted environments.

Reproduction, development and life cycles

Reproduction and development

Ctenodrilidae exhibit a variety of reproductive strategies including both asexual and sexual reproduction. Paratomic asexual reproduction by formation of chains of
differentiated individuals, followed by separation, has been reported for Ctenodrilinae such as Ctenodrilus serratus (see Kennel 1882, Monticelli 1907, Peters 1923, Hartman
1944) and Aphropharynx heterochaeta (see Wilfert 1974). Ben-Eliahu (1976) saw no indication of asexual reproduction in C. paucidentatus. In the Raphidrilinae asexual
reproduction by fragmentation followed by regeneration (architomy) is known for Raphidrilus nemasoma , R. hawaiiensis, Raricirrus beryli, and R. maculatus (Monticelli
1910a, Petersen & George 1991, Magalhães et al 2011). No evidence of asexual reproduction has been observed in Raphidrilus sp. from British Columbia, R. harperi from
Hawaii, and Raricirris variabilis from deep-water off St. Croix (Qian & Chia 1989, Dean 1995, Magalhães et al. 2011).

Petersen & George (1991) observed what they termed dispersal forms in Raricirrus maculatus and R. beryli, distinguishing these from morphologically similar sexual
epitokes which contain well developed gametes. These dispersive forms are smaller than the benthic forms, possess elongate capillary chaetae two to four times longer
than the body width, and appeared to have been formed by asexual fragmentation. Dean (1995) described two specimens of R. variabilis with elongate capillaries as
epitokes but since they contained no gametes they are more correctly be regarded as dispersive stages although there was no evidence of asexual fragmentation (Fig.
7.15.5.1C). The elongate capillaries of these asexual dispersive forms most likely allow for greater dispersive capabilities.

Sexual reproductive modes in the ctenodrilids include gonochoric forms as well as protandric and simultaneous hermaphrodites. Within Ctenodrilinae, Ctenodrilus serratus
has generally been reported as reproducing asexually but Monticelli (1907) first noted female individuals with developing larvae moving freely within the coelom. This
viviparous reproduction has also been described by Rouse & Pleijel (2001) who reported male individuals of C. serratus from Belize ranging from embryos to the 7-chaetiger
stage in the body coelom of females; these 7-chaetiger specimens were released into the water column as ciliated, swimming juveniles. Bastida-Zavala (1994) also noted
the occurrence of a simultaneously hermaphroditic individual of C. serratus from Pacific Mexico. Sexual reproduction was not observed in C. paucidentatus by Ben-Eliahu
(1976) nor did Wilfert (1974) observe any evidence of sexual reproduction in his description of Aphropharynx heterochaeta.

Sexual reproduction within the Raphidrilinae is somewhat more complicated than that reported for the Ctenodrilinae. In Monticelli’s (1910b) description of Raphidrilus

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nemasoma, the type species of the genus, he reported both male and female individuals as well as protandric hermaphrodites and noted the presence of robust, weakly
curved spines on chaetigers 5–9 of the males. The type material has been lost, no specimens could be found in the Gulf of Naples type locality (Petersen & George 1991),
and Magalhães et al. (2011) found no such spines on any specimens collected from the nearby Adriatic Sea. Magalhães et al. (2011) also found no such reproductive
spines on R. harperi or R. hawaiiensis and none were mentioned in the undescribed species of Raphidrilus of Qian & Chia (1989). Therefore, sexual dimorphism as implied
by Monticelli (1910b) for Raphidrilus has not been confirmed in subsequent investigations.

Monticelli (1910b), and later Sokolow (1911), described viviparity in Raphidrilus nemasoma noting the presence of segmented larvae within the maternal coelom and the
subsequent release of juveniles from the body cavity. Magalhães et al. (2011) also found achaetous worm-like organisms within the body cavity of specimens of R. harperi
and R. hawaiiensis but no sexually mature specimens of these ctenodrilid species were seen and it is possible that these organisms were actually intracoelomic gregarine
parasites. The undescribed species of Raphidrilus of Qian & Chia (1989) was found to lay gelatinous egg masses that reached the blastula stage after about 48 hours and
the trochophore stage by day 3. After about 11 days, 3–4 chaetiger young emerged from the egg mass and developed into juveniles about two weeks after emergence.

Reproduction is also varied in the three known species of Raricirrus. Petersen & George (1991) reviewed sexual reproduction in R. maculatus, and R. beryli and reported
mature male and female forms in both species. Some, but not all specimens of R. maculatus with gametes had large hooked spines on one or two anterior segments of the
enlarged posterior body region and coarsely serrated noto- and neurochaetae in subsequent posterior body segments. They also found fragments containing eggs in their
material and saw sperm platelets in a specimen from California but these lacked the elongate chaetae of epitokes so are considered dispersive forms. No female epitokes
were found in R. beryli (Petersen & George, 1991) but they did find a few male epitokes similar in size to the benthic form with elongate (1.5× body width) “natatory”
chaetae. Dean (1995) found simultaneous hermaphroditic individuals of R. variabilis from deep sea wood islands with hooked spines on the first one or two segments of the
widened posterior end and coarsely serrated chaetae in subsequent posterior segments similarly to the arrangement reported for R. maculatus (Fig. 7.15.5.1C).
Additionally, R. variabilis had a ventral, medial pore located anteriorly in the broad posterior region and a reproductive stylet associated with a sac containing what appeared
to be sperm, 5–9 chaetigers anterior to this gonopore. Epitokes with a wider body and a greater number of chaetigers than the benthic form were also present and
possessed elongate capillaries and oocytes.

Irvine et al. (1997) recovered homeobox gene fragments from the chaetopterid polychaete Chaetopterus variopedatus, which has three highly differentiated body regions,
and from Ctenodrilus serratus, which has little variability in body segments. These homeobox genes have been shown to act in the shifts in morphology along the anterior-
posterior axis of various metazoans. Their results indicate that these worms share the same complement of homeobox genes despite their differences in morphology. This
perhaps indicates that it is the regulation of Hox gene expression which may explain the differences in segmental diversity between the two polychaete taxa.

Phylogeny and taxonomy

Morphological studies

The first ctenodrilid was described by Schmidt (1857) as Parthenope serrata Schmidt, 1857, later placed in the genus Ctenodrilus by Claparède (1863), who considered the
species to be in the Oligochaeta. Kennel (1882) more fully described Ctenodrilus pardalis Claparède, 1863 (later placed in synonymy with C. serratus and established the
family Ctenodrilidae but was unclear as to its affinities. Mesnil & Caullery (1897) and Caullery & Mesnil (1898) reviewed C. serratus (Schmidt, 1857) and C. monostylos
Zeppelin, 1883 (later transferred to the genus Zeppelina) and compared them to specimens of the cirratulid genus Dodecaceria. Caullery & Mesnil (1898) pointed out that
the lack of tentacular cirri was a negative character, likely the result of regression, and therefore could not be used as a family-defining character and they referred
Ctenodrilus to the Cirratulidae.

Monticelli (1910a) described Raphidrilus nemasoma Monticelli, 1910a and included it within Ctenodrilidae, separate from Cirratulidae. Raphidrilus was characterized as
possessing filiform branchiae dorsal to the notochaetal bundles and having only one type of chaeta (simple, elongate or spinous) in each bundle. Nevertheless, later
workers (Fauvel 1927, Day 1967) included the ctenodrilids as a subfamily of Cirratulidae. Hartman (1944) reported and described Ctenodrilus serratus from the California
coast and regarded the family Ctenodrilidae as distinct from the Cirratulidae based on ciliation of the prostomium and ventrum of the first segment, the reduced number of
body segments, the lack of tentacular cirri, and simple chaetal fascicles. Hartman (1961) later described Raricirrus maculatus Hartman, 1961 and considered it to be in
Cirratulidae despite its lack of tentacular cirri and the branchiae being limited to a few anterior chaetigers. Its larger number of chaetigers (about 22) and the presence of
branchiae precluded her from including it in Ctenodrilidae with Ctenodrilus. While Ctenodrilidae and Cirratulidae are very similar morphologically it has been difficult to unite
them into a single family given that the dorsal tentacles of Cirratulidae are lacking in ctenodrilids.

Dales (1963) recognized Ctenodrilidae as a separate family and included both Ctenodrilidae and Cirratulidae within Cirratulida. Hartmann-Schröder (1971) also considered
Ctenodrilidae to be a separate family and included it in Drilomorpha, a group which also included Cirratulidae, Arenicolidae, Capitellidae, and perhaps Maldanidae and
Sternaspidae. Fauchald (1977), and later Hartmann-Schröder (1996), placed Ctenodrilidae within an order separate from Cirratulidae, Ctenodrilida, along with Parergodrilidae
but with no explanation. The small body form and the lack of parapodia and anterior appendages in Parergodrilidae is similar to that of Ctenodrilus, but the single pair of
chaetal bundles on each segment and the presence of furcate chaetae or stout spines are not present in Ctenodrilus.

Rouse & Fauchald (1997) were among the first to apply cladistic analysis to understanding the relationships among polychaete families. In coding the characters for
Ctenodrilidae they used simple dorsal branchiae and dentate hooks as the plesiomorphic character states of a Raricirrus/Raphidrilus-like ctenodrilid. Both of these
character states are absent in Ctenodrilus. In their unweighted presence/absence analysis, Ctenodrilidae were grouped with Aeolosomatidae, Parerogodrilidae and
Potamodrilidae while in the weighted presence/absence analysis they were grouped with Acrocirridae, Cirratulidae, Fauveliopsidae, Flabelligeridae, Poeobiidae and
Sternaspidae. Using a multistate data matrix the position of Ctenodrilidae was unresolved. Rouse & Fauchald (1997) established a new classification for the polychaetes
based on a cladistic analysis of a restricted number of families which did not include Ctenodrilidae. Ctenodrilidae were included in Canalipalpata in the clade Terebellida
along with Acrocirridae, Flabelligeridae, Cirratulidae, Alvinellidae, Ampharetidae, Pectinariidae, Terebellidae and Trichobranchidae despite their lacking grooved palps or
tentacles, a synapomorphy of the Canalipalpata.

In a later more focused look at polychaete systematics, Rouse & Pleijel (2003) used Cirratuliformia (various families which had been associated with Cirratulidae) as an
example of paraphyly in polychaetes. Their morphologically based strict consensus cladogram resulted in no clear relationships between Ctenodrilidae, Cirratulidae, and
other families and Ctenodrilidae, Cirratulidae, Fauveliopsidae, Flabelligeridae were not considered monophyletic. They proposed that perhaps Acrocirridae, Ctenodrilidae,
Fauveliopsidae, Flabelligeridae, Flotidae, Poeobiidae and Sternaspidae could all be included within the single family Cirratulidae. They included both Ctenodrilus and
Raphidrilus in their analyses and these two genera were not found within the same clade nor were any of the three species of Cirratulidae. However, only two of the 15
characters utilized in this analysis were appropriate for discerning relationships between the members of Ctenodrilidae and Cirratulidae: 1) branchial occurrence/distribution
and 2) the presence/absence of tentacles. While differentiating these two families from other taxa included in the analysis between Cirratulidae and Ctenodrilidae were not
the main focus of this study, the relationships between and within these two families were not addressed by their analysis.

Salazar-Vallejo et al. (2008) included Cirratulidae and Ctenodrilidae as outgroups in their analysis of phylogenetic affinities of Flabelligeridae. While not the focus of the

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analysis, Ctenodrilidae, Cirratulidae and Fauveliopsidae formed a clade based mainly upon the presence of simple falcate hooks and a smooth epidermis. Ctenodrilus and
Raricirrus showed close affinities to each other based upon the presence of monoserially denticulate neurochaetae. They differed in this analysis only by the median body
segments being scored as indistinct in Ctenodrilus and distinct in Raricirrus. The absence of branchiae in Ctenodrilus was not a character state in the analysis. The
emphasis of this study was the phylogenetic affinities of Flabelligeridae and only eight of the 36 characters included in the analysis were pertinent to the relationships
between members of the out group.

Molecular studies

As with morphological relationships between Ctenodrilidae and other polychaete families, molecular efforts have also often been inconclusive. Bleidorn et al. (2003)
examined 18S rDNA sequences in their analysis of relationships between polychaetes and found that Ctenodrilus serratus had a close affinity with three genera of
Cirratulidae with its closest affinity being with two species of Dodecaceria. Bayesian analysis of the consensus tree also showed a supported sister group relationship
between this clade and three species of Scalibregmatidae. In the Struck & Purschke (2005) analysis of relationships between the Potamodrilidae and the Aeolosomatidae
based on 18S rDNA, they found a close relationship between C. serratus and the Cirratulidae, especially with species of Dodecaceria. While unsupported by bootstrap
values, the Cirratulidae/Ctenodrilidae clade was most closely associated with Opheliidae. Rousset et al. (2007) added sequences from the D1 region of 28S rDNA, Histone
3 and mitochondrial 16S rDNA to the 18S rDNA sequences and again noted a well-supported relationship with C. serratus and the six species of Cirratulids included in the
study with closest kinship to the genus Dodecaceria. A strict consensus tree of the complete data set aligned Ctenodrilidae and Cirratulidae with Capitellidae and the
Echiuran genus Bonellia but jackknife values showed no support for these associations. Struck et al. (2008) assessed both saturation and homoplasy in 18S and 28S r
DNA sequences in order to exclude saturated nucleotide positions from their analysis. Whether excluding all possibly saturated sites or ambiguously aligned positions, C.
serratus showed close affinities to the single species of cirratulid included in their analysis, Cirratulus spectabilis (Kinberg, 1866), while associations with Flabelligeridae
and Poeobiidae, included in the Cirriformia were unsupported. Zrzavý et al. (2009) used both morphological data and six molecular partitions and found that Ctenodrilus
serratus was associated with the only cirratulid included in the analysis, “Cirratulidae”. An association of these two species with Aberranta and Saccocirrus lacked
bootstrap/Bremer support.

Osborn & Rouse (2010) analyzed the molecular phylogeny of Acrocirridae and Flabelligeridae using 18S, 28S, 16S, Cytochrome oxidase 1 and Cytochrome B sequences
and used six species of Cirratulidae and Ctenodrilus serratus as outgroups for the analyses. These results allowed some indication of the associations between C. serratus
and five genera of Cirratulidae. Using 18S and 28s rDNA sequences and morphological data C. serratus was clearly included within Cirratulidae and strongly associated
with the cirratulid genera Dodecaceria and Aphelochaeta.

Phylogenetic conclusions

Morphologically based attempts to resolve the relationships of the Ctenodrilidae to other polychaetes have been inconclusive. Associated families have included such taxa
as Arenicolidae, Capitellidae, Maldanidae, Sternaspidae, and Parergodrilidae but the most frequently associated group to Ctenodrilidae is Cirratulidae. Morphological
cladistic analyses which have included Ctenodrilidae are few and often they have been included only as outgroups. A major problem is the lack of dorsal tentacles in
Ctenodrilidae thus making it difficult to justify their inclusion in Cirratulidae.

Molecular studies of ctenodrilid affinities are also few and results have been variable. Unsupported affinities have been indicated between Ctenodrilidae and Flabelligeridae,
Capitellidae, Potamodrilidae, Aeolosomatidae, Poeobiidae, Polygordiidae, Saccocirridae and Aberranta among others. In all cases, however, there is a strongly supported
relationship between Ctenodrilus serratus and members of Cirratulidae, especially with the genus Dodecaceria. George & Petersen (1991), however, suggested that
Dodecaceria appeared to be more closely related to Ctenodrilidae than Cirratulidae. The analysis by Osborne & Rouse (2010) included several genera of Cirratulidae and
indicated not only an affinity between Ctenodrilus and Dodecaceria but also with the genus Aphelochaeta. There is strong support for the inclusion of C. serratus in
Cirratulidae but there have been no molecular studies of the other genera in Ctenodrilidae such as Raricirrus and Raphidrilus so the abandonment of the ctenodrilid taxon
may be premature.

Taxonomic history

Schmidt (1857) described the first ctenodrilid as Parthenope serrata from the Mediterranean Sea. Claparède (1863) recognized that Parthenope was pre-=occupied and re-
named the homonym Ctenodrilus for Ctenodrilus serratus (Schmidt 1857), a small bodied species lacking parapodia, tentacules and branchiae but with multidentate hooks.
Kennel (1882) more fully described C. pardalis Claparède, 1863 (later placed in synonymy with C. serratus) and established the family Ctenodrilidae to include Ctenodrilus
and another genus and species proposed by Vaillant (1890), Zeppelina monostyla (Zeppelin, 1883). The genus Zeppelina differed from Ctenodrilus by the presence of what
was believed to be an unpaired medio-dorsal tentacule but later descriptions of species in this genus included those with paired lateral tentacules. George & Petersen
(1991) reviewed the genus Zepellina and found that in seven of the eight then recognized species, including the type species Z. monostyla, this tentacule was actually one
of a pair of tentacules similar to those that occur in the cirratulid genus Dodecaceria (the eighth species was a specimen of the ctenodrilid Raphidrilus nemasoma) and the
genus Zepellina was therefore abandoned and effectively synonymized with Dodecaceria. A second species of Ctenodrilus, C. paucidentatus, was described by Ben-Eliahu
(1976) from the Gulf of Elat (Gulf of Aqaba), Israel, differing from C. serratus by only slight differences in chaetal morphology. Westheide et al. (2003) pointed out that the
number of subdistal teeth on the chaetae of C. serratus was highly variable, even in a single individual, suggesting that C. paucidentatus might not be a valid species.
Another species, C. parvulus Scharff, 1887, continues to appear in the literature but it is clearly not a ctenodrilid and is most likely a regenerating posterior fragment of a
Dodecaceria, similar to that described by Gibson & Clark (1976) for D. caulleryi Dehorne, 1933 (later synonymized with D. concharum Örsted, 1843 by George & Petersen
(1991)). In fact, Galvagni (1905) reported the presence of paired tentacules in specimens identified as C. parvulus and indicated that this species was synonymous with
Zeppelina monostyla (Zeppelin, 1883) (which was later identified as a species of Dodecaceria by George & Petersen (1991)). The genus Aphropharynx with the single
species A. heterochaeta, was collected from a museum aquarium in Germany and described by Wilfert (1974). This genus is similar to Ctenodrilus but differs in the
presence of capillary chaetae anteriorly and finely toothed chaetae in addition to coarse multidentate chaetae in subsequent chaetigers.

Monticelli (1910a, b) described Raphidrilus nemasoma Monticelli, 1910 from the Gulf of Naples and referred it to the family Ctenodrilidae, and at the same time, established
the subfamily Heterodrilinae. This subfamily included Zeppelina and Raphidrilus both with a more elongate body form (15–18 chaetigers) than those of Ctenodrilus and with
branchiae or tentacules. Raphidrilus was characterized as possessing filiform branchiae dorsal to the notochaetal bundles and having only one type of chaeta, simple,
elongate or spinous, in each chaetal bundle. Heterodrilinae, however, is an invalid name as there is no polychaete genus from which to derive the family level name;
Hartmann-Schröder (1971) renamed the subfamily as the Raphidrilinae in which she included R. nemasoma and the later to be abandoned genus Zeppelina (George &
Petersen 1991). The Raphidrilinae were longer bodied (>15 segments), possessed branchiae, and capillary chaetae as well as serrate chaetae and spines. Magalhães et al.
(2011) described two new species of Raphidrilus, R. harperi Magalhães, Bailey-Brock & Davenport, 2011, from Venice, Florida (USA) and R. hawaiiensis Magalhães,
Bailey-Brock & Davenport, 2011, from shallow water in Hawaii. Petersen & George (1991) had earlier emended the subfamily Raphidrilinae to include species with pectinate
and coarsely serrate chaetae thus incorporating the genus Raricirrus, described by Hartman (1961) for R. maculatus collected off the coast of California. At the time,
Hartman (1961) considered Raricirrus to belong to the Cirratulidae despite its lack of tentacules and limited number of anterior branchiae; the greater number of chaetigers
(about 22) and the presence of branchiae precluded her, at the time, from including it in the Ctenodrilidae with Ctenodrilus. Petersen & George (1991) redescribed R.

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maculatus and described a new species from the North Sea, R. beryli Petersen & George, 1991. Dean (1995) later described Raricirrus variabilis from experimental wood
islands deployed off the Bahamas at 4.000 m depth.

Current taxonomy

Ctenodrilidae Kennel, 1882

Type genus: Ctenodrilus Claparède, 1863

Diagnosis: Small polychaetes with few to many distinct segments. Prostomium and peristomium lacking appendages, tentacular cirri absent. Partially eversible pharynx
simple with a ventral muscular bulb. Ciliated nuchal organs present. Simple branchiae present or absent. All chaetigers biramous, parapodial lobes lacking with chaetae
emerging directly from body wall. Chaetae simple, include capillaries, pectinate, and coarsely serrate forms; reproductive spines in some species. Dioecious or
hermaphroditic as well as both sexual and asexual forms present.

Ctenodrilinae Kennel, 1882

Diagnosis: Short-bodied Ctenodrilidae with 7–12 segments as adults, branchiae lacking. Chaetae include simple capillaries and coarsely serrate spines.

Ctenodrilus Kennel, 1882

Diagnosis: Short bodied forms with only coarsely serrate noto- and neurochaetae, branchiae lacking.

Type species: Ctenodrilus serratus (Schmidt, 1857)

3 Species:

Ctenodrilus paucidentatus Ben-Eliahu, 1976; intertidal vermetid reef, Gulf of Elat, Israel.

Ctenodrilus serratus (Schmidt, 1857); considered cosmopolitan, intertidal to shallow subtidal waters, seawater aquaria.

Ctenodrilus parvulus Scharff, 1887 questionable species (see above); collected from a seawater aquarium in England.

Aphropharynx Wilfert, 1974

Diagnosis: Short bodied forms with simple capillary and finely serrate chaetae anteriorly, coarsely serrate chaetae posteriorly, branchiae lacking.

Type species: Aphropharynx heterochaeta Wilfert, 1974 (only species, monotypic); add distribution, depth.

Raphidrilinae Hartmann-Schröder, 1971

Diagnosis: Ctenodrilidae with up to 40 chaetigers as adults, with simple branchiae on most segments. Chaetae include capillaries, simple pectinate, coarsely serrate forms,
and spines.

Raphidrilus Monticelli, 1910a

Type species: Raphidrilus nemasoma Monticelli, 1910a

Diagnosis: Peristomium distinct from prostomium dorsally and ventrally, first one or two segments achaetous. Nuchal organs ciliated pits. Heart body from chaetiger 4.
Serrate capillaries throughout. Reproduction sexual and asexual.

4 Species:

Raphidrilus harperi Magalhães, Bailey–Brock & Davenport, 2011; shallow subtidal sand and shell hash, Venice, Florida.

Raphidrilus hawaiiensis Magalhães, Bailey–Brock & Davenport, 2011; shallow subtidal algal beds, off Oahu Island, Hawaii.

Raphidrilus nemasoma Monticelli, 1910b; shallow subtidal sediments, Mediterranean Sea.

Raphidrilus sp. (=R. nemasoma of Qian & Chia (1989). Undescribed species (fide Petersen & George 1991); lower intertidal sandy beach, Vancouver Island, British
Columbia, Canada.

Raricirrus Hartman, 1961

Type species: Raricirrus maculatus Hartman, 1961

Diagnosis: Peristomium not distinct from prostomium dorsally, achaetous segments lacking. Nuchal organs ciliated pits or flat areas surrounded by fields of cilia. Last 6–9
segments shorter than preceding ones, forming distinct posterior region; with enlarged reproductive spines in some species. Heart body present beginning from segment 4
–10. Notochaetae smooth to serrate capillaries, natatory capillaries, and coarsely serrate forms; neurochaetae falcate and finely pectinate, coarsely serrate forms
posteriorly; simple curved reproductive spines present in one or two posterior chaetigers in some species. Reproduction sexual and asexual.

3 Species:

Raricirrus beryli Petersen & George, 1991; organically enriched sediments, 60-300 m, North Sea, off Norway.

Raricirrus maculatus Hartman, 1961; organically enriched sediments 46-300m, off California.

Raricirrus variabilis Dean, 1995; experimental wood islands, deep water, 4.000 m, off Bahama.

Acknowledgements

Dr. Carol Simon of the Department of Botany and Zoology, Stellenbosch University, South Africa, graciously allowed us to photograph specimens of Ctenodrilus serratus
from her collections. The manuscript benefited from a review by Dr. Brigitte Ebbe. The authors recognize that much of what has been written in recent years on the
Ctenodrilidae is due to the research of the late Dr. Mary E. Petersen (Petersen & George 1991). To that end, we dedicate this chapter to Dr. Petersen.

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