Zootaxa 1668:245–264 (2007) ISSN 1175-5326 (Print Edition) ZOOTAXA Copyright © 2007 · Magnolia Press ISSN 1175-5334 (Online Edition)

Home , Aberranta, Aeolosoma, Aeolosomatidae, Aplacophora, Bylgides, Canalipalpata

Annelida*

GREG W. ROUSE1 & FREDRIK PLEIJEL2 1Scripps Institution of Oceanography, UCSD, 9500 Gilman Drive, La Jolla CA, 92093-0202, USA. E-mail: [email protected] 2Department of Marine Ecology, Tjärnö Marine Biological Laboratory, Göteborg University, SE-452 96 Strömstad, Sweden. E-mail: [email protected]

*In: Zhang, Z.-Q. & Shear, W.A. (Eds) (2007) Linnaeus Tercentenary: Progress in Invertebrate Taxonomy. Zootaxa, 1668, 1–766.

Table of contents

Abstract ...... 245 Introduction ...... 245 Major polychaete taxa ...... 250 Monophyly of Annelida ...... 255 Molecular sequence data ...... 258 Rooting the annelid tree ...... 259 References ...... 261

Abstract

The first annelids were formally described by Linnaeus (1758) and we here briefly review the history and composition of the group. The traditionally recognized classes were Polychaeta, Oligochaeta and Hirudinea. The latter two are now viewed as the taxon Clitellata, since recognizing Hirudinea with class rank renders Oligochaeta paraphyletic. Polychaeta appears to contain Clitellata, and so may be synonymous with Annelida. Current consensus would place previously recognized phyla such as Echiura, Pogonophora, Sipuncula and Vestimentifera as annelids, though relationships among these and the various other annelid lineages are still unresolved.

Key words: Polychaeta, Oligochaeta, Clitellata, Echiura, Pogonophora, Vestimentifera, Sipuncula, phylogeny, review

Introduction

Annelida is a group commonly referred to as segmented worms, found worldwide in terrestrial, freshwater and marine habitats. The first annelids were formally named by Linnaeus, including well-known forms such as the earthworm Lumbricus terrestris Linnaeus, 1758, the medicinal leech Hirudo medicinalis Linnaeus, 1758, and the sea-mouse Aphrodite aculeata Linnaeus, 1758. Today we estimate that the current number of accepted species level taxa is around 14 000 (Rouse & Pleijel 2006), though several thousand more have been named and are considered invalid. Lamarck (1802) first used the term ‘Annélides’ when naming a group of organisms taken from the broad taxon Vermes erected by Linnaeus. The name Annélides was based on the Latin word anellus, meaning a little ring, in reference to the presence of ring-like segments that characterize the group. Earthworms are the most familiar annelids to people, but the bulk of the annelid diversity lies among the marine representatives, which are found in nearly every marine habitat, from beach sands and

Accepted by Z.-Q. Zhang: 27 Nov. 2007; published: 21 Dec. 2007 245 intertidal zones, to the plankton and down in the deep-sea sediments. Through much of the 19th and 20th century, Annelida was usually divided into four classes; Archiannelida erected by Hatschek (1878), Polychaeta by Grube (1850), Oligochaeta by Grube (1850), and Hirudinea by Lamarck (1818). A number of authors used the name Clitellata, introduced by Michaelsen (1919), recognizing that Oligochaeta (earthworms and close relatives) and Hirudinea (leeches) were actually a clade. Other taxa that have been considered to be annelids at various times and with varying ranks include Echiura Newby, 1940, Myzostomida Graff, 1877, Pogonophora Johansson, 1939 and most recently Sipuncula Rafinesque, 1814. Archiannelida was erected for a group of generally minute annelids, such as Dinophilus Schmidt, 1848 (Fig 1A), which were presumed to be primitive because of their simple body-structure. This perceived sim- plicity is now regarded as secondary, related to the interstitial habitat and associated small size of the animals (Hermans, 1969; Westheide, 1985). This limits the number of currently accepted annelid classes to two, Poly- chaeta and Clitellata, but recently serious doubts about the monophyly of the former taxon have been raised and will be reviewed here. Polychaeta and the subdivision of the group has been unstable for many years. Over eighty families of polychaetes are currently recognized (Rouse & Pleijel 2001). Until relatively recently the system most commonly used for classifying polychaetes into higher groups was derived from a pre-evolutionary system used in the early 19th century, where Polychaeta was split into Errantia (wandering forms) and Sedentaria (sedentary forms), mainly based on whether they were mobile, or lived in tubes or burrows (e.g., Day 1967a, b; Hartman 1968, 1969). This utilitarian classification was gradually supplanted by ones that split the Polychaeta into as many as 22 orders but without any real linkage between them (Dales, 1962; Fauchald, 1977). This situation was also unsatisfactory and gave no useful insight into polychaete evolution. A morphological cladistic analysis of Annelida and other groups resulted in a new classification of polychaetes (Fauchald & Rouse 1997; Rouse & Fauchald 1997), which is outlined here (see below) with modifications (Rouse & Pleijel 2001), with the caveat that much of this is now being challenged by results from the analysis of molecular sequence data. There is increasing evidence that Clitellata (Fig. 2A, B), along with Echiura (Fig. 1C), Pogonophora (Fig. 5A), Sipuncula (Fig. 1I), and other groups, may well belong inside Polychaeta (see below), thus making the name Polychaeta synonymous with Annelida (McHugh 1997; Westheide 1997; Westheide et al. 1999). Recent molecular studies have all shown that Clitellata are nested among polychaetes (Bleidorn et al. 2003a, b; Brown et al. 1999; Jördens et al. 2004; McHugh 1997; Struck et al. 2002), but none to date have provided robust support for any sister group relationship with a particular polychaete group. No doubt such a relationships will be recovered soon and either the name Polychaeta or Annelida will be redundant. The monophyly of Clitellata [oligochaetes and leeches (Fig. 2A, B)] is strongly supported on both morphological and molecular grounds (Martin 2001; Siddall et al. 2001). Comprehensive phylogenetic studies using molecular sequence data and morphology provide strong support that Lumbriculida is the sister group to the ectoparasitic clade comprised of Hirudinida, Acanthobdellida and Branchiobdellida (Erséus & Källersjö 2004; Martin 2001; Sid- dall et al. 2001) and should be referred to either as Oligochaeta (Siddall et al. 2001), or Clitellata (Erséus & Källersjö 2004; Martin 2001). There are arguments for using either name with respect to a monophyletic taxon but we have used the name Clitellata here. Morphological features supporting monophyly include the presence of a clitellum, the organization of the reproductive system, and features of sperm ultrastructure (Jamieson 2006).

FIGURE 1. —Various annelid groups A. Dinophilus sp. from California (Dinophilidae), dorsal view. —B. Aeolosoma sp. (Aeolosomatidae), dorsal view. —C. Metabonellia haswelli (Johnston and Tiegs, 1920) (Echiura) from the Australia, female specimen. Inset shows Capitella sp. (Capitellidae) anterior, now thought to be the sister group to Echiura. —D. Hypomyzostoma dodecephalcis Grygier, 1992 from Australia, on crinoid host, lateral view. —E. Hypomyzostoma dodecephalcis, ventral view of entire specimen showing parapodia and everted pharynx. F. Polygordius lacteus, lateral view of head and anterior body. —G. Protodrilus rubropharyngeus, whole animal. —H. Nerilla antennata, whole animal. —I. A phascolionid sipunculid. All photos G. Rouse.

246 · Zootaxa 1668 © 2007 Magnolia Press LINNAEUS TERCENTENARY: PROGRESS IN INVERTEBRATE TAXONOMY ROUSE & PLEIJEL: ANNELIDA Zootaxa 1668 © 2007 Magnolia Press · 247 FIGURE 2.—Clitellata and Scolecida. A. Lumbricus terrestris (Clitellata, Lumbricidae) from USA, dorsal view of entire specimen. —B. Macrobdella decora Say, 1824 (Clitellata, Hirudinidae) from USA, dorsal view of entire specimen. —C. Scoloplos arimiger (O.F. Müller, 1776) (Scolecida, Orbiniidae) from Sweden, whole specimen. —D. Euzonus mucrona- tus (Treadwell, 1914) (Scolecida, Opheliidae) from California, whole specimen. —E. Clymenella sp. (Scolecida, Orbini- idae) from Belize. All photos G. Rouse, except 2B. courtesy of Mark Siddall.

248 · Zootaxa 1668 © 2007 Magnolia Press LINNAEUS TERCENTENARY: PROGRESS IN INVERTEBRATE TAXONOMY Echiura (Fig. 1C) were originally considered members of the same group as the annelids (Cuvier 1817; Lamarck 1818). They were grouped with sipunculids and priapulids in the Gephyrea by Quatrefages (1847), a group subsequently not considered valid by Sedgewick (1898). Sedgewick considered echiurids as a group of annelids, but Newby (1940) proposed a separate phylum, Echiura, based on a detailed embryological study of Urechis caupo. His proposal was generally accepted (e.g., Stephen & Edmonds 1972), until McHugh (1997) provided molecular evidence that they should again be considered as annelids. Subsequent morphological studies support this conclusion (Hessling 2002; Hessling & Westheide 2002) and Echiura appear to now be closely related to capitellid polychaetes (Fig. 1C) (Colgan et al. 2006; Rousset et al. 2007; Struck et al. 2007). The taxon Myzostomida was erected by Graff (1877). During the 20th century these animals (Fig. 1D, E) were treated as polychaete annelids with a rank of family or order (Hartman 1969; Pettibone 1982), or treated, not as polychaetes, but as a class of annelids (Dales 1963). Rouse & Fauchald (1995; 1997) argued that Myzostomida were a polychaete group and placed them, after their cladistic analyses, as part of Phyllodocida. Zrzav! et al. (2001) placed Myzostomida outside Annelida in their analysis based on molecular and morphological data and Eeckhaut et al. (2000) suggested that Myzostomida are more closely related to Platyhelm- inthes than to any annelids. The pendulum has swung back in favor of myzostomes being annelids based on a new analysis by Bleidorn et al. (2007). As for Siboglinidae, the name Pogonophora, introduced by Johansson (1939), was used with the rank of phylum from the late 1940’s and for a while they were regarded as not being closely related to Annelida (Ivanov 1963). With the discovery of the segmented posterior end (Webb 1964), and the fact that the nerve cord was ventral (Nørrevang 1970), opinion shifted to regard them as a protostome group (but see Malakhov et al. 1997). Subsequent morphological and molecular analyses placed the group well inside Annelida (Barto- lomaeus 1995; McHugh 1997; Rouse & Fauchald 1995, 1997) and a recommendation that the original name, Siboglinidae (Caullery 1914), be applied to the group (Rouse 2001; Rouse & Fauchald 1997; Rouse & Pleijel 2001). Vestimentifera had also been given the rank of phylum by Jones (1985) and thought to be closer to Annelida than Pogonophora. The basis for this was soon shown to be unfounded by Southward (1988) and the placement of the group (as Vestimentifera) within Siboglinidae, as sister group to Sclerolinum, was shown recently (Halanych et al. 2001; Rouse 2001). A new group of Siboglinidae, Osedax, was recently described (Rouse et al. 2004) that uses bones for nutrition (Fig. 5A). Originally considered among the Vermes Intestina by Linnaeus, sipunculids (Fig. 1I) were related to the Holothuria by both Lamarck (1818) and Cuvier (1817). The name Sipuncula was introduced by Rafinesque (1814). Sedgewick (1898) raised them to the level of phylum and until recently this has been widely accepted (Brusca & Brusca 1990; Cutler 1994; Hyman 1959; Stephen & Edmonds 1972). Sipunculids are triploblastic coelomates with no segmentation; early larvae resemble trochophores. Scheltema (1993) regarded the Sipun- cula as sister group to Mollusca. This, however, involves several ad hoc assumptions and only three taxa were considered by her, molluscs, sipunculids, and annelids. Molecular studies have recently indicated (see below) that Sipuncula should be considered as part of Annelida (e.g., Brown et al. 1999; Struck et al. 2007). As is abundantly clear from the forgoing, the systematics of annelids is undergoing major revision. It would appear that the intensive efforts of a number of workers is resulting in significant movement towards a stable classification for Clitellata (Jamieson 2006; Siddall et al. 2006). This cannot be said for the remaining annelids. For these taxa, those that comprise the various “polychaete” subgroups, we have chosen to outline the most recent comprehensive systematic treatment (Rouse & Fauchald 1997; Rouse & Pleijel 2001), but emphasize that many changes are to come in the future, some of which are foreshadowed here. Rouse & Fauchald (1997) used various cladistic analyses including “complete” and a “restricted” taxon samples and explored different techniques for character coding. There was some incongruence between the different analyses and the choice of topology used to revise the taxonomy was largely arbitrary. Given that the overall topology of their complete analyses were incongruent with the restricted analyses, the placements and delin- eations of a number of these taxa should be further investigated. For example, the position of the clades

ROUSE & PLEIJEL: ANNELIDA Zootaxa 1668 © 2007 Magnolia Press · 249 (Arenicolidae, Capitellidae, Maldanidae), (Acrocirridae, Cirratulidae, Flabelligeridae) and Oweniidae differed markedly between the complete and restricted analyses under one coding. Additionally, in a subsequent analysis, Rouse (1999) added a number of larval characters to the character set of Rouse & Fauchald (1997). This resulted in some slightly different tree topologies, particularly with regards to Chaetopteridae (Fig. 5F) and Oweniidae (Fig. 5B). While these are not taken into consideration in our systematic treatment here, they deserve further attention.

Major polychaete taxa

Scolecida. The name Scolecida, derived from skolex (Greek), meaning worm, was applied with reference to an annelid group by Rouse & Fauchald (1997), though it has historically been used with reference to parasitic non-annelids. Taxa included were Arenicolidae, Capitellidae (Fig. 1C inset), Cossuridae, Maldanidae (Fig. 2E), Opheliidae (Fig. 2D), Orbiniidae (Fig. 2C) and Paraonidae. The name Scolecida is derived from Scoleci- formia, a name introduced by Benham (1896) for a similar group of taxa. Only two apomorphies support the clade Scolecida in Rouse & Fauchald (1997), the presence of parapodia with similar rami and the possession of two or more pairs of pygidial cirri, and both of these are homoplastic. In many ways, this group represents the simple-bodied forms of polychaetes and it is likely that further analysis will show that it is not monophyletic. In fact to date no molecular sequence analyses have recovered any assemblage like Scolecida and it usually appears as a polyphyletic assemblage (e.g., Struck et al. 2007).

Palpata. Palpata was a new name coined by Rouse & Fauchald (1997) and such a group of polychaetes has never been formulated before. Virtually all non-Scolecida polychaetes, except a few incertae sedis taxa, were placed into Palpata. The name is based on an apomorphy for the group, the presence of palps. Palps can be divided into two structurally different groups, grooved “feeding” palps and ventral, “sensory” palps (Orrhage 1980). Feeding palps usually have ciliated paths, often located in a longitudinal groove, giving each palp a U- shaped cross-section. Ventral sensory palps are morphologically more uniform than grooved palps. In most cases they are tapering or digitiform and relatively short, compared to grooved palps. Given the fact that the presence of palps and a limited peristomium were the only synapomorphies supporting this taxon in Rouse & Fauchald (1997), the validity of Palpata requires further investigation and it has yet to be recovered as a monophyletic group in any broad molecular analyses (see below). Rouse & Fauchald (1997) proposed that Palpata contains two major taxa, Aciculata and Canalipalpata.

Aciculata. Aciculata was a new name erected by Rouse & Fauchald (1997) for one of the most the strongly supported clades in their analyses. The name refers to one of the apomorphies for the group; the presence of a particular chaetal type called aciculae. Aciculae are stout chaetae that differ from others in that much or all of the chaeta remains internalized in the parapodium. Numerous other features such as the presence of ventral sensory palps, prostomial antennae, dorsal cirri, ventral cirri, one pair of pygidial cirri, and segmental organs in most segments were proposed to be apomorphic for Aciculata. Aciculata is divided here into the three major clades Amphinomida, Eunicida and Phyllodocida, and also with a few taxa as incertae sedis. Aciculata was recovered as a clade by Struck et al. (2007), if Orbiniidae (usually placed in Scolecida, although some members actually have chaetae that can be interpreted as aciculae) was included.

Phyllodocida. The name Phyllodocida was coined by Dales (1962) and was subsequently used by other workers, such as Fauchald (1977) and Pettibone (1982), for essentially the same group of polychaetes. Prior to Dales (1962), the group had never been formulated as a monophyletic taxon. Rouse & Fauchald (1997) found strong support for the monophyly of this assemblage, indicated by the ventral position of sensory palps, the

250 · Zootaxa 1668 © 2007 Magnolia Press LINNAEUS TERCENTENARY: PROGRESS IN INVERTEBRATE TAXONOMY presence of anterior enlarged cirri, the loss of dorsolateral folds, the presence of an axial muscular proboscis, and the presence of compound chaetae with a single ligament. A major difference in the formulation of Phyl- lodocida by Rouse & Fauchald (1997), and that of previous workers, was that they placed Myzostomida (Fig. 1D, E) (as Myzostomatidae) in the group (but see Eeckhaut et al., 2000). Rouse & Fauchald (1997) did not further subdivide Phyllodocida, since their analyses resulted in dramatically different topologies for various Phyllodocida taxa. Based on the results of Pleijel & Dahlgren (1998), two names were used by Rouse & Pleijel (2001) for clades within Phyllodocida; Aphroditiformia (or scale-worms) and Nereidiformia. The remaining taxa in Phyllodocida are treated as “unplaced”. There are numerous family-ranked taxa in Phyl- lodocida with representatives shown here of Phyllodocidae (Fig. 3A), Sphaerodoridae (Fig. 3B), Nereididae (Fig. 3C), Syllidae (Fig. 3D), Chrysopetalidae (Fig. 4A), Nephtyidae (Fig. 4B), and Polynoidae (Fig. 4E).

Eunicida. The name Eunicida was first used by Dales (1962), but encompassed a well-delineated group known prior to that as Eunicea, Euniceformia, Eunicimorpha or simply Eunicidae. This grouping included polychaetes with a ventral muscularized pharynx with ventral mandibles and dorsal maxillae (and a few that had lost jaws) and is very likely a monophyletic assemblage. Another putative apomorphy for the clade would appear to be a peristomium forming a two rings, although this feature is not present in all the subgroups. Rouse & Fauchald (1997) expanded the traditionally delineated Eunicida to include Amphinomidae and Euphrosinidae although this is not accepted here as the relationships between them is uncertain. Eunicida, fol- lowing Rouse & Pleijel (2001), includes Dorvilleidae (Fig. 4C), Eunicidae, Hartmaniellidae, Histriobdellidae, Lumbrineridae, Oenonidae and Onuphidae. A recent comprehensive molecular phylogeny of Eunicida was undertaken by Struck et al. ( 2006) who found a topology where a labidognath clade (i.e., a “Eunicidae”/ Onuphidae/Lumbrineridae clade) was significantly rejected, a result that goes against most traditional view of the relationships within the group. Prior to this Struck et al. (2005), in a molecular study suggested that Dino- philidae (Fig. 1A)—a group long associated with Eunicida, either as a family or as part of Dorvilleidae (Eibye-Jacobsen & Kristensen 1994)—does not belong in Eunicida.

Amphinomida. Amphinomida contains Amphinomidae (Fig. 4D) and Euphrosinidae and has never been the subject of a detailed modern phylogenetic revision. A taxon, Amphinomae, equivalent to Amphinomida, dates back to Savigny (1822). Amphinomida was first used as a taxon name by Dales (1962), but names such as Amphinomorpha have also been applied. Although Amphinomida is well supported by a number of apomorphies, including calcareous chaetae and nuchal organs forming a caruncle, both their position within Aciculata and the interrelationships within the group are uncertain. Rouse & Fauchald (1997) in their classification included Amphinomidae and Euphrosinidae in Eunicida, whereas Rouse & Pleijel (2001) instead treated them as a separate taxon, Amphinomida.

Aciculata unplaced. Rouse & Fauchald (1997) placed Aberranta Hartman, 1965 (as Aberrantidae), Neril- lidae (Fig. 1H) and Spinther Johnston, 1845 (as Spintheridae) as parts of Aciculata, but did not include them in any other sub-taxon of the group. These three taxa have never been related to each other and are not to be regarded as closely related by being grouped together here. Of these taxa, only Spinther actually has aciculae, but all three are likely to have sister groups with different members of Aciculata. Worsaae et al. (2005) assessed the phylogenetic position of Nerillidae and Aberranta using morphology and 18S rDNA, but failed to provide any strong conclusions as to the placement for either group.

Canalipalpata. Canalipalpata (referring to the presence of grooved palps) is a name that was first used by Rouse & Fauchald (1997) and is a massive group of polychaetes that encompasses around half the number of described species. The only apomorphy for Canalipalpata is the presence of grooved palps and so the clade must be regarded as weakly supported. The groove along each palp is longitudinal and ciliated and, in contrast to those of Aciculata, function as feeding structures. Rouse & Fauchald (1997) identified three major clades

ROUSE & PLEIJEL: ANNELIDA Zootaxa 1668 © 2007 Magnolia Press · 251 within the Canalipalpata (Sabellida, Spionida and Terebellida) and a number of taxa that were regarded as incertae sedis within the group.

Sabellida. The apomorphy for Sabellida, as formulated by Rouse & Fauchald (1997), was the fusion of the prostomium with the peristomium, hence it is weakly supported. This name has been used to contain Sabel- lariidae (Fig. 5I), Sabellidae (Fig. 5C) and Serpulidae (Fitzhugh, 1989) and these three were included by Rouse & Fauchald (1997), plus two other taxa. A dramatic shift compared with traditional systematics was that Rouse & Fauchald (1997) placed Siboglinidae (Fig. 5A), (formerly outside polychaetes as Pogonophora and Vestimentifera), as part of Sabellida. They also included Oweniidae (Fig. 5B), a taxon that has a “che- quered” systematic history as a polychaete. It should be noted that in further analyses by Rouse (1999; 2000), Oweniidae did not group with the remaining Sabellida, whereas Chaetopteridae (Fig. 5F) (included here in as part of Spionida) did. A recent combined analysis of molecular and morphological data (Rousset et al. 2004) also did not recover the Sabellida as formulated here but did suggest Oweniidae and Siboglinidae to be closely related, as did Struck et al. (2007). Clearly further study is required. In addition, similarities between Sabel- lariidae (Fig. 5I) and Pectinariidae (in Terebellida) also deserve further study (Rouse & Pleijel 2001). Sabel- lariidae have previously been considered as part of Terebellida (e.g., Fauchald 1977).

Terebellida (Cirratuliformia, Terebelliformia). The name Terebellida was first used by Dales (1962) and included Ampharetidae, Pectinariidae and Terebellidae, all polychaetes having multiple grooved palps. Prior to this, the names Terebellomorpha or Terebelliformia had often been used for essentially the same grouping of taxa. Terebellida was expanded by Rouse & Fauchald (1997) to include a clade in which most have a single pair of palps (e.g., Acrocirridae, Cirratulidae, Flabelligeridae), but recent studies have not recovered this relationship (see below). Rouse & Fauchald (1997) identified several synapomorphies for this overall grouping, namely the presence of a first segment with no chaetae, a gular membrane, and a heart body. The clade within Terebellida that has taxa with a single pair of palps (with exceptions such as some Cirratulidae with numerous palps and Ctenodrilinae and Fauveliopsidae with none) was referred to as Cirratuliformia in Rouse & Pleijel (2001), a name that has been used previously for a somewhat similar grouping (e.g., Fauchald 1977). It contains Acrocirridae, Cirratulidae, Fauveliopsidae, Flabelligeridae, and Sternaspis Otto, 1821. The clade comprised of Alvinellidae, Ampharetidae, Pectinariidae, Terebellidae and Trichobranchidae is referred to here as Terebelliformia, also a fairly “traditional” formulation.

Spionida. The name Spionida was first used by Dales (1962) to contain Spionidae and a number of similar groups, as well as taxa such as Paraonidae and Sabellariidae. These groups are not considered closely related today, and Spionida in Rouse & Pleijel (2001) contained Apistobranchus Levinsen, 1883, Chaetopteridae, Magelonidae, Heterospio Ehlers, 1875, Poecilochaetus Claparède in Ehlers, 1875, Trochochaeta Levinsen, 1883, and Uncispionidae, though the latter four taxa should reasonably be all treated as members of Spionidae (Blake & Arnofsky 1999). The positions of Chaetopteridae and Magelonidae deserve further investigation. The synapomorphies for Spionida listed by Rouse & Fauchald (1997) were the presence of a pair of peristo- mial grooved palps, nuchal organs forming posterior projections, and anterior excretory nephridia and posterior segmental organs for gamete release.

FIGURE 3. — Aciculata: Phyllodocida. A. Eulalia clavigera Quatrefages, 1866 (Phyllodocidae) from the English Chan- nel, dorsal view of entire specimen. —B. Sphaerodoropsis philippi Fauvel, 1911 (Sphaerodoridae) from the Swedish west-coast, dorsal view of entire specimen. —C. Hediste diversicolor (O.F. Müller, 1776) (Nereididae) from the Swedish west-coast, dorsal view of entire specimen. —D. Trypanosyllis sp. (Syllidae) from North Carolina, dorsal view of entire specimen with stolon. All photos F. Pleijel.

252 · Zootaxa 1668 © 2007 Magnolia Press LINNAEUS TERCENTENARY: PROGRESS IN INVERTEBRATE TAXONOMY ROUSE & PLEIJEL: ANNELIDA Zootaxa 1668 © 2007 Magnolia Press · 253 254 · Zootaxa 1668 © 2007 Magnolia Press LINNAEUS TERCENTENARY: PROGRESS IN INVERTEBRATE TAXONOMY FIGURE 4. — Aciculata: Phyllodocida, Eunicida and Amphinomida. A. Dysponetus sp. (Phyllodocida, Chrysopetal- idae) from California, dorsal view of entire mature male. —B. Nephtys hombergi Savigny, 1818 (Phyllodocida, Nephty- idae) from the Swedish west-coast, dorsal view of entire specimen. —C. Ophryotrocha sp. (Eunicida, Dorvilleidae) from the Swedish west-coast, dorsal and ventral view of entire specimen. —D. Pareurythoe sp. (Amphinomidae) from Cali- fornia, antero-dorsal view. —E. Bylgides elegans (Théel, 1879) (Phyllodocida, Polynoidae) from the Swedish west- coast, dorsal view of entire specimen. All photos F. Pleijel.

Canalipalpata unplaced. Rouse & Fauchald (1997) placed Polygordiidae and Protodrilida (as Protodriloid- idae, Protodrilidae and Saccocirridae) as part of Canalipalpata, but did not place them within any other sub- taxon. In their complete cladistic analyses, these taxa formed a clade that was either associated with taxa that belong within Canalipalpata, Scolecida or were part of a basal polytomy of Polychaeta, so their decision was arbitrary. However, there is good evidence to support Protodrilida being placed in Canalipalpata (Purschke & Jouin 1988), perhaps near Spionida. On the other hand, placement of Polygordiidae in Canalipalpata must be regarded as suspect. Rouse & Fauchald (1997) made scoring errors in regard to Polygordiidae, the most important being that the animals cannot be regarded as having grooved palps. It was suggested by Rouse & Pleijel (2001) that investigation of a sister group relationship with, or within, Opheliidae may be worthwhile, and this is actually an old idea (e.g., Giard 1880).

Annelida unplaced. Rouse & Fauchald (1997) included Aeolosomatidae (Fig. 1B), Potamodrilus Lastockin, 1935 (as Potamodrilidae), Parergodrilidae and Psammodrilidae in their complete taxon set analyses. In one analysis, these taxa either fell as part of a large basal polytomy of polychaetes, or Aeolosomatidae, Potamo- drilus and Parergodrilidae formed a clade with Ctenodrilinae, and Psammodrilidae grouped with Capitellidae (Fig. 1C inset), Arenicolidae and Maldanidae (Fig. 2E). In another analysis, Aeolosomatidae, Potamodrilus and Parergodrilidae either formed a grade with respect to Polygordiidae (Fig. 1F), Protodrilidae (Fig. 1G) and Protodriloididae, or they were a basal clade of polychaetes. Psammodrilidae either were a basal polychaete group, or were sister group to a large clade that was mainly comprised of taxa with grooved palps. Thus, it was not possible to place these taxa with any confidence. Prior to the study by Rouse & Fauchald (1997), Aeolosomatidae (Fig. 1B) and Potamodrilus were usually considered in relation to Clitellata, either as a mem- ber of the group (Bunke 1967), or more recently as the sister group to Clitellata (Bunke 1985). This was then rejected by Bunke (1986), who also could not relate them to any group of polychaetes, thus leaving the two taxa “isolated”. The most recent analysis is from a molecular perspective (Struck et al. 2002), and this study found no support for a relationship of Aeolosomatidae with Clitellata or with any other particular annelid group. Fauchald (1977) grouped Parergodrilidae with Ctenodrilidae, but did not justify this decision. Other- wise, the group has also been treated as “isolated” within polychaetes. A recent molecular study by Jördens et al. (2004) indicated that Parergodrilidae may be closely related to orbiniids; the position of the terrestrial polychaete Hrabeiella Pizl & Chalupsky, 1984, however, was inconclusive. Psammodrilidae have been treated as a singular group of polychaetes since they were first discovered by Swedmark (1952). Rouse & Fauchald (1997) suggested that a relationship for Psammodrilidae with Arenicolidae and Maldanidae should be assessed; this was proposed by Meyer & Bartolomaeus (1996; 1997), but the present anatomical evidence is weak.

Monophyly of Annelida

There have been a number of reviews on the monophyly and membership of Annelida (McHugh, 2000; Rouse & Fauchald, 1995, 1998; Westheide et al., 1999). The morphological and molecular support for the mono-

ROUSE & PLEIJEL: ANNELIDA Zootaxa 1668 © 2007 Magnolia Press · 255 phyly and delineation of Annelida will be outlined here. To date there has not been a combined analysis of morphology and molecular evidence at a broad level with comprehensive taxon sampling. The monophyly of Annelida is not well supported by anatomical features proposed to date, and only two are worthy of discus- sion; segmentation, and chaetae, with nuchal organs representing another possible apomorphy.

Metamerism (segmentation). Annelids have three body regions. In most annelids, the majority of the body is comprised of repeated units called segments or somites. Each segment may be limited by septa dividing it from neighboring segments, and has a fluid-filled cavity within referred to as a coelom. Structures such as the excretory, locomotory and respiratory organs are generally repeated in each segment (e.g., Rouse & Pleijel 2001). Segments are formed sequentially in annelids and are established during development from growth zones located at the posterior end of the body, so the youngest segment in the body of an annelid is always the most posterior. The only parts of the annelid body that are not segmental are the head, including the pro- and peristomium, and a terminal region called the pygidium. The proposed homology of segmentation seen in annelids with that seen in Arthropoda has been used to unite the two as Articulata, a grouping that dates back to Cuvier (1817). The homology of this segmentation has been refuted, most recently by Seaver (2003), and arthropods are now viewed by many as closer to taxa such as Nematoda in the clade Ecdyzosoa (Aguinaldo et al. 1997; Giribet 2003), with annelids grouping with molluscs and other protostomes in the clade Lophotrochozoa (Halanych et al. 1995). This suggests that the form of segmentation seen in annelids may in fact represent an apomorphy. Pogonophora and Vestimentifera had been regarded as outside Annelida and their posterior segmentation (and chaetae) was either overlooked by earlier authors or treated as non-homologous to the annelid segmentation (see Rouse (2001). This segmentation is instead viewed as homologous to that in annelids. With regards to Echiura and Sipuncula, which appear to be unsegmented annelids, Hessling & Westheide (2002), showed that differentiation of the echiuran nervous system proceeds from anterior to posterior, indicating the occurrence of a posterior growth zone. Their results can be interpreted as an indication that the echiuran unsegmented condition represent a loss and that they are derived from segmented ancestors (Hessling & Westheide 2002).

Chaetae. A distinctive feature of annelids are structures called chaetae. Chaetae (also called setae) are bun- dles of chitinous, thin-walled cylinders held together by sclerotinized protein. Chaetae show a huge amount of variation, from long thin filaments (capillary chaetae) to stout multi-pronged hooks. It has been argued that the kind of chaetae found in annelids evolved several times or was plesiomorphic feature for a large group of Metazoa and had been lost a number of times (see Orrhage 1973). This was based on the disparate occurrence of basically identical chaetae in the phyla Annelida, Brachiopoda, Pogonophora, Echiura, as well as in cephalopod molluscs (Brocco et al. 1974). Since this assembly of taxa is no longer perceived as so disparate, chaetae could indeed be an annelid apomorphy, although the position of brachiopods remains to be assessed.

FIGURE 5.—Canalipalpata. A. Osedax rubiplumus Rouse et al. 2004 (Sabellida, Siboglinidae) from California, lateral view of several female specimens. —B. Owenia sp. (Sabellida, Oweniidae) from North Carolina, lateral view of anterior. —C. Pseudopotamilla reniformis (Bruguière, 1789) (Sabellida, Sabellidae) from Iceland, anterior in tube. —D. Terebel- lides stroemi Sars, 1835 (Terebelliformia, Trichobranchidae) from Iceland, lateral anterior end. —E. Pectinaria granu- lata Linnaeus, 1767 (Terebelliformia, Pectinariidae) from Iceland. —F. Phyllochaetopterus lauensis Nishi & Rouse, 2007 (Spionida, Chaetopteridae) from the Lau Basin —G. Cirratulus sp. (Cirratuliformia, Cirratulidae) from Japan, dorsal anterior end. —H. Malacoceros fuliginosus (Claparède, 1868) (Spionida, Spionidae) from Iceland, dorsal anterior end. —I. Sabellaria vulgaris Verrill, 1873 (Sabellida, Sabellariidae) from North Carolina, lateral view of anterior in tube. All photos G. Rouse.

256 · Zootaxa 1668 © 2007 Magnolia Press LINNAEUS TERCENTENARY: PROGRESS IN INVERTEBRATE TAXONOMY ROUSE & PLEIJEL: ANNELIDA Zootaxa 1668 © 2007 Magnolia Press · 257 Nuchal organs. These are ciliated, paired, chemosensory structures, innervated from the posterior part of the brain. They are present in most polychaetes (Purschke 1997) and Rouse & Fauchald (1997), treating Polycha- eta and Clitellata as sister taxa, suggested that they may represent an apomorphy for Polychaeta. This has been challenged by other authors, who suggest that nuchal organs may be an apomorphy for Annelida as a whole and have been lost in Clitellata (Purschke et al. 2000). This latter scenario now appears to be supported by recent phylogenetic studies. Sipuncula have a single nuchal organ that superficially appears to be paired and this was argued to be non-homologous with those of annelids (Purschke et al. 1997). The putative placement of Sipuncula with annelids means this will need further assessment.

Molecular sequence data

The earliest molecular studies relevant to the position of annelid relationships can be found in Winnepen- ninckx et al. (1995) who used 18S rRNA sequences to examine relationships among protostome worms such as Annelida, Echiura, Nemertea, Pogonophora and Vestimentifera. They only included two annelids (Lanice Malmgren, 1866 and Eisenia Michaelsen, 1900) in their study and these did not form a clade in the parsimony analysis. McHugh (1997) and Kojima (1998) then found Clitellata and Pogonophora clustered among various polychaetes using analyses of the sequence of a nuclear gene, EF1 a. The former study also found that Echiura nested among polychaetes. Their taxon sampling was such that the possibility of a number of other protostome taxa also being included in Annelida was not assessed. Brown et al. (1999) then studied relationships within Annelida using DNA sequence data from three genes and a broader taxon sample from among annelids and other protostomes. They also found clitellates and pogonophores nested among annelids and also Sipun- cula. Martin (2001) analyzed available sequences of 18S rRNA with the primary aim of assessing the placement of Clitellata. He could not recover a monophyletic Annelida without also including taxa such as Mollusca and Sipuncula. Subsequent studies that have large samples of protostomes also consistently show taxa from Mollusca, Sipuncula, Brachiopoda and Phoronida nested among annelid taxa (Bleidorn et al. 2007; Bleidorn et al. 2003a, b; Colgan et al. 2006; Jördens et al. 2004; Rousset et al. 2007; Struck et al. 2002; Struck et al. 2007). The most recent of these papers are briefly reviewed here. Colgan et al. (2006) analyzed annelid relationships based on GenBank sequences together with 38 new ones. They used the five genes 18S rDNA, 28S rDNA, histone H3, and snU2, RNA, and COI for 56 terminals. Included terminals that are not traditionally referred to annelids were 12 molluscs, a sipunculid and a phoronid, together with two putative annelids, a myzostomid and an echiuran. The trees were rooted with molluscs. They provided three analyses based on maximum likelihood, Bayesian and parsimony. Unfortu- nately the maximum likelihood tree was not provided with any support values of branches and is therefore dif- ficult to evaluate. However, it suffers from similar problems as many other annelid analyses in that the phylogram shows very short branch lengths for all basal groups together with long branches to the terminals, indicating that there is limited signal available in the data to resolve the relationships among major groups of annelids. The Bayesian analysis yielded a majority rule consensus tree with support values >95% for a number of clades. However most well supported clades were non-basal groupings. Several of these corroborate earlier results, including a clade with two scale-worms, one with two eunicids and one with two cirratulids. Others, however, are less obvious, such as orbiniids as sister to scale-worms, sabellids and fauveliopsids together with spionids and at the exclusion of serpulids and chaetopterids, or a clade including part of the Ter- ebelliformia with myzostomids and a mollusc nested inside. It clearly seems to be a general tendency in the results from Bayesian analyses to obtain even 100% support for clades that contradict all previous knowledge. One interesting grouping that appeared was capitellids and echiurans as sister taxa, a relationship that also was suggested by Struck & Purschke (2005), Struck et al. (2007), and in part by Rousset et al. (2007). The parsimony analysis in Colgan et al. (2006) did not provide much resolution, with only three clades with bootstrap

258 · Zootaxa 1668 © 2007 Magnolia Press LINNAEUS TERCENTENARY: PROGRESS IN INVERTEBRATE TAXONOMY values above 95%, and nine above 50%. All clades with stronger support related to taxa that traditionally are regarded as very close, such as Marphysa Quatrefages, 1866 and Eunice Cuvier, 1817, and Dodecaceria Ørsted, 1843 and Cirratulus Lamarck, 1818. Rousset et al. (2007) presented parsimony analyses of 217 and 211 annelid and outgroup terminals, with data from 18S rDNA, 28S rDNA, histone H3 and 16S rDNA. The data set consisted of 267 new sequences, combined with old ones. Taxon selection was based on the criterion that they should minimally include 18S rDNA data or two other loci. Outgroup terminals initially were three arthropods, one brachiopod, five molluscs, two echiurans, two nemerteans and three sipunculids. A second analysis was carried out where some of the outgroups were removed since the first one, with 217 terminals, resulted in possibly peculiar positions of a series of the outgroups, nested among polychaetes. The first analysis was rooted with an arthropod and the second one with a nemertean. Although a number of the family-ranked taxa did come out as monophyletic, there was very little support for any of the more major groupings. There was clearly better resolution for those few groups with a dense taxon sampling (e.g., clitellates and syllids). As in several other analyses, Sipuncula was nested within the annelids, but without resolving their detailed position. Although a very large data set, the results were obviously a disappointment and failed to resolve any deeper annelid relationships or the issue of monophyly of the whole group. This may be due to the incompleteness of the data sets; only some of the loci were available for many of the terminals. Or it may be that the markers chosen were simply not informa- tive at the levels required. Struck et al. (2007) focused on the position of Echiura and Sipuncula and provided analyses of two different data sets. One was based on nucleotide data from 18S rDNA, 28S rDNA, and EF1 a for 81 terminals, with nine outgroups including two brachiopods, one nemertean, five molluscs and one polyclad flatworm, and another from the same nuclear genes plus eight mitochondrial genes for a set of 10 terminals. Struck et al. (2007) provided two analyses of each data set with maximum likelihood and Bayesian, both of which showed a monophyletic Annelida, given that Sipuncula and Echiura are part of that group. In the first analysis Sipun- cula was closest to terebelliforms, whereas in the second they were sister to orbiniids. Neither of these relationships had strong support. However, whereas the actual position of the Sipuncula within the annelids was uncertain, their position, either as sisters to annelids, or nested within annelids, was shown to be statistically supported. Nevertheless, a more dense taxon sampling among the outgroups would be required to further assess this result. The echiuran position, in contrast, is clearer and they come out as sisters to capitellids (Fig. 1C) with strong support in the first analysis, and to maldanids with weaker support in the second. Given the differences in taxon sampling, these two positions of echiurans are fully congruent in both analyses, and their capitellid affinity corroborate the previous analyses by Struck & Purschke (2005), Colgan et al. (2006), and Rousset et al. (2007). A summary of the Struck et al. (2007) restricted analysis is provided in Fig. 7 as the best evidence of molecular sequence data for annelid to date.

Rooting the annelid tree

Rouse & Pleijel (2001) suggested that the oldest unequivocal fossil polychaetes, such as Canadia Walcott, 1911 from the Cambrian period, belong within Phyllodocida. This view was challenged by Eibye-Jacobsen (2004), who argued that there are no synapomorphies that would place Canadia in Phyllodocida, but did agree they were annelids of some sort. No other fossil polychaetes from the Cambrian can be unequivocally assigned to extant annelid taxa either. There are several likely appearances from the Ordovician, including Serpulidae, Spionidae and the radiation of Eunicida (Rouse & Pleijel 2001). Ensuing appearances suggest that by the end of the Carboniferous most major polychaetes lineages had appeared. The exception appears to be Scolecida, with the earliest known fossils being the dubious Archarenicola Horwood, 1912 (Arenicolidae) from the Triassic, and one assignable to Paraonidae from the Cretaceous. With the rooting option (based on

ROUSE & PLEIJEL: ANNELIDA Zootaxa 1668 © 2007 Magnolia Press · 259 Rouse & Fauchald 1997) employed in Figure 6A, it appears that some of the earliest appearing fossil polychaetes belong to derived clades (e.g., Eunicida and possibly Phyllodocida). This could be interpreted in two ways: 1) the root placement in Fig. 6A is wrong, and so a number of the members of Aciculata may in fact appear as a basal grade; 2) a number of major polychaete clades had already evolved in, or before, the “Cam- brian explosion”, but fossils have not yet been found. The third possibility is that the overall topology used in Fig. 6A may be profoundly incorrect. If we accept that it is correct but do not root the tree, then a diagram as shown in Fig. 6B is the result. This is the most conservative representation of our current understanding of annelid relationships.

FIGURE 6. —A. Cladogram of relationships among the major groups of annelids. Based on Rouse & Pleijel (2001, 2003). The “disconnected” taxa could be attached on many places in the tree, and the dashed line to Spinther also indi- cate uncertainty. —B. Same tree but unrooted.

FIGURE 7. — A summary of the restricted analysis of the largest molecular dataset to date from Struck et al. (2007) showing that Echiura, Sipuncula, Siboglinidae (= Pogonophora and Vestimentifera) form a clade with Clitella and polychaete groups. Unfortunately relationships among these taxa were not resolved with high support.

260 · Zootaxa 1668 © 2007 Magnolia Press LINNAEUS TERCENTENARY: PROGRESS IN INVERTEBRATE TAXONOMY Our conclusion is that we at present have no knowledge whatsoever about the root position of annelids, and that the most “honest” representation is the one in Fig. 6B and this is essentially the same as in Fig. 7. However, given the aim to only recognize monophyletic groups, this also means that we at present cannot name a single clade within the group, unless basing it on the assumption that the root is situated elsewhere on the annelid branch. But we are optimistic in believing that this state of affair is about to change in the near future.

Acknowledgements

We want to thank Zhi-Qiang Zhang for requesting this article and for comments by Chris Glasby and three anonymous reviewers. Mark Siddall kindly provided an image of a leech. This material is based upon work supported by the National Science Foundation AToL program under Grant Nos. 0334932 and 0531757 and funds from Scripps Institution of Oceanography.

References

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