Phyllodocida

Glycera alba, from senckenberg.de.

Belongs within: Annelida.
Contains: Pisionidae, Nephtyidae, Hesionidae, Nereididae, Aphroditiformia, Glyceriformia, Phyllodocidae, Myzostomatida, Typosyllis, Eusyllinae, Sphaerosyllis, Exogone.

The Phyllodocida are a group of mostly active, primarily marine worms. Characteristic features of the group include ventrally positioned sensory palps, an axial eversible pharynx, enlarged anterior cirri, compound chaetae with a single ligament, and metanephromixia (Pleijel & Rouse 2004).

My genitals just grew eyes and swam away: the life of a syllid worm
Published 20 May 2009
The syllid worm Myrianida pachycera with a chain of developing epitokes. Photo by Leslie Harris.

Marine worms of the family Syllidae are small polychaetes, usually less than two centimetres in length and about a millimetre in width. Many syllids are interstitial (living buried in sand), others live in association with corals or sponges (on which they may feed). The main feature of syllids that has captured people’s attention, however, is their extremely multifarious sex lives (Franke 1999).

Syllids are one of a number of polychaete families exhibiting what is called epitoky, a significant metamorphosis between the juvenile or atokous and sexually mature or epitokous stages. The originally benthic worm grows long, extended parapodia, and the eyes and other sensory organs become greatly enlarged. More significantly, the reproductive tissue expands to fill almost the entire body, and other organs such as the digestive system degenerate, so the final epitokous worm is basically a highly sensitive pelagic gonad. In other worms such as members of the family Nereididae, the mature worm will swim up into the water column to meet up with other pelagic gonads, after which the entire mass will explode in a cloud of gametes.

Syllids, however, do things a little differently. Seemingly not as keen on ending life with a bang, they have evolved a number of ways to continue on with their life after maturity. The original syllid mode of reproduction involved metamorphosis to an epitoke as in other related polychaete families, but without the degeneration of the digestive system. And nereidids release their gametes by fatally rupturing the body wall, syllid epitokes release theirs through modified nephridia. Afterwards, the syllid epitoke is able to return to the ocean floor and partially revert back to its original atokous form, ready to reproduce another year. This mode of reproduction, called epigamy, remains the one used in two of the four syllid subfamilies, Eusyllinae and Exogoninae, as well as part of the subfamily Autolytinae.

Some epigamous syllids brood their eggs after fertilisation, and may even retain the offspring after hatching. This is an illustration of one such syllid, Exogone rubescens, from here.

Two other syllid lineages, the remainder of Autolytinae and the subfamily Syllinae, developed a mode of reproduction called schizogamy—the joy of budding. In schizogamous syllids, instead of the whole worm developing into an epitoke, a separate epitoke buds off the original atoke. In the most basic form of schizogamy, it is the posterior part of the worm that metamorphoses into the epitoke, in most cases growing its own separate, fully-developed head before breaking away from the anterior “parent” part (some Syllinae have headless epitokes). In some syllids, another epitoke may begin developing in front of the original epitoke before it breaks away, and possibly even more, so that the animal turns into a chain of developing worms. Others produce a number of epitokes growing in a bunch. After the epitoke(s) break off, the remaining atoke will regenerate any losses. Indeed, the atoke may begin regenerating even before the epitoke breaks off—the left and right sides of the new posterior part grow on either side of the epitoke, and once the epitoke is gone they fuse together down the middle.

Very few syllids have developed true asexual reproduction, where they fragment to give rise to new atokes instead of epitokes. But no survey of syllid budding would be complete without mention of the most bizarre of all syllids, the deep-sea sponge-dwelling Syllis ramosa. In this species (shown above in a drawing from here), buds develop laterally but don’t detach from the parent worm. As these lateral buds grow, they start growing their own lateral buds, so that over time the worm develops into a branched network, spreading through the channels of its hexactinellid host.

Exogone sexoculata, a worm of the interstitial
Published 6 August 2012
Drawings of head and representative chaetae of Exogone sexoculata, from San Martín (2005).

The sort-of-randomly chosen subject of today’s post is the marine annelid worm Exogone (Parexogone) sexoculata, a member of the interstitial fauna around the coast of Australia. A previous record of this species from Italy has since been re-identified as the related species E. gambiae (Lanera et al. 1994). Exogone sexoculata is found among sand, mud, algae and dead coral, and in depths of up to 24 m (San Martín 2005). Despite the species name, it actually has four eyes, plus two eyespots that lack the lenses of the true eyes. As this is a fairly standard arrangement for Exogone species, E. sexoculata can’t really claim to have one of the most distinguishing of species names.

Unidentified species of Exogone (in its epitokous form, perhaps?) from the Biodiversity Institute of Ontario.

Exogone sexoculata is a member of the family Syllidae, whose sometimes dramatic reproductive habits were discussed above. Like other syllids, most Exogone species go through the process known as epitoky, where reproductively mature individuals metamorphose into a more mobile form, with enlarged eyes and parapodia. In the subfamily including Exogone, Exogoninae, the entire animal transforms into an epitoke (rather than epitokes budding off as may happen in other syllids). After releasing its gametes in the water column, the epitoke returns to the substrate and transforms back into the interstitial form. Females of Exogoninae brood their fertilised eggs attached to their body, and juvenile worms hatch out without going through a planktonic larval stage. In Exogone, the brooded eggs are attached on the underside of the female’s body, whereas in other genera brooding may be dorsal. Exogone is also distinguished from other exogonine genera by the absence of a covering of papillae, the presence of only a single pair of tentacular cirri, and palps that are fused along all or almost all of their length. Exogone sexoculata is distinguished from other species in the genus by the absence of dorsal cirri on the second chaeta-bearing segment, its long median antenna, and by features of the chaetae (San Martín 2005).

Systematics of Phyllodocida
<==Phyllodocida [Nereidiformia, Phyllodocemorpha]
    |--+--+--Arkonips topororumPE16
    |  |  |--Fossundecima [Fossundecimidae]PE16
    |  |  |    `--F. konecniorum Thompson 1979W93
    |  |  |--+--NephtyidaeNP10
    |  |  |  `--+--HesionidaeSS07
    |  |  |     |--NereididaePE16
    |  |  |     `--Paralacydonia [Paralacydoniidae]SS07
    |  |  |          `--P. paradoxa Fauvel 1913SS07
    |  |  `--+--AphroditiformiaPE16
    |  |     |--Chrysopetalum [Chrysopetalidae]PE16
    |  |     |    |--C. debilePP64
    |  |     |    `--C. occidentaleKBC03
    |  |     `--Pholoe Johnston 1839H-S86 [PholoidaeRF98]
    |  |          |--P. dorsipapillataPP64
    |  |          |--P. minutaM00
    |  |          `--P. swedmarki Laubier 1975H-S86
    |  `--+--+--GlyceriformiaSS07
    |     |  `--TomopteridaeSS07
    |     |       |--Eotomopteris aldridgei Briggs & Clarkson 1987W93
    |     |       `--TomopterisSS07
    |     |            |--T. catharina [incl. T. helgolandica]B26
    |     |            |--T. nisseni Rosa 1908 [incl. T. longisetis Treadwell 1936, T. opaca Treadwell 1928]H56
    |     |            |--T. pacificaB70
    |     |            |--T. planktonisB26
    |     |            |--T. septentrionalisB26
    |     |            `--T. tentaculata Treadwell 1928H56
    |     `--+--+--TyphloscolecidaeNP10
    |        |  |    |--TyphloscolexNP10
    |        |  |    `--Travisiopsis [incl. Nuchubranchia Treadwell 1928]H56
    |        |  |         |--T. benhami Monro 1936 [incl. Plotobia paucichaeta Treadwell 1943]H56
    |        |  |         |--T. coniceps (Chamberlin 1919) (see below for synonymy)H56
    |        |  |         `--T. lanceolata Southern 1911 [incl. T. atlantica Treadwell 1936]H56
    |        |  `--+--LopadorhynchidaeNP10
    |        |     |    |--Lopadorhynchus varius Treadwell 1943H56
    |        |     |    `--Halyplanes Reibisch 1893 [=Haliplanes; incl. Haliplanella Treadwell 1943]H56
    |        |     |         `--H. gracilis Reibisch 1893 (see below for synonymy)H56
    |        |     `--+--LacydoniidaeRF98
    |        |        `--PhyllodocidaePE16
    |        `--+--SphaerodoridaeF05
    |           |    |--Ephesia gracilisTS02
    |           |    |--SphaerodoropsisPE16
    |           |    |    |--S. garciaalvarezi Moreira, Cacabelos & Troncoso 2004F05
    |           |    |    `--S. parvaPG98
    |           |    `--SphaerodorumBK77
    |           |         |--S. claparedei Greef 1866M62
    |           |         `--S. greefiiBK77
    |           `--+--MyzostomatidaPE16
    |              `--PilargidaeNP10
    |                   |--AncistrosyllisSS07
    |                   |    |--A. groenlandica McIntosh 1879SS07
    |                   |    `--A. tentaculata Treadwell 1941H56
    |                   `--SigambraPE16
    |                        |--S. bassiGAS03
    |                        `--S. hanaokai (Kitamori 1960)H-S86
    `--SyllidaePE16
         |  i. s.: Pterosyllis finmarchicaTS02
         |         AutolytusTS02
         |           |--A. pacificus Treadwell 1943H56
         |           |--A. prismaticusKBC03
         |           |--A. proliferTS02
         |           `--A. varius Treadwell 1941H56
         |         Imajimea Nygren 2004F05
         |           `--*I. japonensis (Imajima & Hartman 1964) [=Autolytus japonensis]F05
         |         Haplosyllis spongicola (Grube 1855) [incl. H. gula Treadwell 1924]H56
         |         Myriana cirrata Treadwell 1931H56
         |         TrypanosyllisH56
         |           |--T. adamanteus Treadwell 1914H56
         |           |--T. coeliacaM62
         |           `--T. zebraBBB-S95
         |--+--Epigamia Nygren 2004RP07, F05
         |  |    |--*E. noroi (Imajima & Hartman 1964) [=Autolytus noroi]F05
         |  |    `--E. magnus Berkeley 1923RP07
         |  `--+--Myrianida pinnigera (Montagy 1808)RP07
         |     `--Proceraea Ehlers 1864RP07, F05 [Procerini]
         |          |  i. s.: P. cornutaPH06
         |          |         P. pleijeli Nygren 2004F05
         |          |--+--P. hanssoni Nygren 2004RP07
         |          |  `--Virchowia clavata Langerhans 1879RP07
         |          `--+--P. aurantiaca Claparède 1868RP07
         |             `--+--P. paraurantiaca Nygren 2003RP07
         |                `--P. rubroproventriculata Nygren & Gidholm 2001RP07
         `--+--+--PionosyllisRP07
            |  |    |--P. augeneri Hartmann-Schröder 1979H-S86
            |  |    |--P. manca Treadwell 1931H56
            |  |    `--P. pulligera (Krohn 1852)RP07
            |  `--+--AmblyosyllisRP07
            |     `--OdontosyllisRP07
            |          |--O. ctenostomaBBB-S95
            |          |--O. enopla Verrill 1900 [incl. Autolytus bidens Treadwell 1941]H56
            |          |--O. gibba Claparède 1863RP07
            |          |--O. maculataKBC03
            |          `--O. octodentata Treadwell 1917H56
            `--+--+--BranchiosyllisRP07
               |  |    |--B. pacifica Rioja 1941H-S86
               |  |    `--B. uncinigeraP71
               |  `--Syllinae [Eurysyllinae]H=S86
               |       |--TyposyllisRP07
               |       |--Paratyposyllis Hartmann-Schröder 1962H-S86
               |       |    `--P. paucicirrata Hartmann-Schröder 1962H-S86
               |       |--Reductotyposyllis Hartmann-Schröder 1974H-S86
               |       |    `--R. atentaculocirrata Hartmann-Schröder 1974H-S86
               |       |--Plakosyllis Hartmann-Schröder 1956H-S86
               |       |    `--P. brevipes Hartmann-Schröder 1956H-S86
               |       |--Eurysyllis Ehlers 1864DW08
               |       |    |--E. nanshaensis Sun & Yang 2004DW08
               |       |    `--E. tuberculataM62
               |       `--SyllisTS02
               |            |--S. armullarisTS02
               |            |--S. gracilis Grube 1840A70
               |            |--S. hyalinaBBB-S95
               |            |--S. krohniiBBB-S95
               |            |--S. licheri Ravara, San Martín & Moreira 2004F05
               |            |--S. proliferaBBB-S95
               |            |--S. spongicolaBBB-S95
               |            `--S. variegataBBB-S95
               `--+--EusyllinaeRP07
                  `--+--Opisthodonta morena Langerhans 1879RP07
                     `--ExogoninaeH-S86
                          |  i. s.: Spermosyllis Claparède 1864H-S86
                          |           `--S. confusa Hartmann-Schröder 1960H-S86
                          |         Brania Quatrefages 1865H-S86
                          |           |--B. articulata Hartmann-Schröder 1982DW08
                          |           |--B. diaphana Ding & Westheide 2008DW08
                          |           |--B. furcelligera (Augener 1913)DW08
                          |           |--B. glandulosa Hartmann-Schröder 1980DW08
                          |           |--B. gracilis Hartmann-Schröder 1960H-S86
                          |           |--B. lumbataBBB-S95
                          |           |--B. oculata Hartmann-Schröder 1960H-S86
                          |           |--B. swedmarki Gidholm 1962H-S86
                          |           `--B. wellfleetensis Pettibone 1956P56
                          |         ProsphaerosyllisDW08
                          |           |--P. campoyi (San Martin, Acero et al. 1982)DW08
                          |           |--P. fujianensis Ding & Westheide 2008DW08
                          |           |--P. hongkongensis Ding & Westheide 2008DW08
                          |           |--P. isabellae (Nogueira, San Martin & Amaral 2001)DW08
                          |           |--P. magnoculata (Hartmann-Schröder 1986)DW08
                          |           |--P. riseri (Perkins 1980)DW08
                          |           |--P. sexpapillata (Hartmann-Schröder 1979)DW08
                          |           `--P. xarifae (Hartmann-Schröder 1960)DW08
                          |         Erinaceusyllis San Martin 2005DW08
                          |           |--*E. erinaceus (Claparède 1863) [=Sphaerosyllis erinaceus] F05
                          |           |--E. belizensis (Russell 1989)DW08
                          |           |--E. centroamericana (Hartmann-Schröder 1959)DW08
                          |           |--E. hartmannschroederae San Martin 2005DW08
                          |           |--E. kathrynae San Martin 2005DW08
                          |           |--E. longicauda (Webster & Benedict 1887) [=Sphaerosyllis longicauda]DW08
                          |           `--E. nana Ding & Westheide 2008DW08
                          |         Parexogone Mesnil & Caullery 1918
                          |           |--P. brevisetosa (Kudenov & Harris 1995) [=Exogone brevisetosa]DW08
                          |           |--P. caribensis (San Martin 1991) [=Exogone caribensis]DW08
                          |           |--P. convoluta (Campoy 1982) [=Exogone convoluta]DW08
                          |           |--P. homosetosa (Hartmann-Schröder 1965) [=Exogone homosetosa]DW08
                          |           |--P. lineata Ding & Westheide 2008DW08
                          |           |--P. molesta (Banse 1972) [=Exogone molesta]DW08
                          |           |--P. sexoculata (Hartmann-Schröder 1979) [=Exogone sexoculata]DW08
                          |           `--P. wilsoni (San Martin 2005) [=Exogone wilsoni]DW08
                          |         Salvatoria McIntosh 1885DW08
                          |           |--S. clavata (Claparède 1863)DW08 [=Brania clavataDW08; incl. Grubea websteriP56]
                          |           |--S. heterocirra (Rioja 1941)DW08
                          |           |--S. koorineclavata San Martin 2005DW08
                          |           `--S. neapolitana (Goodrich 1930) (see below for synonymy)DW08
                          |         Sylline Claparède 1864DW08
                          |--SphaerosyllisRP07
                          `--+--Grubeosyllis Verrill 1900RP07, DW08
                             |    `--G. limbata (Claparède 1868)RP07
                             `--+--ExogoneRP07
                                `--Parapionosyllis Fauvel 1923RP07, H-S86
                                     |--P. brevicirra Day 1954H-S86
                                     |--P. elegans (Pierantoni 1903)H-S86
                                     |--P. gestans (Pierantoni 1903)H-S86
                                     |--P. labronica Cognetti 1965H-S86
                                     |--P. minuta (Pierantoni 1903)H-S86
                                     `--P. subterranea Hartmann-Schröder 1960H-S86
Phyllodocida incertae sedis:
  IchthyotomidaeRF98
  IospilidaeRF98
    |--PhalacrophorusH56
    |    |--P. pictus Greeff 1879 [incl. P. maculatus Treadwell 1943]H56
    |    `--P. uniformis Reibisch 1895 [incl. P. attenuatus Treadwell 1934]H56
    `--Iospilus phalacroides Viguier 1886 [incl. Phalacrophorus niger Treadwell 1943]H56
  NautillienellidaeRF98
  PontodoridaeRF98
  PisionidaeRF98
  PalmyridaeW93
  Epitoka Treadwell 1934H56
    `--E. pelagica Treadwell 1943H56

Halyplanes gracilis Reibisch 1893 [=Haliplanes gracilis; incl. Haliplanella pacifica Treadwell 1943]H56

Salvatoria neapolitana (Goodrich 1930) [=Pionosyllis neapolitana, Grubeosyllis neapolitana; incl. P. subterranea Hartmann-Schröder 1956, Brania subterranea]DW08

Travisiopsis coniceps (Chamberlin 1919) [=Plotobia coniceps; incl. Nuchubranchia palmata Treadwell 1928]H56

*Type species of generic name indicated

References

[A70] Amoureux, L. 1970. Annélides Polychètes du Bassin de chasse d’Ostende: inventaire d’une petite collection. Bulletin de l’Institut Royal des Sciences Naturelles de Belgique 46 (6): 23–24.

[BK77] Barel, C. D. N., & P. G. N. Kramers. 1977. A survey of the echinoderm associates of the north-east Atlantic area. Zoologische Verhandelingen 156: 1–159.

[B26] Bigelow, H. B. 1926. Plankton of the offshore waters of the Gulf of Maine. Bulletin of the Bureau of Fisheries 40 (2): 1–509.

[BBB-S95] Boubezari, K., G. Bitar & D. Bellan-Santini. 1995. Structure et organisation de trois moulières (Mytilus galloprovincialis et Perna perna) de la région d’Alger. Mésogée 54: 63–72.

[B70] Briggs, J. C. 1970. A faunal history of the North Atlantic Ocean. Systematic Zoology 19 (1): 19–34.

[DW08] Ding, Z., & W. Westheide. 2008. Interstitial Exogoninae from the Chinese coast (Polychaeta, Syllidae). Senckenbergiana Biologica 88 (2): 125–159.

[F05] Fernández, J. 2005. Noticia de nuevos táxones para la ciencia en el ámbito Íbero-Balear y Macaronésico. Nuevos táxones animales descritos en la península Ibérica y Macaronesia desde 1994 (IX). Graellsia 61 (2): 261–282.

Franke, H.-D. 1999. Reproduction of the Syllidae (Annelida: Polychaeta). Hydrobiologia 402: 39–55.

[GAS03] Gulbin, V. V., I. S. Arzamastsev & V. M. Shulkin. 2003. Ecological monitoring of the water area of Port Vostochnyi (Wrangel Bay) in the Sea of Japan (1995–2002). Russian Journal of Marine Biology 29 (5): 284–295.

[H56] Hartman, O. 1956. Polychaetous annelids erected by Treadwell, 1891 to 1948, together with a brief chronology. Bulletin of the American Museum of Natural History 109 (2): 239–310.

[H-S86] Hartmann-Schröder, G. 1986. Polychaeta (incl. Archiannelida). In: Botosaneanu, L. (ed.) Stygofauna Mundi: A Faunistic, Distributional, and Ecological Synthesis of the World Fauna inhabiting Subterranean Waters (including the Marine Interstitial) pp. 210–233. E. J. Brill/Dr W. Backhuys: Leiden.

[KBC03] Kashin, I. A., E. V. Bagaveeva & S. F. Chaplygina. 2003. Fouling communities of hydrotechnical constructions in Nakhodka Bay (Sea of Japan). Russian Journal of Marine Biology 29: 267–283.

Lanera, P., P. Sordino & G. San Martín. 1994. Exogone (Parexogone) gambiae, a new species of Exogoninae (Polychaeta, Syllidae) from the Mediterranean Sea. Bolletino di Zoologia 61 (3): 235–240.

[M00] M’Intosh, W. C. 1900. Notes from the Gatty Marine Laboratory, St. Andrews.—No. XX. Annals and Magazine of Natural History, series 7, 5: 254–268, pls 7–8.

[M62] Monniot, F. 1962. Recherches sur les graviers a Amphioxus de la région de Banyuls-sur-Mer. Vie et Milieu 13: 231–322.

[NP10] Nygren, A., & F. Pleijel. 2010. Chimaeras and the origins of the holopelagic annelids Typhloscolecidae and Lopadorhynchidae: a reply to Struck and Halanych (2010). Zoologica Scripta 40 (1): 112–114.

[PE16] Parry, L. A., G. D. Edgecombe, D. Eibye-Jacobsen & J. Vinther. 2016. The impact of fossil data on annelid phylogeny inferred from discrete morphological characters. Proceedings of the Royal Society of London Series B—Biological Sciences 283: 20161378.

[PH06] Passamaneck, Y., & K. M. Halanych. 2006. Lophotrochozoan phylogeny assessed with LSU and SSU data: evidence of lophophorate polyphyly. Molecular Phylogenetics and Evolution 40 (1): 20–28.

[PP64] Peres, J. M., & J. Picard. 1964. Nouveau manuel de bionomie benthique de la mer Mediterranee. Recueil des Travaux de la Station Marine d’Endoume, Bulletin 31 (27): 5–137.

[P56] Pettibone, M. H. 1956. Some polychaete worms of the families Hesionidae, Syllidae, and Nereidae from the east coast of North America. Journal of the Washington Academy of Sciences 46 (9): 281–294.

[P71] Por, F. D. 1971. One hundred years of Suez Canal—a century of Lessepsian migration: retrospect and viewpoints. Systematic Zoology 20 (2): 138–159.

[PG98] Probert, P. K., & S. L. Grove. 1998. Macrobenthic assemblages of the continental shelf and upper slope off the west coast of South Island, New Zealand. Journal of the Royal Society of New Zealand 28: 259–280.

[RF98] Rouse, G. W., & K. Fauchald. 1998. Recent views on the status, delineation and classification of the Annelida. American Zoologist 38: 953–964.

[RP07] Rousset, V., F. Pleijel, G. W. Rouse, C. Erséus & M. E. Siddall. 2007. A molecular phylogeny of annelids. Cladistics 23: 41–63.

San Martín, G. 2005. Exogoninae (Polychaeta: Syllidae) from Australia with the description of a new genus and twenty-two new species. Records of the Australian Museum 57: 39–152.

[SS07] Struck, T. H., N. Schutt, T. Kusen, E. Hickman, C. Bleidorn, D. McHugh & K. M. Halanych. 2007. Annelid phylogeny and the status of Sipuncula and Echiura. BMC Evolutionary Biology 7: 57.

[TS02] Tsetlin, A. B., & M. V. Safonov. 2002. Interstitial polychaetes (Annelida) from the Kandalaksha Bay of the White Sea. Zoologicheskii Zhurnal 81 (8): 899–908.

[W93] Wills, M. A. 1993. Annelida. In: Benton, M. J. (ed.) The Fossil Record 2 pp. 271–278. Chapman & Hall: London.

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