Skip to main content
SpringerLink
Log in

Siboglinid evolution shaped by habitat preference and sulfide tolerance

  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Siboglinids are tube-dwelling annelids that inhabit marine reducing habitats such as anoxic mud bottoms, seeps and hydrothermal vents. As adults, they lack a functional digestive system and rely on chemoautotrophic microbial endosymbionts. Based on morphological analyses, Siboglinidae form a clade with the Sabellariidae, Serpulidae and Sabellidae within the Annelida. The sister group to this clade is the Oweniidae. Three subgroups constitute the Siboglinidae: Frenulata typically inhabit anoxic sediments, Sclerolinium (a.k.a., Monilifera) live on decaying organic matter or reduced sediments and Vestimentifera are mostly found at hydrocarbon seeps and hydrothermal vents. Recent studies suggest that Sclerolinum is the sister group to the Vestimentifera. Within the Vestimentifera, the species inhabiting bare-rock hydrothermal vents represent a derived clade. The seep-inhabiting genus Lamellibrachia forms a basal branch within the Vestimentifera. Trends in siboglinid evolution are most notable with regard to the level of sulfide tolerance and type of substrate. Basal groups inhabit soft substrate with only slightly elevated sulfide levels, whereas more derived species colonize hard substrate and tolerate elevated temperatures and high levels of sulfide. The type of substrate correlates with tube morphology and the function of the opisthosome. The role of the symbionts in habitat selection needs further investigation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Arp, A. J., J. J. Childress & R. D. Vetter, 1987. The sulphide-binding protein in the blood of the vestimentiferan tube-worm, Riftia pachyptila, is the extracellular haemoglobin. J. exp. Biol. 128: 139–158.

    Google Scholar 

  • Black, M. B., K. M. Halanych, P. A. Y. Maas, W. R. Hoeh, J. Hashimoto, D. Desbruyères, R. A. Lutz & R. C. Vrijenhoek, 1997. Molecular systematics of vestimentiferan tubeworms from hydrothermal vents and cold-water seeps. Mar. Biol. 130: 141–149.

    Google Scholar 

  • Bartolomaeus, T., 1995. Structure and formation of the uncini in Pectinaria koreni, Pectinaria auricoma (Terebellida) and Spirorbis spiorbis (Sabellida): implications for annelid phylogeny and the position of the Pogonophora. Zoomorphology 115: 161–177.

    Google Scholar 

  • Boore, J. L. & W. M. Brown, 2000. Mitochondrial genomes of Galathealinum, Helobdella, and Platynereis: sequence and gene arrangement comparisons indicate that Pogonophora is not a phylum and Annelida and Arthropoda are not sister taxa. Mol. Biol. Evol. 17: 87–106.

    PubMed  Google Scholar 

  • Cavanaugh, C. M., S. L. Gardiner, M. L. Jones, H. W. Jannasch & J. B. Waterbury, 1981. Prokaryotic cells in the hydorthermal vent tube worm Riftia pachyptila Jones: possible chemoautotrophic symbionts. Science 213: 340–342.

    Google Scholar 

  • Childress, J. J. & C. R. Fisher, 1992. The biology of hydrothermal vent animals: physiology, biochemistry and autotrophic symbiosis. In Barnes, M. (ed.), Oceanography and Marine Biology Annual Review Vol. 30. Aberdeen University Press, Aberdeen: 337–441.

    Google Scholar 

  • Craddock, C., W. R. Hoeh, R. G. Gustafson, R. A. Lutz, J. Hashimoto & R. J. Vrijenhoek, 1995. Evolutionary relationships among deep-sea mytilids (Bivalvia: Mytilidae) from hydrothermal vents and cold-water methane/sulfide seeps. Mar. Biol. 121: 477–485.

    Google Scholar 

  • Dando, P. R., A. J. Southward, E. C. Southward, D. R. Dixon, A. Crawford & M. Crawford, 1992. Shipwrecked tubeworms. Nature 356: 667.

    Google Scholar 

  • Felbeck, H, 1981. Chemoautotrophic potential of the hydrothermal vent tubeworm Riftia pachyptila. Science 213: 336–338.

    Google Scholar 

  • Feldman, R.A., M. B. Black, C. S. Cary, R.A. Lutz & R. C. Vrijenhoek, 1997. Molecular phylogenetics of bacterial endosymbionts and their vestimentiferan hosts. Mol. Mar. Bio. Biotechnol. 6: 268–277.

    Google Scholar 

  • Fisher, C. R., 1996. Ecophysiology of primary production at deepsea vents and seeps. In Uiblein, F., J. Ott & M. Stachowtisch (eds), Deep-Sea and Extreme Shallow-Water Habitats: Affinities and Adaptations. Biosystematics and Ecology Series Vol. 11: 313–336.

  • Green, A. W., T. Gotoh, T. Suzuki, F. Zal, F. H. Lallier, A. Toulmond & S. N. Vinogradov, 2001. Observations of large, noncovalent globin subassemblies in the appr. 3600 KDa hexagonal bilayer hemoglobins by electrospray ionization time-of-flight spectrometry. J. Mol. Biol. 309: 553–560.

    PubMed  Google Scholar 

  • Halanych, K. M., R. A. Lutz & R. C. Vrijenhoek, 1998. Evolutionary origins and age of vestimentiferan tube-worms. Cah. Biol. Mar. 39: 355–358.

    Google Scholar 

  • Halanych, K. M., R. A. Feldman & R. C. Vrijenhoek, 2001. Molecular evidence that Sclerolinum brattstromi is closely related to vestimentiferans, not frenulate pogonophorans (Siboglinidae, Annelida). Biol. Bull. 201: 65–75.

    PubMed  Google Scholar 

  • Hutchings, P. A., 2000. Familiy Oweniidae. In Beesley, P. L., G. J. B. Ross & C. J. Glasby (eds), Polychaetes and Allies: The Southern Synthesis. Fauna of Australia Vol. 4A. CSIRO Publishing, Melbourne: 173–176.

    Google Scholar 

  • Ivanov, A. V., 1963. Pogonophora. Academic Press, London. 479 pp.

    Google Scholar 

  • Jones, M. L., 1981. Riftia pachyptila, new genus, new species, the vestimentiferan from the Galapagos Rift geothermal vents (Pogonophora). Proc. natl. Acad. Sci. 93: 1295–1313.

    Google Scholar 

  • Jones, M. L., 1985. On the Vestimentifera, new phylum: six new species, and other taxa, from hydrothermal vents and elsewhere. Bull. Biol. Soc. Wash. 6: 117–185.

    Google Scholar 

  • Kojima, S., T. Hashimoto, M. Hasegawa, S. Murata, S. Ohta, H. Seki & N. Okada, 1993. Close phylogenetic relationship between Vestimentifera (tube worms) and Annelida revealed by the amino acid sequence of elongation factor-1?. J. Mol. Evol. 37: 66–70.

    PubMed  Google Scholar 

  • Main, M. B. & W. G. Nelson, 1988. Tolerance of the Sabellariid polychaete Phragmatopoma lapidosa Kinberg to burial, turbidity and hydrogen sulfide. Mar. Environ. Res. 26: 39–55.

    Google Scholar 

  • McHugh, D., 1997. Molecular evidence that echiurans and pogonophorans are derived annelids. Proc. natl. Acad. Sci. U.S.A. 94: 8006–8009.

    PubMed  Google Scholar 

  • Newman, W. A., 1985. The abyssal hydrothermal vent invertebrate fauna: a glimpse of antiquity? Bull. Biol. Soc.Wash. 6: 231–242.

    Google Scholar 

  • Peek, A. S., R. G. Gustafson & R. C. Vrijenhoek, 1997. Evolutionary relationships of deep-sea hydrothermal vent and coldwater seep clams (Bivalvia: Vesicomyidae): results from the mitochondrial cytochrome oxidase subunit I. Mar. Biol. 130: 151–161.

    Google Scholar 

  • Powell, M. A. & G. N. Somero, 1983. Blood components prevent sulfide poisoning of respiration of the hydrothermal vent tubeworm. Science 219: 297–299.

    Google Scholar 

  • Rau, G. H., 1981. Hydrothermal vent clam and vent tubeworm 13C/12C: further evidence of a nonphotosynthetic food source. Science 213: 338–339.

    Google Scholar 

  • Rouse, G., 2001. A cladistic analysis of Siboglinidae Caullery, 1914 (Polychaeta, Annelida): formerly the phyla Pogonophora and Vestimentifera. Zool. J. linn. Soc. 132: 55–80.

    Google Scholar 

  • Rouse, G. & K. Fauchald, 1995. The articulation of annelids. Zool. Scr. 24: 269–301.

    Google Scholar 

  • Rouse, G. & K. Fauchald, 1997. Cladistics and the polychaetes. Zool. Scr. 26: 139–204.

    Google Scholar 

  • Schulze, A. in press. Phylogeny of Vestimentifera (Siboglinidae, Annelida) inferred from morphology. Zool. Scr.

  • Scott, K. M. & C. R. Fisher, 1995. Physiological ecology of sulfide metabolism in hydrothermal vent and cold seep vesicomyid clams and vestimentiferan tube worms. Am. Zool. 35: 102–111.

    Google Scholar 

  • Shank, T., M. B. Black, K. M. Halanych, R. A. Lutz & R. C. Vrijenhoek, 1999. Miocene radiation of deep-sea hydrothermal vent shrimp (Caridea: Bresiliidae): evidence from mitochondrial cytochrome oxidase subunit 1. Mol. Phylogenet. Evol. 13: 244–254.

    PubMed  Google Scholar 

  • Sibuet, M. & K. Olu, 1998. Biogeography, biodiversity, and fluid dependence of deep-sea cold-seep communities at active and passive margins. Deep-Sea Res. II 45: 517–567.

    Google Scholar 

  • Smith, R. P., R. C. Cooper, T. Engen, E. R. Hendrickson, M. Katz, T. H. Milby, J. B. Mudd, A. T. Rossano & J. Redmund Jr., 1979. Hydrogen Sulfide. University Park Press, Baltimore. 183 pp.

    Google Scholar 

  • Southward, A. J., & E. C. Southward, 1981. Dissolved organic matter and the nutrition of the Pogonophora: a reassessment based on recent studies of their morphology and biology. Kieler Meeresforsch. 5: 445–453.

    Google Scholar 

  • Southward, E. C., 1972. On some Pogonophora from the Caribbean and the Gulf of Mexico. Bull. mar. Sci. 22: 739–776.

    Google Scholar 

  • Southward, E. C., 1988. Development of the gut and segmentation of newly settled stages of Ridgeia (Vestimentifera): Implications for the relationship between Vestimentifera and Pogonophora. J. mar. biol. Ass. U.K. 68: 465–487.

    Google Scholar 

  • Southward, E. C., 1993. Pogonophora. In Harrison, F. W. & Rice, M. E. (eds), Onychophora, Chilopoda, and Lesser Protostomata. Microscopic Anatomy of the Invertebrates Vol. 12, Wiley-Liss (NY): 327–369.

  • Southward, E. C., 1999. Development of Perviata and Vestimentifera (Pogonophora). Hydrobiologia 402: 185–202.

    Google Scholar 

  • Southward, E. C., 2000. Class Pogonophora. In P. L. Beesley, G. J. B. Ross & C. J. Glasby (eds), Polychaetes and Allies: The Southern Synthesis. Fauna of Australia Vol. 4A. CSIRO Publishing, Melbourne: 331–351.

    Google Scholar 

  • Suzuki, T., T. Takagi, T. Furokohri & S. Ohta, 1989. The deepsea tube worm hemoglobin: subunit structure and phylogenetic relationship with annelid hemoglobin. Zool. Scr. 6: 915–926.

    Google Scholar 

  • Suzuki, T., T. Takagi & S. Ohta, 1993. N-Terminal amino acid sequences of 440 kDa hemoglobins of the deep-sea tube worms, Lamellibrachia sp.1, Lamellibrachia sp. 2 and slender vestimentifera gen. sp. 1 evolutionary relationship with annelid hemoglobins. Zool. Sci. 10: 141–146.

    PubMed  Google Scholar 

  • Terwilliger, R. C., N. B. Terwilliger, G. M. Hughes, A. J. Southward & E. C. Southward, 1987. Studies on the haemoglobins of the small Pogonophora. J. mar. biol. Ass. U.K. 67: 219–234.

    Google Scholar 

  • Tunnicliffe, V., 1988. Biogeography and evolution of hydrothermalvent fauna in the eastern Pacific Ocean. Proc. r. Soc. Lond. B 233: 347–366.

    Google Scholar 

  • Tunnicliffe, V., A. G. McArthur. & D. McHugh, 1998. A biogeographical perspective of the deep-sea hydrothermal vent fauna. Adv. mar. Biol. 34: 353–442.

    Google Scholar 

  • Uschakov, P. V., 1933. Eine neue Form aus der Familie Sabellidae (Polychaeta). Zool. Anz. 104: 205–208.

    Google Scholar 

  • Van der Land, J. & A. Nørrevang, 1975. The systematic position of Lamellibrachia (Annelida, Vestimentifera). Z. zool. Syst. Evol.-forsch., Sonderheft 1: 86–101.

    Google Scholar 

  • Van Dover, C. L., 2000. The Ecology of Deep-Sea Hydrothermal Vents. Princeton University Press, Princeton (NJ). 424 pp.

    Google Scholar 

  • Warren, L. M. & R. P. Dales, 1980. Glucose degradation in the polychaete annelid Owenia fusiformis Delle Chiaje under anaerobic conditions. Comp. Biochem. Phys. 65B: 443–445.

    Google Scholar 

  • Webb, M., 1964. The posterior extremity of Siboglinum fiordicum (Pogonophora). Sarsia 15: 33–36.

    Google Scholar 

  • Webb, M., 1969. Lamellibrachia barhami, gen. nov., spec. nov. (Pogonophora) from the Northeast Pacific. Bull. mar. Sci. 19: 18–47.

    Google Scholar 

  • Weber, R. E., 1980. Functions of invertebrate hemoglobins with special reference to adaptations to envrionmental hypoxia. Am. Zool. 20: 79–101.

    Google Scholar 

  • Wells, R. G. M., R. P. Dales & L. M. Warren, 1981. Oxygen equilibrium characteristics of the erythrocruorin (extracellular hemoglobin) from Owenia fusiformis Delle Chiaje (Polychaeta: Oweniidae). Comp. Biochem. Physiol. A70: 11–113.

    Google Scholar 

  • Williams, N. C., D. R. Dixon, E. C. Southward & P. W. H. Holland, 1993. Molecular evolution and diversification of the vestimentiferan tube worms. J. mar. biol. Ass. U.K. 73: 437–452.

    Google Scholar 

  • Young, C. M., E. Vázquez, A. Metaxas & P. A. Tyler, 1996. Embryology of vestimentiferan tube worms from deep-sea methane/ sulphide seeps. Nature 381: 514–516.

    Google Scholar 

  • Yuasa, H. J., B. N. Green, T. Takagi, N. Suzuki, S. N. Vinogradov & T. Suzuki, 1996. Electrospray ionization mass spectrometric composition of the 400 kDa hemoglobin from the pogonophoran Oligobrachia mashikoi and the primary structures of three major globin chains. Biochim. Biophys. Acta 1296: 235–244.

    PubMed  Google Scholar 

  • Zal, F., F. H. Lallier, B. N. Green, S. N. Vinogradov & A. Toulmond, 1996. The multi-hemoglobin system of the hydrothermal vent tube worm Riftia pachyptila. J. Biol. Chem. 271: 8875–8881.

    PubMed  Google Scholar 

Download references

Author information

Author notes

  1. Anja Schulze

    Present address: Department of Invertebrate Zoology, Harvard University, MCZ, 26 Oxford Street, Cambridge, MA, 02138, U.S.A

Authors and Affiliations

  1. Department of Systematic Biology, National Museum of Natural History, MRC 16, Smithsonian Institution, Washington, DC, 20560, U.S.A.

    Anja Schulze

  2. Department of Invertebrate Zoology, Harvard University, MCZ, 26 Oxford Street, Cambridge, MA, 02138, U.S.A

    Kenneth M. Halanych

Authors
  1. Anja Schulze
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kenneth M. Halanych
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kenneth M. Halanych.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schulze, A., Halanych, K.M. Siboglinid evolution shaped by habitat preference and sulfide tolerance. Hydrobiologia 496, 199–205 (2003). https://doi.org/10.1023/A:1026192715095

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1026192715095

Search

Navigation