Marine Biology

, Volume 156, Issue 3, pp 395–405 | Cite as

Spawning and development in Osedax boneworms (Siboglinidae, Annelida)

  • Greg W. Rouse
  • Nerida G. Wilson
  • Shana K. Goffredi
  • Shannon B. Johnson
  • Tracey Smart
  • Chad Widmer
  • Craig M. Young
  • Robert C. Vrijenhoek
Original Paper


We report observations on spawning and early development in bone-eating worms of the genus Osedax. Individual females of Osedax rubiplumus were observed at 1820 m depth freely spawning hundreds of oocytes, and females of an undescribed species, Osedax “orange collar”, were observed spawning in laboratory aquaria. Cytological and molecular analysis of the spawned oocytes of two Osedax species revealed no evidence for the bacterial endosymbionts that the female worms require for their nutrition, suggesting that the bacteria must be acquired later from the environment, as they are in other siboglinids. Individual O. “orange collar” females released an average of 335 (±130) eggs per day, but the number of oocytes spawned per day varied greatly, suggesting that not all the females spawned daily. Fertilization rates of the spawned oocytes varied from 0 to 100%, though most females showed nearly 100% fertilization rates. Oocytes spawned in the laboratory at 4–6°C were negatively buoyant. If fertilized, these oocytes extruded polar bodies and then after at least four hours cleaved unequally. Subsequent cleavages occurred in a spiral pattern at roughly 2-h intervals, resulting in free-swimming trochophore larvae after 24 h. These lecithotrophic trochophores swam for 9–16 days before settling with several hooked chaetae, similar to those of dwarf Osedax males. The larval life span of the Osedax species studied in the laboratory appears to be shorter than in closely related Vestimentifera. Osedax rubiplumus, on the other hand, has much larger oocytes and so may have greater dispersal potential than these other Osedax species. The high fecundity and apparently continuous reproduction of Osedax boneworms permits the opportunistic exploitation of sunken vertebrate bones.


Fertilization Rate Hydrothermal Vent Remotely Operate Vehicle Supplemental Video Grey Whale 



Thanks to the pilots of ROV Tiburon and ROV Ventana and crews of RV Western Flyer and RV Point Lobos. We also thank Eddie Kisfaludy (SIO) for essential aquarium facilities, Lonny Lundsten (MBARI) for edited videos, Evelyn York (SIO) for SEM assistance, and Larry Chlebeck (SIO) and Shawn Arellano (OIMB) for laboratory assistance. We thank Victoria J. Orphan at the California Institute of Technology for use of FISH microscopy facilities. Funding was provided by The David and Lucille Packard Foundation (to MBARI), by Scripps Institution of Oceanography (to GWR), and by NSF (OCE-0118733 and OCE-0527139 to CMY). Work carried out in this study complies with the current laws in the USA.

Supplementary material

Supplement Videos 1 (MP4 9706 kb)

Supplement Videos 2 (MP4 4269 kb)

Supplement Videos 3 (MP4 10982 kb)


  1. Bakke T (1976) The early embryos of Siboglinum fiordicum Webb (Pogonophora) reared in the laboratory. Sarsia 60:1–11CrossRefGoogle Scholar
  2. Balzer F (1935) Experiments on sex-developments in Bonellia. Collect Net 10:102–108Google Scholar
  3. Braby CE, Rouse GW, Johnson SB, Jones WJ, Vrijenhoek RC (2007) Bathymetric and temporal variation among Osedax boneworms and associated megafauna on whale-falls in Monterey Bay, California. Deep Sea Res Part I Oceanogr Res Pap 54:1773–1791. doi: CrossRefGoogle Scholar
  4. Carey SC, Felbeck H, Holland ND (1989) Observations of the reproductive biology of the hydrothermal vent tube worm Riftia pachyptila. Mar Ecol Prog Ser 52:89–94. doi: CrossRefGoogle Scholar
  5. Dahlgren T, Wiklund H, Kallstrom B, Lundalv T, Smith CR, Glover AG (2006) A shallow-water whale-fall experiment in the north Atlantic. Cah Biol Mar 47:385–389Google Scholar
  6. Fujikura K, Fujiwara Y, Kawato M (2006) A new species of Osedax (Annelida: Siboglinidae) associated with whale carcasses off Kyushu, Japan. Zool Sci 23:733–740. doi: CrossRefGoogle Scholar
  7. Glover AG, Kallstrom B, Smith CR, Dahlgren TG (2005) World-wide whale worms? A new species of Osedax from the shallow north Atlantic. Proc R Soc Ser B 272:2587–2592CrossRefGoogle Scholar
  8. Goffredi SK, Johnson S, Vrijenhoek RC (2007) Genetic diversity and potential function of microbial symbionts associated with newly discovered species of Osedax polychaete worms. Appl Environ Microbiol 73:2314–2323. doi: CrossRefGoogle Scholar
  9. Goffredi SK, Orphan VJ, Rouse GW, Jahnke L, Embaye T, Turk K, Lee R, Vrijenhoek RC (2005) Evolutionary innovation: a bone-eating marine symbiosis. Environ Microbiol 7:1369–1378. doi: CrossRefGoogle Scholar
  10. Grant A (1990) Mode of development and reproductive effort in marine invertebrates: Should there be any relationship? Funct Ecol 4:128–130Google Scholar
  11. Halanych KM, Feldman RA, Vrijenhoek RC (2001) Molecular evidence that Sclerolinum brattstromi is closely related to vestimentiferans, not to frenulate pogonophorans (Siboglinidae, Annelida). Biol Bull 201:65–75. doi: CrossRefGoogle Scholar
  12. Hart MW, Byrne M, Smith MJ (1997) Molecular phylogenetic analysis of life-history evolution in asterinid starfish. Evolut Int J Org Evolut 51:1848–1861. doi: CrossRefGoogle Scholar
  13. Harvey PH, Pagel M (1991) The comparative method in evolutionary biology. Oxford University Press, OxfordGoogle Scholar
  14. Hilário A, Young CM, Tyler PA (2005) Sperm storage, internal fertilization, and embryonic dispersal in vent and seep tubeworms (Polychaeta: Siboglinidae: Vestimentifera). Biol Bull 208:20–28. doi: CrossRefGoogle Scholar
  15. Jaccarini V, Schembri PJ, Rizzo M (1983) Sex determination and larval sexual interaction in Bonellia viridis Rolando (Echiura: Bonelliidae). J Exp Mar Biol Ecol 66:25–40. doi: CrossRefGoogle Scholar
  16. Jones WJ, Johnson SB, Rouse GW, Vrijenhoek RC (2008) Marine worms (genus Osedax) colonize cow bones. Proc R Soc Ser B 275:387–391. doi: CrossRefGoogle Scholar
  17. MacArthur RH, Wilson EO (1967) The theory of island biogeography. Princeton University Press, PrincetonGoogle Scholar
  18. MacDonald IR, Tunnicliffe V, Southward EC (2002) Detection of sperm transfer and synchronous fertilization in Ridgeia piscesae at Endeavour Segment, Juan de Fuca Ridge. Cah Biol Mar 43:395–398Google Scholar
  19. Marsh AG, Mullineaux LS, Young CM, Manahan DT (2001) Larval dispersal potential of the tubeworm Riftia pachyptila at deep-sea hydrothermal vents. Nature 411:77–80. doi: CrossRefGoogle Scholar
  20. McHugh D, Rouse GW (1998) Life history evolution of marine invertebrates—new views from phylogenetic systematics. Trends Ecol Evol 13:182–186. doi: CrossRefGoogle Scholar
  21. Miyake H, Tsukahara J, Hashimoto J, Uematsu K, Maruyama T (2006) Rearing and observation methods of vestimentiferan tubeworm and its early development at atmospheric pressure. Cah Biol Mar 47:471–475Google Scholar
  22. Nussbaumer AD, Fisher CR, Bright M (2006) Horizontal endosymbiont transmission in hydrothermal vent tubeworms. Nature 441:345–348. doi: CrossRefGoogle Scholar
  23. Olive PJW (1985) Covariability of reproductive traits in marine invertebrates: implications for the phylogeny of the lower invertebrates. In: Conway Morris S, George D, Gibson R, Platt HM (eds) The origins and relationships of lower invertebrates. Clarendon Press, Oxford, pp 42–59Google Scholar
  24. Ramirez-Llodra E (2002) Fecundity and life-history strategies in marine invertebrates. Adv Mar Biol 43:87–170. doi: CrossRefGoogle Scholar
  25. Rouse GW (2001) A cladistic analysis of Siboglinidae Caullery, 1914 (Polychaeta, Annelida): formerly the phyla Pogonophora and Vestimentifera. Zool J Linn Soc 132:55–80. doi: CrossRefGoogle Scholar
  26. Rouse GW, Fitzhugh K (1994) Broadcasting fables: is external fertilization really primitive? Sex, size and larvae in sabellid polychaetes. Zool Scr 23:271–312. doi: CrossRefGoogle Scholar
  27. Rouse GW, Goffredi SK, Vrijenhoek RC (2004) Osedax: bone-eating marine worms with dwarf males. Science 305:668–671. doi: CrossRefGoogle Scholar
  28. Rouse GW, Worsaae K, Johnson SB, Jones WJ, Vrijenhoek RC (2008) Acquisition of dwarf male ‘harems’ by recently settled females of Osedax roseus n. sp. (Siboglinidae; Annelida). Biol Bull 214:67–82CrossRefGoogle Scholar
  29. Smith CR, Baco AR (2003) Ecology of whale falls at the deep sea floor. Oceanogr Mar Biol 41:311–354Google Scholar
  30. Southward EC (1999) Development of Perviata and Vestimentifera (Pogonophora). Hydrobiologia 402:185–202CrossRefGoogle Scholar
  31. Southward EC, Coates KA (1989) Sperm masses and sperm transfer in a Vestimentiferan, Ridgeia piscesae Jones 1985 (Pogonophora Obturata). Can J Zool 67:2776–2781CrossRefGoogle Scholar
  32. Southward EC, Schulze A, Gardiner SL (2005) Pogonophora (Annelida): form and function. Hydrobiologia 535–536:227–251. doi: Google Scholar
  33. Staver JM, Strathmann RR (2002) Evolution of fast development of planktonic embryos to early swimming. Biol Bull 203:58–69. doi: CrossRefGoogle Scholar
  34. Stearns SC (1992) The evolution of life histories. Oxford University Press, OxfordGoogle Scholar
  35. Van Dover CL (1994) In situ spawning of hydrothermal vent tubeworms (Riftia pachyptila). Biol Bull 186:134–135. doi: CrossRefGoogle Scholar
  36. Vrijenhoek RC, Collins PC, Van Dover CL (2008a) Bone-eating marine worms: habitat specialists or generalists? Proc R Soc Lond B Biol Sci 275:1963–1964. doi: CrossRefGoogle Scholar
  37. Vrijenhoek RC, Johnson SB, Rouse GW (2008b) Bone-eating Osedax females and their harems of dwarf males are recruited from a common larval pool. Mol Ecol 17:4535–4544. doi: CrossRefGoogle Scholar
  38. Young CM (2003) Reproduction, development and life history traits. In: Tyler PA (ed) Ecosystems of the World, vol 28. Ecosystems of the Deep Oceans Elsevier, Amsterdam Google Scholar
  39. Young CM, Vásquez E, Metaxas A, Tyler PA (1996) Embryology of vestimentiferan tube worms from deep-sea methane/sulphide seeps. Nature 381:514–516. doi: CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Greg W. Rouse
    • 1
  • Nerida G. Wilson
    • 1
  • Shana K. Goffredi
    • 2
  • Shannon B. Johnson
    • 3
  • Tracey Smart
    • 4
  • Chad Widmer
    • 5
  • Craig M. Young
    • 4
  • Robert C. Vrijenhoek
    • 3
  1. 1.Scripps Institution of Oceanography, UCSDLa JollaUSA
  2. 2.California Institute of TechnologyPasadenaUSA
  3. 3.Monterey Bay Aquarium Research InstituteMoss LandingUSA
  4. 4.Oregon Institute of Marine Biology, University of OregonCharlestonUSA
  5. 5.Monterey Bay AquariumMontereyUSA

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