Skip to main content

Thank you for visiting You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Sulphide mining by the superextensile foot of symbiotic thyasirid bivalves


In a symbiotic association between an invertebrate host and chemoautotrophic bacteria, each partner has different metabolic requirements, and the host typically supplies the bacteria with necessary reduced chemicals (sulphide or methane). Some combination of anatomical, physiological and behavioural adaptations in the host often facilitates uptake and transport of reduced chemicals to the symbionts1,2,3,4. We have studied five species of bivalve molluscs of the family Thyasiridae (that is, thyasirids) three of which harbour chemoautotrophic bacteria. Here we show that the symbiotic bivalves extend their feet to form elongated and ramifying burrows in the sediment, most probably to gain access to reduced sulphur. Closely related bivalves (including some thyasirid species) without bacterial symbionts show no comparable foot extension behaviour. The length and number of burrows formed by chemosymbiotic thyasirids are related to the concentration of hydrogen sulphide in the sediment. The burrows are formed by the foot of each bivalve, which can extend up to 30 times the length of the shell, and may be the most extreme case of animal structure elongation documented to date.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Figure 1: Partial X-radiograph of chemosymbiotic thyasirids burrowing in sediment two weeks after introduction.
Figure 2: Typical structure of sulphide mining burrows formed by chemosymbiotic thyasirids in low and high sulphide conditions.


  1. Childress, J. J., Felbeck, H. & Somero, G. N. Symbiosis in the deep sea. Sci. Am. 256, 114–120 (1986)

    Google Scholar 

  2. Le Pennec, M., Beninger, P. G. & Herry, A. Feeding and digestive adaptations of bivalve molluscs to sulphide-rich habitats. Comp. Biochem. Physiol. A 111, 183–189 (1995)

    Article  Google Scholar 

  3. Julian, D., Gaill, F., Wood, E., Arp, A. J. & Fisher, C. R. Roots as a site of hydrogen sulfide uptake in the hydrocarbon seep vestimentiferan Lamellibrachia sp. J. Exp. Biol. 202, 2245–2257 (1999)

    CAS  Google Scholar 

  4. Giere, O., Conway, N. M., Gastrock, G. & Schmidt, C. ‘Regulation’ of gutless annelid ecology by endosymbiotic bacteria. Mar. Ecol. Prog. Ser. 68, 287–299 (1991)

    ADS  Article  Google Scholar 

  5. Dando, P. R., Southward, A. J. & Southward, E. C. Chemoautotrophic symbionts in the gills of the bivalve mollusc Lucinoma borealis and the sediment chemistry of its habitat. Proc. R. Soc. Lond. B 227, 227–247 (1986)

    ADS  CAS  Article  Google Scholar 

  6. Dando, P. R. & Southward, A. J. Chemoautotrophy in bivalve molluscs of the genus Thyasira. J. Mar. Biol. Assoc. UK 66, 915–929 (1986)

    CAS  Article  Google Scholar 

  7. Seilacher, A. Aberrations in bivalve evolution related to photo- and chemosymbiosis. Hist. Biol. 3, 289–311 (1990)

    Article  Google Scholar 

  8. Allen, J. A. On the basic form and adaptations to habitat in the Lucinacea (Eulamellibranchia). Phil. Trans. R. Soc. Lond. B 241, 421–484 (1958)

    ADS  Article  Google Scholar 

  9. Allen, J. A. Function of the foot in the Lucinacea (Eulamellibranchia). Nature 171, 1117–1118 (1953)

    CAS  Article  Google Scholar 

  10. Payne, C. M. & Allen, J. A. The morphology of deep-sea Thyasiridae (Mollusca: Bivalvia) from the Atlantic Ocean. Phil. Trans. R. Soc. Lond. B 334, 481–562 (1991)

    ADS  Article  Google Scholar 

  11. Southward, E. C. Gill symbionts in thyasirids and other bivalve molluscs. J. Mar. Biol. Assoc. UK 66, 889–914 (1986)

    Article  Google Scholar 

  12. Trueman, E. R., Brown, A. C. & Stenton-Dozey, J. Blood flow in a burrowing bivalve at pedal extension and retraction. J. Moll. Stud. 52, 265–266 (1986)

    Article  Google Scholar 

  13. Arp, A. J., Childress, J. J. & Fisher, C. R. Metabolic and blood gas transport characteristics of the hydrothermal vent bivalve Calyptogena magnifica. Physiol. Zool. 57, 648–662 (1984)

    CAS  Article  Google Scholar 

  14. Childress, J. J., Fisher, C. R., Favuzzi, J. A., Arp, A. J. & Oros, D. R. The role of a zinc-based, serum-borne sulphide-binding component in the uptake and transport of dissolved sulphide by the chemoautotrophic symbiont-containing clam Calyptogena elongata. J. Exp. Biol. 179, 131–158 (1993)

    CAS  Google Scholar 

  15. Stanley, S. M. Relation of shell form to life habits in the bivalvia (Mollusca). Geol. Soc. Am. Mem. 125, 1–293 (1970)

    Google Scholar 

  16. Zuschin, M., Mandic, O., Harzhauser, M. & Pervesler, P. Fossil evidence for chemoautotrophic bacterial symbiosis in the thyasirid bivalve Thyasira michelottii from the Middle Miocene (Badenium) of Austria. Hist. Biol. 15, 123–134 (2001)

    Article  Google Scholar 

  17. McAlester, A. L. Evolutionary and systematic implications of a transitional ordovician lucinoid bivalve. Malacologia 3, 433–439 (1966)

    Google Scholar 

  18. Reid, R. G. B. & Brand, D. G. Sulfide-oxidizing symbiosis in lucinaceans: implications for bivalve evolution. Veliger 29, 3–24 (1986)

    Google Scholar 

  19. Gilboa-Garber, N. Direct spectrophotometric determination of inorganic sulfide in biological materials and in other complex mixtures. Anal. Biochem. 43, 129–133 (1971)

    CAS  Article  Google Scholar 

Download references


We thank J. B. C. Jackson, N. D. Holland and E. Kisfaludy for discussion and advice, and A. Aadnesen, P. Johannessen, T. Sorlie and T. Høisæter for help in collecting thyasirids and running experiments at the University of Bergen Biological Station, Espegrend. We are grateful to O. K. Dalland and A. Lerheim for allowing the use of X-ray equipment at the veterinary clinic at Stend, Norway. This work was supported by the Scripps Institution of Oceanography graduate department, the Baxter and Alma Ricard Foundation, and the National Science Foundation.

Author information

Authors and Affiliations


Corresponding author

Correspondence to Suzanne C. Dufour.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Dufour, S., Felbeck, H. Sulphide mining by the superextensile foot of symbiotic thyasirid bivalves. Nature 426, 65–67 (2003).

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI:

This article is cited by


By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.


Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing