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.

Tubicolous enteropneusts from the Cambrian period


This article has been updated


Hemichordates are a marine group that, apart from one monospecific pelagic larval form, are represented by the vermiform enteropneusts and minute colonial tube-dwelling pterobranchs. Together with echinoderms, they comprise the clade Ambulacraria1. Despite their restricted diversity, hemichordates provide important insights into early deuterostome evolution, notably because of their pharyngeal gill slits2. Hemichordate phylogeny has long remained problematic3,4, not least because the nature of any transitional form that might serve to link the anatomically disparate enteropneusts and pterobranchs is conjectural. Hence, inter-relationships have also remained controversial. For example, pterobranchs have sometimes been compared to ancestral echinoderms1. Molecular data identify enteropneusts as paraphyletic, and harrimaniids5,6,7,8 as the sister group of pterobranchs. Recent molecular phylogenies suggest that enteropneusts are probably basal within hemichordates, contrary to previous views9, but otherwise provide little guidance as to the nature of the primitive hemichordate7,8. In addition, the hemichordate fossil record is almost entirely restricted to peridermal skeletons of pterobranchs, notably graptolites10,11. Owing to their low preservational potentials, fossil enteropneusts are exceedingly rare12,13,14,15, and throw no light on either hemichordate phylogeny or the proposed harrimaniid–pterobranch transition. Here we describe an enteropneust, Spartobranchus tenuis (Walcott, 1911), from the Middle Cambrian-period (Series 3, Stage 5) Burgess Shale. It is remarkably similar to the extant harrimaniids, but differs from all known enteropneusts in that it is associated with a fibrous tube that is sometimes branched. We suggest that this is the precursor of the pterobranch periderm, and supports the hypothesis that pterobranchs are miniaturized and derived from an enteropneust-like worm5,6. It also shows that the periderm was acquired before size reduction and acquisition of feeding tentacles, and that coloniality emerged through aggregation of individuals, perhaps similar to the Cambrian rhabdopleurid Fasciculitubus11. The presence of both enteropneusts and pterobranchs in Middle Cambrian strata, suggests that hemichordates originated at the onset of the Cambrian explosion.

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

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Prices vary by article type



Prices may be subject to local taxes which are calculated during checkout

Figure 1: Spartobranchus tenuis (Walcott, 1911) individuals from the Burgess Shale.
Figure 2: Spartobranchus tenuis (Walcott, 1911) individuals associated with tubular structures, from the Burgess Shale.

Change history

  • 27 March 2013

    Two citations in the text to Fig. 1 were corrected to Fig. 2.


  1. Swalla, B. J. & Smith, A. B. Deciphering deuterostome phylogeny: molecular, morphological and palaeontological perspectives. Phil. Trans. R. Soc. B 363, 1557–1568 (2008)

    Article  Google Scholar 

  2. Gonzalez, P. & Cameron, C. B. The gill slits and pre-oral ciliary organ of Protoglossus (Hemichordata: Enteropneusta) are filter-feeding structures. Biol. J. Linn. Soc. 98, 898–906 (2009)

    Article  Google Scholar 

  3. Winchell, C. J., Sullivan, J., Cameron, C. B., Swalla, B. J. & Mallatt, J. Evaluating hypotheses of deuterostome phylogeny and chordate evolution with new LSU and SSU ribosomal DNA data. Mol. Biol. Evol. 19, 762–776 (2002)

    Article  CAS  Google Scholar 

  4. Cameron, C. B. A phylogeny of the hemichordates based on morphological characters. Can. J. Zool. 83, 196–215 (2005)

    Article  Google Scholar 

  5. Cannon, J. T., Rychel, A. L., Eccleston, H., Halanych, K. M. & Swalla, B. J. Molecular phylogeny of Hemichordata, with updated status of deep-sea enteropneusts. Mol. Phylogenet. Evol. 52, 17–24 (2009)

    Article  CAS  Google Scholar 

  6. Cameron, C. B., Garey, J. R. & Swalla, B. J. Evolution of the chordate body plan: new insights from phylogenetic analyses of deuterostome phyla. Proc. Natl Acad. Sci. USA 97, 4469–4474 (2000)

    Article  ADS  CAS  Google Scholar 

  7. Worsaae, K., Sterrer, W., Kaul-Strehlow, S., Hay-Schmidt, A. & Giribet, G. An anatomical description of a miniaturized acorn worm (Hemichordata, Enteropneusta) with asexual reproduction by paratomy. PLoS ONE 7, e48529 (2012)

    Article  ADS  CAS  Google Scholar 

  8. Osborn, K. J. et al. Diversification of acorn worms (Hemichordata, Enteropneusta) revealed in the deep sea. Proc. R. Soc. B 279, 1646–1654 (2012)

    Article  Google Scholar 

  9. Hyman, L. H. in The Invertebrates. Vol. 5, 72–207 (McGraw-Hill, 1959)

    Google Scholar 

  10. Mitchell, C. E., Melchin, M. J., Cameron, C. B. & Maletz, J. Phylogenetic analysis reveals that Rhabdopleura is an extant graptolite. Lethaia 46, 34–56 (2012)

    Article  Google Scholar 

  11. Rickards, R. B. & Durman, P. N. in Studies in Palaeozoic Palaeontology National Museum of Wales Geological Series Vol. 25 (eds Bassett, M. G. & Deisler, V. K. ) 5–92 (National Museum of Wales, 2006)

    Google Scholar 

  12. Bardack, D. in Richardson's guide to the fossil fauna of Mazon Creek (eds Shabica, C. W. & Hay, A. A. ) 89–92 (Northeastern Illinois University, 1997)

    Google Scholar 

  13. Arduini, P., Pinna, G. & Terruzzi, G. Megaderaion sinemuriense n.g. n.sp., a new fossil enteropneust of the Sinemurian of Osteno in Lombardy. Atti della Societa Italiana di Scienze Naturali e del Museo Civico di Storia Naturale di Milano 122, 104–108 (1981)

    Google Scholar 

  14. Alessandrello, A., Bracchi, G. & Riou, B. Polychaete, sipunculan and enteropneust worms from the Lower Callovian (Middle Jurassic) of La Voulte-sur-Rhône (Ardèche, France). Memoire della Società Italiana di Scienze Naturali e del Museo Civico di Storia Naturale di Milano (Fascicolo I). 32, 1–16 (2004)

  15. Bechly, G. & Frickhinger, K. A. in The fossils of Solnhofen 2. 76–79 (Goldschneck-Verlag, 1999)

    Google Scholar 

  16. Walcott, C. Cambrian Geology and Paleontology II. Middle Cambrian annelids. Smiths. Misc. Collect. 57, 109–145 (1911)

    Google Scholar 

  17. Conway Morris, S. The Burgess Shale (Middle Cambrian) fauna. Annu. Rev. Ecol. Syst. 10, 327–349 (1979)

    Article  Google Scholar 

  18. Conway Morris, S. Fossil priapulid worms. Special Papers in Palaeontology 20, 1–95 (1977)

    Google Scholar 

  19. Conway Morris, S. The community structure of the Middle Cambrian phyllopod bed (Burgess Shale). Palaeontology 29, 423–467 (1986)

    Google Scholar 

  20. Caron, J.-B. & Jackson, D. A. Paleoecology of the Greater Phyllopod Bed community, Burgess Shale. Palaeogeogr. Palaeoclimatol. Palaeoecol. 258, 222–256 (2008)

    Article  Google Scholar 

  21. Stach, T. & Kaul, S. The postanal tail of the enteropneust Saccoglossus kowalevskii is a ciliary creeping organ without distinct similarities to the chordate tail. Acta Zool. 92, 150–160 (2011)

    Article  Google Scholar 

  22. Ruppert, E. E. Key characters uniting hemichordates and chordates: homologies or homoplasies? Can. J. Zool. 83, 8 (2005)

    Article  Google Scholar 

  23. Pani, A. M. et al. Ancient deuterostome origins of vertebrate brain signalling centres. Nature 483, 289–294 (2012)

    Article  ADS  CAS  Google Scholar 

  24. Lowe, C. J. et al. Anteroposterior patterning in hemichordates and the origins of the chordate nervous system. Cell 113, 853–865 (2003)

    Article  CAS  Google Scholar 

  25. Rickards, R. B. & Stait, B. A. Psigraptus, its classification, evolution and zooid. Alcheringa 8, 101–111 (1984)

    Article  Google Scholar 

  26. Kaźmierczak, J. & Pszczólkowski, A. Burrows of Enteropneusta in Muschelkalk (Middle Triassic) of the Holy Cross Mountains, Poland. Acta Palaeontol. Pol. 14, 299–318 (1969)

    Google Scholar 

  27. Wetzel, W. Flintgefüllte enteropneusten — wohnröhren in einen oberkreide-Geschiebe. Schriften des Naturwissenschaftlichen Vereins für Schleswig-Holstein 42, 104–107 (1972)

    Google Scholar 

  28. Twitchett, R. J. The resting trace of an acorn-worm (Class: Enteropneusta) from the Lower Triassic. J. Paleontol. 70, 128–131 (1996)

    Article  Google Scholar 

Download references


We thank C. Lowe for constructive comments, D. Erwin and M. Florence for access to the Smithsonian Institution collections, Parks Canada for collection and research permits, P. Fenton and V. Brown for assistance, R. Gaines for donation of specimens from Utah, and M. Collins (ARTofFACT) for reconstructions. J.-B.C. and C.B.C. are supported by Natural Sciences and Engineering Research Council Discovery Grants, and S.C.M. is supported by St John’s College, University of Cambridge, UK. This is Royal Ontario Museum Burgess Shale project number 41.

Author information

Authors and Affiliations



All authors contributed to write the main paper and commented on the manuscript at all stages. J.-B.C. conducted the observations and photography of specimens, prepared figures and wrote the Supplementary Information.

Corresponding author

Correspondence to Jean-Bernard Caron.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Additional information

The LSIDs (article) and (taxon) have been deposited in ZooBank.

Supplementary information

Supplementary Information

This file contains Supplementary Figures 1-6. (PDF 4214 kb)

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Caron, JB., Morris, S. & Cameron, C. Tubicolous enteropneusts from the Cambrian period. Nature 495, 503–506 (2013).

Download citation

  • Received:

  • Accepted:

  • Published:

  • 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