Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-12T07:08:18.417Z Has data issue: false hasContentIssue false
  • English
  • Français

The morphological diversity of Osedax worm borings (Annelida: Siboglinidae)

Published online by Cambridge University Press:  26 June 2014

Nicholas D. Higgs Open the ORCID record for Nicholas D. Higgs [Opens in a new window] ,
Adrian G. Glover ,
Thomas G. Dahlgren ,
Craig R. Smith ,
Yoshihiro Fujiwara ,
Florence Pradillon ,
Shannon B. Johnson ,
Robert C. Vrijenhoek  and
Crispin T.S. Little
Nicholas D. Higgs*
Affiliation:
Department of Life Sciences, Natural History Museum, London SW7 5BD, UK School of Earth and Environment, University of Leeds, Leeds LS2 9JT, UK
Adrian G. Glover
Affiliation:
Department of Life Sciences, Natural History Museum, London SW7 5BD, UK
Thomas G. Dahlgren
Affiliation:
Uni Research, Postboks 7810, N-5020 Bergen, Norway
Craig R. Smith
Affiliation:
Department of Oceanography, University of Hawaii, 1000 Pope Road, Honolulu, USA
Yoshihiro Fujiwara
Affiliation:
Marine Biodiversity Research Program, Japan Agency for Marine-Earth Science and Technology, Yokosuka Kanagawa 237-0061, Japan
Florence Pradillon
Affiliation:
Marine Biodiversity Research Program, Japan Agency for Marine-Earth Science and Technology, Yokosuka Kanagawa 237-0061, Japan Département des Ressources physiques et Ecosystèmes de fond de mer, IFREMER, Centre de Brest, BP 70, 29280 Plouzané, France
Shannon B. Johnson
Affiliation:
Monterey Bay Aquarium Research Institute, 7700 Sandholdt Road, Moss Landing, CA 95039, USA
Robert C. Vrijenhoek
Affiliation:
Monterey Bay Aquarium Research Institute, 7700 Sandholdt Road, Moss Landing, CA 95039, USA
Crispin T.S. Little
Affiliation:
School of Earth and Environment, University of Leeds, Leeds LS2 9JT, UK
*
Correspondence should be addressed to: N.D. Higgs, Current address: Marine Institute, Plymouth University, Drake Circus, Plymouth PL4 8AA, UK email: nicholas.higgs@plymouth.ac.uk
Get access Rights & Permissions [Opens in a new window]

Abstract

Marine worms in the genus Osedax, have specialized ‘root’ tissues used to bore into the bones of decomposing vertebrate skeletons and obtain nutrition. We investigated the borings of nine Osedax species, using micro computed tomography to quantitatively describe the morphology of the borings and provide three-dimensional reconstructions of the space occupied by Osedax root tissues inside the bone. Each Osedax species displayed a consistent boring morphology in any given bone, but these differed between bones. In bones where multiple species coexisted there was limited evidence for spatial niche partitioning by Osedax root tissues inside the bones investigated here. The new morphological data may be applied to Osedax traces in fossil bones, showing that borings can be used to indicate minimum species richness in these bones.

Keywords

bioerosiondeep-seawhale-fallPolychaetataphonomytrace fossilcomputed tomography
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 94 , Issue 7 , November 2014 , pp. 1429 - 1439
Copyright
Copyright © Marine Biological Association of the United Kingdom 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Adler, P.B., Hillerislambers, J. and Levine, J.M. (2007) A niche for neutrality. Ecology Letters 10, 95–104.CrossRefGoogle ScholarPubMed
Amano, K., Little, C.T.S. and Inoue, K. (2007) A new Miocene whale-fall community from Japan. Palaeogeography, Palaeoclimatology, Palaeoecology 247, 236–242.CrossRefGoogle Scholar
Braby, C.E., Rouse, G.W., Johnson, S.B., Jones, W.J. and Vrijenhoek, R.C. (2007) Bathymetric and temporal variation among Osedax boneworms and associated megafauna on whale-falls in Monterey Bay, California. Deep-Sea Research Part I: Oceanographic Research Papers 54, 1773–1791.CrossRefGoogle Scholar
Bromley, R.G. (1994) The palaeoecology of bioerosion. InDonovan, S.K. (ed.) The palaeobiology of trace fossils. Chichester, England: John Wiley & Sons, pp. 134–154.Google Scholar
Chesson, P. (2000) Mechanisms of maintenance of species diversity. Annual Review of Ecology and Systematics 31, 343–366.CrossRefGoogle Scholar
Fujikura, K., Fujiwara, Y. and Kawato, M. (2006) A new species of Osedax (Annelida: Siboglinidae) associated with whale carcasses off Kyushu, Japan. Zoological Science 23, 733–740.CrossRefGoogle ScholarPubMed
Fujiwara, Y., Kawato, M., Yamamoto, T., Yamanaka, T., Sato-Okoshi, W., Noda, C., Tsuchida, S., Komai, T., Cubelio, S.S., Sasaki, T., Jacobsen, K., Kubokawa, K., Fujikura, K., Maruyama, T., Furushima, Y., Okoshi, K., Miyake, H., Miyazaki, M., Nogi, Y., Yatabe, A. and Okutani, T. (2007) Three-year investigations into sperm whale-fall ecosystems in Japan. Marine Ecology 28, 219–232.CrossRefGoogle Scholar
Glover, A.G., Källström, B., Smith, C.R. and Dahlgren, T.G. (2005) World-wide whale worms? A new species of Osedax from the shallow north Atlantic. Proceedings of the Royal Society B: Biological Sciences 272, 2587–2592.CrossRefGoogle Scholar
Glover, A.G., Wiklund, H., Taboada, S., Avila, C., Cristobo, J., Smith, C.R., Kemp, K.M., Jamieson, A.J. and Dahlgren, T.G. (2013) Bone-eating worms from the Antarctic: the contrasting fate of whale and wood remains on the Southern Ocean seafloor. Proceedings of the Royal Society B: Biological Sciences 280, 20131390.CrossRefGoogle ScholarPubMed
Goffredi, S.K., Johnson, S.B. and Vrijenhoek, R.C. (2007) Genetic diversity and potential function of microbial symbionts associated with newly discovered species of Osedax polychaete worms. Applied and Environmental Microbiology 73, 2314–2323.CrossRefGoogle ScholarPubMed
Goffredi, S.K., Orphan, V.J., Rouse, G.W., Jahnke, L., Embaye, T., Turk, K., Lee, R. and Vrijenhoek, R.C. (2005) Evolutionary innovation: a bone-eating marine symbiosis. Environmental Microbiology 7, 1369–1378.CrossRefGoogle ScholarPubMed
Higgs, N.D. (2012) The taphonomy of giants: whale-falls and the bioerosion of whale skeletons in the deep sea. PhD thesis. University of Leeds, UK.Google Scholar
Higgs, N.D., Glover, A.G., Dahlgren, T.G. and Little, C.T.S. (2010) Using computed-tomography to document borings by Osedax mucofloris in whale bone. Cahiers de Biologie Marine 51, 401–405.Google Scholar
Higgs, N.D., Glover, A.G., Dahlgren, T.G. and Little, C.T.S. (2011a) Bone boring worms: characterizing the morphology, rate and method of bioerosion by Osedax mucofloris (Annelida, Siboglinidae). Biological Bulletin. Marine Biological Laboratory, Woods Hole 221, 307–316.CrossRefGoogle ScholarPubMed
Higgs, N.D., Little, C.T. and Glover, A.G. (2011b) Bones as biofuel: a review of whale bone composition with implications for deep-sea biology and palaeoanthropology. Proceedings of the Royal Society B: Biological Sciences 278, 9–17.CrossRefGoogle ScholarPubMed
Higgs, N.D., Little, C.T.S., Glover, A.G., Dahlgren, T.G., Smith, C.R. and Dominici, S. (2012) Evidence of Osedax worm borings in Pliocene (~3 Ma) whale bone from the Mediterranean. Historical Biology 24, 269–277.Google Scholar
Hubbell, S. (2005) Neutral theory in community ecology and the hypothesis of functional equivalence. Functional Ecology 19, 166–172.CrossRefGoogle Scholar
Huusgaard, R.S., Vismann, B., Kühl, M., Macnaugton, M., Colmander, V., Rouse, G.W., Glover, A.G., Dahlgren, T.G. and Worsaae, K. (2012) The potent respiratory system of Osedax mucofloris (Siboglinidae, Annelida) – a prerequisite for the origin of bone-eating Osedax? PLoS One 7, e35975. doi:10.1371/journal.pone.0035975.CrossRefGoogle ScholarPubMed
Jones, W.J., Johnson, S.B., Rouse, G.W. and Vrijenhoek, R.C. (2008) Marine worms (genus Osedax) colonize cow bones. Proceedings of the Royal Society B: Biological Sciences 275, 387–391.CrossRefGoogle ScholarPubMed
Katz, S., Klepal, W. and Bright, M. (2010) The skin of Osedax (Siboglinidae, Annelida): an ultrastructural investigation of its epidermis. Journal of Morphology 271, 1272–1280.CrossRefGoogle ScholarPubMed
Kiel, S., Goedert, J.L., Kahl, W.A. and Rouse, G.W. (2010) Fossil traces of the bone-eating worm Osedax in early Oligocene whale bones. Proceedings of the National Academy of Sciences of the United States of America 107, 8656–8659.CrossRefGoogle ScholarPubMed
Kiel, S., Kahl, W.A. and Goedert, J.L. (2012) Traces of the bone-eating annelid Osedax in Oligocene whale teeth and fish bones. Paläontologische Zeitschrift 87, 161–167.CrossRefGoogle Scholar
Leibold, M. A., Holyoak, M., Mouquet, N., Amarasekare, P., Chase, J.M., Hoopes, M.F., Holt, R.D., Shurin, J.B., Law, R., Tilman, D., Loreau, M. and Gonzalez, A. (2004) The metacommunity concept: a framework for multi-scale community ecology. Ecology Letters 7, 601–613.CrossRefGoogle Scholar
Lundsten, L., Schlining, K.L., Frasier, K., Johnson, S.B., Kuhnz, L.A., Harvey, J.B.J., Clague, G. and Vrijenhoek, R.C. (2010) Time-series analysis of six whale-fall communities in Monterey Canyon, California, USA. Deep-Sea Research Part I: Oceanographic Research Papers 57, 1573–1584.CrossRefGoogle Scholar
Pirrone, C.A., Buatois, L.A. and Bromley, R.G. (2014) Ichnotaxobases for bioerosion trace fossils in bones. Journal of Paleontology 88, 195–203.CrossRefGoogle Scholar
Pradillon, F., Kawato, M., Kubokawa, K. and Fujiwara, F. (2009) Contrasted reproductive and dispersal strategies in Osedax species from different depths around Japan. InFujiwara, Y. and Takeoka, Y. (eds) Abstracts Book: The 4th International Symposium on Chemosynthesis-Based Ecosystems; 29 June–3 July 2009, Okinawa, Japan. Yokosuka, Japan: JAMSTEC, p. 45.Google Scholar
Rouse, G.W., Goffredi, S.K., Johnson, S.B. and Vrijenhoek, R.C. (2011) Not whale-fall specialists, Osedax worms also consume fishbones. Biology Letters 7, 736–739.CrossRefGoogle ScholarPubMed
Rouse, G.W., Goffredi, S.K. and Vrijenhoek, R.C. (2004) Osedax: bone-eating marine worms with dwarf males. Science 305, 668.CrossRefGoogle ScholarPubMed
Rouse, G.W., Worsaae, K., Johnson, S.B., Jones, W.J. and Vrijenhoek, R.C. (2008) Acquisition of dwarf male “harems” by recently settled females of Osedax roseus n. sp. (Siboglinidae; Annelida). Biological Bulletin. Marine Biological Laboratory, Woods Hole 214, 67–82.CrossRefGoogle Scholar
Salathé, R.M. and Vrijenhoek, R.C. (2012) Temporal variation and lack of host specificity among bacterial endosymbionts of Osedax bone worms (Polychaeta: Siboglinidae). BMC Evolutionary Biology 12, 189.CrossRefGoogle ScholarPubMed
Schenk, H.J. (2006) Root competition: beyond resource depletion. Journal of Ecology 94, 725–739.CrossRefGoogle Scholar
Schenk, H.J., Callaway, R.M. and Mahall, B.E. (1999) Spatial root segregation: are plants territorial? Advances in Ecological Research 28, 145–180.CrossRefGoogle Scholar
Schuller, D., Kadko, D. and Smith, C.R. (2004) Use of 210Pb/226Ra disequilibria in the dating of deep-sea whale falls. Earth and Planetary Science Letters 218, 277–289.CrossRefGoogle Scholar
Smith, C.R. and Baco, A.R. (2003) Ecology of whale falls at the deep-sea floor. Oceanography and Marine Biology: a [an] Annual Review 41, 311–354.Google Scholar
Smith, C.R., Baco, A.R. and Glover, A. (2002) Faunal succession on replicate deep-sea whale falls: timescales and vent-seep affinities. Cahiers de Biologie Marine 43, 293–297.Google Scholar
Tresguerres, M., Katz, S. and Rouse, G.W. (2013) How to get into bones: proton pump and carbonic anhydrase in Osedax boneworms. Proceedings of the Royal Society B: Biological Sciences 280, 20130625.CrossRefGoogle ScholarPubMed
Verna, C., Ramette, A., Wiklund, H., Dahlgren, T.G., Glover, A.G., Gaill, F. and Dubilier, N. (2010) High symbiont diversity in the bone-eating worm Osedax mucofloris from shallow whale-falls in the North Atlantic. Environmental Microbiology 12, 2355–2370.CrossRefGoogle ScholarPubMed
Vrijenhoek, R.C., Collins, P. and Van Dover, C.L. (2008a) Bone-eating marine worms: habitat specialists or generalists? Proceedings of the Royal Society B: Biological Sciences 275, 1963–1964.CrossRefGoogle Scholar
Vrijenhoek, R.C., Johnson, S.B. and Rouse, G.W. (2008b) Bone-eating Osedax females and their ‘harems’ of dwarf males are recruited from a common larval pool. Molecular Ecology 17, 4535–4544.CrossRefGoogle ScholarPubMed
Vrijenhoek, R.C., Johnson, S.B. and Rouse, G.W. (2009) A remarkable diversity of bone-eating worms (Osedax; Siboglinidae; Annelida). BMC Biology 7, 74.CrossRefGoogle ScholarPubMed
Warme, J.E. (1975) Borings as trace fossils and the process of marine bioerosion. InFrey, R.W. (ed.) The study of trace fossils. New York: Springer-Verlag, pp. 181–227.CrossRefGoogle Scholar