Evidence of Osedax worm borings in Pliocene (~3 Ma) whale bone from the Mediterranean

Historical Biology

Volumn 24, Issue 3, 2012, Pages 269-277

  Higgs, Nicholas D ^a,b   Little, Crispin T S ^a   Glover, Adrian G ^b   Dahlgren, Thomas G ^c   Smith, Craig R ^d   Dominici, Stefano ^e  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b DEPARTMENT OF LIFE SCIENCES   (United Kingdom)

^c Uni Environment Uni Research   (Norway)

^d UNIVERSITY OF HAWAII   (United States)

^e UNIVERSITY OF FLORENCE   (Italy)

Author keywords

ichnology; Italy; Siboglinidae; taphonomy; trace fossil; whale fall

Indexed keywords

BONE; FOSSIL; FOSSIL RECORD; ICHNOLOGY; PALEOGEOGRAPHY; PALEONTOLOGY; PLIOCENE; POLYCHAETE; SEAFLOOR; SKELETON; TAPHONOMY; VERTEBRATE; WHALE;

ITALY; MEDITERRANEAN SEA;

CETACEA; OSEDAX; SIBOGLINIDAE; VERTEBRATA;

EID: 84861955451     PISSN: 08912963     EISSN: 10292381     Source Type: Journal    
DOI: 10.1080/08912963.2011.621167     Document Type: Article

References (64)

1. Bertling, M, Braddy, SJ, Bromley, RG, Demathieu, GR, Genise, J, Mikulá, R, Nielsen, JK, Nielsen, KSS, Rindsberg, AKSchlirf, M. 2006. Names for trace fossils: a uniform approach. Lethaia, 39: 265-286.
2. Beuck, L and Freiwald, A. 2005. "Bioerosion patterns in a deep-water Lophelia pertusa (Scleractinia) thicket (Propeller Mound, northern Porcupine Seabight)". In Coldwater corals and ecosystems, 915-936. Berlin: Springer-Verlag.
3. Bianucci, G and Landini, W. 2005. I paleositi a vertebrati fossili della Provincia di Pisa: Atti della Società toscana di Scienze naturali. Memorie, Serie A, 110: 1-21.
4. Bianucci, G, Sorbi, S, Vaiani, SC and Landini, W. 2009. Pliocene marine mammals from Italy: a systematic and stratigraphic overview, Paper presented at: Bologna, International Conference on Vertebrate Palaeobiogeography; 28-29 September 2009, Bologna, Italy. Abstracts Book 9-12.
5. Bolotin, J, Hrs-Brenko, M, Tutman, P, Glavic, N, Kozul, V, Skaramuca, B, Lucic, D and Dulcic, J. 2005. First record of Idas simpsoni (Mollusca: Bivalvia: Mytilidae) in the Adriatic sea. J Mar Biol Ass UK, 85(4): 977-978.
6. Boreske, JR, Goldberg, L and Cameron, B. 1972. A reworked Cetacean with clam borings: Miocene of North Carolina. J Paleontol, 46(1): 130-139.
7. Braby, CE, Rouse, GW, Johnson, SB, Jones, WJ and Vrijenhoek, RC. 2007. Bathymetric and temporal variation among Osedax boneworms and associated megafauna on whale-falls in Monterey Bay, California. Deep-Sea Res Pt I, 54(10): 1773-1791.
8. Bromley, RG. 1970. "Borings as trace fossils and Entobia cretacea Portlock, as an example". In Trace fossils, 49-90. Liverpool, UK: Seel House Press.
9. Bromley, RG. 1981. Concepts in ichnotaxonomy illustrated by small round holes in shells. Acta Geologica Hispanica, 16(1-2): 55-64.
10. Bromley, RG. 1994. "The palaeoecology of bioerosion". In The palaeobiology of trace fossils, 134-154. Chichester: Wiley.
11. Bromley, RG. 2004. A stratigraphy of marine bioerosion. Geol Soc London, Spec Publ, 228: 455-479.
12. Bromley, RG and D'Alessandro, A. 1984. The inchnogenus Entobia from the Miocene, Pliocene and Pleistocene of Southern Italy. Riv It Paleont Strat, 90(2): 227-296.
13. Bromley, RG, Beuck, L and Taddei Ruggiero, E. 2008. "Endolithic sponge versus terebratulid brachiopod, Pleistocene, Italy: accidental symbiosis, bioclaustration and deformity". In Current developments in bioerosion, 361-368. Berlin, Germany: Springer-Verlag.
14. Calcinai, B, Bavestrello, G and Cerrano, C. 2005. Excavating sponge species from the Indo-Pacific Ocean. Zool Stud, 44(1): 5-18.
15. Coates, AG, Collins, LS, Aubry, M-P and Berggren, WA. 2004. The Geology of the Darien, Panama, and the late Miocene-Pliocene collision of the Panama arc with northwestern South America. Geol Soc Am Bull, 116(11): 1327-1344.
16. Dahlgren, TG, Wiklund, H, Källstrom, B, Lundälv, T, Smith, CR and Glover, AG. 2006. A shallow-water whale-fall experiment in the north Atlantic. Cah Biol Mar, 47(4): 385-389.
17. D'Ancona, C. 1871. Malacologia Pliocenica Italiana descritta e illustrata da Cesare D'Ancona. Fascicolo I. Generi Strombus, Murex, Typhis. Memorie del Regio Comitato Geologico d'Italia, 1: 307-358.
18. Danise, S, Dominici, S and Betocchi, U. 2010. Mollusk species at a Pliocene shelf whale fall (Orciano Pisano, Tuscany). Palaios, 25: 449-456.
19. Davis, PG. 1997. The bioerosion of bird bones. Int J Osteoarchaeol, 7(4): 388-401.
20. Dominici, S, Cioppi, E, Danise, S, Betocchi, U, Gallai, G, Tangocci, F, Valleri, G and Monechi, S. 2009. Mediterranean fossil whale falls and the adaptation of mollusks to extreme habitats. Geology, 37: 815-818.
21. Emig CC, Geistdoerfer P. 2004. The Mediterranean deep-sea fauna: historical evolution, bathymetric variations and geographical changes. Carnets de Géologie-Notebooks on Geology, Maintenon, Article 2004/01 (G2004_A01_CCE-PG).
22. Fernandez-Jalvo, Y and Andrews, P. 2003. Experimental effects of water abrasion on bone fragments. J Taphonomy, 1(3): 147-163.
23. Frick, M, Williams, K and Robinson, M. 1998. Epibionts associated with nesting loggerhead sea turtles (Caretta caretta) in Georgia, USA. Herpetol Rev, 29(4): 211-213.
24. Fujikura, K, Fujiwara, Y and Kawato, M. 2006. A new species of Osedax (Annelida: Siboglinidae) associated with whale carcasses off Kyushu, Japan. Zool Sci, 23(8): 733-740.
25. Garcia-Castellanos, D, Estrada, F, Jiménez-Munt, I, Gorini, C, Fernàndez, M, Vergés, J and De Vicente, R. 2009. Catastrophic flood of the Mediterranean after the Messinian salinity crisis. Nature, 462: 778-781.
26. Glover, AG, Källstrom, B, Smith, C and Dahlgren, TG. 2005. World-wide whale worms? A new species of Osedax from the shallow north Atlantic. Proc R Soc B, 272(1581): 2587-2592.
27. Goffredi, S, Paull, C, Fulton-Bennett, K, Hurtado, L and Vrijenhoek, R. 2004. Unusual benthic fauna associated with a whale fall in Monterey Canyon, California. Deep-Sea Res Pt I, 51(10): 1295-1306.
28. Goffredi, S, Johnson, S and Vrijenhoek, R. 2007. Genetic diversity and potential function of microbial symbionts associated with newly discovered species of Osedax polychaete worms. Appl Environ Microbiol, 73(7): 2314-2323.
29. Higgs, ND, Glover, AG, Dahlgren, TG and Little, CTS. 2010. Using computed-tomography to document borings by Osedax mucofloris in whale bone. Cah Biol Mar., 51: 401-405.
30. Higgs, ND, Glover, AG, Dahlgren, TG and Little, CTS. In Press. Bone boring worms: characterizing the morphology, rate and method of bioerosion by Osedax mucofloris (Annelida, Siboglinidae). Biol Bull,
31. Hilário, A, Capa, M, Dahlgren, TG, Halanych, KM, Little, CTS, Thornhill, DJ, Verna, C and Glover, AG. 2011. New perspectives on the ecology and evolution of Siboglinid tubeworms. PloS one, 6(2): e16309 doi:10.1371/journal.pone.0016309
32. Hoeksema, BW. 1983. Excavation patterns and spicule dimensions of the boring sponge Cliona celata from the SW Netherlands. Senckenbergiana Marit, 15(1): 55-85.
33. Hsü, K, Montadert, L, Bernoulli, D, Cita, MB, Erickson, A, Garrison, RE, Kidd, RB, Melieres, F, Muller, C and Wright, R. 1977. History of the Mediterranean salinity crisis. Nature, 267: 399-403.
34. Johnson, SB, Waren, A, Lee, RW, Kano, Y, Kaim, A, Davis, A, Strong, EE and Vrijenhoek, RC. 2010. Rubyspira, new genus and two new species of bone-eating deep-sea snails with ancient habits. Biol Bull, 219(2): 166-177.
35. Jones, WJ, Johnson, SB, Rouse, GW and Vrijenhoek, RC. 2008. Marine worms (genus Osedax) colonize cow bones. Proc R Soc B, 275(1633): 387-391.
36. Katz, S, Klepal, W and Bright, M. 2010. The Skin of Osedax (Siboglinidae, Annelida): an ultrastructural investigation of its epidermis. J Morphol, 271(10): 1272-1280.
37. Kelly, SR and Bromley, RG. 1984. Ichnological nomenclature of clavate borings. Palaeontology, 27(4): 793-807.
38. Kiel, S, Goedert, JL, Kahl, W-A and Rouse, GW. 2010. Fossil traces of the bone-eating worm Osedax in early Oligocene whale bones. Proc Natl Acad Sci USA, 107(19): 8656-8659.
39. Kiel, S, Kahl, W-A and Goedert, JL. 2011. Osedax borings in fossil marine bird bones. Naturwissenschaften, 98(1): 51-55.
40. Lawley, R. 1876. Nuovi studi sopra ai pesci ed altri vertebrati fossili delle Colline Toscane, Firenze: Tipografia dell'Arte della Stampa.
41. Marx, F and Uhen, M. 2010. Climate, critters, and cetaceans: Cenozoic drivers of the evolution of modern whales. Science, 327(5968): 993-996.
42. Marshall, BA. 1987. Osteopeltidae (Mollusca: Gastropoda): a new family of limpets associated with whale bone in the deep sea. J Moll Stud, 53: 121-127.
43. Muñiz, F, De Gibert, JM and Esperante, R. 2010. First trace-fossil evidence of bone-eating worms in whale carcasses. Palaios, 25(3-4): 269-273.
44. Owen, R. 1889. Monograph on the British Fossil Cetacea from the Red Crag, London: Palaeontographical Society.
45. Pilleri, G. 1987. Cetacea of the Italian Pliocene, Berne: Brain Anatomy Institute.
46. Pradillon, F, Kawato, M, Kubokawa, K and Fujiwara, F. 2009. Contrasted reproductive and dispersal strategies in Osedax species from different depths around Japan, Paper presented at: The 4th International Symposium on Chemosynthesis-based Ecosystems; 29 June-3 July 2009, Okinawa, Japan
47. Pyenson, ND, Irmis, RB and Lipps, JH. 2010. Comment on 'Climate, critters, and cetaceans: Cenozoic drivers of the evolution of modern whales'. Science, 330: 178
48. Rice, ME. 1969. Possible boring structures of sipunculids. Am Zool, 9(3): 803-812.
49. Rouse, GW, Goffredi, SK and Vrijenhoek, RC. 2004. Osedax: Bone-eating marine worms with dwarf males. Science, 305(5684): 668-671.
50. Rouse, GW, Worsaae, K, Johnson, SB, Jones, WJ and Vrijenhoek, RC. 2008. Acquisition of dwarf male SPiquotSPiharemsSPiquotSPi by recently settled females of Osedax roseus n. sp (Siboglinidae; Annelida). Biol Bull, 214: 67-82.
51. Rouse, GW, Goffredi, SK, Johnson, SB and Vrijenhoek, RC. 2011. Not whale-fall specialists, Osedax worms also consume fishbones. Biol Lett, 7(5): 736-739.
52. Schander, C, Rapp, HT and Dahlgren, TG. 2010. Osedax mucofloris (Polychaeta, Siboglinidae), a bone-eating marine worm new to Norway. Fauna Norv, 30: 5-8.
53. Schwimmer, DA. 2002. King of the crocodylians: the paleobiology of Deinosuchus, Bloomington, IN: Indiana University Press. Chapter 5. Deinosuchus localities and their ancient environments. p. 81-106
54. Smith, C and Baco, A. 2003. Ecology of whale falls at the deep-sea floor. Oceanogr Mar Biol, 41: 311-354.
55. Steptoe, DP and Wood, WB. 2002. The human remains from HMS Pandora. Internet Archaeology, [Internet]. [cited 2011 September 4] 11. Available from: http://intarch.ac.uk
56. Taviani, M. 2002. The Mediterranean benthos from Late Miocene up to present: ten million years of dramatic climatic and geological vicissitudes. Biol Mar Medit, 9(1): 445-463.
57. Thomas, PA. 1979. Boring sponges destructive to economically important molluscan beds and coral reefs in Indian seas. Indian J Fish, 26(1&2): 163-200.
58. Trueman, C and Martill, DM. 2002. The long-term survival of bone: the role of bioerosion. Archaeometry, 44(3): 371-382.
59. Verna, C, Ramette, A, Wiklund, H, Dahlgren, TG, Glover, AG, Gaill, F and Dubilier, N. 2010. High symbiont diversity in the bone-eating worm Osedax mucofloris from shallow whale-falls in the North Atlantic. Env Microbiol, 12(8): 2355-2370.
60. Vrijenhoek, RC, Johnson, SB and Rouse, GW. 2009. A remarkable diversity of bone-eating worms (Osedax; Siboglinidae; Annelida). BMC Biol, 7: 74
61. Warme, JE. 1970. "Traces and significance of marine rock borers". In Trace fossils, 515-526. Liverpool: Seel House Press.
62. Warme, JE. 1975. "Borings as trace fossils and the process of marine bioerosion". In The study of trace fossils, 181-227. New York: Springer-Verlag.
63. Wilson, MA and Palmer, TJ. 2006. Patterns and processes in the Ordovician bioerosion revolution. Ichnos, 13: 109-112.
64. Wood, WB and Hodgson, G. 1996. "The skeleton from the wreck of HMS Pandora". In History, health & heritage: proceedings of the Fourth Biennial Conference of the Australian Society of the History of Medicine, 303-308. Brisbane, Australia: Australian Society of the History of Medicine.