Early bioerosion in skeletal tissues: Persistence through deep time

Neues Jahrbuch fur Geologie und Palaontologie - Abhandlungen

Volumn 265, Issue 2, 2012, Pages 165-183

  Turner Walker, Gordon ^a,b  

^a NATIONAL YUNLIN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Taiwan)

^b UNIVERSITY OF BERGEN   (Norway)

Author keywords

Bacterial tunnelling; Bioerosion; BSEM; Cyanobacteria; Diagenesis; EDX; Fossil bones

Indexed keywords

ARCHAEOLOGY; BIOEROSION; BONE; DIAGENESIS; FOSSIL ASSEMBLAGE; HISTOLOGY; SKELETAL REMAINS; SURVIVAL; VERTEBRATE;

TAIWAN;

BACTERIA (MICROORGANISMS); CYANOBACTERIA; VERTEBRATA;

EID: 84876132056     PISSN: 00777749     EISSN: None     Source Type: Journal    
DOI: 10.1127/0077-7749/2012/0253     Document Type: Conference Paper

References (83)

1. Ascenzi, A. & Silvestrini, G. (1984): Bone-boring marine micro-organisms: an experimental investigation. - Journal of Human Evolution, 13: 531-536.
2. Bell, L.S. (1990): Paleopathology and diagenesis: an SEM evaluation of structural changes using backscattered electron imaging. - Journal of Archaeological Science, 17: 85-102.
3. Bell, L.S. & Elkerton, A. (2008): Unique marine taphonomy in human skeletal material recovered from the medieval warship the Mary Rose. - International Journal of Osteoarchaeology, 18(5): 523-535.
4. Bell, L.S., Boyde, A. & Jones, S.J. (1991): Diagenetic alteration to teeth in situ illustrated by backscattered electron imaging. - Scanning, 13(2): 173-183.
5. Bell, L.S., Skinner, M.F. & Jones, S.J. (1996): The speed of post mortem change to the human skeleton and its taphonomic significance. - Forensic Science International, 82 (2): 129-140.
6. Blissett, D.J. & Pickerill, R.K. (2007): Systematic ichnology of microborings from the Cenozoic White Limestone Group, Jamaica, West Indies. - Scripta Geologica, 134: 77-108.
7. Boreske, J.R., Goldberg, L. & Cameron, B. (1972): A reworked cetacean with clam borings: Miocene of North Carolina. - Journal of Paleontology, 46: 130-139.
8. Britt, B.B., Scheetz, R.D. & Dangerfield, A. (2008): A suite of dermestid beetle traces on dinosaur bone from the Upper Jurassic Morrison Formation, Wyoming, USA. - Ichnos, 15 (2): 59-71.
9. Bromley, R.G. (2004): A stratigraphy of marine bioerosion. - In: Mcilroy, D. (Ed.): The application of ichnology to palaeoenvironmental and stratigraphic analysis. - Geological Society Special Publication, 228: 455-479.
10. Butler, I., Rickard, D. & Grimes, S. (2000): Framboidal pyrite: self organisation in the Fe-S system. - Journal of Conference Abstracts, 5 (2): 276-277.
11. Carver, M. (2002): Field Archaeology. - In: Barker, G. (Ed.): Companion Encyclopaedia of Archaeology Volume 1, 128-182; Routledge (London and New York).
12. Davis, P.G. (1997): The bioerosion of bird bones. - International Journal of Osteoarchaeology, 7: 388-401.
13. Dohnalkova, A., Bilskis, C. & Kennedy, D.W. (2006): TEM Study of Manganese Biosorption by Cyanobaterium Synechocystis 6803. - Microscopy and Microanalysis, 12: 444-445.
14. Efremov, I.A. (1940): Taphonomy: a new branch of paleontology. - Pan-American Geology, 74: 81-93.
15. Esperante, R. & Muñiz Guinae, F. (2008): Bioerosion structures on Pliocene whale bones and their ethological classification. - In: Uchman, A. (Ed.): The Second International Congress on Ichnology, Cracow, Poland, Abstract Book, 38; Polish Geological Institute (Cracow).
16. Esperante, R., Muñiz Guinae, F. & Nick, K.E. (2009): Taphonomy of a Mysticeti whale in the Lower Pliocene Huelva Sands Formation (Southern Spain). - Geologica Acta, 7: 489-505.
17. Fernández-Jalvo, Y., Andrews, P., Pesquero, D., Smith, C., Marín-Monfort, D., Sánchez, B., Geigl, E.-M. & Alonso, A. (2010): Early bone diagenesis in temperate environments Part I: Surface features and histology. - Palaeogeography, Palaeoclimatology, Palaeoecology, 288: 62-81.
18. Garland, A.N. (1989): Microscopical analysis of fossil bone. - Applied Geochemistry 4 (3): 215-229.
19. Glaub, I., Vogel, K. & Gektidis, M. (2001): The role of modern and fossil cyanobacterial borings in bioerosion and bathymetry. - Ichnos, 8 (3): 185-95.
20. Glover, A.G., Källström, B., Smith, C.R. & Dahlgren, T.G. (2005): Worldwide whale worms? A new species of Osedax from the shallow north Atlantic. - Proceedings of the Royal Society B, 272: 2587-2592.
21. Glover, A.G., Kemp, K.M., Smith, C.R. & Dahlgren, T.G. (2008): On the role of bone-eating worms in the degradation of marine vertebrate remains. - Proceedings of the Royal Society B, 275: 1959-1961.
22. Grupe, G. & Garland, A.N. (1993): Histology of Ancient Human Bone: Methods and Diagnosis. - Proceeding of Paleohistology Workshop, 3-5 October 1990 at Goettingen, Berlin (Springer-Verlag).
23. Gutierrez, M.A. (2001): Bone Diagenesis and Taphonomic History of the Paso Otero 1 Bone Bed, Pampas of Argentina. - Journal of Archaeological Science, 28: 1277-1290.
24. Hackett, C.J. (1981): Microscopical focal destruction (tunnels) in exhumed human bones. - Medicine, Science and the Law, 21 (4): 243-265.
25. Hedges, R.E.M. (2002): Bone diagenesis: an overview of processes. - Archaeometry, 44: 319-328.
26. Hennessy, J. & Knauth, L.P. (1985): Isotopic variations in dolomite concretions from the Monterey Formation, California. - Journal of Sedimentary Petrology, 55 (1): 129-130.
27. Higgs, N.D., Glover, A.G., Dahlgren, T.G. & Little, C.T.S. (2011a): Bone-Boring Worms: Characterizing the Morphology, Rate, and Method of Bioerosion by Osedax mucofloris (Annelida, Siboglinidae). - Biological Bulletin, 221: 307-316.
28. Higgs, N.D., Glover, A.G., Dahlgren, T.G., Smith, C.R. & Dominici, S. (2011b): Evidence of Osedax worm borings in Pliocene (~3 Ma) whale bone from the Mediterranean. - Historical Biology: DOI:10.1080/08912963.2011.621167.
29. Hutchet, J.-B., Deverly, D., Gutierrez, B. & Chauchat, C. (2011): Taphonomic Evidence of a Human Skeleton Gnawed by Termites in a Moche-Civilisation Grave at Huaca de la Luna, Peru. - International Journal of Osteoarchaeology, 21: 92-102.
30. Jackes, M., Sherburne, R., Lubell, D., Barker, C. & Wayman, M. (2001): Destruction of microstructure in archaeological bone: a case study from Portugal. - International Journal of Osteoarchaeology, 11: 415-432.
31. Janaway, R.C., Percival, S.L. & Wilson, A.S. (2009): Decomposition of Human Remains. In: Percival, S.L. (Ed.): Microbiology and Aging, 313-334; New York (Humana Press, Springer Science and Business Media).
32. Jans, M.M.E. (2005): Histological characterisation of the degradation of archaeological bone. - Unpublished PhD Thesis, Institute for Geo and Bioarchaeology, Vrije Universiteit, Amsterdam.
33. Jans, M.M.E. (2008): Microbial bioerosion of bone - a review. - In: Wisshak, M. & Tapanila, L. (Eds.): Current developments in bioerosion, 397-413; Berlin and Heidelberg (Erlangen Earth Conference Series. Springer-Verlag).
34. Jans, M.M.E., Kars, H., Nielsen-Marsh, C.M., Smith, C.I., Nord, A.G., Arthur, P. & Earl, N. (2002): In situ preservation of archaeological bone: a histological study within a multidisciplinary approach. - Archaeometry, 44 (3): 343-352.
35. Jans, M.M.E., Nielsen-Marsh, C.M., Smith, C.I., Collins, M.J. & Kars, H. (2004): The characterisation of microbial attack in archaeological bone. - Journal of Archaeological Science, 31: 87-95.
36. Kasem, M.A., Russo, R.E. & Harith, M.A. (2011): Influence of biological degradation and environmental effects on the interpretation of archeological bone samples with laser-induced breakdown spectroscopy. - Journal of Analytical Atomic Spectrometry, 26: 1733-1739.
37. Kelley, P.H. (2008): Role of bioerosion in taphonomy: effect of predatory drillholes on preservation of mollusc shells. - In: Wisshak, M. & Tapanila, L. (Eds.): Current developments in bioerosion, 451-470; Berlin and Heidelberg (Erlangen Earth Conference Series, Springer-Verlag).
38. Königshof, P. & Glaub, I. (2004): Traces of microboring organisms in Palaeozoic conodont elements - Geobios, 37: 416-424.
39. Kölliker, A. (1859-1860): On the Frequent Occurrence of Vegetable Parasites in the Hard Structures of Animals. - Proceedings of the Royal Society of London, 10: 95-99.
40. Lyman, R.L. (1994): Vertebrate taphonomy. - Cambridge (Cambridge University Press).
41. Marchiafava, V., Bonucci, E. & Ascenzi, A. (1974): Fungal osteoclasia: A model of dead bone resorption. - Calcified Tissue Research, 14: 195-210.
42. Megirian, D., Murray, P., Schwartz, L. & Von Der Borch, C. (2004): Late Oligocene Kangaroo Well Local Fauna from the Ulta Limestone (new name), and climate of the Miocene oscillation across central Australia. - Australian Journal of Earth Sciences, 51 (5): 701-741.
43. Muñiz, F., De Gilbert, J.M. & Esperante, R. (2010): First trace-fossil evidence of bone-eating worms in whale carcasses. - Palaios, 25 (4): 269-273.
44. Müller, K.J. & Nogami, Y. (1972): Entöken und Bohrspuren bei den Conodontophorida. - Paläontologische Zeitschrift, 46 (1-2): 68-86.
45. 2-. - Journal of Archaeological Science, 27: 1151-1159.
46. O'Brien, T.G. & Kuehner, A.C. (2007). Waxing grave about adipocere: Soft tissue change in an aquatic context. - Journal of Forensic Sciences, 52 (2): 294-301.
47. O'Connor, T. (2000): The Archaeology of Animal Bones. - College Station (Texas A & M Press).
48. Ottoni, C., Koon, H.E.C., Collins, M.J., Penkman, K.E.H., Rickards, O. & Craig, O.E. (2009): Preservation of ancient DNA in thermally damaged archaeological bone. - Naturwissenschaften, 96: 267-278.
49. Pawlowska, A.M., Palinska, K.A. & Piekarek-Jankowska, H. (2008): Colonisation and bioerosion of marine bivalve shells from the Baltic Sea by euendolithic cyanobacteria: an experimental study. - Wisshak, M. & Tapanila, L. (Eds.): Current developments in bioerosion, 109-122; Berlin and Heidelberg (Erlangen Earth Conference Series, Springer-Verlag).
50. Perry, C.T. (1998): Macroborers within coral framework at Discovery Bay, north Jamaica: species distribution and abundance, and effects on coral preservation. - Coral Reefs, 17: 277-287.
51. Pesquero, M.D., Ascaso, C., Alcalá, L. & Fernández- Jalvo, Y. (2010): A new taphonomic bioerosion in a Miocene lakeshore environment. - Palaeogeography, Palaeoclimatology, Palaeoecology, 295 (1-2): 192-198.
52. Piepenbrink, H. (1986): Two examples of biogenous dead bone decomposition and their consequences for taphonomic interpretation. - Journal of Archaeological Science, 13: 417-430.
53. Piepenbrink, H. (1989): Examples of chemical changes during fossilization. - Applied Geochemistry, 4: 273-280.
54. Pomi, L.H. & Tonni, E.P. (2011): Termite Traces on Bones from the Late Pleistocene of Argentina. - Ichnos, 18 (3): 166-171.
55. Pfretzschner, H.-U. & Tütken, T. (2011): Rolling bones - Taphonomy of Jurassic dinosaur bones inferred from diagenetic microcracks and mineral infillings. - Palaeogeography, Palaeoclimatology, Palaeoecology, 310: 117-123.
56. Rice, M.E. (1969): Possible boring structures of sipunculids. - American Zoologist, 9: 803-812.
57. Ronchi, P., Ortenzi, A., Borromeo, O., Claps, M. & Zem-Polich, W.G. (2010): Depositional setting and diagenetic processes and their impact on the reservoir quality in the late Visean-Bashkirian Kashagan carbonate platform (Pre-Caspian Basin, Kazakhstan). - American Association of Petroleum Geologist, Bulletin, 94 (9): 1313-1348.
58. Rouse, G., Goffredi, S. & Vrijenhoek, R. (2004): Osedax: bone-eating marine worms with dwarf males. - Science, 305: 668-671.
59. Roux. W. (I887): Über eine im Knochen lebende Gruppe von Fadenpilzen (Mycelitis ossifragus). - Zeitschrift für wissenschaftliche Zoologie, 45: 221-254.
60. Sergi, S., Ascenzi, A. & Bonucci, E. (1972): Torus palatinus in the Neanderthal. Circeo I Skull. A histologic, microradiographic and electron microscopic investigation. - American Journal of Physical Anthropology, 36: 189-198.
61. Smith, C.I. Craig, O.E., Prigodich, R.V., Nielsen-Marsh, C.M., Jans, M.M.E., Vermeer, C. & Collins, M.J. (2005): Diagenesis and survival of osteocalcin in archaeological bone. - Journal of Archaeological Science, 32: 105-113.
62. Smith, C.I., Faraldos, M. & Fernández-Jalvo, Y. (2008): The precision of porosity measurements: Effects of sample pre-treatment on porosity measurements of modern and archaeological bone. - Palaeogeography, Palaeoclimatology, Palaeoecology, 266: 175-182.
63. Spangler, E. & Shapiro, R. (2007): New evidence of bacterial degradation in fossil whale falls: not just a boring tale! - Geological Society of America Cordilleran Section, 103rd Annual Meeting, Bellingham, Washington. http://gsa.confex.com/gsa/2007CD/finalprogram/abstract-121147.htm.
64. Trueman, C.N. (1999): Rare earth element geochemistry and taphonomy of terrestrial vertebrate assemblages. - Palaios, 14: 555-568.
65. Trueman, C.N. & Benton, M.J. (1997): A geochemical method to trace the taphonomic history of reworked bones in sedimentary settings. - Geology, 25: 263-266.
66. Trueman, C.N. & Martill, D.M. (2002): The long term preservation of bone: the role of bioerosion. - Archaeometry, 44: 371-382.
67. Turner-Walker, G. (1998a): The West Runton fossil elephant: a pre-conservation evaluation of its condition, chemistry and burial environment. - The Conservator, 22: 26-35.
68. Turner-Walker, G. (1998b): Pyrite and bone diagenesis in terrestrial sediments: Evidence from the West Runton Fresh Water Bed. - Bulletin of the Geological Society of Norfolk, 48: 3-23.
69. Turner-Walker, G. (2008): The chemical and microbial degradation of bones and teeth. - In: Ron Pinhasi, R. & Mays, S. (Eds.): Advances in Human Palaeopathology, 1-25; Chichester (Wiley).
70. Turner-Walker, G. (2009): Degradation pathways and conservation strategies for ancient bone from wet, anoxic sites. - In: Huisman, H.D.J. & Strætkvern, K. (Eds.): Proceedings of the 10th Triennial Meeting of the ICOM-CC Working Group for Wet Organic Archaeological Materials, 10-15th September 2007: 659-675.
71. Turner-Walker, G. & Jans, M. (2008): Reconstructing taphonomic histories using histological analyses. - Palaeogeography, Palaeoclimatology Palaeoecology, 266: 227-235.
72. Turner-Walker, G. & Parry, T.V. (1995): The tensile strength of archaeological bone. - Journal of Archaeological Science, 22: 185-191.
73. Turner-Walker, G. & Peacock, E.E. (2008): Preliminary results of bone diagenesis in Scandinavian bogs. - Palaeogeography, Palaeoclimatology Palaeoecology, 266: 151-159.
74. Turner-Walker, G. & Syversen, U. (2002): Quantifying histological changes in archaeological bones using BSESEM image analysis. - Archaeometry, 44 (3): 161-168.
75. Turner-Walker, G. Nielsen-Marsh, C.M., Syversen, U., Kars, H. & Collins, M.J. (2002): Sub-micron spongiform porosity is the major ultra-structural alteration occurring in archaeological bone. - International Journal of Osteoarchaeology, 12: 407-414.
76. Underwood, C.J., Mitchell, S.F. & Veltkamp, C.J. (1999): Microborings in mid Cretaceous fish teeth. - Proceedings of the Yorkshire Geological Society, 52: 269-274.
77. Underwood, C.J. & Mitchell, S.F. (2004): Sharks, bony fishes and endodental borings from the Miocene Montpelier Formation (White Limestone Group) of Jamaica. - Cainozoic Research, 3: 157-165.
78. Wedl, C. (1864): Über einen im Zahnbein und Knochen keimenden Pilz. - Sitzungsberichte der Kaiserlichen Akademie der Wissenschaften zu Wien, Mathematisch-Naturwissenschaftliche Classe, 50, Abt. I: 171-193.
79. Widge, C.C. (2006): Bison, Bogs and Big Bluestream: The Subsistance Ecology of Middle Holocene Hunter-Gatherers in the Eastern Great Plains. - Unpublished PhD Thesis, University of Kansas, Lawrence.
80. Wisshak, M. (2006): High-lattitude bioerosion: The Kosterfjord experiment. - Lecture Notes in Earth Sciences, 109: 49-114; Springer-Verlag (Berlin and Heidelberg).
81. Wisshak, M., Seuß, B. & Nützel, A. (2008): Evolutionary implications of an exceptionally preserved Carboniferous microboring assemblage in the Buckhorn Asphalt lagerstätte (Oklahoma, USA). - In: Wisshak, M. & Ta-Panila, L. (Eds.): Current developments in bioerosion, 21-54; Berlin and Heidelberg (Erlangen Earth Conference Series, Springer-Verlag).
82. Yoshino, M., Kimijima, T., Miyasaka, S., Sato, H. & Seta, S. (1991): Microscopical study on estimation of time since death in skeletal remains. - Forensic Science International, 49: 143-158.
83. Zhang, X.-G. & Pratt, B.R. (2008): Microborings in Early Cambrian phosphatic and phosphatized fossils. - Palaeogeography, Palaeoclimatology, Palaeoecology, 267: 185-195.