Shipworm bioerosion of lithic substrates in a freshwater setting, Abatan River, Philippines: Ichnologic, paleoenvironmental and biogeomorphical implications

Autoři: J. Reuben Shipway aff001;  Gary Rosenberg aff003;  Gisela P. Concepcion aff004;  Margo G. Haygood aff005;  Charles Savrda aff006;  Daniel L. Distel aff002
Působiště autorů: School of Biological Sciences, University of Portsmouth, Portsmouth, United Kingdom aff001;  Ocean Genome Legacy Center, Department of Marine and Environmental Science, Northeastern University, Nahant, MA, United States of America aff002;  Academy of Natural Sciences, Drexel University, Philadelphia, PA, United States of America aff003;  Marine Science Institute, University of the Philippines, Diliman, Quezon City, Philippines aff004;  Department of Medicinal Chemistry, University of Utah, Salt Lake City, UT, United States of America aff005;  Department of Geosciences, Auburn University, Auburn, AL, United States of America aff006
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article


Teredinid bivalves, commonly referred to as shipworms, are known for their propensity to inhabit, bioerode, and digest woody substrates across a range of brackish and fully marine settings. Shipworm body fossils and/or their borings, which are most allied with the ichnotaxon Teredolites longissimus, are found in wood preserved in sedimentary sequences ranging in age from Early Cretaceous to Recent and traditionally they have been regarded as evidence of marginal marine or marine depositional environments. Recent studies associated with the Philippine Mollusk Symbiont International Collaboration Biodiversity Group (PMS-ICBG) expedition on the island of Bohol, Philippines, have identified a new shipworm taxon (Lithoredo abatanica) that is responsible for macrobioerosion of a moderately indurated Neogene foraminiferal packstone cropping out along a freshwater reach of the Abatan River. In the process of drilling into and ingesting the limestone, these shipworms produce elongate borings that expand in diameter very gradually toward distal termini, exhibit sinuous or highly contorted axes and circular transverse outlines, and are lined along most of their length by a calcite tube. Given their strong resemblance to T. longissimus produced in wood but their unusual occurrence in a lithic substrate, these shipworm borings can be regarded as incipient Gastrochaenolites or, alternatively, as Apectoichnus. The alternate names reflect that the borings provide a testbed for ideas of the appropriateness of substrate as an ichnotaxobasis. The discovery of previously unrecognized shipworm borings in lithic substrates and the co-occurrence of another shipworm (Nausitora) in submerged logs in the same freshwater setting have implications for interpreting depositional conditions based on fossil teredinids or their ichnofossils. Of equal significance, the Abatan River study demonstrates that macrobioerosion in freshwater systems may be just as important as it is in marine systems with regard to habitat creation and landscape development. L. abatanica serve as ecosystems engineers in the sense that networks of their abandoned borings provide habitats for a variety of nestling invertebrates, and associated bioerosion undoubtedly enhances rates of mechanical and chemical degradation, thus influencing the Abatan River profile.

Klíčová slova:

Calcite – Fresh water – Limestone – Marine biology – Marine fossils – Rivers – Ichnology – Paleoxylology


1. Turner R.D. 1966. A survey and illustrated catalogue of the Teredinidae (Mollusca: Bivalvia), Museum of Comparative Zoology, Harvard University, 265 p.

2. Bromley R.G., 2004. A stratigraphy of marine bioerosion. In: McIlroy D. (Ed.), The Application of Ichnology to Palaeoenvironmental and Stratigraphic Analysis, Geological Society of London Special Publication 228, pp. 455–479.

3. Kelly S.R.A., Bromley R.G. 1984. Ichnological nomenclature of clavate borings. Palaeontology 27, 793–807.

4. Savrda C.E., Smith M.W. 1996. Behavioral implications of branching and tube-lining in Teredolites. Ichnos 4, 191–198.

5. Bromley R.G., Pemberton S.G., Rahmani R.A. 1984. A Cretaceous woodground: the Teredolites ichnofacies. Journal of Paleontology 58, 488–498.

6. Savrda C.E. 1991. Teredolites, wood substrates, and sea-level dynamics. Geology 19, 905–908.

7. Savrda C.E., King D.T. Jr. 1993. Log-ground and Teredolites lagerstätte in a transgressive sequence, Upper Cretaceous (Lower Campanian) Mooreville Chalk, central Alabama. Ichnos 3, 69–77.

8. Savrda C.E., Ozalas K., Demko T.H., Huchison R.A., Scheiwe T.D. 1993. Log-grounds and the ichnofossil Teredolites in transgressive deposits of the Clayton Formation (Lower Paleocene), western Alabama. Palaios 8, 311–324.

9. Savrda C.E., Counts J., McCormick O., Urash R., Williams J., 2005. Log-grounds and Teredolites in transgressive deposits, Eocene Tallahatta Formation (southern Alabama, U.S.A.). Ichnos 12, 47–57.

10. Gingras M., MacEachern J.A., Pickerill R., 2004. Modern perspectives on the Teredolites ichnofacies: Observations from Willapa Bay, Washington. Palaios 19, 79–88.

11. Distel D.L., Altamia M.A., Lin Z., Shipway J.R., Han A., Forteza I., et al., 2017. Discovery of chemoautotrophic symbiosis in the giant shipworm Kuphus polythalamia (Bivalvia: Teredinidae) extends wooden-steps theory. PNAS

12. Shipway J.R., Altamia M.A., Rosenberg G., Concepcion G.P., Haygood M.G., Distel D.L., 2019. A rock-boring and rock-ingesting freshwater bivalve (shipworm) from the Philippines. Proceedings of the Royal Society B 286(1905): 20190434. doi: 10.1098/rspb.2019.0434 31213180

13. Barretto J.A.L., Dimalanta C.B., Yumul G.P., 2000. Gravity variations along the southeast Bohol ophiolite complex (SEBOC), central Philippines: Implications on ophiolite emplacement. Island Arc 9, 575–583.

14. Faustino D.V., Yumul G.P., De Jesus J.V., Dimalanta C.B., Aitchison J.C., Zhou M-F., et al., 2003. Geology of southeast Bohol, central Philippines: Accretion and sedimentation in a marginal basin. Australian Journal of Earth Sciences 50, 571–583.

15. Huggett J.M., Gale A.S. 1995. Palaeoecology and diagenesis of bored wood from the London Clay Formation of Sheppey, Kent. Proceedings of the Geologist’s Association 106, 119–136.

16. Bromley R.G., Asgaard U. 1993. Endolithic community replacement on a Pliocene rocky coast. Ichnos 2, 93–116

17. Tapanila L., Roberts E.M., Bouaré M.L., Sissoko F., O’Leary M.A., 2004. Bivalve borings in phosphatic coprolites and bone, Cretaceous-Paleogene, northeastern Mali. Palaios 19, 565–573

18. Leymerie M.A., 1842. Suite de mémoire sur le terrain Crétacé du départment de l’Aube. Memoire de la Société Géologique de France 5, 1–34.

19. Bromley R.G., D’Alessandro A., 1987. Bioerosion of the Plio-Pleistocene transgression of southern Italy. Rivista Italiana di Paleontologia e Stratigrafia 93, 379–442.

20. Wilson M.A., Palmer T.J., 1998. The earliest Gastrochaenolites (Early Pennsylvanian), Arkansas, USA): an Upper Paleozoic bivalve boring? Journal of Paleontology 72, 769–772.

21. Ekdale A.A., Bromley R.G., 2001. Bioerosional innovation for living in carbonate hardgrounds in the early Ordovician of Sweden. Lethaia 34, 1–12.

22. Donovan S.K., 2002. A new ichnospecies of Gastrochaenolites Leymerie from the Pleistocene Port Morant Formation of southeast Jamaica and the taphonomy of calcareous linings in clavate borings. Ichnos 9, 61–66.

23. Kleemann K., 2009. Gastrochaenolites hospitium isp. Nov., trace fossil by a coral-associated boring bivalve from the Eocene and Miocene of Austria. Geologica Carpathica 60, 339–342.

24. Edinger E.N., Risk M.J., 1994. Oligocene-Miocene extinction and geographic restriction of Caribbean corals: Roles of turbidity, temperature, and nutrients. Palaios 9, 576–598.

25. Donovan S.K., 2018. A new ichnogenus for Teredolites longissimus Kelly and Bromley. Swiss Journal of Palaeontology 137, 95–98.

26. Turner, R.D. 1971. Identification of marine wood-boring molluscs. In: Jones, E.B.G., Eltringham, S.K. (Eds.), Marine borers, fungi, and fouling organisms of wood, Workshop Proceedings, Organisation for Economic Co-operation and Development, pp. 17–64.

27. Turner, R.D., Johnson, A.C. 1971. Biology of marine wood-boring molluscs. In Jones, E.B.G., Eltringham, S.K. (Eds.), Marine borers, fungi, and fouling organisms of wood, Workshop Proceedings, Organisation for Economic Co-operation and Development, pp. 259–301.

28. Hoagland K.E., Turner R.D. 1981. Evolution and adaptive radiation of wood-boring bivalves (Pholadacea). Malacologia, 21, 111–148.

29. Turner, R.D. 1984. An overview of research on marine borers: past progress and future direction. In: Costlow, J.D., Tipper, R.C. (Eds.), Marine Biodeterioration- and Interdisciplinary Study, Proceedings of the Symposium on Marine Biodeterioration, Naval Institute Press, Annapolis, pp. 3–16.

30. Bertling M., Braddy S.J., Bromley R.G., DeMathieu G.R., Genise J., Milkuláš R., et al., 2006. Names for trace fossils: a uniform approach. Lethaia 39, 265–286.

31. Donovan S.K., Ewin T.A.M., 2018. Substrate is a poor ichnotaxobase: a new demonstration. Swiss Journal of Palaeontology 137, 103–107.

32. Bertling M., 2007. What’s in a name? Nomenclature, systematics, ichnotaxonomy. In: Miller W. (Ed.), Trace Fossils: Concepts Problems Products, Elsevier, Amsterdam, pp. 81–91.

33. Kleemann K., 1990. Boring and growth of chemically boring bivalves from the Caribbean, eastern Pacific and Australia’s Great Barrier Reef. Senckenbergiana maritima 21, 101–154.

34. Kleemann K., 1996. Biocorrosion by bivalves. Marine Ecology 17, 145–158.

35. Waterbury J.B., Calloway C.B., Turner R.D., 1983. A cellulytic-nitrogen fixing bacterium cultured from the gland of Deshayes in shipworms (Bivalvia: Teredinidae). Science 221, 1401–1403. doi: 10.1126/science.221.4618.1401 17759016

36. Distel D.L., 2003. The biology of marine wood boring bivalves and their bacterial symbionts. Wood Deterioration and Preservation 845, 253–271.

37. O’Connor R.M., Fung J.M., Sharp K.H., Benner J.S., McClung C., Cushing, et al., 2014. Gill bacteria enable a novel digestive strategy in a wood-feeding mollusk. Proceedings of the National Academy of Sciences, 111(47), E5096–E5104.

38. Shipway J.R., Altamia M.A., Haga T., Velasquez M., Albano J., Dechavez R., et al., 2018. Observations on the life history and geographic range of the giant chemosymbiotic shipworm Kuphus polythalamius (Bivalvia: Teredinidae). Biological Bulletin 235, 167–177. doi: 10.1086/700278 30624120

39. Altamia M.A., Shipway J.R., Concepcion G.P., Haygood M.G., Distel D.L., 2018. Thiosocius teredinicola gen. nov., sp. nov., a sulfur-oxidizing chemolithoautotrophic endosymbiont cultivated from the gills of the giant shipworm, Kuphus polythalamius. International Journal of Systematic and Evolutionary Microbiology. doi: 10.1099/ijsem.0.003143 30540238

40. Plint A.G., Pickerill R.K., 1985. Non-marine Teredolites from the Middle Eocene of southern England. Lethaia 18, 341–347.

41. Tewari A., Hart M.B., Watkinson M.P. 1998. Teredolites from the Garudamangalam Sandstone Formation (late Turonian-Coniacian), Cauvery Basin, southeast India. Ichnos 6, 75–98.

42. Lopes S.G.B.C., Narchi W., 1993. Levantamento e distribção das espécies de Teredinidae (Mollusca-Bivalvia) no manguezal de Praia Dura, Ubatuba, São Paulo, Brasil. Boletim do Instituto Oceanográfico 41, 29–38.

43. Leonel R.M.V., Lopes S.B.G.C., Zago D., 1998. Morphological basis of excretory function in Nausitora fusticula (Jeffreys, 1860) (Bivalvia:Teredinidae). Journal of Molluscan Studies 64, 223–237.

44. Bolotov I.N., Aksenova O.V., Bakken T., Glasby C.J., Gofarov M.Y., Kondakov A.V., et al., 2018. Discovery of a silicate rock-boring organisms and macrobioerosion in fresh water. Nature Communications, 9:2882 doi: 10.1038/s41467-018-05133-4 30038289

45. Warme J.E., 1975. Borings as trace fossils, and the processes of marine bioerosion. In Frey R.W. (Ed.), The Study of Trace Fossils, Springer-Verlag, Berlin, pp. 181–227.

46. Bromley R.G. 1975. Trace fossils at omission surfaces. In: Frey R.W. (Ed.), The Study of Trace Fossils, Springer-Veralg, Berlin, pp. 399–428.

47. Bromley R.G. 1994. The Palaeoecology of bioerosion. In: Donovan S.K. (Ed.), The Palaeobiology of Trace Fossils, John Hopkins, Baltimore, pp. 134–154.

48. Wilson M.A., 2007. Macroborings and the evolution of marine bioerosion. In: Miller W.M. (Ed.), Trace Fossils- Concepts Problems Prospects, Elsevier, Amsterdam, pp. 356–367.

49. de Gibert J.M., Domènech R., Martinell J., 2012. Chapter 15. Rocky shorelines. In: Knaust D., Bromley R.G. (Eds.), Trace Fossils as Indicators of Sedimentary Environments, Developments in Sedimentology 64, Elsevier, Amsterdam, pp. 441–462.

50. Naylor L.A., Viles H.A., Carter N.E.A., 2002. Biogeomorphology revisited: looking towards the future. Geomorphology 47, 3–14.

51. Naylor L.A., Coombes M.A., Viles H.A., 2012. Reconceptualising the role of organisms in the erosion of rock coasts: a new model. Geomorphology 157–158, 17–30.

52. Naylor L.A., Viles H.A., 2002. A new technique for evaluating short-term rates of coastal bioerosion and bioprotection. Geomorphology 47, 31–44.

53. Spencer T., Viles H., 2002. Bioconstruction, bioerosion and disturbance on tropical coasts: coral reefs and rocky limestone shores. Geomorphology 48, 23–50.

54. Savrda C.E., 2019. Bioerosion of a modern bedrock stream bed by insect larvae (Conecuh River, Alabama): Implications for ichnotaxonomy, continental ichnofacies, and biogeomorphology. Palaeogeography, Palaeoclimatology, Palaeoecology 513, 3–13.

Článek vyšel v časopise


2019 Číslo 10
Nejčtenější tento týden