Close encounters in the substrate: when macroborers meet microborers

Abstract

Coral cores taken from Great Barrier Reef massive Porites sp. were assessed for bioerosion by the brown demosponge Cliona orientalis Thiele, 1900, but also yielded evidence for microbial bioerosion that was partly simultaneously active with the sponge bioerosion. The most common microborer traces throughout wereIchnoreticulina elegans (Radtke, 1991) produced by the chlorophyte alga Ostreobium quekettii Bornet and Flahault, 1889 and Scolecia serrata Radtke, 1991, likely a bacterial trace. Additional, less common traces belonging to the ichnogenera Saccomorpha and Orthogonum were attributed to fungal tracemakers. Especially I. elegans was found partly colonizing the so-called sponge scars, new surfaces formed by the bioeroding sponge, indicating that the alga was still actively bioeroding after infestation by the sponge. In addition, a very small but abundant trace was discovered directly associated with the sponge’s etching scars. It is a yet-undescribed trace apparently of either fungal or bacterial origin. We found evidence that this and some other microbial euendoliths can at least temporarily co-exist with the clionaid sponge, both eroding simultaneously, and potentially even being engaged in a yet-unspecified symbiotic relationship. Observations on such endolithic borer relationships across different taxa are very rare. Further studies are needed to elucidate the roles of different bioeroders as well as their potential interactions.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3

References

  1. Bentis CJ, Kaufman L, Golubic S (2000) Endolithic fungi in reef-building corals (Order: Scleractinia) are common, cosmopolitan, and potentially pathogenic. Biol Bull 198:254–260

    Google Scholar 

  2. Bornet ME, Flahault C (1889) Sur quelques plantes vivant dans le test calcaire des mollusques. Bull Soc Bot France 36:CXLVII–LXXVI. https://doi.org/10.1080/00378941.1889.10835893

    Google Scholar 

  3. Del Campo J, Pombert JF, Šlapeta J, Larkum A, Keeling PJ (2017) The “other” coral symbiont: Ostreobium diversity and distribution. ISME J 11:296–299. https://doi.org/10.1038/ismej.2016.101

    Article  Google Scholar 

  4. Fang JKH, Schönberg CHL (2015) Carbonate budgets of coral reefs: recent developments in excavating sponge research. Reef Encount 30:43–46

    Google Scholar 

  5. Glaub I (1994) Mikrobohrspuren in ausgewählten Ablagerungsräumen des europäischen Jura und der Unterkreide (Klassifikation und Palökologie). Cour Forsch Inst Senckenberg 174:1–324

    Google Scholar 

  6. Glynn PW (1997) Bioerosion and coral reef growth: a dynamic balance. In: Birkeland C (ed) Life and death of coral reefs. Chapman and Hall, New York, pp 69–98

    Google Scholar 

  7. Golubic S, Brent G, Le Campion T (1970) Scanning electron microscopy of endolithic algae and fungi using a multipurpose casting-embedding technique. Lethaia 3:203–209

    Google Scholar 

  8. Golubic S, Radtke G, Le Campion-Alsumard T (2005) Endolithic fungi in marine ecosystems. Trends Microbiol 13:229–235. https://doi.org/10.1016/j.tim.2005.03.007

    Article  Google Scholar 

  9. Gutner-Hoch E, Fine M (2011) Genotypic diversity and distribution of Ostreobium quekettii within scleractinian corals. Coral Reefs 30:643–650

    Google Scholar 

  10. Heindel K, Wisshak M, Westphal H (2009) Microbioerosion in Tahitian reefs: a record of environmental change during the last deglacial sea-level rise (IODP 310). Lethaia 42:322–340. https://doi.org/10.1111/j.1502-3931.2008.00140.x

    Google Scholar 

  11. ICZN [International Commission for Zoological Nomenclature] (1999) International code of zoological nomenclature, adopted by the International Union of Biological Sciences, 4th edn. International Trust for Zoological Nomenclature, London

    Google Scholar 

  12. Ivarsson M, Bengtson S, Belivanova V, Stampanoni M, Marone F, Tehler A (2012) Fossilized fungi in subseafloor Eocene basalts. Geology 40:163–166. https://doi.org/10.1130/G32590.1

    Google Scholar 

  13. Kendrick B, Risk MJ, Michaelides J, Bergman K (1982) Amphibious microborers: bioeroding fungi isolated from live corals. Bull Mar Sci 32:862–867

    Google Scholar 

  14. Königshof P, Glaub I (2004) Traces of microboring organisms in Palaeozoic conodont elements. Geobios 37:416–424. https://doi.org/10.1016/j.geobios.2003.06.002

    Google Scholar 

  15. Le Campion-Alsumard T, Golubic S, Priess K (1995a) Fungi in corals: symbiosis or disease? Interaction between polyps and fungi causes pearl-like skeleton biomineralization. Mar Ecol Prog Series 117:137–147

    Google Scholar 

  16. Le Campion-Alsumard T, Golubic S, Hutchings P (1995b) Microbial endoliths in skeletons of live and dead corals: Porites lobata (Moorea, French Polynesia). Mar Ecol Prog Series 117:149–157

    Google Scholar 

  17. López-Victoria M, Zea S (2005) Current trends of space occupation by encrusting excavating sponges on Colombian coral reefs. Mar Ecol 26:33–41. https://doi.org/10.1111/j.1439-0485.2005.00036.x

    Google Scholar 

  18. Massé A, Domart-Coulon I, Golubic S, Duché D, Tribollet A (2018) Early skeletal colonization of the coral holobiont by the microboring Ulvophyceae Ostreobium sp. Sci Rep 8:2293. https://doi.org/10.1038/s41598-018-20196-5

    Google Scholar 

  19. Meyer N, Wisshak M, Schönberg CHL (in press) Sponge bioerosion versus aqueous CO2: morphometric assessment of chips and etching fissures. Facies

  20. Neumann AC (1966) Observations on coastal erosion in Bermuda and measurements of the boring rate of the sponge, Cliona lampa. Limnol Oceanogr 11:92–108. https://doi.org/10.4319/lo.1966.11.1.0092

    Google Scholar 

  21. Pita L, Rix L, Slaby BM, Franke A, Hentschel U (2018) The sponge holobiont in a changing ocean: from microbes to ecosystems. Microbiome 6:46. https://doi.org/10.1186/s40168-018-0428-1

    Google Scholar 

  22. Priess K, Le Campion-Alsumard T, Golubic S, Gadel F, Thomassin BA (2000) Fungi in corals: black bands and density-banding of Porites lutea and P. lobata skeleton. Mar Biol 136:19–27. https://doi.org/10.1007/s002270050003

    Google Scholar 

  23. Radtke G (1991) Die mikroendolithischen Spurenfossilien im Alt-Tertiär West-Europas und ihre palökologische Bedeutung. Cour Forsch Inst Senckenberg 138:1–185

    Google Scholar 

  24. Risk MJ, Pagani SE, Elias RJ (1987) Another internal clock: preliminary estimates of growth rates based on cycles of algal boring activity. Palaios 2:323–331

    Google Scholar 

  25. Schneider J (1976) Biological and inorganic factors in the destruction of limestone coasts. Contr Sedimentol 62:1–11

    Google Scholar 

  26. Schneider J, Torunski H (1983) Biokarst on limestone coasts, morphogenesis and sediment production. PSZNI Mar Ecol 4:45–63. https://doi.org/10.1111/j.1439-0485.1983.tb00287.x

    Google Scholar 

  27. Schönberg CHL (2000) Bioeroding sponges common to the central Australian Great Barrier Reef: descriptions of three new species, two new records, and additions to two previously described species. Senckenb Marit 30:161–221. https://doi.org/10.1007/BF03042965

    Google Scholar 

  28. Schönberg CHL (2001) Small-scale distribution of Great Barrier Reef bioeroding sponges in shallow water. Ophelia 55:39–54. https://doi.org/10.1080/00785236.2001.10409472

    Google Scholar 

  29. Schönberg CHL (2002) Substrate effects on the bioeroding demospongeCliona orientalis. 1. Bioerosion rates. Mar Ecol 23:313–326. https://doi.org/10.1046/j.1439-0485.2002.02811.x

    Google Scholar 

  30. Schönberg CHL (2008) A history of sponge erosion: from past myths and hypotheses to recent approaches. In: Wisshak M, Tapanila L (eds) Current developments in bioerosion. Springer, Berlin, pp 165–202. https://doi.org/10.1007/978-3-540-77598-0_9

    Google Scholar 

  31. Schönberg CHL (2017) Culture, demography and biogeography of sponge science: from past conferences to strategic research? Mar Ecol 38:e12416. https://doi.org/10.1111/maec.12416

    Google Scholar 

  32. Schönberg CHL, Wilkinson CR (2001) Induced colonization of corals by a clionid bioeroding sponge. Coral Reefs 20:69–76. https://doi.org/10.1007/s003380100143

    Google Scholar 

  33. Schönberg CHL, Fang JKH, Carballo JL (2017a) Bioeroding sponges and the future of coral reefs. In: Carballo JL, Bell JJ (eds) Climate change, ocean acidification and sponges. Springer, Cham, pp 179–372. https://doi.org/10.1007/978-3-319-59008-0_7

    Google Scholar 

  34. Schönberg CHL, Fang JKH, Carreiro-Silva M, Tribollet A, Wisshak M (2017b) Bioerosion: the other ocean acidification problem. ICES J Mar Sci 74:895–925. https://doi.org/10.1093/icesjms/fsw254

    Google Scholar 

  35. Titlyanov EA, Kiyashko SI, Titlyanova TV, Yakovleva IM (2009) δ13C and δ15N in tissues of reef building corals and the endolithic alga Ostreobium quekettii under their symbiotic and separate existence. Galaxea 11:169–175. https://doi.org/10.3755/galaxea.11.169

    Google Scholar 

  36. Tribollet A (2008) The boring microfauna in modern coral reef ecosystems: a review of its roles. In: Wisshak M, Tapanila L (eds) Current developments in bioerosion. Springer, Berlin, pp 67–94

    Google Scholar 

  37. Verbruggen H, Marcelino VR, Guiry MD, Cremen MC, Jackson CJ (2017) Phylogenetic position of the coral symbiont Ostreobium (Ulvophyceae) inferred from chloroplast genome data. J Phycol 53:790–803. https://doi.org/10.1111/jpy.12540

    Google Scholar 

  38. Wisshak M (2006) High-latitude bioerosion. The Kosterfjord experiment. Lect Notes Earth Sci 109:1–202

    Google Scholar 

  39. Wisshak M (2012) Microbioerosion. In: Knaust D, Bromley RG (eds) Developments in sedimentology 64. Elsevier, Amsterdam, pp 213–243

    Google Scholar 

  40. Wisshak M, Schönberg CHL, Form A, Freiwald A (2013) Effects of ocean acidification and global warming on bioerosion—lessons from a clionaid sponge. Aquat Biol 19:111–127. https://doi.org/10.3354/ab00527

    Google Scholar 

  41. Wisshak M, Schönberg CHL, Form A, Freiwald A (2014) Sponge bioerosion accelerated by ocean acidification across species and latitudes? Helgol Mar Res 68:253–263. https://doi.org/10.1007/s10152-014-0385-4

    Google Scholar 

  42. Zebrowski G (1936) New genera of Cladochytriaceae. Ann Missouri Bot Garden 23:553–564

    Article  Google Scholar 

  43. Zu Castell W, Fleischmann F, Heger T, Matyssek R (2016) Shaping theoretic foundations of holobiont-like systems. In: Lüttge U, Cánovas F, Matyssek R (eds) Progress in botany, vol 77. Springer, Cham, pp 219–244. https://doi.org/10.1007/978-3-319-25688-7_7

    Google Scholar 

Download references

Acknowledgements

MW’s and CS’s experimental work was conducted at the Orpheus Island Research Station and strongly relied on the support of the station staff. R. and D. Wisdom, N. Lee and C. Ansell assisted during field and experimental work. The experimental phase was financially supported by Deutsche Forschungsgemeinschaft (Grant Fr 1134/19) and co-funded by the Australian Institute of Marine Science. S. Harii (Tropical Biosphere Research Center University of the Ryukyus, Okinawa) provided Fig. 1b.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Christine H. L. Schönberg.

Additional information

This article is part of a Topical Collection in Facies on Bioerosion: An interdisciplinary approach, guest edited by Ricci, Uchman, and Wisshak.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Schönberg, C.H.L., Gleason, F.H., Meyer, N. et al. Close encounters in the substrate: when macroborers meet microborers. Facies 65, 22 (2019). https://doi.org/10.1007/s10347-019-0567-2

Download citation

Keywords

  • Coral bioerosion
  • Bioeroder interaction
  • Cliona orientalis
  • Euendoliths
  • Ostreobium quekettii
  • Fungal and bacterial microbioerosion