Advertisement

Marine Biodiversity

, Volume 48, Issue 4, pp 1855–1862 | Cite as

Euendolithic Conchocelis stage (Bangiales, Rhodophyta) in the skeletons of live stylasterid reef corals

  • Aline TribolletEmail author
  • Daniela Pica
  • Stefania Puce
  • Gudrun Radtke
  • Susan E. Campbell
  • Stjepko Golubic
Original Paper

Abstract

Stylasterids are azooxanthellate lace corals, which may show an unusual colouration in coral reef ecosystems, ranging from red to purple on the light-exposed side of their colonies. In the present study, it was discovered that the calcareous skeletons of such corals are actually invaded and eroded by cryptic carbonate boring algae that represent Conchocelis phases in the life cycle of bangialean rhodophytes. For the first time, the shape, organisation and distribution of Conchocelis filaments within the skeletons of two different genera of lace corals are reported and documented by light and electron microscopy. Such description and characterisation of Conchocelis can help to distinguish between morphologically and taxonomically different endolithic microorganisms penetrating coral skeletons, including their recognition in fossil borings as indicators of depositional depth, i.e. of the extent of the photic zone and light conditions in ancient marine environments. The results are discussed in the light of a possible symbiotic or parasitic relationship between Conchocelis phases and their stylasterid host corals.

Keywords

Coral reefs Coral skeleton Cryptic development Fossil record Microborers 

Notes

Acknowledgements

We thank Sandrine Caquineau for her assistance with the SEM on the platform Alysés at the Center IRD France-Nord (Bondy) and the Institut de Recherche pour le Développement for financial support. International collaborations were supported by the Alexander von Humboldt Foundation, Bonn, and Hanse Institute for Advanced Studies, Delmenhorst, Germany to S. Golubic. We also thank the Coral Eye Research Center for the logistic support in Indonesia. Specimens were imported by CITES permit code 04291/IV/SATS-LN/2011. We thank the editor Dr. Bert Hoeksema and the two anonymous reviewers for their positive and constructive comments and improvements of the manuscript.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

References

  1. Ame EC, Ayson JP, Okuda K, Andres R (2010) Porphyra fisheries in the Northern Philippines: some environmental issues and the socio-economic impact on the Ilocano fisherfolk. Kuroshio Sci 4:53–58Google Scholar
  2. Bao-Fu Z (1984) Studies on the morphology of conchocelis of Porphyra katadai var. hemiphylla and related species. Dev Hydrobiol 22:209–212CrossRefGoogle Scholar
  3. Batters EAL (1892) On Conchocelis, a new genus of perforating algae. Phycol Mem 1:25–29Google Scholar
  4. Behrendt L, Larkum AWD, Norman A, Qvortrup K, Chen M, Ralph P, Sørensen SJ, Trampe E, Kühl M (2011) Endolithic chlorophyll d-containing phototrophs. ISME J 5:1072–1076CrossRefGoogle Scholar
  5. Bornet E, Flahault C (1888) Note sur deux nouveaux genres d’algues perforantes. J Bot 2:161–165Google Scholar
  6. Bornet ME, Flahault C (1889) Sur quelques plantes vivant dans le test calcaire des mollusques. Bull Soc Bot Fr 36:147–176CrossRefGoogle Scholar
  7. Bundschuh M (2000) Silurische Mikrobohrspuren. Ihre Beschreibung und Verteilung in verschiedenen Faziesräumen (Schweden, Litauen, Großbritannien und USA). Dissertation, Johann Wolfgang Goethe University, pp. 1–129Google Scholar
  8. Butterfield NJ (2000) Bangiomorpha pubescens n. gen., n. sp.: implications for the evolution of sex, multicellularity, and the Mesoproterozoic/Neoproterozoic radiation of eukaryotes. Paleobiology 26:386–404CrossRefGoogle Scholar
  9. Butterfield NJ (2015) Early evolution of the Eukaryota. Paleontology 58:5–17CrossRefGoogle Scholar
  10. Campbell SE (1980) Palaeoconchocelis starmachii, a carbonate boring microfossil from the Upper Silurian of Poland (425 million years old): implications for the evolution of the Bangiaceae (Rhodophyta). Phycologia 19:25–36CrossRefGoogle Scholar
  11. Campbell SE, Cole K (1984) Developmental studies on cultured endolithic conchocelis (Rhodophyta). Hydrobiologia 116(117):201–208CrossRefGoogle Scholar
  12. Clokie JJP, Boney AD, Farrow GE (1979) The significance of Conchocelis as an indicator organism: data from the Firth of Clyde and N.W. Shelf. Br Phycol J 14:120–121Google Scholar
  13. Clokie JJP, Scoffin TP, Boney AD (1981) Depth maxima of Conchocelis and Phymatolithon rugulosum on the N. W. Shelf and Rockall Plateau. Mar Ecol Prog Ser 4:131–133CrossRefGoogle Scholar
  14. Dixon PS, Richardson WN (1969) The life histories of Bangia and Porphyra and the photoperiodic control of spore production. Proc Int Seaweed Symp 6:133–139Google Scholar
  15. Drew KM (1949) Conchocelis-phase in the life-history of Porphyra umbilicalis (L.) Kütz. Nature 164:748–749CrossRefGoogle Scholar
  16. Drew KM (1954) Studies in the Bangioideae III. The life-history of Porphyra umbilicalis (L.) Kütz. var. lociniata (Lightf.) J. Ag.: A. The Conchocelis-phase in culture. Ann Bot 18:183–184CrossRefGoogle Scholar
  17. Drew KM (1956) Reproduction in the Bangiophycidae. Bot Rev 22:553–611CrossRefGoogle Scholar
  18. Ercegović A (1932a) Ekološke i sociološke studije o litofitskim cijanoficejama sa jugoslavenske obale Jadrana. Rad Jugosl Akad Znan Umjet 244:129–220Google Scholar
  19. Ercegović A (1932b) Études écologiques et sociologiques des Cyanophycées lithophytes de la côte Yougoslave de l’Adriatique. Bull Int Acad Yougosl Sci Beaux Arts 26:33–56Google Scholar
  20. Fine M, Loya Y (2002) Endolithic algae: an alternative source of photoassimilates during coral bleaching. Proc R Soc Lond 269:1205–1210CrossRefGoogle Scholar
  21. Försterra G, Häussermann V (2008) Unusual symbiotic relationships between microendolithic phototrophic organisms and azooxanthellate cold-water corals from Chilean fjords. Mar Ecol Prog Ser 370:121–125CrossRefGoogle Scholar
  22. Fox DL (1972) Pigmented calcareous skeletons of some corals. Comp Biochem Physiol B 43:919–927CrossRefGoogle Scholar
  23. Glaub I (1994) Mikrobohrspuren in ausgewählten Ablagerungsräumen des europäischen Jura und der Unterkreide. Cour Forschungsinst Senck 174:1–324Google Scholar
  24. Glazer AN (1985) Light harvesting by phycobilisomes. Annu Rev Biophys Biophys Chem 14:47–77CrossRefGoogle Scholar
  25. Godinot C, Tribollet A, Grover R, Ferrier-Pagès C (2012) Bioerosion by euendoliths decreases in phosphate-enriched skeletons of living corals. Biogeosciences 9:2377–2384CrossRefGoogle Scholar
  26. Golubic S, Brent G, Lecampion T (1970) Scanning electron microscopy of endolithic algae and fungi using a multipurpose casting-embedding technique. Lethaia 3:203–209CrossRefGoogle Scholar
  27. Golubic S, Friedmann I, Schneider J (1981) The lithobiontic ecological niche, with special reference to microorganisms. J Sediment Petrol 51:475–478Google Scholar
  28. Guiry MD, Guiry GM (2017) AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. http://www.algaebase.org; searched in January 2016
  29. Kazmierczak J, Golubic S (1979) Paleoconchocelis starmachii n. gen., n. sp., a Silurian endolithic rhodophyte (Bangiaceae). Acta Palaeontol Pol 24:405–408Google Scholar
  30. Koehne B, Elli G, Jennings RC, Wilhelm C, Trissl H-W (1999) Spectroscopic and molecular characterization of a long wavelength absorbing antenna of Ostreobium sp. Biochim Biophys Acta 1412:94–107CrossRefGoogle Scholar
  31. Kołodziej B, Golubic S, Bucur II, Radtke G, Tribollet A (2012) Early Cretaceous record of microboring organisms in skeletons of growing corals. Lethaia 45:34–45CrossRefGoogle Scholar
  32. Kornmann P (1959) Die heterogene Gattung Gomontia I. Der sporangiale Anteil, Codiolum polyrhizum. Helgoländer Wiss Meeresun 6:229–238CrossRefGoogle Scholar
  33. Kornmann P (1960) Die heterogene Gattung Gomontia. lI. Der fadige Anteii, Eaffomontia saccalata nov. gen. nov. spec. Helgoländer Wiss Meeresun 7:59–71CrossRefGoogle Scholar
  34. Kornmann P (1961) Die Entwicklung von Porphyra leucosticta im Kulturversuch. Helgoländer Wiss Meeresun 8:167–175CrossRefGoogle Scholar
  35. Kornmann P (1962) Die Entwicklung von Monostroma grevillei. Helgoländer Wiss Meeresun 8:195–202CrossRefGoogle Scholar
  36. Kornmann P, Sahling PH (1980) Kalkbohrende Mikrothalli bei Helminthocladia und Scinaia (Nemaliales, Rhodophyta). Helgoländer Wiss Meeresun 34:31–40CrossRefGoogle Scholar
  37. Laborel J, Le Campion-Alsumard T (1979) Infestation massive du squelette de coraux vivants par des rhodophycées de type Conchocelis. CR Acad Sci Paris Ser D 288:1575–1577Google Scholar
  38. LeCampion-Alsumard T, Campbell SE, Golubic S (1982) Endoliths and the depth of the photic zone: discussion. J Sediment Petrol 52:1333–1334CrossRefGoogle Scholar
  39. Le Campion-Alsumard T, Golubic S, Hutchings P (1995) Microbial endoliths in skeletons of live and dead corals: Porites lobata (Moorea, French Polynesia). Mar Ecol Prog Ser 117:149–157CrossRefGoogle Scholar
  40. Li S, Ming J, Delin D (2006) Formation of primary pit connection during conchocelis phase of Porphyra yezoensis (Bangiophyceae, Rhodophyta). Chin J Oceanol Limnol 24:291–294CrossRefGoogle Scholar
  41. Lindstrom SC, Fredericq S (2003) rbcL gene sequences reveal relationships among north-east Pacific species of Porphyra (Bangiales, Rhodophyta) and a new species, P. aestivalis. Phycol Res 51:211–224CrossRefGoogle Scholar
  42. Lindstrom SC, Hughey JR, Aguilar-Rosas LE (2015) Four new species of Pyropia (Bangiales, Rhodophyta) from the west coast of North America: the Pyropia lanceolata species complex updated. PhytoKeys 52:1–22CrossRefGoogle Scholar
  43. Lukas KJ (1973) Taxonomy and ecology of the endolithic microflora of reef corals, with a review of the literature on endolithic microphytes. Dissertation, University of Rhode IslandGoogle Scholar
  44. Magnusson SH, Fine M, Kühl M (2007) Light microclimate of endolithic phototrophs in the scleractinian corals Montipora monasteriata and Porites cylindrica. Mar Ecol Prog Ser 332:119–128CrossRefGoogle Scholar
  45. Müller KM, Cannone JJ, Sheath RG (2005) A molecular phylogenetic analysis of the Bangiales (Rhodophyta) and description of a new genus and species, Pseudobangia kaycoleia. Phycologia 44:146–155CrossRefGoogle Scholar
  46. Odum HT, Odum EP (1955) Trophic structure and productivity of a windward coral reef community on Eniwetok Atoll, Marshall Islands. Ecol Monogr 25:291–320CrossRefGoogle Scholar
  47. Pica D, Tribollet A, Golubic S, Bo M, Di Camillo CG, Bavestrello G, Puce S (2016) Microboring organisms in living stylasterid corals (Cnidaria, Hydrozoa). Mar Biol Res 12:573–582CrossRefGoogle Scholar
  48. Puce S, Tazioli S, Bavestrello G (2009) First evidence of a specific association between a stylasterid coral (Cnidaria: Hydrozoa: Stylasteridae) and a boring cyanobacterium. Coral Reefs 28:177CrossRefGoogle Scholar
  49. Radtke G (1991) Die mikroendolithischen Spurenfossilien im Alt-Tertiär West-Europas und ihre palökologische Bedeutung. Cour Forschungsinst Senck 138:1–185Google Scholar
  50. Radtke G (1993) The distribution of microborings in molluscan shells from recent reef environments at Lee Stocking Island, Bahamas. Facies 29:81–92CrossRefGoogle Scholar
  51. Radtke G, Le Campion-Alsumard T, Golubic S (1996) Microbial assemblages of the bioerosional “notch” along tropical limestone coasts. Algol Stud 83:469–482Google Scholar
  52. Radtke G, Campbell SE, Golubic S (2016) Conchocelichnus seilacheri igen. et isp. nov., a complex microboring trace of Bangialean rhodophytes. Ichnos 23:228–236CrossRefGoogle Scholar
  53. Roux W (1887) Über eine im Knochen lebende Gruppe von Fadenpilzen (Mycelites ossifragus). Z Wiss Zool 45:227–254Google Scholar
  54. Ruangchuay R, Notoya M (2003) Physiological responses of blade and conchocelis of Porphyra vietnamensis Tanaka et Pham-Hoang Ho (Bangiales, Rhodophyta) from Thailand in culture. Algae 18:21–28CrossRefGoogle Scholar
  55. Schlichter D, Zscharnack B, Krisch H (1995) Transfer of photoassimilates from endolithic algae to coral tissue. Naturwissenschaften 82:561–564CrossRefGoogle Scholar
  56. Schmidt H (1992) Mikrobohrspuren ausgewählter Faziesbereiche der tethyalen und germanischen Trias (Beschreibung, Vergleich und bathymetrische Interpretation). Frankf Geowiss Arb A 12:1–228Google Scholar
  57. Sutherland DA, MacCready P, Banas NS, Smedstad LF (2011) A model study of the Salish Sea estuarine circulation. J Phys Oceanogr 41:1125–1143CrossRefGoogle Scholar
  58. Tribollet A (2008) The boring microflora in modern coral reef ecosystems: a review of its roles. In: Wisshak M, Tapanila L (eds) Current developments in bioerosion. Springer, Berlin, pp 67–94CrossRefGoogle Scholar
  59. Tribollet A, Decherf G, Hutchings P, Peyrot-Clausade M (2002) Large-scale spatial variability in bioerosion of experimental coral substrates on the Great Barrier Reef (Australia): importance of microborers. Coral Reefs 21:424–432Google Scholar
  60. Tribollet A, Radtke G, Golubic S (2011) Bioerosion. In: Reitner J, Thiel V (eds) Encyclopedia of geobiology. Springer, Berlin, pp 117–133CrossRefGoogle Scholar
  61. Tseng CK, Borowitzka M (2003) Algae culture. In: Lucas JS, Southgate PC (eds) Aquaculture: farming aquatic animals and plants. Blackwell, Oxford, pp 253–275Google Scholar
  62. Tseng CK, Chang TJ (1955) Studies on the life history of Porphyra tenera Kjellm. Sci Sinica 4:375–398Google Scholar
  63. Vadas RL, Steneck RS (1988) Zonation of deep water benthic algae in the Gulf of Maine. J Phycol 24:338–346CrossRefGoogle Scholar
  64. van Oppen MJH, Lough JM (eds) (2009) Coral bleaching. Springer, Berlin, pp 1–176Google Scholar
  65. Vogel K, Gektidis M, Golubic S, Kiene WE, Radtke G (2000) Experimental studies on microbial bioerosion at Lee Stocking Island, Bahamas and One Tree Island, Great Barrier Reef, Australia: implications for paleoecological reconstructions. Lethaia 33:190–204CrossRefGoogle Scholar
  66. Wang L, Mao Y, Kong F, Li G, Ma F, Zhang B, Sun P, Bi G, Zhang F, Xue H, Cao M (2013) Complete sequence and analysis of plastid genomes of two economically important red algae: Pyropia haitanensis and Pyropia yezoensis. PLoS One 8:e65902CrossRefGoogle Scholar
  67. Wisshak M, López-Correa M, Zibrowius H, Jakobsen J, Freiwald A (2009) Skeletal reorganisation affects geochemical signals, exemplified in the stylasterid hydrocoral Errina dabneyi (Azores Archipelago). Mar Ecol Prog Ser 397:197–208CrossRefGoogle Scholar

Copyright information

© Senckenberg Gesellschaft für Naturforschung and Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.IRD-Sorbonne Universités (Univ. Paris 6) UPMC-CNRS-MNHN, Laboratoire IPSL-LOCEANParis CedexFrance
  2. 2.Dipartimento di Scienze della Vita e dell’AmbienteUniversità Politecnica delle MarcheAnconaItaly
  3. 3.Hessisches Landesamt für Naturschutz, Umwelt und Geologie (HLNUG)WiesbadenGermany
  4. 4.Biological Science CenterBoston UniversityBostonUSA

Personalised recommendations