Biological and chemical characteristics of the coral gastric cavity

Abstract

All corals have a common structure: two tissue layers enclose a lumen, which forms the gastric cavity. Few studies have described the processes occurring inside the gastric cavity and its chemical and biological characteristics. Here, we show that the coral gastric cavity has distinct chemical characteristics with respect to dissolved O2, pH, alkalinity, and nutrients (vitamin B12, nitrate, nitrite, ammonium, and phosphate) and also harbors a distinct bacterial community. From these results, the gastric cavity can be described as a semi-closed sub-environment within the coral. Dissolved O2 shows very low constant concentrations in the deepest parts of the cavity, creating a compartmentalized, anoxic environment. The pH is lower in the cavity than in the surrounding water and, like alkalinity, shows day/night variations different from those of the surrounding water. Nutrient concentrations in the cavity are greater than the concentrations found in reef waters, especially for phosphate and vitamin B12. The source of these nutrients may be internal production by symbiotic bacteria and/or the remineralization of organic matter ingested or produced by the corals. The importance of the bacteria inhabiting the gastric cavity is supported by the finding of a high bacterial abundance and a specific bacterial community with affiliation to bacteria found in other corals and in the guts of other organisms. The findings presented here open a new area of research that may help us to understand the processes that maintain coral health.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. Agostini S, Suzuki Y, Casareto BE, Nakano Y, Fairoz MFM, Shiroma K, Irikawa A, Daigo K (2008) New approach to study the coral symbiotic complex: application to vitamin B12. Proc 11th Int Coral Reef Symp 2: 917–921

    Google Scholar 

  2. Agostini S, Suzuki Y, Casareto BE, Nakano Y, Hidaka M, Badrun N (2009) Coral symbiotic complex: hypothesis through vitamin B12 for a new evaluation. Galaxea 11:1–11

    Article  Google Scholar 

  3. Al-Horani F, Al-Moghrabi S, De Beer D (2003) The mechanism of calcification and its relation to photosynthesis and respiration in the scleractinian coral Galaxea fascicularis. Mar Biol 142:419–426

    CAS  Google Scholar 

  4. Borell E, Yuliantri A, Bischof K, Richter C (2008) The effect of heterotrophy on photosynthesis and tissue composition of two scleractinian corals under elevated temperature. J Exp Mar Biol Ecol 364:116–123

    Article  Google Scholar 

  5. Boschma H (1925) On the feeding reactions and digestion in the coral polyp Astrangia danæ, with notes on its symbiosis with zoöxanthellæ. Biol Bull 49:407–439

    Article  CAS  Google Scholar 

  6. Casareto BE, Charpy L, Langlade MJ, Suzuki T, Ohba H, Niraula M, Suzuki Y (2008) Proc 11th Int Coral Reef Symp 2:896–900

    Google Scholar 

  7. Cuet P, Pierret C, Cordier E, Atkinson MJ (2011) Water velocity dependence of phosphate uptake on a coral-dominated fringing reef flat, La Réunion Island, Indian Ocean. Coral Reefs 30:37–43

    Article  Google Scholar 

  8. Disalvo L (1971) Regenerative functions and microbial ecology of coral reefs: labelled bacteria in a coral reef microcosm. J Exp Mar Biol and Ecol 7:123–136

    Article  Google Scholar 

  9. Dubinsky Z, Jokiel P (1994) Ratio of energy and nutrient fluxes regulates symbiosis between zooxanthellae and corals. Pac Sci 48:313–324

    Google Scholar 

  10. Ducklow HW, Mitchell R (1979a) Bacterial populations and adaptations in the mucus layers on living corals. Limnol Oceanogr 24:715–725

    Google Scholar 

  11. Ducklow HW, Mitchell R (1979b) Composition of mucus released by coral reef coelenterates. Limnol Oceanogr 24:706–714

    Article  CAS  Google Scholar 

  12. Frankignoulle M, Gattuso J, Biondo R, Bourge I, Copin-Montégut G, Pichon M (1996) Carbon fluxes in coral reefs. II. Eulerian study of inorganic carbon dynamics and measurement of air-sea CO2 exchanges. Mar Ecol Prog Ser 145:123–132

    Article  Google Scholar 

  13. Galloway SB, Work TM, Bochsler VS, Harley RA, Kramarsky-Winters E, McLaughlin SM, Meteyer CU, Morado JF, Nicholson JH, Parnell PG, Peters EC, Reynolds TL, Rotstein DS, Sileo L, Woodley CM (2007) Coral disease and health workshop: coral histopathology II. NOAA technical memorandum NOS NCCOS 56 and NOAA technical memorandum CRCP 4. National Oceanic and Atmospheric Administration, Silver Spring, MD, p 84

    Google Scholar 

  14. Gattuso J, Pichon M, Delesalle B, Canon C, Frankignoulle M (1996) Carbon fluxes in coral reefs. I. Lagrangian measurement of community metabolism and resulting air-sea CO2 disequilibrium. Mar Ecol Prog Ser 145:109–121

    Article  Google Scholar 

  15. Gladfelter EH (1983) Circulation of fluids in the gastrovascular system of the reef coral Acropora cervicornis. Biol Bull 165:619–636

    Article  Google Scholar 

  16. Goldberg W (2002) Gastrodermal structure and feeding responses in the scleractinian Mycetophyllia reesi, a coral with novel digestive filaments. Tissue Cell 34:246–261

    Google Scholar 

  17. Grover R, Maguer J-F, Allemand D, Ferrier-Pagès C (2008) Uptake of dissolved free amino acids by the scleractinian coral Stylophora pistillata. J Exp Biol 211:860–865

    PubMed  Article  CAS  Google Scholar 

  18. Hansen HP, Koroleff F, Grasshoff K, Kremling K, Ehrhardt M (1999) Determination of nutrients. In: Grasshoff K, Kremling K, Ehrhardt M (eds) Methods of seawater analysis, 3rd edn. Wiley-VCH Verlag GmbH, Weinheim, Germany, pp 159–228

    Google Scholar 

  19. Herndl G, Velimirov B (1985) Bacteria in the coelenteron of Anthozoa: control of coelenteric bacterial density by the coelenteric fluid. J Exp Mar Biol Ecol 93:115–130

    Article  Google Scholar 

  20. Herndl G, Velimirov B (1986) Role of bacteria in the gastral cavity of Anthozoa. Deuxième colloque international de bacteriologie marine. IFREMER, Brest, France, pp 407–414

  21. Hoegh-Guldberg O, Williamson J (1999) Availability of two forms of dissolved nitrogen to the coral Pocillopora damicornis and its symbiotic zooxanthellae. Mar Biol 133:561–570

    Article  CAS  Google Scholar 

  22. Houlbrèque F, Tambutté E, Richard C, Ferrier-Pagès C (2004) Importance of a micro-diet for scleractinian corals. Mar Ecol Prog Ser 282:151–160

    Article  Google Scholar 

  23. Kinsey D (1985) Metabolism, calcification and carbon production. Proc 5th Int Coral Reef Symp 4, pp 515–526

  24. Klaus JS, Frias-Lopez J, Bonheyo GT, Heikoop JM, Fouke BW (2004) Bacterial communities inhabiting the healthy tissues of two Caribbean reef corals: interspecific and spatial variation. Coral Reefs 24:129–137

    Article  Google Scholar 

  25. Klimant I, Meyer V, Kühl M (1995) Fiber-optic oxygen microsensors, a new tool in aquatic biology. Limnol Oceanogr 40:1159–1165

    Article  CAS  Google Scholar 

  26. Kooperman N, Ben-Dov E, Kramarsky-Winter E, Barak Z, Kushmaro A (2007) Coral mucus-associated bacterial communities from natural and aquarium environments. FEMS Microbiol Lett 276:106–113

    Google Scholar 

  27. Kühl M, Cohen Y, Dalsgaard T, Jørgensen BB, Revsbech NP (1995) The microenvironment and photo-synthesis of zooxanthellae in scleractinian corals studied with microsensors for dissolved O2, pH and light. Mar Ecol Prog Ser 117:159–172

    Google Scholar 

  28. Kühl M, Holst G, Larkum AWD, Ralph PJ (2008) Imaging of oxygen dynamics within the endolithic algal community of the massive coral Porites lobata (Dana). J Phycol 44:541–550

    Google Scholar 

  29. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TH, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 1, 23(21):2947–2948

  30. Ley RE, Lozupone CA, Hamady M, Knight R, Gordon JI (2009) Worlds within worlds: evolution of the vertebrate gut microbiota. Computer 6:776–788

    Google Scholar 

  31. Moya A, Tambutté S, Bertucci A, Tambutté E, Lotto S, Vullo D, Supuran CT, Allemand D, Zoccola D (2008) Carbonic anhydrase in the scleractinian coral Stylophora pistillata: characterization, localization, and role in biomineralization. J Biol Chem 283:25475–25484

    PubMed  Article  CAS  Google Scholar 

  32. Muller-Parker G, Cook CD, Elia C (1990) Feeding affects phosphate fluxes in the symbiotic sea anemone Aiptasia pallida. Mar Ecol Prog Ser 60:283–290

    Article  CAS  Google Scholar 

  33. Murdock G (1978) Digestion, assimilation, and transport of food in the gastrovascular cavity of a gorgonian octocoral (Cnidaria; Anthozoa). Bull Mar Sci 28:354–362

    Google Scholar 

  34. Muscatine L, Falkowski PG, Dubinsky Z, Cook PA, McCloskey LR (1989) The effect of external nutrient resources on the population dynamics of zooxanthellae in a reef coral. Proc R Soc B 236: 311-324

    Google Scholar 

  35. Oksanen J, Blanchet FG, Kindt R, Legendre P, OHara RB, Simpson GL, Solymos P, Henry M, Stevens H, Wagner H (2011) Vegan: community ecology package. Diversity, pp 1–14

  36. Patterson MR, Sebens KP, Olson RR (1991) In situ measurements of flow effects on primary production and dark respiration in reef corals. Limnol Oceanogr 36:936–948

    Article  CAS  Google Scholar 

  37. Porter JW (1978) Coral feeding on zooplankton. In: Stoddart DR, Johannes RE (eds) Coral reefs: research methods. UNESCO, Paris, pp 515–521

    Google Scholar 

  38. Risk MJ, Muller HJ (1983) Porewater in coral heads: evidence for nutrient regeneration. Limnol Oceanogr 28:1004–1008

    Article  Google Scholar 

  39. Rohwer F, Breitbart M, Jara J, Azam F, Knowlton N (2001) Diversity of bacteria associated with the Caribbean coral Montastraea franksi. Coral Reefs 20:85–91

    Article  Google Scholar 

  40. Rohwer F, Seguritan V, Azam F, Knowlton N (2002) Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser 243:1–10

    Article  Google Scholar 

  41. Roosen-Runge EC (1967) Gastrovascular system of small hydromedusae: mechanisms of circulation. Science 156:74–76

    PubMed  Article  CAS  Google Scholar 

  42. Rosenberg E, Koren O, Reshef L, Efrony R (2007) The role of microorganisms in coral health, disease and evolution. Nat Rev Microb 5:355–362

    Article  CAS  Google Scholar 

  43. Schiller C, Herndl GJ (1989) Evidence of enhanced microbial activity in the interstitial space of branched corals: possible implications for coral metabolism. Coral Reefs 7:179–184

    Article  Google Scholar 

  44. Shashar N, Cohen Y, Loya Y (1993) Extreme diel fluctuations of oxygen in diffusive boundary layers surrounding stony corals. Biol Bull 185:455–461

    Article  Google Scholar 

  45. Shashar N, Cohen Y, Loya Y, Sar N (1994) Nitrogen fixation (acetylene reduction) in stony corals: evidence for coral-bacteria interactions. Mar Ecol Prog Ser 111:259–264

    Article  CAS  Google Scholar 

  46. Siboni N, Ben-Dov E, Sivan A, Kushmaro A (2008) Global distribution and diversity of coral-associated Archaea and their possible role in the coral holobiont nitrogen cycle. Environ Microbiol 10:2979–2990

    PubMed  Article  CAS  Google Scholar 

  47. Sorokin YI (1973) On the feeding of some scleractinian corals with bacteria and dissolved organic matter. Limnol Oceanogr 18:380–385

    Article  CAS  Google Scholar 

  48. Sweet MJ, Croquer A, Bythell JC (2010) Bacterial assemblages differ between compartments within the coral holobiont. Coral Reefs 30:39–52

    Article  Google Scholar 

  49. R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, ISBN 3-900051-07-0, URL:http://www.R-project.org/

  50. Titlyanov E, Titlyanova T, Leletkin V, Tsukahara J, van Woesik R, Yamazato K (1996) Degradation of zooxanthellae and regulation of their density in hermatypic corals. Mar Ecol Prog Ser 139:167–178

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by a Grant-in-Aid for Scientific Research on Innovative Areas for “Coral reef science for symbiosis and coexistence of human and ecosystem under combined stresses” (20121003) of the Ministry of Education, Culture, Sports, Science and Technology (MEXT), Japan and by the Global Coral Reef Conservation Project of Mitsubishi Corporation, Japan. The author would like to thank the anonymous reviewers for their helpful comments to improve this manuscript.

Author information

Affiliations

Authors

Corresponding author

Correspondence to S. Agostini.

Additional information

Communicated by Biology Editor Dr. Ruth Gates

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Agostini, S., Suzuki, Y., Higuchi, T. et al. Biological and chemical characteristics of the coral gastric cavity. Coral Reefs 31, 147–156 (2012). https://doi.org/10.1007/s00338-011-0831-6

Download citation

Keywords

  • Gastric cavity
  • Dissolved oxygen
  • Galaxea fascicularis
  • Microbiome
  • Nutrients