Marine Biology

, Volume 160, Issue 10, pp 2631–2645 | Cite as

Maintenance of coelomic fluid pH in sea urchins exposed to elevated CO2: the role of body cavity epithelia and stereom dissolution

  • Wiebke C. Holtmann
  • Meike Stumpp
  • Magdalena A. Gutowska
  • Stephanie Syré
  • Nina Himmerkus
  • Frank Melzner
  • Markus BleichEmail author
Original Paper


Experimental ocean acidification leads to a shift in resource allocation and to an increased [HCO3 ] within the perivisceral coelomic fluid (PCF) in the Baltic green sea urchin Strongylocentrotus droebachiensis. We investigated putative mechanisms of this pH compensation reaction by evaluating epithelial barrier function and the magnitude of skeleton (stereom) dissolution. In addition, we measured ossicle growth and skeletal stability. Ussing chamber measurements revealed that the intestine formed a barrier for HCO3 and was selective for cation diffusion. In contrast, the peritoneal epithelium was leaky and only formed a barrier for macromolecules. The ossicles of 6 week high CO2-acclimatised sea urchins revealed minor carbonate dissolution, reduced growth but unchanged stability. On the other hand, spines dissolved more severely and were more fragile following acclimatisation to high CO2. Our results indicate that epithelia lining the PCF space contribute to its acid–base regulation. The intestine prevents HCO3 diffusion and thus buffer leakage. In contrast, the leaky peritoneal epithelium allows buffer generation via carbonate dissolution from the surrounding skeletal ossicles. Long-term extracellular acid–base balance must be mediated by active processes, as sea urchins can maintain relatively high extracellular [HCO3 ]. The intestinal epithelia are good candidate tissues for this active net import of HCO3 into the PCF. Spines appear to be more vulnerable to ocean acidification which might significantly impact resistance to predation pressure and thus influence fitness of this keystone species.


Ocean Acidification High pCO2 Septate Junction Seawater pCO2 Primary Spine 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This study was funded by the German “Biological impacts of ocean acidification (BIOACID)” project 3.1.4, funded by the Federal Ministry of Education and Research (BMBF, FKZ 03F0608M). The authors would like to thank U. Schuldt and A. Lettmann (Institute of Geosciences) for their support at the scanning electron microscope, T. Stegmann, R. Lingg and A. Cipriano for laboratory help, and the workshop of the Physiological Institute for the construction of special technical equipment.

Supplementary material

227_2013_2257_MOESM1_ESM.pdf (666 kb)
Supplementary material 1 (PDF 665 kb)


  1. Ahearn GA (1980) Intestinal electrophysiology and transmural ion transport in freshwater prawns. Am J Physiol Cell Physiol 239(1):C1–C10Google Scholar
  2. Ahearn GA, Franco P (1991) Electrogenic 2Na+/H+ antiport in echinoderm gastrointestinal epithelium. J Exp Biol 158(1):495–507Google Scholar
  3. Akberali HB (1980) 45Calcium uptake and dissolution in the shell of Scrobicularia plana (da Costa). J Exp Mar Biol Ecol 43(1):1–9. doi: 10.1016/0022-0981(80)90143-4 CrossRefGoogle Scholar
  4. Barnes RD (1980) Invertebrate zoology. Saunders College, PhiladelphiaGoogle Scholar
  5. Beyenbach KW, Skaer H, Dow JAT (2010) The developmental, molecular, and transport biology of Malpighian tubules. Annu Rev Entomol 55(1):351–374. doi: 10.1146/annurev-ento-112408-085512 CrossRefGoogle Scholar
  6. Boolootian R (1964) A histological study of the food canal of Strongylocentrotus franciscanus. Helgolander Wiss Meeresunters 11(2):118–127. doi: 10.1007/bf01611135 CrossRefGoogle Scholar
  7. Calosi P, Rastrick SPS, Graziano M, Thomas SC, Baggini C, Carter HA, Hall-Spencer JM, Milazzo M, Spicer JI (2013) Distribution of sea urchins living near shallow water CO2 vents is dependent upon species acid–base and ion-regulatory abilities. Mar Pollut Bull. doi: 10.1016/j.marpolbul.2012.11.040 Google Scholar
  8. Catarino A, Bauwens M, Dubois P (2012) Acid–base balance and metabolic response of the sea urchin Paracentrotus lividus to different seawater pH and temperatures. Environ Sci Pollut Res 19(6):2344–2353. doi: 10.1007/s11356-012-0743-1 CrossRefGoogle Scholar
  9. Clark D, Lamare M, Barker M (2009) Response of sea urchin pluteus larvae (Echinodermata: Echinoidea) to reduced seawater pH: a comparison among a tropical, temperate, and a polar species. Mar Biol 156(6):1125–1137. doi: 10.1007/s00227-009-1155-8 CrossRefGoogle Scholar
  10. Decker GL, Morrill JB, Lennarz WJ (1987) Characterization of sea urchin primary mesenchyme cells and spicules during biomineralization in vitro. Development 101(2):297–312Google Scholar
  11. Ebert TA, Southon J (2003) Red sea urchins (Strongylocentrotus franciscanus) can live over 100 years: confirmation with A-bomb 14carbon. Fish Bull 101(4):915–922Google Scholar
  12. Esbaugh A, Heuer R, Grosell M (2012) Impacts of ocean acidification on respiratory gas exchange and acid–base balance in a marine teleost, Opsanus beta. J Comp Physiol [B] 182(7):921–934. doi: 10.1007/s00360-012-0668-5 CrossRefGoogle Scholar
  13. Fabry VJ, Seibel BA, Feely RA, Orr JC (2008) Impacts of ocean acidification on marine fauna and ecosystem processes. ICES J Mar Sci 65(3):414–432CrossRefGoogle Scholar
  14. Feely RA, Alin SR, Newton J, Sabine CL, Warner M, Devol A, Krembs C, Maloy C (2010) The combined effects of ocean acidification, mixing, and respiration on pH and carbonate saturation in an urbanized estuary. Estuar Coast Shelf Sci 88(4):442–449. doi: 10.1016/j.ecss.2010.05.004 CrossRefGoogle Scholar
  15. Furuse M, Tsukita S (2006) Claudins in occluding junctions of humans and flies. Trends Cell Biol 16(4):181–188. doi: 10.1016/j.tcb.2006.02.006 CrossRefGoogle Scholar
  16. Gizurarson S (1993) The relevance of nasal physiology to the design of drug absorption studies. Adv Drug Deliv Rev 11(3):329–347. doi: 10.1016/0169-409X(93)90015-V CrossRefGoogle Scholar
  17. Green CR, Bergquist PR (1982) Phylogenetic relationships within the invertebrata in relation to the structure of septate junctions and the development of ‘occluding’ junctional types. J Cell Sci 53(1):279–305Google Scholar
  18. Green CR, Bergquist PR, Bullivant S (1979) An anastomosing septate junction in endothelial cells of the phylum echinodermata. J Ultrastruct Res 68(1):72–80CrossRefGoogle Scholar
  19. Greger R (1981) Cation selectivity of the isolated perfused cortical thick ascending limb of Henle’s loop of rabbit kidney. Pflugers Arch Eur J Physiol 390(1):30–37. doi: 10.1007/bf00582707 CrossRefGoogle Scholar
  20. Guerinot ML, Patriquin DG (1981) The association of N2-fixing bacteria with sea urchins. Mar Biol 62(2–3):197–207. doi: 10.1007/bf00388183 CrossRefGoogle Scholar
  21. Gutowska M, Melzner F, Langenbuch M, Bock C, Claireaux G, Pörtner HO (2010) Acid–base regulatory ability of the cephalopod (Sepia officinalis) in response to environmental hypercapnia. J Comp Physiol [B] 180(3):323–335. doi: 10.1007/s00360-009-0412-y CrossRefGoogle Scholar
  22. Heatfield BM, Travis DF (1975) Ultrastructural studies of regenerating spines of the sea urchin Strongylocentrotus purpuratus I. Cell types without spherules. J Morphol 145(1):13–49. doi: 10.1002/jmor.1051450103 CrossRefGoogle Scholar
  23. Hyman LH (1955) The invertebrates. Vol IV Echinodermata. McGraw-Hill Book Company, INC., New YorkGoogle Scholar
  24. Jokumsen A, Fyhn HJ (1982) The influence of aerial exposure upon respiratory and osmotic properties of haemolymph from two intertidal mussels, Mytilus edulis L. and Modiolus modiolus L. J Exp Mar Biol Ecol 61(2):189–203. doi: 10.1016/0022-0981(82)90008-9 CrossRefGoogle Scholar
  25. Kobayashi S, Taki J (1969) Calcification in sea urchins. Calcif Tissue Int 4(1):210–223. doi: 10.1007/bf02279124 CrossRefGoogle Scholar
  26. Larsen BK, Pörtner HO, Jensen FB (1997) Extra- and intracellular acid–base balance and ionic regulation in cod (Gadus morhua) during combined and isolated exposures to hypercapnia and copper. Mar Biol 128(2):337–346. doi: 10.1007/s002270050099 CrossRefGoogle Scholar
  27. Magie CR, Martindale MQ (2008) Cell–cell adhesion in the cnidaria: insights into the evolution of tissue morphogenesis. Biol Bull 214(3):218–232CrossRefGoogle Scholar
  28. Mall M, Bleich M, Greger R, Schreiber R, Kunzelmann K (1998) The amiloride-inhibitable Na+ conductance is reduced by the cystic fibrosis transmembrane conductance regulator in normal but not in cystic fibrosis airways. J Clin Investig 102(1):15–21. doi: 10.1172/jci2729 CrossRefGoogle Scholar
  29. Märkel K, Röser U (1983) The spine tissues in the echinoid Eucidaris tribuloides. Zoomorphology 103(1):25–41. doi: 10.1007/bf00312056 CrossRefGoogle Scholar
  30. Meidel SK, Scheibling RE (1999) Effects of food type and ration on reproductive maturation and growth of the sea urchin Strongylocentrotus droebachiensis. Mar Biol 134(1):155–166. doi: 10.1007/s002270050534 CrossRefGoogle Scholar
  31. Melzner F, Gutowska MA, Langenbuch M, Dupont S, Lucassen M, Thorndyke MC, Bleich M, Pörtner HO (2009) Physiological basis for high CO2 tolerance in marine ectothermic animals: pre-adaptation through lifestyle and ontogeny? Biogeosciences 6(10):2313–2331. doi: 10.5194/bg-6-2313-2009 CrossRefGoogle Scholar
  32. Melzner F, Thomsen J, Koeve W, Oschlies A, Gutowska MA, Bange HW, Hansen H-P, Körtzinger A (2012) Future ocean acidification will be amplified by hypoxia in coastal habitats. Mar Biol 1–14. doi: 10.1007/s00227-012-1954-1
  33. Michaelidis B, Ouzounis C, Paleras A, Pörtner HO (2005) Effects of long-term moderate hypercapnia on acid–base balance and growth rate in marine mussels Mytilus galloprovincialis. Mar Ecol Prog Ser 293:109–118. doi: 10.3354/meps293109 CrossRefGoogle Scholar
  34. Miles H, Widdicombe S, Spicer JI, Hall-Spencer J (2007) Effects of anthropogenic seawater acidification on acid–base balance in the sea urchin Psammechinus miliaris. Mar Pollut Bull 54(1):89–96. doi: 10.1016/j.marpolbul.2006.09.021 CrossRefGoogle Scholar
  35. Moitoza DJ, Phillips DW (1979) Prey defence, predator preference, and non-random diet - the interactions between Pycnopodia helianthoides and two species of sea urchins. Mar Biol 53(4):299–304. doi: 10.1007/bf00391611 CrossRefGoogle Scholar
  36. Pane EF, Barry JP (2007) Extracellular acid–base regulation during short-term hypercapnia is effective in a shallow-water crab, but ineffective in a deep-sea crab. Mar Ecol Prog Ser 334:1–9. doi: 10.3354/meps334001 CrossRefGoogle Scholar
  37. Pörtner H-O (2008) Ecosystem effects of ocean acidification in times of ocean warming: a physiologist’s view. Mar Ecol Prog Ser 373:203–217CrossRefGoogle Scholar
  38. Ries JB, Cohen AL, McCorkle DC (2009) Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 37(12):1131–1134. doi: 10.1130/g30210a.1 CrossRefGoogle Scholar
  39. Rodolfo-Metalpa R, Houlbreque F, Tambutte E, Boisson F, Baggini C, Patti FP, Jeffree R, Fine M, Foggo A, Gattuso JP, Hall-Spencer JM (2011) Coral and mollusc resistance to ocean acidification adversely affected by warming. Nat Clim Change 1(6):308–312. doi: 10.1038/nclimate1200 CrossRefGoogle Scholar
  40. Romero M, Fulton C, Boron W (2004) The SLC4 family of HCO3 transporters. Pflügers Archiv Eur J Physiol 447(5):495–509. doi: 10.1007/s00424-003-1180-2 CrossRefGoogle Scholar
  41. Sawabe T, Oda Y, Shiomi Y, Ezura Y (1995) Alginate degradation by bacteria isolated from the gut of sea urchins and abalones. Microb Ecol 30(2):193–202. doi: 10.1007/bf00172574 CrossRefGoogle Scholar
  42. Scheibling RS, Anthony SA (2001) Feeding, growth and reproduction of sea urchins Strongylocentrotus droebachiensis on single and mixed diets of kelp (Laminaria spp.) and the invasive alga Codium fragile ssp. tomentosoides. Mar Biol 139(1):139–146. doi: 10.1007/s002270100567 CrossRefGoogle Scholar
  43. Scheibling RE, Hatcher BG (2007) Ecology of Strongylocentrotus droebachiensis. In: Lawrence JM (ed) Edible sea urchins: biology and ecology, 2nd edn. Elsevier, Amsterdam, pp 353–392 CrossRefGoogle Scholar
  44. Shirayama Y, Thornton H (2005) Effect of increased atmospheric CO2 on shallow water marine benthos. J Geophys Res Oceans 110(C9):C09S08. doi: 10.1029/2004jc002618
  45. Siikavuopio SI, Mortensen A, Dale T, Foss A (2007) Effects of carbon dioxide exposure on feed intake and gonad growth in green sea urchin, Strongylocentrotus droebachiensis. Aquaculture 266(1–4):97–101. doi: 10.1016/j.aquaculture.2007.02.044 CrossRefGoogle Scholar
  46. Spicer JI (1995) Oxygen and acid–base status of the sea urchin Psammechinus miliaris during environmental hypoxia. Mar Biol 124(1):71–76. doi: 10.1007/bf00349148 CrossRefGoogle Scholar
  47. Spicer JI, Widdicombe S (2012) Acute extracellular acid–base disturbance in the burrowing sea urchin Brissopsis lyrifera during exposure to a simulated CO2 release. Sci Total Environ 427–428:203–207. doi: 10.1016/j.scitotenv.2012.02.051 CrossRefGoogle Scholar
  48. Spicer JI, Taylor AC, Hill AD (1988) Acid–base status in the sea urchins Psammechinus miliaris and Echinus esculentus (Echinodermata: Echinoidea) during emersion. Mar Biol 99(4):527–534. doi: 10.1007/bf00392560 CrossRefGoogle Scholar
  49. Spicer J, Raffo A, Widdicombe S (2007) Influence of CO2- related seawater acidification on extracellular acid–base balance in the velvet swimming crab Necora puber. Mar Biol 151(3):1117–1125. doi: 10.1007/s00227-006-0551-6 CrossRefGoogle Scholar
  50. Spicer JI, Widdicombe S, Needham HR, Berge JA (2011) Impact of CO2-acidified seawater on the extracellular acid–base balance of the northern sea urchin Strongylocentrotus dröebachiensis. J Exp Mar Biol Ecol 407(1):19–25. doi: 10.1016/j.jembe.2011.07.003 CrossRefGoogle Scholar
  51. Storch V, Welsch U (2009) Kükenthal Zoologisches Praktikum. Spektrum Akademischer Verlag, HeidlebergCrossRefGoogle Scholar
  52. Stumpp M, Trübenbach K, Brennecke D, Hu MY, Melzner F (2012) Resource allocation and extracellular acid–base status in the sea urchin Strongylocentrotus droebachiensis in response to CO2 induced seawater acidification. Aquat Toxicol 110–111:194–207. doi: 10.1016/j.aquatox.2011.12.020 CrossRefGoogle Scholar
  53. Swan EF (1961) Some observations on the growth rate of sea urchins in the genus Strongylocentrotus. Biol Bull 120(3):420–427CrossRefGoogle Scholar
  54. Tegner MJ, Levin LA (1983) Spiny lobsters and sea-urchins—analysis of a predator prey interaction. J Exp Mar Biol Ecol 73(2):125–150. doi: 10.1016/0022-0981(83)90079-5 CrossRefGoogle Scholar
  55. Thomsen J, Gutowska MA, Saphörster J, Heinemann A, Trübenbach K, Fietzke J, Hiebenthal C, Eisenhauer A, Körtzinger A, Wahl M, Melzner F (2010) Calcifying invertebrates succeed in a naturally CO2-rich coastal habitat but are threatened by high levels of future acidification. Biogeosciences 7(11):3879–3891. doi: 10.5194/bg-7-3879-2010 CrossRefGoogle Scholar
  56. Thomsen J, Casties I, Pansch C, Körtzinger A, Melzner F (2013) Food availability outweighs ocean acidification effects in juvenile Mytilus edulis: laboratory and field experiments. Glob Change Biol 19(4):1017–1027. doi: 10.1111/gcb.12109 CrossRefGoogle Scholar
  57. Tokin IB, Filimonova GF (1977) Electron microscope study of the digestive system of Strongylocentrotus droebachiensis (Echinodermata: Echinoidea). Mar Biol 44(2):143–155. doi: 10.1007/bf00386954 CrossRefGoogle Scholar
  58. Truchot JP, Duhamel-Jouve A (1980) Oxygen and carbon dioxide in the marine intertidal environment: diurnal and tidal changes in rockpools. Respir Physiol 39(3):241–254. doi: 10.1016/0034-5687(80)90056-0 CrossRefGoogle Scholar
  59. Unkles SE (1977) Bacterial flora of the sea urchin Echinus esculentus. Appl Environ Microbiol 34(4):347–350Google Scholar
  60. Van Itallie CM, Anderson JM (2004) The molecular physiology of tight junction pores. Physiology 19(6):331–338. doi: 10.1152/physiol.00027.2004 CrossRefGoogle Scholar
  61. Waldbusser GG, Voigt EP, Bergschneider H, Green MA, Newell RIE (2011) Biocalcification in the eastern oyster (Crassostrea virginica) in relation to long-term trends in Chesapeake Bay pH. Estuaries Coasts 34(2):221–231. doi: 10.1007/s12237-010-9307-0 CrossRefGoogle Scholar
  62. Weiner S, Addadi L (2011) Crystallization pathways in biomineralization. Annu Rev Mater Res 41(1):21–40. doi: 10.1146/annurev-matsci-062910-095803 CrossRefGoogle Scholar
  63. Zhuang Z, Duerr J, Ahearn G (1995) Ca2+ and Zn2+ are transported by the electrogenic 2Na+/1H+ antiporter in echinoderm gastrointestinal epithelium. J Exp Biol 198(5):1207–1217Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Wiebke C. Holtmann
    • 1
  • Meike Stumpp
    • 1
    • 2
    • 3
  • Magdalena A. Gutowska
    • 1
    • 2
  • Stephanie Syré
    • 2
  • Nina Himmerkus
    • 1
  • Frank Melzner
    • 2
  • Markus Bleich
    • 1
    Email author
  1. 1.Physiologisches InstitutKielGermany
  2. 2.GEOMAR Helmholtz Centre for Ocean Research KielKielGermany
  3. 3.Department of Biological and Environmental Sciences, The Sven Lovén Centre for Marine ScienceUniversity of GothenburgFiskebäckskilSweden

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