pH Regulation and Excretion in Echinoderms

  • Meike StumppEmail author
  • Marian Y. Hu


As osmoconformers with low metabolic rates, echinoderms are generally regarded as rather weak acid–base regulators. Accordingly, little attention has been placed on whether echinoderms have evolved mechanisms to regulate ionic homeostasis. In the last century, only few studies examined the acid–base physiology of echinoderms, mostly sea urchins. These studies were conducted in an environmental context as some species inhabit rock pools and experience periodic emersion from their marine environment that can cause a metabolic acidosis. Lately, acid–base physiology in marine invertebrates, especially calcifying species, has received considerable attention as these animals were considered as particularly vulnerable in the context of CO2-induced ocean acidification. A substantial extracellular pH regulatory ability has been hypothesized to determine the degree of sensitivity in marine taxa. The emerging field of ocean acidification research in the last decade also shed new light on the acid–base physiology in echinoderms. Therefore, most of the available literature on echinoderm acid–base physiology describes the effects of CO2-induced seawater acidification on the extracellular acid–base homeostasis of echinoderm adults and larvae. This book chapter will summarize the most recent advances of acid–base physiology and nitrogen excretion in echinoderms in the face of ocean acidification. It will cover adult pH regulation as far as mechanistic data is available and also echinoderm larval physiology in respect to intracellular and extracellular acid–base regulation. Finally, it will make a short excursion into the ocean acidification research field, since most of the conducted research started because of this.


Ocean Acidification Elevated pCO2 Coelomic Fluid Brittle Star Extracellular Acid 
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.


  1. Appelhans JS, Thomsen J, Pansch C, Melzner F, Wahl M (2012) Sour times: seawater acidification effects on growth, feeding behaviour and acid-base status of Asterias rubens and Carcinus maenas. Mar Ecol Prog Ser 459:85–97CrossRefGoogle Scholar
  2. Basse WC, Gutowska MA, Findeisen U, Stumpp M, Dupont ST, Jackson DJ, Himmerkus N, Melzner F, Bleich M (2015) A sea urchin Na+K+ 2Cl cotransporter is involved in the maintenance of calcification-relevant cytoplasmic cords in Strongylocentrotus droebachiensis larvae. Comp Biochem Physiol A Mol Integr Physiol 187:184–192CrossRefPubMedGoogle Scholar
  3. Beniash E, Aizenberg J, Addadi L, Weiner S (1997) Amorphous calcium carbonate transforms into calcite during sea urchin larval spicule growth. Proc R Soc Lond B 264:461–465CrossRefGoogle Scholar
  4. Bleich M, Köttgen M, Schlatter E, Greger R (1995) Effect of NH4 +/NH3 on cytosolic pH and the K+ channels of freshly isolated cells from the thick ascending limb of Henle’s loop. Pflugers Arch 429:345–354CrossRefPubMedGoogle Scholar
  5. Boron WF (2004) Regulation of intracellular pH. Adv Physiol Educ 28:160–179CrossRefPubMedGoogle Scholar
  6. Boron WF, De Weer P (1976) Intracellular pH transients in squid giant axons caused by CO2, NH3, and metabolic inhibitors. J Gen Physiol 67:91–112CrossRefPubMedGoogle Scholar
  7. Boudko DY, Moroz LL, Harvey WR, Linser PJ (2001) Alkalization by chloride/bicarbonate pathway in larval mosquito midgut. Proc Natl Acad Sci U S A 98:15354–15359CrossRefPubMedPubMedCentralGoogle Scholar
  8. Buitenhuis ET, de Baar HJW, Veldhuis MJW (1999) Photosynthesis and calcification by Emiliania huxleyi (Prymnesiophyceae) as a function of inorganic carbon species. J Phycol 35:949–959CrossRefGoogle Scholar
  9. Burke DR (1981) Structure of the digestive tract of pluteus larva of Dendraster excentricus (Echinodermata: Echinoidea). Zoomorph 98:209–225CrossRefGoogle Scholar
  10. Byrne M, Gonzalez-Bernat M, Doo S, Foo S, Soars N, Lamare M (2013) Effects of ocean warming and acidification on embryos and non-calcifying larvae of the invasive sea star Patiriella regularis. Mar Ecol Prog Ser 473:235–246CrossRefGoogle Scholar
  11. 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 Poll Bull 30:470–484CrossRefGoogle Scholar
  12. 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 Poll Res 19:2344–2355CrossRefGoogle Scholar
  13. Collard M, Eeckhaut I, Dehairs F, Dubois P (2014a) Acid-base physiology response to ocean acidification of two ecologically and economically important holothuroids from contrasting habitats, Holothuria scabra and Holothuria parva. Environ Sci Poll Res 21:13602–13614CrossRefGoogle Scholar
  14. Collard M, Srey A, Dehairs F, Dubois P (2014b) Euechinoidea and Cidaroidea respond differently to ocean acidification. Comp Biochem Physiol A 174:45–55CrossRefGoogle Scholar
  15. Crawford BJ (1990) Changes in the arrangement of the extracellular matrix, larval shape, and mesenchyme cell migration during asteroid larval development. J Morphol 206:147–161CrossRefGoogle Scholar
  16. Decker GL, Morrill JKB, Lennarz WJ (1987) Characterization of sea urchin primary mesenchyme cells and spicules during biomineralization, in vitro. Development 101:297–312PubMedGoogle Scholar
  17. Dow JA (1984) Extremely high pH in biological systems: a model for carbonate transport. Am J Physiol 246:R633–R636PubMedGoogle Scholar
  18. Dupont S, Ortega-Martinez O, Thorndyke MC (2010a) Impact of near-future ocean acidification on echinoderms. Ecotoxicology 19:449–462CrossRefPubMedGoogle Scholar
  19. Dupont ST, Dorey N, Stumpp M, Melzner F, Thorndyke MC (2012) Long-term and trans-life-cycle effects of exposure to ocean acidification in the green sea urchin Strongylocentrotus droebachiensis. Mar Biol. Volume 160, Issue 8, pp 1835–1843. doi:  10.1007/s00227-012-1921-x
  20. Dupont ST, Havenhand JN, Thorndyke W, Peck L, Thorndyke MC (2008) Near-future level of CO2-driven ocean acidification radically affects larval survival and development in the brittlestar Ophiothrix fragilis. MEPS, Volume373, pp285-294Google Scholar
  21. Dupont ST, Lundve B, Thorndyke MC (2010b) Near future ocean acidification increases growth rate of the lecithotrophic larvae and juveniles of the sea star Crossaster papposus. J Exp Zool 314B:1–8CrossRefGoogle Scholar
  22. Dupont ST, Thorndyke MC (2012) Relationship between CO2-driven changes in extracellular acid-base balance and cellular immune response in two polar echinoderm species. J Exp Mar Biol Ecol 424–425:32–37CrossRefGoogle Scholar
  23. Felton GW, Duffey SS (1991) Reassessment of the role of gut alkalinity and detergency in insect herbivory. J Chem Ecol 17:1821–1836CrossRefPubMedGoogle Scholar
  24. Gonzalez-Bernat MJ, Lamare M, Barker M (2012) Effects of reduced seawater pH on fertilisation, embryogenesis and larval development in the Antarctic seastar Odontaster validus. Polar Biol 36:235–247CrossRefGoogle Scholar
  25. Gunaratne HJ, Vacquier VD (2007) Sequence, annotation and developmental expression of the sea urchin Ca2+-ATPase family. Gene 397:67–75CrossRefGoogle Scholar
  26. Hasselblatt P, Warth R, Schulz-Baldes A, Greger R, Bleich M (2000) pH regulation in isolated in vitro perfused rat colonic crypts. Pflugers Arch 441:118–124CrossRefPubMedGoogle Scholar
  27. Holtmann WC, Stumpp M, Gutowska MA, Syré S, Himmerkus N, Melzner F, Bleich M (2013) Maintenance of coelomic fluid pH in sea urchins exposed to elevated CO2: the role of body cavity epithelia and stereom dissolution. Mar Biol 160:2631–2645CrossRefGoogle Scholar
  28. Hu MY, Casties I, Stumpp M, Ortega-Martinez O, Dupont ST (2014) Energy metabolism and regeneration are impaired by seawater acidification in the infaunal brittlestar Amphiura filiformis. J Exp Biol 217:2411–2421CrossRefPubMedGoogle Scholar
  29. Hwang SP, Lennarz WJ (1993) Studies on the cellular pathway involved in assembly of the embryonic sea urchin spicule. Exp Cell Res 205:383–387CrossRefPubMedGoogle Scholar
  30. Jońezyk E, Klak M, Międzybrodzi R, Górski A (2011) The influence of external factors on bacteriophages-review. Folia Microbiol 56:191–200CrossRefGoogle Scholar
  31. Martin S, Richier S, Pedrotti M-L, Dupont S, Castejon C, Gerakis Y, Kerros M-E, Oberhänsli F, Teyssié J-L, Jeffree R, Gattuso J-P (2011) Early development and molecular plasticity in the Mediterranean sea urchin Paracentrotus lividus exposed to CO2-driven acidification. J Exp Biol 214:1357–1368Google Scholar
  32. McConnaughey TA, Whelan JF (1996) Calcification generates protons for nutrient and bicarbonate uptake. Earth Sci Rev 41:95–117Google Scholar
  33. 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. Biogeosci 6:2313–2331CrossRefGoogle Scholar
  34. Miles H, Widdicombe S, Spicer JI, Hall-Spencer JM (2007) Effects of anthropogenic seawater acidification on acid-base balance in the sea urchin Psammechinus miliaris. Mar Poll Bull 54:89–96CrossRefGoogle Scholar
  35. Moody WJ (1981) The ionic mechanism of intracellular pH regulation in crayfish neurones. J Physiol 316:293–308CrossRefPubMedPubMedCentralGoogle Scholar
  36. Nakano E, Okazaki K, Iwamatsu T (1963) Accumulation of radioactive calcium in the larvae of the sea urchin Pseudecentrotus depressus. Biol Bull 125:125–136CrossRefGoogle Scholar
  37. Pedersen MF, Hansen PJ (2003) Effects of high pH on the growth and survival of six marine heterotrophic protists. Mar Ecol Prog Ser 260:33–41CrossRefGoogle Scholar
  38. Pennington JT, Strathmann RR (1990) Consequences of the calcite skeletons of planktonic echinoderm larvae for orientation, swimming, and shape. Biol Bull 179:121–133CrossRefGoogle Scholar
  39. Politi Y, Arad T, Klein E, Weiner S, Addadi L (2004) Sea urchin spine calcite forms via a transient amorphous calcium carbonate phase. Science 306:1161–1164CrossRefPubMedGoogle Scholar
  40. Politi Y, Metzler RA, Abrecht M, Gilbert B, Wilt FH, Sagi I, Addadi L, Weiner S, Gilbert PUPA (2008) Transformation mechanisms of amorphous calcium carbonate into calcite in the sea urchin larval spicule. Proc Natl Acad Sci U S A 105:17362–17366CrossRefPubMedPubMedCentralGoogle Scholar
  41. Pond DW, Harris RP, Brownlee C (1995) A microinjection technique using a pH-sensitive dye to determine the gut pH of Calanus helgolandicus. Mar Biol 123:75–79CrossRefGoogle Scholar
  42. Raz S, Hamilton PC, Wilt FH, Weiner S, Addadi L (2003) The transient phase of amorphous calcium carbonate in sea urchin larval spicules: the involvement of proteins and magnesium ions in its formation and stabilization. Adv Funct Mater 13:480–486CrossRefGoogle Scholar
  43. Ries JB, Cohen AL, McCorkle DC (2009) Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 37:1131–1134CrossRefGoogle Scholar
  44. Robertson JD (1949) Ionic regulation in some marine invertebrates. J Exp Biol 26:182–200PubMedGoogle Scholar
  45. Sikes CS, Okazaki K, Fink RD (1981) Respiratory CO2 and the supply of inorganic carbon for calcification of sea urchin embryos. Comp Biochem Physiol A 70:285–291CrossRefGoogle Scholar
  46. Strathmann RR (1989) Existence and functions of a gel filled primary body cavity in development of echinoderms and hemichordates. Biol Bull 176:25–31CrossRefGoogle Scholar
  47. Stumpp M, Hu MY, Casties I, Saborowski R, Bleich M, Melzner F, Dupont S (2013) Digestion in sea urchin larvae impaired under ocean acidification. Nat Climate Change 3:1044–1049CrossRefGoogle Scholar
  48. Stumpp M, Hu MY, Melzner F, Gutowska MA, Dorey N, Himmerkus N, Holtmann WC, Dupont ST, Thorndyke MC, Bleich M (2012a) Acidified seawater impacts sea urchin larvae pH regulatory systems relevant for calcification. Proc Natl Acad Sci U S A 109:18192–18197CrossRefPubMedPubMedCentralGoogle Scholar
  49. Stumpp M, Hu MY, Tseng Y-C, Guh YJ, Chen YC, Yu JK, Su YH, Hwang PP (2015) Evolution of extreme stomach pH in bilateria inferred from gastric alkalization mechanisms in basal deuterostomes. Sci Rep 5:1–9CrossRefGoogle Scholar
  50. Stumpp M, Trübenbach K, Brennecke D, Hu MY, Melzner F (2012b) Resource allocation and extracellular acid-base status in the sea urchin Strongylocentrotus droebachiensis in response to CO2 induced seawater acidification. Aquat Toxicol 110–111:194–207CrossRefPubMedGoogle Scholar
  51. Wieczorek H, Putzenlechner M, Zeiske W, Klein U (1991) A vacuolar-type proton pump energizes K+/H+ antiport in an animal plasma membrane. J Biol Chem 266:15340–15347PubMedGoogle Scholar
  52. Wilt FH (2002) Biomineralization of the spicules of sea urchin embryos. Zool Sci 19:253–261CrossRefPubMedGoogle Scholar
  53. Zhu X, Mahairas G, Illies M, Cameron RA, Davidson EH, Ettensohn CA (2001) A large-scale analysis of mRNAs expressed by primary mesenchyme cells of the sea urchin embryo. Development 128:2615–2627PubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2017

Authors and Affiliations

  1. 1.RD 3: Marine EcologyHelmholtz Centre for Marine Sciences Kiel (GEOMAR)KielGermany
  2. 2.Institute of PhysiologyChristian-Albrechts-University of KielKielGermany

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