Marine Biology

, Volume 161, Issue 5, pp 1127–1138 | Cite as

Effects of ocean acidification on the early developmental stages of the horned turban, Turbo cornutus

  • Toshihiro OnitsukaEmail author
  • Ryo Kimura
  • Tsuneo Ono
  • Hideki Takami
  • Yukihiro Nojiri
Original Paper


To estimate the impact of CO2-driven ocean acidification on the early life stages of gastropods, the effects of increased partial pressure of seawater carbon dioxide (pCO2) (800–2,000 μatm) on the early developmental stages and larval shell length of the commercially important gastropod, the horned turban snail, Turbo cornutus were investigated. Increase in experimental seawater pCO2 had an increasingly negative impact on the early developmental rate; the proportion of embryos or larvae displaying retarded development increased at higher pCO2. The proportion of embryos that developed to the 4-cell stage at 2 h after fertilization decreased linearly with increasing pCO2. At ~1,000 μatm pCO2, retarded development was observed in ~50 % of larvae. No embryos developed to the 4-cell stage at 2,000 μatm pCO2 within 2 h of fertilization. A similar trend continued until 24–26 h after fertilization; the proportion of larvae attaining veliger stage by 24–26 h also decreased with increasing pCO2. The shell length of T. cornutus veligers decreased gradually as seawater pCO2 increased, but markedly decreased in seawater under nearly unsaturated and unsaturated conditions (≤1.04) of the aragonite saturation state (Ω aragonite). The results indicate that increased pCO2 seawater has a progressive and acute effect on embryonic and larval T. cornutus, and imply that the extended early developmental period and/or the downsized larval shell produced by ocean acidification will have a negative impact on survival, settlement and recruitment well into the future.


Dissolve Inorganic Carbon Shell Length Ocean Acidification Larval Shell pCO2 Level 
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.



We specifically thank Ryota Suwa of the Seto Marine Biological Laboratory, Kyoto University, for the original schematic figure of the CO2 manipulation system. We thank the reviewers for critical reading and providing helpful comments. This work was supported by the AICAL project (Acidification Impact on CALcifiers, led by Yukihiro Nojiri) funded by the Environment Research and Technology Development Fund of the Ministry of the Environment, Japan (A-0804).

Supplementary material

227_2014_2405_MOESM1_ESM.eps (587 kb)
Supplementary material 1 (EPS 586 kb)
227_2014_2405_MOESM2_ESM.eps (576 kb)
Supplementary material 2 (EPS 575 kb)


  1. Ai T (1965) Spawning and early development of the topshell, Turbo cornutus Solander—II. Induction of spawning and larval development. Bull Jap Soc Sci Fish 31:105–112 (Japanese with English abstract)CrossRefGoogle Scholar
  2. Bibby R, Cleall-Harding P, Rundle S, Widdicombe S, Spicer J (2007) Ocean acidification disrupts induced defences in the intertidal gastropod Littorina littorea. Biol Lett 3:699–701CrossRefGoogle Scholar
  3. Byrne M, Soars NA, Ho MA, Wong E, McElroy D, Selvakumaraswamy P, Dworjanyn SA, Davis AR (2010) Fertilization in a suite of coastal marine invertebrates from SE Australia is robust to near-future ocean warming and acidification. Mar Biol 157:2061–2069CrossRefGoogle Scholar
  4. Byrne M, Ho M, Wong E, Soars NA, Selvakumaraswamy P, Shepard-Brennand H, Dworjanyn SA, Davis AR (2011) Unshelled abalone and corrupted urchins: development of marine calcifiers in a changing ocean. Proc R Soc B 278:2376–2383CrossRefGoogle Scholar
  5. Caldeira K, Wickett ME (2003) Anthropogenic carbon and ocean pH. Nature 425:365CrossRefGoogle Scholar
  6. Crim RN, Sunday JM, Harley CDG (2011) Elevated seawater CO2 concentrations impair larval development and reduce larval survival in endangered northern abalone (Haliotis kamtschatkana). J Exp Mar Biol Ecol 400:272–277CrossRefGoogle Scholar
  7. Dickson AG (1990) Standard potential of the reaction: AgCl(s) + 1/2 H2(g) = Ag(s) + HCl(aq), and the standard acidity constant of the ion HSO4 in synthetic seawater from 273.15 to 318.15 K. J Chem Therm 22:113–127CrossRefGoogle Scholar
  8. Doo SS, Dworjanyn SA, Foo SA, Soars NA, Byrne M (2012) Impacts of ocean acidification on development of the meroplanktonic larval stage of the sea urchin Centrostephanus rodgersii. ICES J Mar Sci 69:460–464CrossRefGoogle Scholar
  9. Ellis RP, Bersey J, Rundle SD, Hall-Spencer JM, Spicer JI (2009) Subtle but significant effects of CO2 acidified seawater on embryos of the intertidal snail, Littorina obtusata. Aquat Biol 5:41–48CrossRefGoogle Scholar
  10. Ericson JA, Ho MA, Miskelly A, King CK, Virtue P, Tilbrook B, Byrne M (2012) Combined effects of two ocean change stressors, warming and acidification, on fertilization and early development of the Antarctic echinoid Sterechinus neumayeri. Polar Biol 35:1027–1034CrossRefGoogle Scholar
  11. Fabry VJ, Seibel BA, Feely RA, Orr JC (2008) Impacts of ocean acidification on marine fauna and ecosystem processes. ICES J Mar Sci 65:414–432CrossRefGoogle Scholar
  12. Feely RA, Sabine CL, Lee K, Berelson W, Kleypas J, Fabry VJ, Millero FJ (2004) Impact of anthropogenic CO2 on the CaCO3 system in the oceans. Science 305:362–366CrossRefGoogle Scholar
  13. Findlay HS, Kendall MA, Spicer JI, Widdicombe S (2010) Post-larval development of two intertidal barnacles at elevated CO2 and temperature. Mar Biol 157:725–735CrossRefGoogle Scholar
  14. Fujita K, Hikami M, Suzuki A, Kuroyanagi A, Sakai K, Kawahata H, Nojiri Y (2011) Effects of ocean acidification on calcification of symbiont-bearing reef foraminifers. Biogeosciences 8:2089–2098CrossRefGoogle Scholar
  15. Gattuso JP, Buddemeier RW (2000) Ocean biogeochemistry—calcification and CO2. Nature 407:311–313CrossRefGoogle Scholar
  16. Gazeau F, Quiblier C, Jansen JM, Gattuso JP, Middelburg JJ, Heip CHR (2007) Impact of elevated CO2 on shellfish calcification. Geophys Res Lett 34:L07603CrossRefGoogle Scholar
  17. Gosselin LA, Qian PY (1997) Juvenile mortality in benthic marine invertebrates. Mar Ecol Prog Ser 146:265–282CrossRefGoogle Scholar
  18. Green MA, Jones ME, Boudreau CL, Moore RL, Westman BA (2004) Dissolution mortality of juvenile bivalves in coastal marine deposits. Limnol Oceanogr 49:727–734CrossRefGoogle Scholar
  19. Hikami M, Ushie H, Irie T, Fujita K, Kuroyanagi A, Sakai K, Nojiri Y, Suzuki A, Kawahata H (2011) Contrasting calcification responses to ocean acidification between two reef foraminifers harboring different algal symbionts. Geophys Res Lett 38:L19601CrossRefGoogle Scholar
  20. Hunt HL, Scheibling RE (1997) Role of early post-settlement mortality in recruitment of benthic marine invertebrates. Mar Ecol Prog Ser 155:269–301CrossRefGoogle Scholar
  21. Iwata K (1978) A study on calcification of the protoconch of Haliotis discus hannai Ino (Archaeogastropoda). Earth Sci 32:51–57 (Japanese with English abstract)Google Scholar
  22. Kimura R, Takami H, Ono T, Onitsuka T, Nojiri Y (2011) Effects of elevated pCO2 on the early development of the commercially important gastropod, Ezo abalone Haliotis discus hannai. Fish Oceanogr 20:357–366CrossRefGoogle Scholar
  23. Kurihara H (2008) Effects of CO2-driven ocean acidification on the early developmental stages of invertebrates. Mar Ecol Prog Ser 373:275–284CrossRefGoogle Scholar
  24. Kurihara H, Shirayama Y (2004) Effects of increased atmospheric CO2 on sea urchin early development. Mar Ecol Prog Ser 274:161–169CrossRefGoogle Scholar
  25. Kurihara H, Kato S, Ishimatsu A (2007) Effects of increased seawater pCO2 on early development of the oyster Crassostrea gigas. Aquat Biol 1:91–98CrossRefGoogle Scholar
  26. Kurihara H, Asai T, Kato S, Ishimatsu A (2009) Effects of elevated pCO2 on early development in the mussel Mytilus galloprovincialis. Aquat Biol 4:225–233CrossRefGoogle Scholar
  27. Landes A, Zimmer M (2012) Acidification and warming affect both a calcifying predator and prey, but not their interaction. Mar Ecol Prog Ser 450:1–10CrossRefGoogle Scholar
  28. Martin S, Richier S, Pedrotti ML, Dupont S, Castejon C, Gerakis Y, Kerros ME, Oberhansli F, Teyssie JL, Jeffree R, Gattuso JP (2011) Early development and molecular plasticity in the Mediterranean Sea urchin Paracentrotus lividus exposed to CO2-driven acidification. J Exp Biol 214:1357–1368CrossRefGoogle Scholar
  29. Mehrbach C, Culberson CH, Hawley JE, Pytkowicz RM (1973) Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnol Oceanogr 18:897–907CrossRefGoogle Scholar
  30. Michaelidis B, Ouzounis C, Paleras A, Portner HO (2005) Effects of long-term moderate hypercapnia on acid-base balance and growth rate in marine mussels Mytilus galloprovincialis. Mar Ecol Prog Ser 293:109–118CrossRefGoogle Scholar
  31. Miller AW, Reynolds AC, Sobrino C, Riedel GF (2009) Shellfish face uncertain future in high CO2 world: Influence of acidification on oyster larvae calcification and growth in estuaries. PLoS One 4:e5661 Google Scholar
  32. Ono T, Yasuda I, Narita H, Tsunogai S (1998) Chemical alternation of waters in the Kuroshio/Oyashio interfrontal zone. J Oceanogr 54:681–694CrossRefGoogle Scholar
  33. Parker LM, Ross PM, O’Connor WA (2009) The effect of ocean acidification and temperature on the fertilization and embryonic development of the Sydney rock oyster Saccostrea glomerata (Gould 1850). Glob Change Biol 15:2123–2136CrossRefGoogle Scholar
  34. Pierrot D, Lewis E, Wallace DWR (2006) MS Excel program developed for CO2 system calculations. ORNL/CDIAC-105a. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, U.S. Department of Energy, Oak Ridge, TennesseeGoogle Scholar
  35. Pörtner HO (2008) Ecosystem effects of ocean acidification in times of ocean warming: a physiologist’s view. Mar Ecol Prog Ser 373:203–217CrossRefGoogle Scholar
  36. Pörtner HO (2012) Integrating climate-related stressor effects on marine organisms: unifying principles linking molecule to ecosystem-level changes. Mar Ecol Prog Ser 470:273–290CrossRefGoogle Scholar
  37. Riebesell U, Zondervan I, Rost B, Tortell PD, Zeebe RE, Morel FMM (2000) Reduced calcification of marine plankton in response to increased atmospheric CO2. Nature 407:364–367CrossRefGoogle Scholar
  38. Sabine CL, Feely RA, Gruber N, Key RM, Lee K, Bullister JL, Wanninkhof R, Wong CS, Wallace DWR, Tilbrook B, Millero FJ, Peng TH, Kozyr A, Ono T, Rios AF (2004) The oceanic sink for anthropogenic CO2. Science 305:367–371CrossRefGoogle Scholar
  39. Seki T (1997) Biological studies on the seed production of the northern Japanese abalone, Haliotis discus hannai Ino. Bull Tohoku Natl Res Inst 59:1–71 (Japanese with English abstract)Google Scholar
  40. Sheppard Brennand H, Soars N, Dworjanyn SA, Davis AR, Byrne M (2010) Impact of ocean warming and ocean acidification on larval development and calcification in the sea urchin Tripneustes gratilla. PLoS One 5:e11372Google Scholar
  41. Shirayama Y, Thornton H (2005) Effect of increased atmospheric CO2 on shallow water marine benthos. J Geophys Res 110:C09S08Google Scholar
  42. Stumpp M, Wren J, Melzner F, Thorndyke MC, Dupont ST (2011) CO2 induced seawater acidification impacts sea urchin larval development I: elevated metabolic rates decrease scope for growth and induce developmental delay. Comp Biochem Physiol A 160:331–340CrossRefGoogle Scholar
  43. Suwa R, Nojiri Y, Ono T, Shirayama Y (2013) Effects of low pCO2 conditions on sea urchin larval size. Mar Ecol. doi: 10.1111/maec.12044 Google Scholar
  44. Talmage SC, Gobler CJ (2009) The effects of elevated carbon dioxide concentrations on the metamorphosis, size, and survival of larval hard clams (Mercenaria mercenaria), bay scallops (Argopecten irradians), and Eastern oysters (Crassostrea virginica). Limnol Oceanogr 54:2072–2080CrossRefGoogle Scholar
  45. Talmage SC, Gobler CJ (2011) Effects of elevated temperature and carbon dioxide on the growth and survival of larvae and juveniles of three species of northwest Atlantic bivalves. PLoS One 6:e26941Google Scholar
  46. Thiyagarajan V, Ko GWK (2012) Larval growth response of the Portuguese oyster (Crassostrea angulata) to multiple climate change stressors. Aquaculture 370:90–95CrossRefGoogle Scholar
  47. Van Colen C, Debusschere E, Braeckman U, Van Gansbeke D, Vincx M (2012) The early life history of the clam Macoma balthica in a high CO2 world. PLoS One 7:e44655Google Scholar
  48. Watson SA, Peck LS, Tyler PA, Southgate PC, Tan KS, Day RW, Morley SA (2012) Marine invertebrate skeleton size varies with latitude, temperature and carbonate saturation: implications for global change and ocean acidification. Glob Change Biol 18:3026–3038CrossRefGoogle Scholar
  49. Weiss IM, Tuross N, Addadi L, Weiner S (2002) Mollusc larval shell formation: amorphous calcium carbonate is a precursor phase for aragonite. J Exp Zool 293:478–491CrossRefGoogle Scholar
  50. Wittmann AC, Pörtner HO (2013) Sensitivities of extant animal taxa to ocean acidification. Nature Clim Change 3:995–1001CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Toshihiro Onitsuka
    • 1
    • 5
    Email author
  • Ryo Kimura
    • 1
    • 6
  • Tsuneo Ono
    • 2
  • Hideki Takami
    • 3
  • Yukihiro Nojiri
    • 4
  1. 1.National Research Institute of Aquaculture (Yokosuka Station)Fisheries Research AgencyYokosukaJapan
  2. 2.National Research Institute of Fisheries ScienceFisheries Research AgencyYokohamaJapan
  3. 3.Tohoku National Fisheries Research InstituteFisheries Research AgencyShiogamaJapan
  4. 4.Center for Global Environment ResearchNational Institute for Environmental StudiesTsukubaJapan
  5. 5.Hokkaido National Fisheries Research InstituteFisheries Research AgencyKushiroJapan
  6. 6.Fisheries Research AgencyYokohamaJapan

Personalised recommendations