Skip to main content
SpringerLink
Log in

Effects of ocean acidification driven by elevated CO2 on larval shell growth and abnormal rates of the venerid clam, Mactra veneriformis

  • Biology
  • Published:
Chinese Journal of Oceanology and Limnology Aims and scope Submit manuscript

Abstract

The venerid clam (Mactra veneriformis Reeve 1854) is one of the main cultured bivalve species in intertidal and shallow subtidal ecosystems along the west coast of Korea. To understand the effects of ocean acidification on the early life stages of Korean clams, we investigated shell growth and abnormality rates and types in the D-shaped, umbonate veliger, and pediveliger stages of the venerid clam M. veneriformis during exposure to elevated seawater pCO2. In particular, we examined abnormal types of larval shell morphology categorized as shell deformations, shell distortions, and shell fissures. Specimens were incubated in seawater equilibrated with bubbled CO2-enriched air at (400±25)×10-6 (ambient control), (800±25)×10-6 (high pCO2), or (1 200±28)×10-6 (extremely high pCO2), the atmospheric CO2 concentrations predicted for the years 2014, 2084, and 2154 (70-year intervals; two human generations), respectively, in the Representative Concentration Pathway (RCP) 8.5 scenario. The mean shell lengths of larvae were significantly decreased in the high and extremely high pCO2 groups compared with the ambient control groups. Furthermore, under high and extremely high pCO2 conditions, the cultures exhibited significantly increased abundances of abnormal larvae and increased severity of abnormalities compared with the ambient control. In the umbonate veliger stage of the experimental larvae, the most common abnormalities were shell deformations, distortions, and fissures; on the other hand, convex hinges and mantle protuberances were absent. These results suggest that elevated CO2 exerts an additional burden on the health of M. veneriformis larvae by impairing early development.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Barros P, Sobral P, Range P, Chícharo L, Matias D. 2013. Effects of sea-water acidification on fertilization and larval development of the oyster C rassostrea gigas. Journal of Exp erimental Marine Bio logy and Ecology, 440: 200–206.

    Article  Google Scholar 

  • Blackford J C, Gilbert F J. 2007. pH variability and CO2 induced acidification in the North Sea. Journal of Marine Syst ems, 64 (1-4): 229–241.

    Article  Google Scholar 

  • Carriker M R. 1986. Influence of suspended particles on biology of oyster larvae in estuaries. Am erican Malacological Bull etin, 3: 41–49.

    Google Scholar 

  • Carriker M R. 1996. The shell and ligament. In: Kennedy V S, Newell R I E, Eble A eds. The Eastern Oyster Crassostrea Virginica. Maryland Sea Grant, College Park, Maryland. p.75–168.

    Google Scholar 

  • Cooley S R, Lucey N, Kite-Powell H, Doney S C. 2012. Nutrition and income from molluscs today imply vulnerability to ocean acidification tomorrow. Fish and Fish eries, 13(2): 182–215.

    Article  Google Scholar 

  • Fabry V J, Seibel B A, Feely R A, Orr J C. 2008. Impacts of ocean acidification on marine fauna and ecosystem processes. ICES Journal of Marine Sci ence, 65(3): 414–432.

    Article  Google Scholar 

  • Findlay H S, Kendall M A, Spicer J I, Widdicombe S. 2009. Future high CO2 in the intertidal may compromise adult barnacle Semibalanus balanoides survival and embryonic development rate. Marine Ecology Prog ress Series, 389: 193–202.

    Article  Google Scholar 

  • Gazeau F, Parker L M, Comeau S, Gattuso J P, O’Connor W A, Martin S, Pörtner H O, Ross P M. 2013. Impacts of ocean acidification on marine shelled molluscs. Marine Biology, 160(8): 2207–2245.

    Article  Google Scholar 

  • Gazeau F, Quiblier C, Jansen J M, Gattuso J P, Middelburg J J, Heip C H R. 2007. Impact of elevated CO2 on shellfish calcification. Geophys ical Res earch Lett ers, 34 (7): L07603.

    Google Scholar 

  • Ginger K W K, Vera C B S, Dineshram R, Dennis C K S, Adela L J, Yu Z N, Thiyagarajan V. 2013. Larval and post-larval stages of pacific oyster (Crassostrea gigas) are resistant to elevated CO2. PLoS O ne, 8(5): e64147.

    Article  Google Scholar 

  • Gosselin L A, Qian P Y. 1997. Juvenile mortality in benthic marine invertebrates. Marine Ecology Prog ress Series, 146: 265–282.

    Article  Google Scholar 

  • Gutiérrez J L, Jones C G, Strayer D L, Iribarne O O. 2003. Mollusks as ecosystem engineers: the role of shell production in aquatic habitats. Oikos, 101(1): 79–90.

    Article  Google Scholar 

  • Hayakaze E, Tanabe K. 1999. Early larval shell development in mytilid bivalve M ytilus galloprovincialis. Venus, 58: 119–127.

    Google Scholar 

  • Hendriks I E, Duarte C M, Álvarez M. 2010. Vulnerability of marine biodiversity to ocean acidification: a metaanalysis. Estuar ine Coast al Shelf Sci ence, 86(2): 157–164.

    Article  Google Scholar 

  • His E, Seaman M N L, Beiras R. 1997. A simplification the bivalve embryogenesis and larval development bioassay method for water quality assessment. Water Res earch, 31(2): 351–355.

    Article  Google Scholar 

  • Hoegh-Guldberg O, Mumby P J, Hooten A J et al. 2007. Coral reefs under rapid climate change and ocean acidification. S cience, 318(5857): 1737–1742.

    Google Scholar 

  • Hur Y B, Bae J H, Hur S B. 2005. Comparison of development and larval growth of four venerid clams. Journal of the World Aquac ulture Society, 36(2): 179–187.

    Article  Google Scholar 

  • Kleypas J A, Buddemeier R W, Archer D, Gattuso J P, Langdon C, Opdyke B N. 1999). Geochemical consequences of increased atmospheric carbon dioxide on coral reefs. Science, 284(5411): 118–120.

    Article  Google Scholar 

  • Kleypas J A, Yates K K. 2009. Coral reefs and ocean acidification. Oceanography, 22(4): 108–117.

    Article  Google Scholar 

  • Kurihara H, Asai T, Kato S, Ishimatsu A. 2008. Effects of elevated pCO2 on early development in the mussel M ytilus galloprovincialis. Aquat ic Biology, 4(3): 225–233.

    Article  Google Scholar 

  • Kurihara H, Kato S, Ishimatsu A. 2007. Effects of increased seawater pCO2 on early development of the oyster C rassostrea gigas. Aquat ic Biology, 1(1): 91–98.

    Article  Google Scholar 

  • Kurihara H. 2008. Effects of CO2-driven ocean acidification on the early developmental stages of invertebrates. Marine Ecology Progress Series, 373: 275–284.

    Article  Google Scholar 

  • Marin F, Luquet G. 2004. Molluscan shell proteins. C omptes R endus Palevol, 3(6): 469–492.

    Article  Google Scholar 

  • Orr J C, Fabry V J, Aumont O et al. 2005. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature, 437(7059): 681–686.

    Article  Google Scholar 

  • Parker L M, Ross P M, O’Connor W A. 2010. Comparing the effect of elevated pCO2 and temperature on the fertilization and early development of two species of oysters. Marine Biology, 157(11): 2435–2452.

    Article  Google Scholar 

  • Parker L M, Ross P M, O’Connor W A. 2011. Populations of the Sydney rock oyster, S accostrea glomerata, vary in response to ocean acidification. Marine Biology, 158(3): 689–697.

    Article  Google Scholar 

  • Parker L M, Ross P M, O’Connor W A, Borysko L, Raftos D A, Pörtner H O. 2012. Adult exposure influences offspring response to ocean acidification in oysters. Global Chang e Biology, 18(1): 82–92.

    Article  Google Scholar 

  • Parker L M, Ross P M, O’Connor W A. 2009. The effect of ocean acidification and temperature on the fertilization and embryonic development of the Sydney rock oyster Saccostrea glomerata (Gould 1850). Global Chang e Biology, 15(9): 2123–2136.

    Article  Google Scholar 

  • Range P, Piló D, Ben-Hamadou R, Chicharo M A, Matias D, Joaquim S, Oliveira A P, Chícharo L. 2012. Seawater acidification by CO2 in a coastal lagoon environment: effects on life history traits of juvenile mussels Mytilus galloprovincialis. Journal of Exp erimental Marine Biology and Ecology, 424-425: 89–98.

    Article  Google Scholar 

  • Scanes E, Parker L M, O’Connor W A, Ross P M. 2014. Mixed effects of elevated pCO2 on fertilisation, larval and juvenile development and adult responses in the mobile subtidal scallop M imachlamys asperrima (Lamarck, 1819). PLoS One, 9 (4): e93649.

    Article  Google Scholar 

  • Schulz K G, Riebesell U, Bellerby R G J, Biswas H, Meyerhöfer M, Müller M N, Egge J K, Nejstgaard J C, Neill C, Wohlers J, Zöllner E. 2008. Build-up and decline of organic matter during PeECE III. Biogeosciences, 5(3): 707–718.

    Article  Google Scholar 

  • Stocker T F, Qin D, Plattner G K, Tignor M M B, Allen S K, Boschung J, Nauels A, Xia Y, Bex V, Midgley P M. 2013. Climate Change 2013. The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of IPCC the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, New York.

    Google Scholar 

  • Talmage S C, Gobler C J. 2010. Effects of past, present, and future ocean carbon dioxide concentrations on the growth and survival of larval shellfish. Proc eedings of the Nat iona l Acad emy of Sci ences of the United States of A merica, 107(40): 17246–17251.

    Article  Google Scholar 

  • Talmage S C, Gobler C J. 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(10): e26941.

    Article  Google Scholar 

  • Talmage S C, Gobler C J. 2012. Effects of CO2 and the harmful alga Aureococcus anophagefferens on growth and survival of oyster and scallop larvae. Marine Ecology Prog ress Series, 464: 121–134.

    Article  Google Scholar 

  • Tunnicliffe V, Davies K T A, Butterfield D A, Embley R W, Rose J M, Chadwick W W. 2009. Survival of mussels in extremely acidic waters on a submarine volcano. Nat ure Geosci ence, 2(5): 344–348.

    Article  Google Scholar 

  • 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(9): e44655.

    Article  Google Scholar 

  • Waldbusser G G, Bergschneider H, Green M A. 2010. Sizedependent pH effect on calcification in post-larval hard clam M ercenaria spp. Marine Ecology Prog ress Series, 417: 171–182.

    Article  Google Scholar 

  • Walther K, Anger K, Pörtner H O. 2010. Effects of ocean acidification and warming on the larval development of the spider crab H yas araneus from different latitudes (54° vs. 79°N). Marine Ecology Prog ress Series, 417: 159–170.

    Article  Google Scholar 

  • Watson S A, Southgate P C, Tyler P A, Peck L S. 2009. Early larval development of the Sydney rock oyster S accostrea glomerata under near-future predictions of CO2 -driven ocean acidification. Journal of Shellfish Res earch, 28(3): 431–437.

    Article  Google Scholar 

  • Weiss I M, Schönitzer V. 2006. The distribution of chitin in larval shells of the bivalve mollusk M ytilus galloprovincialis. Journal of Structural Biology, 153(3): 264–277.

    Article  Google Scholar 

  • Weiss I M, Tuross N, Addadi L, Weiner S. 2002. Mollusc larval shell formation: amorphous calcium carbonate is a precursor phase for aragonite. Journal of Exp erimental Zoology, 293(5): 478–491.

    Article  Google Scholar 

  • White M M, McCorkle D C, Mullineaux L S, Cohen A L. 2013. Early exposure of bay scallops (A rgopecten irradians ) to high CO2 causes a decrease in larval shell growth. PLoS One, 8(4): e61065.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Division of Polar Ocean Environment Research, Korea Polar Research Institute, Korea Institute of Ocean Science and Technology, 26 Songdomirae-ro, Yeonsu-gu, Incheon, 21990, Republic of Korea

    Jee-Hoon Kim, Eun Jin Yang, Sung-Ho Kang & Eun Jung Choy

  2. Marine Ecosystem Research Division, Korea Institute of Ocean Science and Technology, 787 Haean-ro, Sangnok-gu, Ansan, 15627, Republic of Korea

    Ok Hwan Yu

  3. School of Biological Sciences, Seoul National University, 1 Gwanak-ro, Gwanak-gu, Seoul, 08826, Republic of Korea

    Jee-Hoon Kim & Won Kim

Authors
  1. Jee-Hoon Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ok Hwan Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Eun Jin Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sung-Ho Kang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Won Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Eun Jung Choy
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Eun Jung Choy.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kim, JH., Yu, O.H., Yang, E.J. et al. Effects of ocean acidification driven by elevated CO2 on larval shell growth and abnormal rates of the venerid clam, Mactra veneriformis . Chin. J. Ocean. Limnol. 34, 1191–1198 (2016). https://doi.org/10.1007/s00343-016-5159-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00343-016-5159-1

Keywords

Search

Navigation