Marine Biology

, Volume 158, Issue 9, pp 2043–2053 | Cite as

Impacts of temperature and acidification on larval calcium incorporation of the spider crab Hyas araneus from different latitudes (54° vs. 79°N)

  • Kathleen WaltherEmail author
  • Franz J. Sartoris
  • Hans O. Pörtner
Original Paper


The combined effects of ocean warming and acidification were compared in larvae from two populations of the cold-eurythermal spider crab Hyas araneus, from one of its southernmost populations (around Helgoland, southern North Sea, 54°N, habitat temperature 3–18°C; collection: January 2008, hatch: January–February 2008) and from one of its northernmost populations (Svalbard, North Atlantic, 79°N, habitat temperature 0–6°C; collection: July 2008, hatch: February–April 2009). Larvae were exposed to temperatures of 3, 9 and 15°C combined with present-day normocapnic (380 ppm CO2) and projected future CO2 concentrations (710 and 3,000 ppm CO2). Calcium content of whole larvae was measured in freshly hatched Zoea I and after 3, 7 and 14 days during the Megalopa stage. Significant differences between Helgoland and Svalbard Megalopae were observed at all investigated temperatures and CO2 conditions. Under 380 ppm CO2, the calcium content increased with rising temperature and age of the larvae. At 3 and 9°C, Helgoland Megalopae accumulated more calcium than Svalbard Megalopae. Elevated CO2 levels, especially 3,000 ppm, caused a reduction in larval calcium contents at 3 and 9°C in both populations. This effect set in early, at 710 ppm CO2 only in Svalbard Megalopae at 9°C. Furthermore, at 3 and 9°C Megalopae from Helgoland replenished their calcium content to normocapnic levels and more rapidly than Svalbard Megalopae. However, Svalbard Megalopae displayed higher calcium contents under 3,000 ppm CO2 at 15°C. The findings of a lower capacity for calcium incorporation in crab larvae living at the cold end of their distribution range suggests that they might be more sensitive to ocean acidification than those in temperate regions.


Calcium Content Ocean Acidification Ovigerous Female Spider Crab Zoeal Stage 
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 work is a contribution to the “European Project on Ocean Adification” (EPOCA) which received funding from the European Community’s Seventh Framework programme (FP7/2007–2013) under grant agreement n° 211384. EPOCA is endorsed by the International Programme LOICZ. Supported by the Mar Co Pol I research programme of the Alfred-Wegener-Institute and the BIOACID programme of the Federal Ministry of Research, Germany. We would like to thank Karin Boos, Pauline Dierichsweiler, Katharina Michael, Stefanie Schnell, Karoline Schreiber and Lena Weber for excellent technical assistance.

Supplementary material

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Supplementary material 1 (DOC 23.5 kb)
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Supplementary material 2 (DOC 21 kb)
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Supplementary material 3 (DOC 23 kb)


  1. Anger K (1983) Temperature and the larval development of Hyas araneus L. (Decapoda: Majidae); extrapolation of laboratory data to field conditions. J Exp Mar Biol Ecol 69:203–215CrossRefGoogle Scholar
  2. Anger K (2001) The biology of decapod crustacean larvae. Crustacean Issue 14. A.A. Balkema Publishers, Swets and Zeitlinger, Lisse, pp 1–420Google Scholar
  3. Anger K, Nair KKC (1979) Laboratory experiments on the larval development of Hyas araneus (Decapoda, Majidae). Helgol Meeresunters 32:36–54CrossRefGoogle Scholar
  4. Arnold KE, Findlay HS, Spicer JI, Daniels CL, Boothroyd D (2009) Effect of CO2-related acidification on aspects of the larval development of the European lobster, Homarus gammarus (L.). Biogeosciences 6:1747–1754CrossRefGoogle Scholar
  5. Boßelmann F, Romano P, Fabritius H, Raabe D, Epple M (2007) The composition of the exoskeleton of two crustacea: the American lobster Homarus americanus and the edible crab Cancer pagurus. Thermochimica Acta 463:65–68CrossRefGoogle Scholar
  6. Brewer PG, Bradshow AL, Williams RT (1986) Measurement of total carbon dioxide and alkalinity in the North Atlantic Ocean in 1981. In: Trabalka JR, Reichle DE (eds) The changing carbon cycle—a global analysis. Springer, New York, pp 358–381Google Scholar
  7. Caldeira K, Wickett ME (2005) Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean. J Geophys Res 110:C09S04CrossRefGoogle Scholar
  8. Cameron JN (1985a) Compensation of hypercapnic acidosis in the aquatic blue crab, Callinectes sapidus: the predominance of external sea water over carapace carbonate as the proton sink. J Exp Biol 114:197–206Google Scholar
  9. Cameron JN (1985b) Post-moult calcification in the blue crab (Callinectes sapidus): relationships between apparent net H+ excretion, calcium and bicarbonate. J Exp Biol 119:275–285Google Scholar
  10. Cameron JN, Wood CM (1985) Apparent H+ excretion and CO2 dynamics accompanying carapace mineralization in the blue crab (Callinectes sapidus) following moulting. J Exp Biol 114:181–196Google Scholar
  11. Christiansen ME (ed) (1969) Crustacea Decapoda Brachyura. In: Marine Invertebrates of Scandinavia. No. 2. Universitetsforlaget, Oslo, pp 115–118Google Scholar
  12. Christiansen ME (1971) Larval development of Hyas araneus (Linnaeus) with and without antibiotics (Decapoda, Brachyura, Majidae). Crustaceana 21:307–315CrossRefGoogle Scholar
  13. Clavier J, Castets M-D, Bastian T, Hily C, Boucher G, Chauvaud L (2009) An amphibious mode of life in the intertidal zone: aerial and underwater contribution of Chthamalus montagui to CO2 fluxes. Mar Ecol Prog Ser 375:185–194CrossRefGoogle Scholar
  14. Coleman RA, Underwood AJ, Benedetti-Cecchi L, Åberg P, Arenas F, Arrontes J, Castro J, Hartnoll RG, Jenkins SR, Paula J, Della Santina P, Hawkins SJ (2006) A continental scale evaluation of the role of limpet grazing on rocky shores. Oecologia 147:556–564CrossRefGoogle Scholar
  15. Dickson AG, Millero FJ (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep Sea Res 34:1733–1743CrossRefGoogle Scholar
  16. Dupont S, Havenhand J, Thorndyke W, Peck L, Thorndyke M (2008) Near-future level of CO2-driven ocean acidification radically affects larval survival and development in the brittlestar Ophiothrix fragilis. Mar Ecol Prog Ser 373:285–294CrossRefGoogle Scholar
  17. Dupont S, Lundve B, Thorndyke M (2010) Near future ocean acidification increases growth rate of the lecithotrophic larvae and juveniles of the sea star Crossaster papposus. J Exp Zool (Mol Dev Evol) 314B:382–389CrossRefGoogle Scholar
  18. 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
  19. Feely RA, Doney SC, Cooley SR (2009) Ocean acidification—present conditions and future changes in a high-CO2 world. Oceanography 22:36–47CrossRefGoogle Scholar
  20. Findlay HS, Kendall MA, Spicer JI, Widdicombe S (2009) Future high CO2 in the intertidal may comprise adult barnacle Semibalanus balanoides survival and embryonic development rate. Mar Ecol Prog Ser 389:193–202CrossRefGoogle Scholar
  21. Findlay HS, Kendall MA, Spicer JI, Widdicombe S (2010a) Relative influences of ocean acidification and temperature on intertidal barnacle post-larvae at the northern edge of their geographic distribution. Estuar Coast Shelf Sci 86:675–682CrossRefGoogle Scholar
  22. Findlay HS, Kendall MA, Spicer JI, Widdicombe S (2010b) Post-larval development of two intertidal barnacles at elevated CO2 and temperature. Mar Biol 157:725–735CrossRefGoogle Scholar
  23. Flik G, Verbost PM, Atsam W (1994) Calcium transport in gill plasma membranes of the crab Carcinus maenas: evidence for carriers driven by ATP and a Na+ gradient. J Exp Biol 195:109–122PubMedGoogle Scholar
  24. Gattuso J-P, Frankignoulle M, Bourge I, Romaine S, Buddemeier RW (1998) Effect of calcium carbonate saturation of seawater on coral calcification. Glob Planet Change 18:37–46CrossRefGoogle Scholar
  25. Giraud M-M (1981) Carbonic anhydrase activity in the integument of the crab Carcinus maenas during the intermolt cycle. Comp Biochem Physiol 69:381–387CrossRefGoogle Scholar
  26. Gooding RA, Harley CDG, Tang E (2009) Elevated water temperature and carbon dioxide concentration increase the growth of a keystone echinoderm. PNAS 106:9316–9321CrossRefGoogle Scholar
  27. Henry RP, Cameron JN (1983) The role of carbonic anhydrase in respiration, ion regulation and acid-base balance in the aquatic crab Callinectes sapidus and the terrestrial crab Gecarcinus lateralis. J Exp Biol 103:205–223Google Scholar
  28. Henry RP, Kormanik GA, Smatresk NJ, Cameron JN (1981) The role of CaCO3 dissolution as a source of HCO3 for the buffering of hypercapnic acidosis in aquatic and terrestrial decapod crustaceans. J Exp Biol 94:269–274Google Scholar
  29. Höcker B (1988) Licht- und elektronenmikroskopische Untersuchungen zur Larval- und Juvenilentwicklung der Seespinne (Hyas araneus) unter besonderer Berücksichtigung des Y-Organs. M. Sc. Thesis, Universität Hamburg, Germany, pp 1–111Google Scholar
  30. Hop H, Pearson T, Hegseth EN, Kovacs KM, Wiencke C, Kwasniewski S, Eiane K, Mehlum F, Gulliksen B, Wlodarska-Kowalczuk M, Lydersen C, Weslawski JM, Cochrane S, Gabrielsen GW, Leakey RJG, Lønne OJ, Zajaczkowski M, Falk-Petersen S, Kendall M, Wängberg S-Å, Bischof K, Voronkov AY, Kovaltchouk NA, Wiktor J, Poltermann M, di Prisco G, Papucci C, Gerland S (2002) The marine ecosystem of Kongsfjorden, Svalbard. Polar Res 21:167–208CrossRefGoogle Scholar
  31. IPCC (Intergovernmental Panel on Climate Change) (2001) Climate change 2001: third assessment report of the intergovernmental panel on climate change. Cambridge University Press, CambridgeGoogle Scholar
  32. IPCC (Intergovernmental Panel on Climate Change) (2007) Climate change 2007: fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  33. Kleypas JA, Feely RA, Fabry VJ, Langdon C, Sabine CL, Robbins LL (2006) Impacts of ocean acidification on coral reefs and other marine calcifiers: a guide for future research. Report of a workshop held 18–20 April 2005. St. Petersburg, FL, sponsored by NSF, NOAA, and the US Geological Survey, p 88Google Scholar
  34. Kurihara H (2008) Effects of CO2-driven ocean acidification on the early developmental stages of invertebrates. Mar Ecol Prog Ser 373:275–284CrossRefGoogle Scholar
  35. Kurihara H, Shimode S, Shirayama Y (2004) Effects of raised CO2 concentration on the egg production rate and early development of two marine copepods (Acartia steueri and Acartia erythraea). Mar Poll Bull 49:721–727CrossRefGoogle Scholar
  36. Lahti E (1988) Calcification of the exoskeleton and gastrolithes in Astacus astacus L. in calcium-poor water. Comp Biochem Physiol 91:171–173CrossRefGoogle Scholar
  37. Lewis E, Wallace DWR (1998) Program developed for CO2 system calculations. ORNL/CDIAC-105. Carbon Dioxide Information Analysis Center. Oak Ridge National Laboratory, U.S. Department of Energy, Oak RidgeCrossRefGoogle Scholar
  38. Mayer DJ, Matthews C, Cook K, Zuur AF, Hay S (2007) CO2-induced acidification affects hatching success in Calanus finmarchicus. Mar Ecol Prog Ser 350:91–97CrossRefGoogle Scholar
  39. McDonald MR, McClintock JB, Amsler CD, Rittschof D, Angus RA, Orihuela B, Lutostanski K (2009) Effects of ocean acidification over the life history of the barnacle Amphibalanus amphitrite. Mar Ecol Prog Ser 385:179–187CrossRefGoogle Scholar
  40. Mehrbach C, Culberson C, Hawley J, Pytkovicz R (1973) Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnol Oceanogr 18:897–907CrossRefGoogle Scholar
  41. Mezquita F, Roca J, Wansard G (1999) Moulting, survival and calcification: the effects of temperature and water chemistry on an ostracod crustacean (Herpetocypris intermedia) under experimental conditions. Arch Hydrobiol 146:219–238CrossRefGoogle Scholar
  42. Neufeld DS, Cameron JN (1993) Transepithelial movement of calcium in crustaceans. J Exp Biol 184:1–16PubMedGoogle Scholar
  43. Orr JC, Maier-Reimer E, Mikolajewicz U, Monfray P, Samiento JL, Toggweiler JR, Taylor NK, Palmer J, Gruber N, Sabine CL, Le Quéré C, Key RM, Boutin J (2001) Estimates of anthropogenic carbon uptake from four three-dimensional global ocean models. Global Biogeochem Cy 15:43–60CrossRefGoogle Scholar
  44. Pörtner HO (2006) Climate-dependent evolution of Antarctic ectotherms: an integrative analysis. Deep Sea Res 54:1071–1104CrossRefGoogle Scholar
  45. 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
  46. Pörtner HO, Langenbuch M, Michaelidis B (2005) Synergistic effects of temperature extremes, hypoxia, and increases in CO2 on marine animals: from Earth history to global change. J Geophys Res 110:C09S10. doi: 10.1029/2004JC002561 CrossRefGoogle Scholar
  47. Pörtner HO, Dupont S, Melzner F, Storch D, Thorndyke M (2010) Chapter 10: studies of metabolic rate and other characters across life stages. In: Riebesell U, Fabry VJ, Hansson L, Gattuso J-P (eds) Guide to best practices for ocean acidification research and data reporting. Publications Office of the European Union, Luxemburg, p 260Google Scholar
  48. Pratoomchat B, Sawangwong P, Guedes R, De Lurdes Reis M, Machado J (2002) Cuticle ultrastructure changes in the crab Scylla serrata over the molt cycle. J Exp Zool 293:414–426CrossRefGoogle Scholar
  49. Pratoomchat B, Sawangwong P, Machado J (2003) Effects of controlled pH on organic and inorganic composition in haemolymph, epidermal tissue and cuticle of mud crab Scylla serrata. J Exp Zool 295:47–56Google Scholar
  50. Price SWC, Dendigner JE (1983) Calcium deposition into the cuticle of the blue crab, Callinectes sapidus, related to external salinity. Comp Biochem Physiol A 74:903–907CrossRefGoogle Scholar
  51. Pütz K, Buchholz F (1991) Comparative ultrastructure of the cuticle of some pelagic, nektobenthic and benthic malacostracan crustaceans. Mar Biol 110:49–58CrossRefGoogle Scholar
  52. Ries JB, Cohen AL, McCorkle DC (2009) Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 37:1131–1134CrossRefGoogle Scholar
  53. Roer R, Dillaman R (1984) The structure and calcification of the crustacean cuticle. Amer Zool 24:893–909CrossRefGoogle Scholar
  54. Starr M, Therriault J-C, Conan GY, Comeau M, Robichaud G (1994) Larval release in a sub-euphotic zone invertebrate triggered by sinking phytoplankton particles. J Plankton Res 16:1137–1147CrossRefGoogle Scholar
  55. Svendsen H, Breszczynska-Møller A, Hagen JO, Lefauconnier B, Tverberg V, Gerland S, Ørbæk JB, Bischof K, Papucci C, Zajaczkowski M, Azzolini R, Bruland O, Wiencke C, Winther J-G, Dallmann W (2002) The physical environment of Kongsfjorden-Krossfjorden, an Arctic fjord system in Svalbard. Polar Res 21:133–166Google Scholar
  56. Travis DF (1955) The molting cycle of the spiny lobster, Panulirus agrus Latreille. II. Pre-ecdysial histological and histochemical changes in the hepatopancreas and integumental tissues. Biol Bull 108:88–112CrossRefGoogle Scholar
  57. Underwood AJ (1997) Experiments in ecology. Their logical design and interpretation using analysis of variance. Cambridge University Press, CambridgeGoogle Scholar
  58. Waldbusser GG, Bergschneider H, Green MA (2010) Size-dependent pH effect on calcification in post-larval hard clam Mercenaria spp. Mar Ecol Prog Ser 417:171–182CrossRefGoogle Scholar
  59. Walther K, Anger K, Pörtner HO (2010) Effects of ocean acidification and warming on the larval development of the spider crab Hyas araneus from different latitudes (54° vs. 79°N). Mar Ecol Prog Ser 417:159–170CrossRefGoogle Scholar
  60. Wheatly MG (1999) Calcium homeostasis in crustacea: the evolving role of branchial, renal, digestive and hypodermal epithlia. J Exp Zool 283:620–640CrossRefGoogle Scholar
  61. Wiltshire KH, Manly BFJ (2004) The warming trend at Helgoland Roads, North Sea: phytoplankton response. Helgol Mar Res 58:269–273CrossRefGoogle Scholar
  62. Wood HL, Spicer JI, Widdicombe S (2008) Ocean acidification may increase calcification rates, but at a cost. Proc R Soc B 275:1767–1773CrossRefGoogle Scholar
  63. Wootton JT, Pfister CA, Forester JD (2008) Dynamic patterns and ecological impacts of declining ocean pH in a high-resolution multi-year dataset. PNAS 105:18848–18853CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Kathleen Walther
    • 1
    Email author
  • Franz J. Sartoris
    • 1
  • Hans O. Pörtner
    • 1
  1. 1.Alfred-Wegener-Institute for Polar and Marine ResearchBremerhavenGermany

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