Polar Biology

, Volume 35, Issue 7, pp 1027–1034 | Cite as

Combined effects of two ocean change stressors, warming and acidification, on fertilization and early development of the Antarctic echinoid Sterechinus neumayeri

  • J. A. Ericson
  • M. A. Ho
  • A. Miskelly
  • C. K. King
  • P. Virtue
  • B. Tilbrook
  • M. Byrne
Original Paper

Abstract

The effects of concurrent ocean warming and acidification on Antarctic marine benthos warrant investigation as little is known about potential synergies between these climate change stressors. We examined the interactive effects of warming and acidification on fertilization and embryonic development of the ecologically important sea urchin Sterechinus neumayeri reared from fertilization in elevated temperature (+1.5°C and 3°C) and decreased pH (−0.3 and −0.5 pH units) treatments. Fertilization using gametes from multiple males and females, to represent populations of spawners, was resilient to acidification at ambient temperature (0°C). At elevated temperatures, there was a negative interactive effect of temperature and pH on percentage of fertilization (11% reduction at 3°C). For cleavage stage embryos, there was a significant, but small reduction (6%) in the percentage of normal embryos at pH 7.5. For blastulae, a 10–11% decrease in normal development occurred in the +3°C treatments across all pH levels. Our results highlight the importance of considering the impacts of both temperature and pH in assessing the life history response of S. neumayeri in a changing polar ocean. While fertilization and development to the blastula stage were robust to levels of temperature and pH change predicted over coming decades, deleterious interactive effects were evident between these stressors at levels projected to occur by 2100 and beyond.

Keywords

Ocean acidification Ocean warming Antarctica Echinoderm Early life history 

Notes

Acknowledgments

This work was supported by a grant from the Australian Antarctic Division (AAD). Thanks to AAD staff and students who provided assistance and logistical support including Rob King, Steve Whiteside, John van den Hoff, Andrew Bryant, Clive Strauss, Charmaine Alford, Kathryn Brown, Lara Marcus, Sarah Payne, Bianca Sfiligoj, Claire Wallis, Debbie Lang, Jane Wasley, Dougie Gray, and Leigh Hornsby.

References

  1. Barnes DKA, Fuentes V, Clarke A, Schloss IR, Wallace MI (2006) Spatial and temporal variation in shallow seawater temperatures around Antarctica. Deep Sea Res II 53:853–865CrossRefGoogle Scholar
  2. Bay S, Burgess R, Nacci D (1993) Status and applications of echinoid (phylum Echinodermata) toxicity test methods. In: Landis WG, Hughes JS, Lewis MA (eds) Environmental toxicology and risk assessment. American Society for Testing and Materials, Philadelphia, pp 281–302CrossRefGoogle Scholar
  3. Benitez Villalobos F, Tyler PA, Young CM (2006) Temperature and pressure tolerances of embryos and larvae of the Atlantic seastars Asterias rubens and Marthasterias glacialis: potential for deep-sea invasion from the North Atlantic. Mar Ecol Prog Ser 314:109–117CrossRefGoogle Scholar
  4. Brewer PG (2009) A changing ocean seen with clarity. Proc Natl Acad Sci 106:12213–12214PubMedCrossRefGoogle Scholar
  5. Brey T, Pearse J, Basch L, McClintock JB, Slattery M (1995) Growth and production of Sterechinus neumayeri (Echinoidea: Echinodermata) in McMurdo Sound, Antarctica. Mar Biol 124:279–292CrossRefGoogle Scholar
  6. Byrne M (2010) Impact of climate change stressors on marine invertebrate life histories with a focus on the Mollusca and Echinodermata. In: Yu Y, Henderson-Sellers A (eds) Climate alert: climate change monitoring and strategy. Sydney, University of Sydney Press, pp 142–185Google Scholar
  7. Byrne M (2011a) Global change ecotoxicology: identification of early life history bottlenecks in marine invertebrates, variable species responses and variable experimental approaches. Mar Env Res. doi: 10.1016/j.marenvres.2011.10.004
  8. Byrne M (2011b) Impact of ocean warming and ocean acidification on marine invertebrate life history stages: vulnerabilities and potential for persistence in a changing ocean. Oceanogr Mar Biol Ann Rev 49:1–42Google Scholar
  9. Byrne M, Ho M, Selvakumaraswamy P, Nguyen HD, Dworjanyn SA, Davis AR (2009) Temperature, but not pH, compromises sea urchin fertilization and early development under near-future climate change scenarios. Proc R Soc B 276:1883–1935PubMedCrossRefGoogle Scholar
  10. 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
  11. Caldeira K, Wickett ME (2003) Anthropogenic carbon and ocean pH. Nature 425:365PubMedCrossRefGoogle Scholar
  12. Cao L, Caldeira K (2008) Atmospheric CO2 stabilization and ocean acidification. Geophys Res Lett. doi: 10.1029/2008GL035072
  13. Carr RS, Biedenbach JM, Nipper M (2006) Influence of potentially confounding factors on sea urchin porewater toxicity tests. Arch Env Cont Tox 51:573–579CrossRefGoogle Scholar
  14. Catarino, AI, Ridder, CD, Gonzalez M, Gallardo P, Dubois P (2011) Sea urchin Arbacia dufresnei (Blainville 1825) larvae response to ocean acidification. Polar Biol. doi: 10.1007/s00300-011-1074-2
  15. Christen R, Schackmann RW, Shapiro BM (1982) Elevation of the intracellular pH activates respiration and motility of sperm of the sea urchin, Strongylocentrotus purpuratus. J Biol Chem 257:4881–4890Google Scholar
  16. Clark D, Lamare M, Barker M (2009) Response of sea urchin pluteus larvae (Echinodermata: Echinoidea) to reduced seawater pH: a comparison among tropical, temperate, and a polar species. Mar Biol 156:1125–1137CrossRefGoogle Scholar
  17. Clarke A, Murphy EJ, Meredith MP, King JC, Peck LS, Barnes DKA, Smith RC (2007) Climate change and the marine ecosystem of the western Antarctic Peninsula. Phil Trans R Soc B Biol Sci 362:149–166CrossRefGoogle Scholar
  18. Comeau S, Gorsky G, Jeffree R, Teyssie JL, Gattuso JP (2009) Impact of ocean acidification on a key Arctic pelagic mollusc (Limacina helicina). Biogeosci 6:1877–1882CrossRefGoogle Scholar
  19. Cowart DA, Ulrich PN, Miller DC, Marsh AG (2009) Salinity sensitivity of early embryos of the Antarctic sea urchin, Sterechinus neumayeri. Polar Biol 32:435–441CrossRefGoogle Scholar
  20. Darszon A, Guerrero A, Galindo BE, Nishigaki T, Wood CD (2008) Sperm-activating peptides in the regulation of ion fluxes, signal transduction and motility. Int J Devel Biol 52:595–606CrossRefGoogle Scholar
  21. Dickson AG, Sabine CL, Christian JR (2007) Guide to best practices for ocean CO2 measurements, vol. 3. PICES Special Publication, p 191Google Scholar
  22. Doney SC, Fabry VJ, Feely RA, Kleypas JA (2009) Ocean acidification: the other CO2 problem. Ann Rev Mar Sci 1:169–192PubMedCrossRefGoogle Scholar
  23. Dupont S, Ortega-Martínez O, Thorndyke MC (2010) Impact of near future ocean acidification on echinoderms. Ecotoxicology 19:440–462CrossRefGoogle Scholar
  24. Ericson JA, Lamare MD, Morley SA, Barker MF (2010) The response of two ecologically important Antarctic invertebrates (Sterechinus neumayeri and Parborlasia corrugatus) to reduced seawater pH: effects on fertilisation and embryonic development. Mar Biol 157:2689–2702CrossRefGoogle Scholar
  25. Fabry VJ, McClintock JB, Mathis JT, Grebmeier JM (2009) Ocean acidification at high latitudes: the bellwether. Oceanography 22:160–171CrossRefGoogle Scholar
  26. Fujisawa H (1989) Differences in temperature dependence of early development of sea urchins with different growing seasons. Biol Bull 176:96–102CrossRefGoogle Scholar
  27. Gibson JE, Trull T (1999) Annual cycle of fCO2 under sea-ice and in open water in Prydz Bay, East Antarctica. Mar Chem 66:187–200CrossRefGoogle Scholar
  28. Hamdoun A, Epel D (2007) Embryo stability and vulnerability in an always changing world. Proc Natl Acad Sci USA 104:1745–1750PubMedCrossRefGoogle Scholar
  29. Hansen JE, Ruedy R, Glascoe J, Sato M (1999) GISS analysis of surface temperature change. J Geophys Res 104:30997–31022CrossRefGoogle Scholar
  30. Hoegh-Guldberg O, Bruno JF (2010) The impact of climate change on the world’s marine ecosystems. Science 328:1523–1528PubMedCrossRefGoogle Scholar
  31. Intergovernmental Panel on Climate Change (IPCC) (2007) Climate Change 2007: the fourth assessment report of the intergovernmental panel on climate change (IPCC). Cambridge University Press, CambridgeGoogle Scholar
  32. King CK, Riddle MJ (2001) Effects of metal contaminants on the development of the common Antarctic sea urchin Sterechinus neumayeri and comparisons of sensitivity with tropical and temperate echinoids. Mar Ecol Prog Ser 215:143–154CrossRefGoogle Scholar
  33. Krug PJ, Rifell JA, Zimmer RK (2009) Endogenous signaling pathways and chemical communication between sperm and egg. J Exp Biol 212:1092–1100PubMedCrossRefGoogle Scholar
  34. Kupriyanova EK, Havenhand JN (2005) Effects of temperature on sperm swimming behaviour, respiration and fertilization success in the serpulid polychaete, Galeolaria caesepitosa (Annelida: Serpulidae). Invert Repr Dev 48:7–17CrossRefGoogle Scholar
  35. Kurihara H, Shirayama Y (2004) Effects of increased atmospheric CO2 on sea urchin early development. Mar Ecol Prog Ser 274:161–169CrossRefGoogle Scholar
  36. Lamare MD, Barker MF (1999) In situ estimates of larval development and mortality in the New Zealand sea urchin Evechinus chloroticus (Echinodermata: Echinoidea). Mar Ecol Prog Ser 180:197–211CrossRefGoogle Scholar
  37. Lamare MD, Barker MF, Lesser MP (2007) In situ rates of DNA damage and abnormal develoment in Antarctic and non-Antarctic sea urchin embryos. Aquat Biol 1:21–32CrossRefGoogle Scholar
  38. Lister KN, Lamare MD, Burritt DJ (2010) Sea ice protects embryos of the Antarctic sea urchin Sterechinus neumayeri from oxidative damage due to naturally enhanced levels of UV-B radiation. J Exp Biol 213:1967–1975PubMedCrossRefGoogle Scholar
  39. McClintock JB (1994) Trophic biology of Antarctic shallow-water echinoderms. Mar Ecol Prog Ser 111:191–202CrossRefGoogle Scholar
  40. McNeil BI, Matear R (2008) Southern Ocean acidification: a tipping point at 450-ppm atmospheric CO2. Proc Natl Acad Sci USA 105:18860–18864PubMedCrossRefGoogle Scholar
  41. 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
  42. Meredith MP, King JC (2005) Rapid climage change in the ocean west of the Antarctic Peninsula during the second half of the 20th Century. Geophys Res Lett 32:L19604CrossRefGoogle Scholar
  43. Mita M, Hino A, Yasumasu I (1984) Effect of temperature on interaction between eggs and spermatozoa of sea urchin. Biol Bull 166:68–77CrossRefGoogle Scholar
  44. Palumbi SR (1999) All males are not created equal: fertility differences depend on gamete recognition polymorphisms in sea urchins. Proc Natl Acad Sci USA 96:12632–12637PubMedCrossRefGoogle Scholar
  45. Pearse JS, McClintock JB, Bosch I (1991) Reproduction of Antarctic Benthic marine invertebrates: tempos, modes, and timing. American Zool 31:65–80Google Scholar
  46. Peck LS (2005) Prospects for survival in the Southern Ocean: vulnerability of benthic species to temperature change. Antarctic Sci 17:497–507CrossRefGoogle Scholar
  47. Peck LS, Webb KE, Bailey DM (2004) Extreme sensitivity of biological function to temperature in Antarctic marine species. Funct Ecol 18:625–630CrossRefGoogle Scholar
  48. Pierrot D, Lewis E, Wallace DWR (2006) MS excel program developed for CO2 system calculations. ORNL/CDIAC-105a. Oak Ridge, Tennessee: carbon dioxide information analysis center, Oak Ridge National Laboratory, U.S. Department of EnergyGoogle Scholar
  49. Rumrill SS (1990) Natural mortality of marine invertebrate larvae. Ophelia 32:163–198CrossRefGoogle Scholar
  50. Rupp JH (1973) Effects of temperature on fertilization and early cleavage of some tropical echinoderms, with emphasis on Echinometra mathaei. Mar Biol 23:183–189CrossRefGoogle Scholar
  51. Sewell MA, Young CM (1999) Temperature limits to fertilization and early development in the tropical sea urchin Echinometra lucunter. J Exp Mar Biol Ecol 236:291–305CrossRefGoogle Scholar
  52. 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. PlosOne 5:e11372Google Scholar
  53. Sorte CJB, Jones SJ, Miller LP (2011) Geographic variation in temperature tolerance as an indicator of potential responses to climate change. J Exp Mar Biol Ecol 400:209–217CrossRefGoogle Scholar
  54. Stanwell-Smith D, Peck LS (1998) Temperature and embryonic development in relation to spawning and field occurrence of larvae of three Antarctic echinoderms. Biol Bull 194:44–52CrossRefGoogle Scholar
  55. Staver JM, Strathmann RR (2002) Evolution of fast development of planktonic embryos to early swimming. Biol Bull 203:58–69PubMedCrossRefGoogle Scholar
  56. Sunday JM, Crim RN, Harley CDG, Hart MW (2011) Quantifying rates of evolutionary adaptation in response to ocean acidification. PLoS ONE 6. doi: 10.1371/journal.pone.0022881
  57. US EPA (2002) Short-term methods for estimating the chronic toxicity of effluents and receiving waters to marine and estuarine organisms. Third Edition. United States Environmental Protection AgencyGoogle Scholar
  58. Wright DA, Kennedy VS, Roosenburg WH, Castagna M, Mihursky JA (1983) Temperature tolerance of embryos and larvae of five bivalve species under simulated power plant entrainment conditions: a synthesis. Mar Biol 77:271–278CrossRefGoogle Scholar
  59. Zeebe RE, Wolf-Gladrow D (2005) CO2 in seawater: equilibrium, kinetics, isotopes. Elsevier Oceanography Series 65. Elsevier Inc, San DiegoGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • J. A. Ericson
    • 1
    • 2
  • M. A. Ho
    • 1
  • A. Miskelly
    • 1
  • C. K. King
    • 3
  • P. Virtue
    • 4
  • B. Tilbrook
    • 5
    • 6
  • M. Byrne
    • 1
    • 7
  1. 1.School of Medical SciencesUniversity of SydneySydneyAustralia
  2. 2.University of OtagoDunedinNew Zealand
  3. 3.Australian Antarctic DivisionKingstonAustralia
  4. 4.Institute for Marine and Antarctic StudiesUniversity of TasmaniaHobartAustralia
  5. 5.Centre for Australian Weather and Climate Research, a partnership between CSIRO and the Bureau of MeteorologyHobartAustralia
  6. 6.Antarctic Climate and Ecosystems Cooperative Research CentreHobartAustralia
  7. 7.School of Biological SciencesUniversity of SydneySydneyAustralia

Personalised recommendations