Skip to main content
Log in

Impacts of near future sea surface pH and temperature conditions on fertilisation and embryonic development in Centrostephanus rodgersii from northern New Zealand and northern New South Wales, Australia

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Oceans are warming and becoming more acidic. While higher temperature and lower pH can have negative effects on fertilisation and development of marine invertebrates, warming may partially ameliorate the negative effect of lower pH. This study determined the effect of warming (3 °C) and decreased pH (0.3, 0.5, 1.1 units below ambient) on fertilisation and development in two populations of the sea urchin Centrostephanus rodgersii, one at its northern range limit (Coffs Harbour, New South Wales NSW, 30°27′S, 153°14′E) and the other one in New Zealand where the species may be a recent arrival (Mokohinau Islands, 35°56′S, 175°9′E). Both populations were sampled in August 2011. The two populations exhibited a differential response to temperature, while pH affected them similarly. Fertilisation was robust to pH levels forecast for 2100, and it was only slightly reduced at pH values forecast for 2300 (i.e. ≈5 and ≈8 % for the northern NSW and the New Zealand populations, respectively). Decreased pH (pH = 7.6) reduced the percentage of succeeding developmental stages. Progression through cleavage and hatching stages was faster at +3 °C in the New Zealand population but not in northern NSW urchins, while for the NSW population, there was a positive interaction between temperature and pH at hatching. Gastrulation was negatively affected by an extreme pH 7.0 treatment (60–80 % reduction) and least affected by increased temperature. The percentage of abnormal embryos at gastrulation increased significantly at +3 °C treatment in the northern NSW population. Predicted future increases in temperature may facilitate further expansion of the geographical range of C. rodgersii in New Zealand, with a minimal effect of concurrent reduced pH.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Arnberg M, Calosi P, Spicer JI, Tandberg AHS, Nilsen MN, Westerlund S, Bechmann RK (2012) Elevated temperature elicits greater effects than decreased pH on the development, feeding and metabolism of northern shrimp (Pandalus borealis) larvae. Mar Biol. doi:10.1007/s00227-012-2072-9

    Google Scholar 

  • Brierley AS, Kingsford MJ (2009) Impacts of climate change on marine organisms and ecosystems. Curr Biol 19:602–614

    Article  Google Scholar 

  • Byrne M (2011) 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 Annu Rev 49:1–42

    Google Scholar 

  • Byrne M (2012) Global change ecotoxicology: identification of early life history bottlenecks in marine invertebrates, variable species responses and variable experimental approaches. Mar Environ Res 76:3–15

    Article  CAS  Google Scholar 

  • Byrne M, Andrew NL (2013) Centrostephanus rodgersii. In: Lawrence JM (ed), Sea urchins: biology and ecology. Elsevier B.V., Amsterdam, in press

  • Byrne M, Andrew NL, Worthington DG, Brett PA (1998) Reproduction in the diadematoid sea urchin Centrostephanus rodgersii in contrasting habitats along the coast of New South Wales, Australia. Mar Biol 132:305–318

    Article  Google Scholar 

  • Byrne M, Ho M, Selvakumaraswamy P, Nguyen HD, Dworjanyn SA, Davis AR (2009) Temperature, but not pH, compromises sea urchin fertilisation and early development under near-future climate change scenarios. Proc R Soc Queensl 276:1883–1935

    Article  Google Scholar 

  • Byrne M, Soars NA, Ho MA, Wong E, McElroy D, Selvakumarasvamy P, Dworjanyn S, Davis AR (2010a) Fertilisation in a suite of coastal marine invertebrates from SE Australia is robust to near-future ocean warming and acidification. Mar Biol 157:2061–2069

    Article  Google Scholar 

  • Byrne M, Soars N, Selvakumaraswamy P, Dworjanyn S, Davis AR (2010b) Sea urchin fertilisation in a warm, acidified and high pCO2 ocean across a range of sperm densities. Mar Environ Res 69:234–239

    Article  CAS  Google Scholar 

  • Byrne M, Selvakumarasvamy P, Ho MA, Woolsey E, Nguyen HD (2011) Sea urchin development in a global change hotspot, potential for southerly migration of thermotolerant propagules. Deep-Sea Res 58:712–719 2 Trop Stud Oceanogr

    CAS  Google Scholar 

  • Caldeira K, Wickett ME (2003) Anthropogenic carbon and ocean pH. Nature 425:365

    Article  CAS  Google Scholar 

  • Chang FH, Zeldis J, Gall M, Hall J (2003) Seasonal and spatial variation of phytoplankton assemblages, biomass and cell size from spring to summer across the north-eastern New Zealand continental shelf. J Plankton Res 25:737–758

    Article  CAS  Google Scholar 

  • 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 257:14881–14890

    CAS  Google Scholar 

  • Christensen AB, Nguyen HD, Byrne M (2011) Thermotolerance and the effects of hypercapnia on the metabolic rate of the ophiuroid Ophionereis schayeri: inferences for survivorship in a changing ocean. J Exp Mar Biol Ecol 403:31–38

    Article  Google Scholar 

  • Doney SC, Fabry VJ, Feely RA, Kleypas JA (2009) Ocean acidification: the other CO2 problem. Ann Rev Mar Sci 1:169–192

    Article  Google Scholar 

  • 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 69:460–464

    Article  Google Scholar 

  • 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 fertilisation and early development of the Antarctic echinoid Sterechinus neumayeri. Polar Biol 35:1027–1034

    Article  Google Scholar 

  • Evans JP, Marshall DJ (2005) Male-by-female interactions influence fertilisation success and mediate the benefits of polyandry in the sea urchin Heliocidaris erythrogramma. Evolution 59:106–112

    Google Scholar 

  • 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 305:362–366

    Article  CAS  Google Scholar 

  • Feely RA, Doney SC, Cooley SR (2009) Ocean acidification: present conditions and future changes in a high-CO2 world. Oceanography 22:36–47

    Article  Google Scholar 

  • Findlay HS, Kendall MA, Spicer JI, Widdicombe S (2010a) Post-larval development of two intertidal barnacles at elevated CO2 and temperature. Mar Biol 157:725–735

    Article  Google Scholar 

  • Findlay HS, Kendall MA, Spicer JI, Widdicombe S (2010b) Relative influences of ocean acidification and temperature on intertidal barnacle post-larvae at the northern edge of their geographic distribution. Estuar Coast Shelf Sci 86:675–682

    Article  CAS  Google Scholar 

  • Foo SA, Dworjanyn SA, Poore AGB, Byrne M (2012) Adaptive capacity of the habitat modifying sea urchin Centrostephanus rodgersii to ocean warming and ocean acidification: performance of early embryos. PLoS ONE 7:e42497

    Article  CAS  Google Scholar 

  • Gatti JL, Christen R (1985) Regulation of internal pH of sea urchin sperm. A role for Na/K pump. J Biol Chem 260:7599–7602

    CAS  Google Scholar 

  • Halpern BS, Walbridge S, Selkoe KA, Kappel CV, Micheli F, D’Agrosa C, Bruno JF, Casey KS, Ebert C, Fox HE, Fujita R, Heinemann D, Lenihan HS, Madin EMP, Perry MT, Selig ER, Spalding M, Steneck R, Watson R (2008) A global map of human impact on marine ecosystems. Science 319:948–952

    Article  CAS  Google Scholar 

  • Haugan PM, Drange H (1996) Effects of CO2 on the ocean environment. Energy Convers Manage 37:1019–1022

    Article  CAS  Google Scholar 

  • Havenhand JN, Butler FR, Thorndyke MC, Williamson JE (2008) Near-future levels of ocean acidification reduce fertilisation success in a sea urchin. Curr Biol 18:651–652

    Article  Google Scholar 

  • Huggett MJ, King CK, Williamson JE, Steinberg PD (2005) Larval development and metamorphosis of the Australian diadematid sea urchin Centrostephanus rodgersii. Invertebr Reprod Dev 47:197–204

    Google Scholar 

  • IPCC (2007) Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change (eds Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL), pp 996. Cambridge University Press, New York

  • Ishida J (1936) An enzyme dissolving the fertilisation membrane of sea urchin eggs. Annot Zool Jap 15:453–459

    Google Scholar 

  • Kurihara H, Shirayama Y (2004) Effects of increased atmospheric CO2 on sea urchin early development. Mar Ecol Prog Ser 274:161–169

    Article  Google Scholar 

  • Lewis E, Wallace D (1998) Program developed for CO2 system calculations. Computer program, http://cdiac.ornl.gov/oceans/co2rprt.html

  • Ling SD, Johnson CR, Frusher S, King CK (2008) Reproductive potential of a marine ecosystem engineer at the edge of a newly expanded range. Glob Change Biol 14:907–915

    Article  Google Scholar 

  • Ling SD, Johnson CR, Frusher SD, Ridgway KR (2009a) Overfishing reduces resilience of kelp beds to climate driven catastrophic phase shift. Proc Natl Acad Sci USA 106:22341–22345

    Article  CAS  Google Scholar 

  • Ling SD, Johnson CR, Ridgway K, Hobday AJ, Haddon JH (2009b) Climate-driven range extension of a sea urchin: inferring future trends by analysis of recent population dynamics. Glob Change Biol 15:719–731

    Article  Google Scholar 

  • 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? Biogeosciences 6:2313–2331

    Article  CAS  Google Scholar 

  • Moulin L, Catrino AI, Claessens T, Dubois P (2011) Effects of seawater acidification on early development of the intertidal sea urchin Paracentrotus lividus (Lamarck 1916). Mar Poll Bull 62:48–54

    Article  CAS  Google Scholar 

  • Nguyen HD, Doo SS, Soars NA, Byrne M (2012) Noncalcifying larvae in a changing ocean: warming, not acidification/hypercapnia, is the dominant stressor on development of the sea star Meridiaster calcar. Glob Change Biol 18:2466–2476

    Article  Google Scholar 

  • Orr JC, Fabry VJ, Aumont O, Bopp L, Doney SC, Feely RA, Gnanadesikan A, Gruber N, Ishida A, Joos F, Key RM, Lindsay K, Maier-Reimer E, Matear R, Monfray P, Mouchet A, Najjar RG, Plattner GK, Rodgers KB, Sabine CL, Sarmiento JL, Schlitzer R, Slater RD, Totterdell IJ, Weirig MF, Yamanaka Y, Yool A (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437:681–686

    Article  CAS  Google Scholar 

  • Palumbi SR (1999) All males are not created equal: fertility differences depend on gamete recognition polymorphisms in sea urchins. Proc Natl Acad Sci USA 96:12632–12637

    Article  CAS  Google Scholar 

  • Parker LM, Ross PM, O’Connor WA (2010) Comparing the effect of elevated pCO2 and temperature on the fertilisation and early development of two species of oysters. Mar Biol 157:2435–2452

    Article  Google Scholar 

  • Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impact across natural systems. Nature 421:37–42

    Article  CAS  Google Scholar 

  • Pecorino D, Lamare MD, Barker MF (2012) Reproduction of the Diadematidae sea urchin Centrostephanus rodgersii in a recently colonized area of northern New Zealand. Mar Biol Res 9:157–168

    Article  Google Scholar 

  • Pecorino D, Lamare MD, Barker MF, Byrne M (2013) How does embryonic and larval thermal tolerance contribute to the distribution of the sea urchin Centrostephanus rodgersii (Diadematidae) in New Zealand? J Exp Mar Biol Ecol 445:120–128

    Article  Google Scholar 

  • Perry AL, Low PJ, Ellis JR, Reynolds JD (2005) Climate change and distribution shifts in marine fishes. Science 308:1912–1915

    Article  CAS  Google Scholar 

  • Pörtner HO (2008) Ecosystem effects of ocean acidification in times of ocean warming: a physiologist’s view. Mar Ecol Prog Ser 373:203–217

    Article  Google Scholar 

  • R Development Core Team (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. http://www.R-project.org

  • Rahman S, Tsuchiya M, Uehara T (2009) Effects of temperature on hatching rate, embryonic development and early larval survival of the edible sea urchin, Tripneustes gratilla. Biologia 64:768–775

    Article  Google Scholar 

  • Reuter KE, Lotterhos KE, Crim RN, Thompson CA, Harley CDG (2011) Elevated pCO2 increases sperm limitation and risk of polyspermy in the red sea urchin Strongylocentrous franciscanus. Glob Change Biol 17:163–171

    Article  Google Scholar 

  • Sagarin RD, Barry JP, Gilman SE, Baxter CH (1999) Climate-related change in an intertidal community over short and long time scales. Ecol Monograph 69:465–490

    Article  Google Scholar 

  • Sheppard-Brennand H, Soars N, Dworjanyn S, Davis AR, Byrne M (2010) Impact of ocean warming and ocean acidification on development and calcification in the sea urchin Tripneustes gratilla. PLoSONE 5:1–7

    Article  Google Scholar 

  • Stumpp M, Wren J, Melzner F, Thorndyke MC, Dupont ST (2011a) CO2 induced seawater acidification impacts sea urchin larval development I: elevated metabolic rates decrease scope for growth and induce developmental delay. Comp Biochem Physiol Part A 160:331–340

    Article  CAS  Google Scholar 

  • Stumpp M, Dupont S, Thorndyke MC, Melzner F (2011b) CO2 induced seawater acidification impacts sea urchin larval development II: gene expression patterns in pluteus larvae. Comp Biochem Physiol Part A 160:320–330

    Article  CAS  Google Scholar 

  • 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. doi:10.1371/journal.pone.0026941

    Google Scholar 

  • Wolfe K, Dworjanyn S, Byrne M (2013) Effects of ocean warming and acidification on survival, growth and skeletal development in the early benthic juvenile sea urchin (Heliocidaris erythrogramma). Glob Chang Biol http://dx.doi.org/10.1111/gcb.12249

Download references

Acknowledgments

The authors wish to thank the staff of the Leigh Marine Laboratory of the University of Auckland and the staff of NMSC at Coffs Harbour for their help during the collection of the sea urchins and while running the experiments. This research was supported by a New Zealand Marine Sciences Society Student Research Grant and by a Grant of the Australian Research Council (MB, SD) that supported the construction of the facility in Coffs Harbour.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to D. Pecorino.

Additional information

Communicated by U. Sommer.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 21 kb)

227_2013_2318_MOESM2_ESM.tiff

Photomicrographs of a representative fertilised egg and subsequent developmental stages of Centrostephanus rodgersii. From left to right: fertilised egg, cleaved embryo, hatched blastula, gastrula and abnormal embryo. Scale bars represent 100 μm. (TIFF 897 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pecorino, D., Barker, M.F., Dworjanyn, S.A. et al. Impacts of near future sea surface pH and temperature conditions on fertilisation and embryonic development in Centrostephanus rodgersii from northern New Zealand and northern New South Wales, Australia. Mar Biol 161, 101–110 (2014). https://doi.org/10.1007/s00227-013-2318-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-013-2318-1

Keywords

Navigation