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Effects of elevated pCO2 and the effect of parent acclimation on development in the tropical Pacific sea urchin Echinometra mathaei

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Abstract

Effects of acclimation to projected near-future ocean acidification (OA) conditions on physiology, reproduction and development were investigated in the tropical sea urchin Echinometra mathaei. Following 6 weeks in control or one of the three elevated pCO2 (pHNIST 7.5–8.1; pCO2 ~485–1,770 μatm) conditions, adult urchins exhibited a slight decline of growth in low pH treatments and moderately reduced respiration at intermediate levels. At 7 weeks, gametes from adults were used to produce larvae that were reared in their respective parental treatments. To assess whether larvae from acclimated parents are more resilient to elevated pCO2 than those not acclimated, larvae from control animals were also reared in the elevated pCO2 treatments. There was no difference in female ‘spawnability’ and oocyte size between treatments, but male spawning ability was reduced in increased pCO2 conditions. In elevated pCO2 treatments, the percentage of normal larvae and larval size decreased in the progeny of control- and elevated pCO2-acclimated parents, and arm asymmetry increased. Thus, acclimation of the parents did not make the progeny more resilient or sensitive to OA effects. Negative effects of increased pCO2 on reproduction and development may impact on recruitment and population maintenance of this species.

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References

  • Abramoff MD, Magalhaes PJ, Ram SJ (2004) Image processing with Image J. Biophotonics Intern 11:36–42

    Google Scholar 

  • Allen JD (2008) Size-specific predation on marine invertebrate larvae. Biological Bull 214:42

    Article  Google Scholar 

  • Allen JD, Pechenik JA (2010) Understanding the effects of low salinity on fertilization success and early development in the sand dollar Echinarachnius parma. Biological Bull 218:189

    Google Scholar 

  • Anthony KRN, Kline DI, Diaz-Pulido G, Dove S, Hoegh-Guldberg O (2008) Ocean acidification causes bleaching and productivity loss in coral reef builders. Proc Nat Acad Sci 105:17442

    Article  CAS  Google Scholar 

  • Anthony K, A Kleypas J, Gattuso JP (2011) Coral reefs modify their seawater carbon chemistry—implications for impacts of ocean acidification. Glob Change Biol. doi:10.1111/j.1365-2486.2011.02510.x

  • Bingham BL, Bacigalupi M, Johnson LG (1997) Temperature adaptations of embryos from intertidal and subtidal sand dollars (Dendraster excentricus, Eschscholtz). Northwest Sci 71:108–114

    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 Ann 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

    Google Scholar 

  • 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 Biol Sci 276:1883

    Article  Google Scholar 

  • Byrne M, Soars N, Selvakumaraswamy P, Dworjanyn SA, Davis AR (2010) Sea urchin fertilization 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, Selvakumaraswamy P, Ho MA, Nguyen HD (2011) Sea urchin development in a global change hot spot, potential for southerly migration of thermotolerant propagules. Deep Sea Res II 58:712–719

    Google Scholar 

  • Caldeira K, Wickett ME (2005) Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean. J Geophys Res 110:12

    Article  Google Scholar 

  • Carr RS, Biedenbach JM, Nipper M (2006) Influence of potentially confounding factors on sea urchin pore water toxicity tests. Arch Environ Contam Toxicol 51:573–579

    Article  CAS  Google Scholar 

  • Chan KYK, Grünbaum D, O’Donnell MJ (2011) Effects of ocean-acidification-induced morphological changes on larval swimming and feeding. J Exp Biol 214:3857–3867

    Article  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 

  • Clark D, Lamare M, Barker M (2009) Response of sea urchin pluteus larvae (Echinodermata: Echinoidea) to reduced seawater pH: a comparison among a tropical, temperate, and a polar species. Mar Biol 156:1125–1137

    Article  Google Scholar 

  • De’ath G, Lough JM, Fabricius KE (2009) Declining coral calcification on the Great Barrier Reef. Science 323:116

    Article  Google Scholar 

  • Diaz-Pulido G, Gouezo M, Tilbrook B, Dove S, Anthony KRN (2011) High CO2 enhances the competitive strength of seaweeds over corals. Ecol Lett 14:156–162

    Article  Google Scholar 

  • Dickson AG, Sabine CL, Christian JR (2007) Guide to best practices for ocean CO2 measurements. PICES Special Publication 3, Sidney

  • Doo SS, Dworjanyn SA, Foo SA, Soars NA, Byrne M (2011) Impacts of ocean acidification on development of the meroplanktonic larval stage of the sea urchin Centrostephanus rodgersii. ICES J Mar Sci: J du Conseil Adv View. doi:10.1093/icesjms/fsr123

  • Dupont S, Dorey N, Stumpp M, Melzner F, Thorndyke M (2012) Long-term and trans-life-cycle effects of exposure to ocean acidification in the green sea urchin Strongylocentrotus droebachiensis. Mar Biol. (online first). doi:10.1007/s00227-012-1921-x:1-9

  • Eckman JE (1996) Closing the larval loop: linking larval ecology to the population dynamics of marine benthic invertebrates. J Exp Mar Biol Ecol 200:207–237

    Article  Google Scholar 

  • 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 157:2689–2702

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

    Google Scholar 

  • Fabricius KE, Langdon C, Uthicke S, Humphrey C, Noonan S, De’ath G, Okazaki R, Muehllehner N, Glas MS, Lough JM (2011) Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nat Clim Change 1:165–169

    Article  CAS  Google Scholar 

  • Gonzalez-Bernat M, Lamare M, Uthicke S, Byrne M (2012) Fertilisation, embryogenesis and larval development in the tropical intertidal sand dollar Arachnoides placenta in response to reduced seawater pH. Mar Biol (this volume)

  • Hall-Spencer JM, Rodolfo-Metalpa R, Martin S, Ransome E, Fine M, Turner SM, Rowley SJ, Tedesco D, Buia MC (2008) Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 454:96–99

    Article  CAS  Google Scholar 

  • Havenhand JN, Buttler FR, Thorndyke MC, Williamson JE (2008) Near-future levels of ocean acidification reduce fertilization success in a sea urchin. Curr Biol 18:R651–R652

    Article  CAS  Google Scholar 

  • Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737

    Article  CAS  Google Scholar 

  • Hönisch B, Hemming NG, Archer D, Siddall M, McManus JF (2009) Atmospheric carbon dioxide concentration across the mid-Pleistocene transition. Science 324:1551

    Article  Google Scholar 

  • Johnson LG, Babcock RC (1994) Temperature and the larval ecology of the crown-of-thorns starfish, Acanthaster planci. Biological Bull 187:304

    Article  Google Scholar 

  • Kominami T, Takata H (2003) Timing of early developmental events in embryos of a tropical sea urchin Echinometra mathaei. Zool Sci 20:617–626

    Article  Google Scholar 

  • Kroeker KJ, Kordas RL, Crim RN, Singh GG (2010) Meta analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecol Lett 13:1419–1434

    Article  Google Scholar 

  • Kurihara H (2008) Effects of CO2-driven ocean acidification on the early developmental stages of invertebrates. Mar Ecol Prog Ser 373:275–284

    Article  CAS  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 

  • 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 180:197–211

    Article  Google Scholar 

  • Langenbuch M, Pörtner HO (2002) Changes in metabolic rate and N excretion in the marine invertebrate Sipunculus nudus under conditions of environmental hypercapnia. J Exp Biol 205:1153

    CAS  Google Scholar 

  • Lannig G, Eilers S, Pörtner HO, Sokolova IM, Bock C (2010) Impact of ocean acidification on energy metabolism of oyster, Crassostrea gigas—changes in metabolic pathways and thermal response. Mar Drugs 8:2318–2339

    Article  CAS  Google Scholar 

  • Martin S, Richier S, Pedrotti ML, Dupont S, Castejon C, Gerakis Y, Kerros ME, Oberhänsli F, Teyssié JL, Jeffree R (2011) Early development and molecular plasticity in the Mediterranean sea urchin Paracentrotus lividus exposed to CO2-driven acidification. J Exp Biol 214:1357

    Article  CAS  Google Scholar 

  • McClanahan TR, Muthiga NA (1988) Changes in Kenyan coral reef community structure and function due to exploitation. Hydrobiologia 166:269–276

    Article  Google Scholar 

  • McClanahan TR, Muthiga NA (2007) Ecology of Echinometra. Dev Aquac Fish Sci 37:297–317

    Article  Google Scholar 

  • McClanahan TR, Shafir SH (1990) Causes and consequences of sea urchin abundance and diversity in Kenyan coral reef lagoons. Oecologia 83:362–370

    Google Scholar 

  • McClanahan TR, Nugues M, Mwachireya S (1994) Fish and sea urchin herbivory and competition in Kenyan coral reef lagoons: the role of reef management. J Exp Mar Biol Ecol 184:237–254

    Article  Google Scholar 

  • McClintock JB, Amsler MO, Angus RA, Challener RC, Schram JB, Amsler CD, Mah CL, Cuce J, Baker BJ (2011) The Mg-Calcite composition of Antarctic echinoderms: important implications for predicting the impacts of ocean acidification. J Geol 119:457–466

    Article  CAS  Google Scholar 

  • McElroy DJ, Nguyen HD, Byrne M (2012) Respiratory response of the intertidal seastar Parvulastra exigua to contemporary and near-future pulses of warming and hypercapnia. J Exp Mar Biol Ecol

  • Michaelidis B, Ouzounis C, Paleras A, Pörtner HO (2005) Effects of long-term moderate hypercapnia on acid-base balance and growth rate in marine mussels Mytilus galloprovincialis. Mar Ecol Prog Ser 293:109–118

    Article  Google Scholar 

  • Miles H, Widdicombe S, Spicer JI, Hall-Spencer J (2007) Effects of anthropogenic seawater acidification on acid-base balance in the sea urchin Psammechinus miliaris. Mar Pollut Bull 54:89–96

    Google Scholar 

  • Moss RH, Edmonds JA, Hibbard KA, Manning MR, Rose SK, van Vuuren DP, Carter TR, Emori S, Kainuma M, Kram T (2010) The next generation of scenarios for climate change research and assessment. Nature 463:747–756

    Article  CAS  Google Scholar 

  • Moulin L, Catarino AI, Claessens T, Dubois P (2011) Effects of seawater acidification on early development of the intertidal sea urchin Paracentrotus lividus (Lamarck 1816). Mar Pollut Bull 62:48–54

    Article  CAS  Google Scholar 

  • Munday PL, Dixson DL, Donelson JM, Jones GP, Pratchett MS, Devitsina GV, Døving KB (2009) Ocean acidification impairs olfactory discrimination and homing ability of a marine fish. PNAS 106:1848–1852

    Article  CAS  Google Scholar 

  • Norstrom AV, Nystrom M, Lokrantz J, Folke C (2008) Alternative states on coral reefs: beyond coral-macroalgal phase shifts. Mar Ecol Prog Ser 376:295–306

    Article  Google Scholar 

  • O’Donnell MJ, Todgham AE, Sewell MA, Hammond LTM, Ruggiero K, Fangue NA, Zippay ML, Hofmann GE (2010) Ocean acidification alters skeletogenesis and gene expression in larval sea urchins. Mar Ecol Prog Ser 398:157–171

    Article  Google Scholar 

  • O’Connor C, Mulley JC (1977) Temperature effects on periodicity and embryology, with observations on the population genetics, of the aquacultural echinoid Heliocidaris tuberculata. Aquaculture 12:99–114

    Article  Google Scholar 

  • Parker LM, Ross PM, O'Connor WA, Borysko L, Raftos DA, Poertner HO (2012) Adult exposure influences offspring response to ocean acidification in oysters. Glob Chang Biol 18:82–92

    Google Scholar 

  • Pechenik JA (1987) Environmental influences on larval survival and development. In: Giese AC, Pearse JS (eds) Reproduction of marine invertebrates, vol 2. Academic Press, New York, pp 551–608

  • Pörtner HO (2008) Ecosystem effects of ocean acidification in times of ocean warming: a physiologist’s view. Eff Ocean Acidif Mar Ecosyst 373:203–217

    Google Scholar 

  • Pörtner HO, Langenbuch M, Reipschläger A (2004) Biological impact of elevated ocean CO2 concentrations: lessons from animal physiology and earth history. J Oceanogr 60:705–718

    Article  Google Scholar 

  • Przeslawski R, Ahyong S, Byrne M, WoeRheide G, Hutchings P (2008) Beyond corals and fish: the effects of climate change on noncoral benthic invertebrates of tropical reefs. Glob Change Biol 14:2773–2795

    Article  Google Scholar 

  • R Development Core Team (2010) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Ries JB, Cohen AL, McCorkle DC (2009) Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 37:1131

    Article  CAS  Google Scholar 

  • 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:e11372

    Article  Google Scholar 

  • Shirayama Y, Thornton H (2005) Effect of increased atmospheric CO2 on shallow water marine benthos. J Geophys Res 110:C09S08

    Article  Google Scholar 

  • Siikavuopio SI, Mortensen A, Dale T, Foss A (2007) Effects of carbon dioxide exposure on feed intake and gonad growth in green sea urchin, Strongylocentrotus droebachiensis. Aquaculture 266:97–101

    Article  CAS  Google Scholar 

  • Soars NA, Prowse TAA, Byrne M (2009) Overview of phenotypic plasticity in echinoid larvae’, Echinopluteus transversus’ type vs. typical echinoplutei. Mar Ecol Prog Ser 383:113–125

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Stumpp M, Wren J, Melzner F, Thorndyke MC, Dupont S (2011b) 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 Mol Integr Physiol 160:331–340

    Article  CAS  Google Scholar 

  • Stumpp M, Truebenbach K, Brennecke D, Hu MY, Melzner F (2012) Resource allocation and extracellular acid-base status in the sea urchin Strongylocentrotus droebachiensis in response to CO2 induced seawater acidification. Aquat Toxicol 110:194–207

    Article  Google Scholar 

  • Sunday JM, Crim RN, Harley CDG, Hart MW (2011) Quantifying rates of evolutionary adaptation in response to ocean acidification. PLoS One 6:e22881

    Google Scholar 

  • Thomsen J, Melzner F (2010) Moderate seawater acidification does not elicit long-term metabolic depression in the blue mussel Mytilus edulis. Mar Biol 157:1–10

    Google Scholar 

  • Uthicke S, Schaffelke B, Byrne M (2009) A boom-bust phylum? Ecological and evolutionary consequences of density variations in echinoderms. Ecol Monogr 79:3–24

    Article  Google Scholar 

  • Uthicke S, Vogel N, Doyle J, Schmidt C, Humphrey C (2011) Interactive effects of climate change and eutrophication on the dinoflagellate bearing benthic foraminifera Marginopora vertebralis. Coral Reefs. doi:10.1007/s00338-011-0851-2

    Google Scholar 

  • Wood HL, Spicer JI, Widdicombe S (2008) Ocean acidification may increase calcification rates, but at a cost. Proc R Soc B Biol Sci 275:1767–1773

    Article  Google Scholar 

  • Wood HL, Spicer JI, Lowe DM, Widdicombe S (2010) Interaction of ocean acidification and temperature; the high cost of survival in the brittlestar Ophiura ophiura. Mar Biol 157:2001–2013

    Article  Google Scholar 

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Acknowledgments

We are grateful to Murray Logan for help with the statistical analysis, and Florita Flores, Paolo Momigliano and Nikolas Vogel for assistance with the aquarium system. The work was supported by a Discovery Grant from the Australian Research Council and conducted with the support of funding from the Australian Government’s National Environmental Research Program.

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  1. Australian Institute of Marine Science, PMB No 3, Townsville, QLD, 4810, Australia

    S. Uthicke

  2. Schools of Biomedical and Biological Sciences, University of Sydney, Sydney, NSW, Australia

    N. Soars & M. Byrne

  3. School of Medical Sciences, F13, University of Sydney, Sydney, NSW, 2006, Australia

    S. Foo

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  1. S. Uthicke
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  2. N. Soars
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Correspondence to S. Uthicke.

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Communicated by S. Dupont.

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Uthicke, S., Soars, N., Foo, S. et al. Effects of elevated pCO2 and the effect of parent acclimation on development in the tropical Pacific sea urchin Echinometra mathaei . Mar Biol 160, 1913–1926 (2013). https://doi.org/10.1007/s00227-012-2023-5

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