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Effects of reduced seawater pH on fertilisation, embryogenesis and larval development in the Antarctic seastar Odontaster validus

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Abstract

The effects of ocean acidification will be pronounced in high-latitude marine communities, although little is known on how reproduction in free-spawning polar invertebrates will respond. Using the circum-Antarctic sea star Odontaster validus, we examined fertilisation, larval survival and development under a controlled seawater treatment (temperature = −0.5 °C, pH 8.1, pCO2(aq) = 326.6 μatm, TA = 2,274.2 μmol kg soln−1), two near-future pH treatments (pH 7.8 and 7.6) and an extreme treatment (pH 7.0). At a sperm concentration of 3.5 × 105 sperm ml−1, percentage of fertilisation was 98–90 % across a pH 8.1–7.0 range. At near-future pH ranges (pH 7.8 and 7.6), fertilisation was not significantly lower than in the control pH 8.1 except at the lowest sperm concentration (2.2 × 103 sperm ml−1) where fertilisation was reduced to 60 and 61 % in pH 7.6 and 7.8, respectively. Larval survival was not significantly affected by a decrease in pH of 0.3 units, but at pH 7.6 survival was significantly reduced. This difference was apparent at 9 days, and at the end of the experiment at 58 days, survival was 55 % compared with 85 % in the ambient treatment. Near-future changes to pH yielded smaller larvae, a result of both subtle differences in their morphology and slowed development rates, while larvae at pH 7.0 showed evidence of abnormal development. O. validus fertilisation and larval success declines in seawater pH conditions expected in coastal Antarctica over the coming decades, although the responses observed are within the range observed in warmer-water echinoderms.

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References

  • Benzie JAH, Dixon P (1994) The effects of sperm concentration, sperm:egg ratio, and gamete age on fertilization success in crown-of-thorns starfish (Acanthaster planci) in the laboratory. Biol Bull 186:139–152

    Article  Google Scholar 

  • Bosch I, Beauchamp KA, Steele ME, Pearse JS (1987) Development, metamorphosis, and seasonal abundance of embryos and larvae of the Antarctic sea urchin Sterechinus neumayeri. Biol Bull 173:126–135

    Article  Google Scholar 

  • Byrne M (2010) Impact of climate change stressors on marine invertebrate life histories with a focus on the Mollusca and Echinodermata. In: Yu J, Henderson-Sellers A (eds) Climate alert: climate change monitoring and strategy. University of Sydney Press, Sydney, pp 142–185

    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 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 276:1883–1888

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Caldwell GS, Fitzer S, Gillespie CS, Pickavance G, Turnbull E, Bentley MG (2011) Ocean acidification takes sperm back in time. Invert Repr Dev 55:217–221

    Article  Google Scholar 

  • Catarino AI, De Ridder C, Gonzalez M, Gallardo P, Dubois P (2011) Sea urchin Arbacia dufresni (Blainville 1825) larvae response to ocean acidification. Polar Biol 35:455–461

    Article  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  PubMed  Google Scholar 

  • Chiantore M, Cattaneo-Vietti R, Elia L, Guidetti M, Antonini M (2002) Reproduction and condition of the scallop Adamussium colbecki (Smith 1902), the sea-urchin Sterechinus neumayeri (Meissner 1900) and the sea-star Odontaster validus Koehler 1911 at Terra Nova Bay (Ross Sea): different strategies related to inter-annual variations in food availability. Polar Biol 25:251–255

    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

    PubMed  CAS  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 

  • Clarke A (1983) Life in cold water: the physiological ecology of polar marine ectotherms. Oceanogr Mar Biol 21:341–453

    Google Scholar 

  • Comeau S, Jeffree R, Teyssié J-L, Gattuso J-P (2010a) Impact of ocean acidification on a key Arctic pelagic mollusc (Limacina helicina). Biogeosciences 6:1877–1882

    Article  Google Scholar 

  • Comeau S, Jeffree R, Teyssié J-L, Gattuso J-P (2010b) Response of the Arctic Pteropod Limacina helicina to projected future environmental conditions. PLoS Biol 5:e11362

    Google Scholar 

  • Cummings V, Hewitt J, Van Rooyen A, Currie K, Beard S, Thrush S, Norkko J, Barr N, Heath P, Halliday NJ, Sedcole R, Gomez A, McGraw C, Metcalf V (2011) Ocean acidification at high latitudes: potential effects on functioning of the Antarctic bivalve Laternula elliptica. PLoS Biol 6:e16069

    CAS  Google Scholar 

  • Dayton PK (1989) Interdecadal variation in an Antarctic sponge and its predators from oceanographic climate shifts. Science 245:1484–1486

    Google Scholar 

  • Dickson AG, Millero FJ (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep-Sea Res 34:1733–1743

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Dupont S, Ortega-Martinez O, Thorndyke M (2010) Impact of near-future ocean acidification on echinoderms. Ecotoxicology 19:449–462

    Article  PubMed  CAS  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

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

    Article  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 Chang 1:165–169

    Article  CAS  Google Scholar 

  • Fabry VJ, McClintock JB, Mathis JT, Grebmeier JM (2010) Ocean acidification at high latitudes: the Bellwether. Oceanography 22:160–171

    Article  Google Scholar 

  • Grange LJ (2005) Reproductive success in Antarctic marine invertebrates. Dissertation, University of Southampton

  • Grange LJ, Tyler PA, Peck LS (2007) Multi-year observations on the gametogenic ecology of the Antarctic seastar Odontaster validus. Mar Biol 153:15–23

    Article  Google Scholar 

  • Grange LJ, Tyler PA, Peck LS (2011) Fertilisation success of the circumpolar Antarctic seastar Odontaster validus (Koehler, 1906): A diver-collected study. In: Pollock NW (ed) Diving for science 2011. Proceedings of the American academy of underwater sciences 30th symposium, Dauphin Island, Alabama, pp 140–151

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

    Article  Google Scholar 

  • Heine JN, McClintock JB, Slattery M, Weston J (1991) Energetic composition, biomass, and chemical defense in the common Antarctic nemertean Parborlasia corrugatus McIntosh. J Exp Biol 153:15–25

    Article  Google Scholar 

  • Hofmann GE, Todgham AE (2010) Living in the now: physiological mechanisms to tolerate a rapidly changing environment. Annu Rev Physiol 72:127–145

    Article  PubMed  CAS  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 

  • Leong PKK, Manahan DT (1997) Metabolic importance of Na+/K+-ATPase activity during sea urchin development. J Exp Biol 200:2881–2892

    PubMed  CAS  Google Scholar 

  • Leong PK, Manahan DT (1999) Na+/K+-ATPase activity during early development and growth of an Antarctic sea urchin. J Exp Biol 202:2051–2058

    PubMed  CAS  Google Scholar 

  • Levitan DR, Sewell MA, Chia F-S (1991) Kinetics of fertilization in the sea urchin Strongylocentrotus franciscanus: interaction of gamete dilution, age, and contact time. Biol Bull 181:371–378

    Article  Google Scholar 

  • Mauchly JW (1940) Significance test for sphericity of a normal n-variate distribution. Ann Math Stat 11:204–209

    Google Scholar 

  • Marsh AG, Manahan DT (1999) A method for accurate measurement of the respiration rate of marine invertebrate embryos and larvae. Mar Ecol-Prog Ser 184:1–10

    Article  Google Scholar 

  • Marsh AG, Maxson RE, Manahan DT (2001) High macromolecular synthesis with low metabolic cost in Antarctic sea urchin embryos. Science 291:1950–1952

    Article  PubMed  CAS  Google Scholar 

  • Matson PG, Martz TR, Hofmann GE (2011) High-frequency observations of pH under Antarctic sea ice in the southern Ross Sea. Antarct Sci 23:607–613

    Article  Google Scholar 

  • McClintock JB, Angus RA, McDonald MR, Amsler CD, Catledge SA, Vohra YK (2009) Rapid dissolution of shells of weakly calcified Antarctic benthic macroorganisms indicates high vulnerability to ocean acidification. Antarct Sci 21:449–456

    Article  Google Scholar 

  • McNeil BI, Matear RJ (2008) Southern Ocean acidification: a tipping point at 450-ppm atmospheric CO2. Proc Natl Acad Sci USA 105:18860–18864

    Article  PubMed  CAS  Google Scholar 

  • McNeil BI, Tagliabue A, Sweeney C (2010) A multi-decadal delay in the onset of corrosive ‘acidified’ water in the Ross Sea of Antarctica due to strong air-sea CO2 equilibrium. Geophys Res Lett 37:L19607. doi:10.1029/2010GL044597

    Article  Google Scholar 

  • Mehrbach C, Culberson CH, Hawley JE, Pytkowicz RM (1973) Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnol Oceanogr 18:897–907

    Article  CAS  Google Scholar 

  • Melzner F, Gutowska MA, Langenbuch M, Dupont S, Lucassen M, Thorndyke MC, Bleich M, Pörtner H-O (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 

  • Morita M, Suwa R, Iguchi A, Nakamura M, Shimada K, Sakai K, Suzuki A (2010) Ocean acidification reduces sperm flagellar motility in broadcast spawning reef invertebrates. Zygote 18:103–107

    Article  PubMed  CAS  Google Scholar 

  • O’Donnell MJ, Todgham AE, Sewell MA, Hammond LM, 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 

  • Olson RR, Bosch I, Pearse JS (1987) The hypothesis of Antarctic larval starvation examined for the asteroid Odontaster validus. Limnol Oceanogr 32:686–690

    Article  Google Scholar 

  • Orr JC, Fabry VJ, Aumont O, Bopp L, Doney SC, Feely RA, Gnanadesikan A, Gruber N, Ishida A, Joos F et al (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437:681–686

    Article  PubMed  CAS  Google Scholar 

  • Pace DA, Manahan DT (2007) Cost of protein synthesis and energy allocation during development of Antarctic sea urchin embryos and larvae. Biol Bull 212:115–129

    Article  PubMed  CAS  Google Scholar 

  • Pearse JS (1969) Slow developing demersal embryos and larvae of the Antarctic sea star Odontaster validus. Mar Biol 3:110–116

    Article  Google Scholar 

  • Pechenik JA (1999) On the advantages and disadvantages of larval stages in benthic marine invertebrate lifecycles. Mar Ecol-Prog Ser 177:269–297

    Article  Google Scholar 

  • Peck LS (1993) Larval development in the Antarctic nemertean Parborlasia corrugatus (Heteronemertea: Lineidae). Mar Biol 116:301–310

    Article  Google Scholar 

  • Peck LS, Prothero-Thomas E (2002) Temperature effects on the metabolism of larvae of the Antarctic starfish Odontaster validus, using a novel micro-respirometer method. Mar Biol 141:271–276

    Article  CAS  Google Scholar 

  • Peck LS, Morley SA, Clark MS (2010) Poor acclimation capacities in Antarctic marine ectotherms. Mar Biol 157:2051–2059

    Article  Google Scholar 

  • Pennington JT (1985) The ecology of fertilization of echinoid eggs: the consequences of sperm dilution, adult aggregation, and synchronous spawning. Biol Bull 169:417–430

    Article  Google Scholar 

  • Powell DK, Tyler PA, Peck LS (2001) Effect of sperm concentration and sperm ageing on fertilisation success in the Antarctic soft-shelled clam Laternula elliptica and the Antarctic limpet Nacella concinna. Mar Ecol-Prog Ser 215:191–200

    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 Strongylocentrotus franciscanus. Glob Chang Biol 17:163–171

    Article  Google Scholar 

  • Scheiner SM, Gurevitch J (1993) The design and analysis of ecological experiments. Chapman and Hall, New York

  • Sewell MA, Hofmann GE (2011) Antarctic echinoids and climate change: a major impact on the brooding forms. Glob Chang Biol 17:734–744

    Article  Google Scholar 

  • Shilling FM, Manahan DT (1994) Energy metabolism and amino acid transport during early development of Antarctic and temperate echinoderms. Biol Bull 187:398–407

    Article  CAS  Google Scholar 

  • 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 194:44–52

    Article  Google Scholar 

  • Stokes MD, Stewart B, Epel D (1996) The kinetics of the cortical reaction and respiratory burst following fertilization of Sterechinus neumayeri eggs. Antarct J US 31:119–120

    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 development delay. Comp Biochem Phys A 160:331–340

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Vogel S (1994) Life in moving fluids. Princeton University Press, Princeton

    Google Scholar 

  • Wanninkhof R, Lewis E, Feely RA, Millero FJ (1999) The optimal carbonate dissociation constants for determining surface water pCO2 from alkalinity and total inorganic carbon. Mar Chem 65:291–301

    Article  CAS  Google Scholar 

  • Watson SA, Peck LS, Tyler PA, Southgate PC, Tan KS, Day RW, Morley SA (2012) Marine invertebrate skeleton size varies with latitude, temperature and carbonate saturation: implications for global change and ocean acidification. Glob Chang Biol 18:3026–3038

    Article  Google Scholar 

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Acknowledgments

We thank Antarctica New Zealand for their logistical support in Antarctica, and staff at the Portobello Marine Laboratory, University of Otago. This research was funded by a University of Otago Research Grant. Maria Gonzalez-Bernat was supported by a New Zealand AID scholarship. We disclose no conflicts of interest in regard to this research.

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Correspondence to Miles Lamare.

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Gonzalez-Bernat, M.J., Lamare, M. & Barker, M. Effects of reduced seawater pH on fertilisation, embryogenesis and larval development in the Antarctic seastar Odontaster validus . Polar Biol 36, 235–247 (2013). https://doi.org/10.1007/s00300-012-1255-7

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