Skip to main content
SpringerLink
Log in

Fertilisation, embryogenesis and larval development in the tropical intertidal sand dollar Arachnoides placenta in response to reduced seawater pH

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

Abstract

We examined the response of the tropical sand dollar Arachnoides placenta to reduced seawater pH in experiments spanning ca. 50 % of the planktonic larval duration. A. placenta inhabits intertidal sandy beaches where we observed a minimum in situ pH range 0.06 pH units (pH 8.10–8.16). The responses of gametes and larvae to seawater pH were tested in vitro in ambient (pH 8.14, pCO2 = 525.7 μatm, total alkalinity = 2,651 μmol kg soln−1) and three reduced pH seawater treatments (7.8–7.0). Percentage fertilisation decreased significantly with decreasing pH across a range of sperm/egg ratios (4:1 up to 4,000:1). A. placenta reached the advanced pluteus stage in 4 days, and during this time, we saw no difference in survival rate of larvae between the ambient (67 %) and pH 7.79 (72 %) treatments. Four-day survival was, however, reduced to 44 and 11 % in the pH 7.65 and 7.12 treatments, respectively. Larval development and morphometrics varied among pH treatments. Embryos reared in pH 7.12 exhibited arrested development. Larvae reared at pH 7.65 showed delayed development and greater mortality compared with those reared at pH 7.79 and 8.14. When larval morphometrics are compared among larvae of the same size, differences in larval width and total arm length between pH treatments disappear. These results suggest that variation in larval size among the three highest pH treatments at a given time are likely the result of slower development and apparent shrinkage of surviving larvae and not direct changes in larval shape. There were no differences in the percentage inorganic content (a proxy for calcification) in larvae reared in either an ambient or a pH 7.7 treatment. The responses of fertilisation and development to decreased pH/increased pCO2 in A. placenta are within the range of those reported for other intertidal and subtidal echinoid species from colder latitudes.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Allen JD (2008) Size-specific predation on marine invertebrate larvae. Biol Bull 214:42–49

    Article  Google Scholar 

  • Anthony KRN, Kleypas JA, Gattuso J-P (2011) Coral reefs modify their seawater carbon chemistry—implications for impacts of ocean acidification. Glob Change Biol 17:3655–3666

    Article  Google Scholar 

  • Brierley AS, Kingsford MJ (2009) Impacts of climate change on marine organisms and ecosystems. Curr Biol 19:R602–R614

    Article  CAS  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

  • 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

    Article  CAS  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 embryonic development under near-future climate change scenarios. Proc R Soc B 276:1883–1888

    Article  Google Scholar 

  • Byrne M, Soars NA, Ho MA, Wong E, McElroy D, Selvakumaraswamy P, Dworjanyn SA, Davis AR (2010a) Fertilization 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 SA, Davis AR (2010b) Sea urchin fertilization in a warm, acidified ocean and high pCO2 ocean across a range of sperm densities. Mar Environ Res 69:234–239

    Article  CAS  Google Scholar 

  • Caldeira K, Wicket ME (2003) Anthropogenic carbon and ocean pH. Nature 425(6956):365

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Catarino AI, De Ridder C, Gonzalez M, Gallardo P, Dubois P (2012) Sea urchin Arbacia dufresnei (Blainville 1825) larvae response to ocean acidification. Polar Biol 35:455–461

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Chen C-P, Chen B-Y (1992) Effects of high temperature on larval development and metamorphosis of Arachnoides placenta (Echinodermata: Echinoidea). Mar Biol 112:445–449

    Article  Google Scholar 

  • Christen R, Schackmann RW, Shapiro BM (1982) Elevation of intracellular pH activates respiration and motility of sperm of the sea urchin, Strongylocentrotus purpuratus. J Biol Chem 257(24):14881–14890

    CAS  Google Scholar 

  • Christen R, Schackmann RW, Shapiro BM (1983a) Metabolism of sea urchin sperm Strongylocentrotus purpuratus. J Biol Chem 258(9):5392–5399

    CAS  Google Scholar 

  • Christen R, Schackmann RW, Shapiro BM (1983b) Interactions between sperm and sea urchin egg jelly. Develop Biol 98:1–14

    Article  CAS  Google Scholar 

  • Christensen AB, Nguyen HD, Byrne M (2011) Thermotolerance and the effects of hypercapnia on the metabolic rate of the ophioroid Ophioneris schayeri: inferences for survival in a changing ocean. J ExpMar 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 

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

    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. PICES Special Publication 3, IOCCP report No. 8

  • 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 373:285–294

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

  • 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 (2011) Combined effects of two ocean change stressors, warming and acidification, on fertilization and early development of the Antarctic echinoid Sterechinus neumayeri. Polar Biol 135:1027–1034

    Google Scholar 

  • Fabricius KE, Langdon C, Uthicke S, Humprey 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. doi:10.1038/NClimate1122

    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

  • Gattuso JP, Lavigne H (2009) Perturbation experiments to investigate the impact of ocean acidification: approaches and software tools. Biogeosci Disc 6:4413–4439

    Article  Google Scholar 

  • Gnaiger E, Gluth G, Weiser W (1978) pH fluctuations in an intertidal beach in Bermuda. Limn Oceanogr 23:851–857

    Article  Google Scholar 

  • Grosberg RK, Cunningham CW (2000) Genetic structure in the sea. From populations to communities. In: Bertness MD, Gaines SD, Hay ME (eds) Marine community ecology. Sinauer Associates, Sunderland, pp 61–84

  • Harley CDG, Hughes AR, Hultgren KM, Miner BG, Sorte CJB, Thornber CS, Rodriguez LF, Tomanek L, Williams SL (2006) The impacts of climate change in coastal marine systems. Ecol Lett 9:228–241

    Article  Google Scholar 

  • Hart MW, Strathmann RR (1994) Functional consequences of phenotypic plasticity in echinoid larvae. Biol Bull 186:291–299

    Article  Google Scholar 

  • Havenhand JN, Buttlet F-R, 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 

  • Havenhand JN, Schlegel P (2009) Near-future levels of ocean acidification do not affect sperm motility and fertilization kinetics in the oyster Crassostrea gigas. Biogeosciences 6:3009–3015

    Google Scholar 

  • Haycock (2004) The reproduction and recruitment of the sand dollar Arachnoides placenta (L.) (Echinoidea: Echinodermata) from differing habitats of the North Queensland coast. Unpublished BSc(Hons Thesis) James Cook University, Australia

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

    Article  CAS  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 

  • 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 

  • Levitan DR, Petersen C (1995) Sperm limitation in the sea. TREE 10:228–231

    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 

  • Martin S, Richier S, Pedrotti M-L, Dupont S, Castejon C, Gerakis C, Kerros M-E, Oberhansli F, Teyssie J-L, Gattuso J-P (2011) Early development and molecular plasticity in the Mediterranean sea urchin Paracentrotus lividus exposed to CO2 driven ocean acidification. J Exp Biol 214:1357–1368

    Article  CAS  Google Scholar 

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

    Google Scholar 

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

    Article  CAS  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 

  • Miner BG (2005) Evolution of feeding structure plasticity in marine invertebrate larvae: a possible trade-off between arm length and stomach size. J Exp Mar Biol Ecol 315:117–125

    Article  Google Scholar 

  • Miner BG, McEdwards LA, McEdwards LR (2005) The relationship between egg size and the duration of the facultative period in marine invertebrate larvae. J Exp Mar Biol Ecol 321:135–144

    Article  Google Scholar 

  • Morita M, Suwa R, Iguchi A, Nakamura M, Shimada K, Sakai K, Suzuki A (2009) Ocean acidification reduces sperm flagellar motility in broadcast spawning reef invertebrates. Zygote 18:103–107

    Article  Google Scholar 

  • Morris S, Taylor AC (1983) Diurnal and seasonal variation in physio-chemical conditions within intertidal rockpools. Est Cont Shelf Sci 17:339–355

    Article  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 Poll Bull 62:48–54

    Article  CAS  Google Scholar 

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

    Article  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 

  • Parker LM, Ross PM, O’Connor WA (2009) The effect of ocean acidification and temperature on the fertilization and embryonic development of the Sydney rock oyster Saccostrea glomeratea (Gould 1850). Glob Change Biol 15:2123–2136

    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 

  • 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 Change Biol 17:163–171

    Article  Google Scholar 

  • Robbins LL, Hansen ME, Kleypas JA, Meylan SC (2010) CO2calc: a user-friendly carbon calculator for windows, Mac OS X, and iOS (iPhone): U.S. geological survey open file report 2010–1280

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

  • 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 

  • 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 

  • Somero GN (2010) The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine ‘winners’ and loosers’. J Exp Biol 213:912–920

    Article  CAS  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 induced development delay. Comp Biochem Physiol 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 Physiol A 160:320–330

    Article  CAS  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

    Article  CAS  Google Scholar 

  • Todgham AE, Hofmann GE (2009) Transcriptomic response of sea urchin larvae Strongylocentrotus purpuratus to CO2-driven seawater acidification. J Exp Biol 212:2579–2594

    Article  CAS  Google Scholar 

  • Truchot JP, Duhamel-Jouve A (1980) Oxygen and carbon dioxide in the marine intertidal environment: diurnal and tidal changes in rockpools. Respir Physiol 39:241–254

    Article  CAS  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, Soars N, Foo S, Byrne M (2012) Physiological effects of increased pCO2 and the effect of parent acclimation on development in the tropical Pacific sea urchin Echinometra mathaei. Mar Biol doi:10.1007/s00227-012-2023-5

  • 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 Chemist 65:291–301

    Article  CAS  Google Scholar 

  • Ward CR, Kopf GS (1993) Molecular events mediating sperm activation. Dev Biol 158:9–34

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank staff at the Australian Institute of Marine Sciences, especially Dr Chris Battershill for hosting MDL during 2010. This research was funded by a University of Otago Research Grant and University of Otago Research and Study Leave grant (MDL) and a grant from the Australian Research Council (MB). Maria J. Gonzalez-Bernat was supported by a New Zealand AID scholarship.

Author information

Author notes

  1. Maria J. Gonzalez-Bernat

    Present address: Marine Biology Association of Guatemala, Guatemala City, Guatemala

Authors and Affiliations

  1. Department of Marine Science, University of Otago, Dunedin, New Zealand

    Maria J. Gonzalez-Bernat & Miles Lamare

  2. Australian Institute of Marine Science, Townsville, QLD, Australia

    Sven Uthicke

  3. Schools of Medical and Biological Sciences, University of Sydney, Sydney, NSW, Australia

    Maria Byrne

Authors
  1. Maria J. Gonzalez-Bernat
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Miles Lamare
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sven Uthicke
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Maria Byrne
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Miles Lamare.

Additional information

Communicated by S. Dupont.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 74.8 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gonzalez-Bernat, M.J., Lamare, M., Uthicke, S. et al. Fertilisation, embryogenesis and larval development in the tropical intertidal sand dollar Arachnoides placenta in response to reduced seawater pH. Mar Biol 160, 1927–1941 (2013). https://doi.org/10.1007/s00227-012-2034-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-012-2034-2

Keywords

Search

Navigation