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Impact of near-future ocean acidification on echinoderms

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Abstract

As a consequence of increasing atmospheric CO2, the world’s oceans are warming and slowly becoming more acidic (ocean acidification, OA) and profound changes in marine ecosystems are certain. Calcification is one of the primary targets for studies of the impact of CO2-driven climate change in the oceans and one of the key marine groups most likely to be impacted by predicted climate change events are the echinoderms. Echinoderms are a vital component of the marine environment with representatives in virtually every ecosystem, where they are often keystone ecosystem engineers. This paper reviews and analyses what is known about the impact of near-future ocean acidification on echinoderms. A global analysis of the literature reveals that echinoderms are surprisingly robust to OA and that important differences in sensitivity to OA are observed between populations and species. However, this is modulated by parameters such as (1) exposure time with rare longer term experiments revealing negative impacts that are hidden in short or midterm ones; (2) bottlenecks in physiological processes and life-cycle such as stage-specific developmental phenomena that may drive the whole species responses; (3) ecological feedback transforming small scale sub lethal effects into important negative effects on fitness. We hypothesize that populations/species naturally exposed to variable environmental pH conditions may be pre-adapted to future OA highlighting the importance to understand and monitor environmental variations in order to be able to to predict sensitivity to future climate changes. More stress ecology research is needed at the frontier between ecotoxicology and ecology, going beyond standardized tests using model species in order to address multiple water quality factors (e.g. pH, temperature, toxicants) and organism health. However, available data allow us to conclude that near-future OA will have negative impact on echinoderm taxa with likely significant consequences at the ecosystem level.

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References

  • Ablanedo N, Gonzàlez H, Ramirez M, Torres I (1990) Evaluación del erizo de mar Echinometra lucunter como indicator de contaminación por metals pesados, Cuba. Aquat Living Resour 3:113–120

    Article  Google Scholar 

  • Agnello M, Filosto S, Scudiero E, Rinaldi AM, Coccheri MC (2007) Cadmium induces an apoptotic response in sea urchin embryos. Cell Stress Chaperones 12:44–50

    Article  CAS  Google Scholar 

  • Anderson S, Hoffmann E, Steward D, Harte J (1990) Ambient toxicity characterization of San Francisco Bay and adjacent wetland ecosystems. LBL Report 29579

  • Barbaglio A, Sugni M, Mozzi D, Invernizzi A, Doria A, Pacchetti G, Tremolada O, Bonasoro F, Candia Carnevali MD (2004) Exposure of organotin compounds (TPT-C1) on regenerative potential of crinoids. In: Heinzeller T, Nebelsick JH (eds) Echinoderms: München. Taylor & Francis group, London, pp 91–95

    Google Scholar 

  • Bay S, Burgess R, Nacci D (1993) Status and applications of Echinoid (Phylum Echinodermata) toxicity test methods. In: Landis WG, Hugues JS, Lewis MA (eds) Environmental Toxicology and Risk Assessment. American Society for Testing and Materials, Philadelphia, pp 281–302

    Chapter  Google Scholar 

  • Bellas J (2008) Prediction and assessment of a mixture toxicity of compounds in antifouling paints. Aquat Toxicol 88:308–315

    Article  CAS  Google Scholar 

  • Bowmer T, Keegan BF (1983) Field survey of the occurrence and significance of regeneration in Amphiura filiformis (Echinodermata: Ophiuroidea) from Galway Bay, west coast of Ireland. Mar Biol 74:65–71

    Article  Google Scholar 

  • Byrne M (1994) Ophiuroidea. In: Harrison FW, Chia FS (eds) Microscopic anatomy of invertebrates, Echinodermata, vol 14. Wiley-Liss Inc, New-York, pp 247–343

    Google Scholar 

  • Byrne M, Ho M, Selvakumaraswamy P, Nguyen HD, Dworjanyn SA, Davis AR (2009a) 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  Google Scholar 

  • Byrne M, Soars N, Selvakumaraswamy P, Dworjanyn SA, David AR (2009b) Sea urchin fertilization in a warm, acidified and high pCO2 ocean across a range of sperm densities. Mar Environ Res doi:10.1016/j.marenvres.2009.10.014

  • Calabrese EJ (2005) Toxicological awakenings: the rebirth of hormesis as a central pillar of toxicology. Toxicol Appl Pharmacology 204:1–8

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Calosi P, Bilton DT, Spicer JI, Atfield A (2008) Thernal tolerance and geographical range size in the Agabus brunneus group of European diving beetles (Coleoptera: Dytiscidae). J Biogeogr 35:295–305

    Google Scholar 

  • Candia Carnevali MD, Bonasoro F, Patruno M, Thorndyke MC, Galassi S (2001a) PCB exposure and regeneration in crinoids (Echinodermata). Mar Ecol Prog Ser 215:155–167

    Article  Google Scholar 

  • Candia Carnevali MD, Galassi S, Bonasoro F, Patruno M, Thorndyke MC (2001b) Regenerative response and endocrine disrupters in crinoid echinoderms: arm regeneration in Antedon mediterranea after experimental exposure to polychlorinated biphenyls. J Exp Biol 204:835–842

    CAS  Google Scholar 

  • Candia Carnevali MD, Bonasoro F, Ferreri P, Galassi S (2003) regenerative potential and effect of exposure to pseudo-estrogenic contaminants (4-nonyphenol) in the crinoids Antedon mediterranea. In: Feral JP, David B (eds) Echinoderm Research 2001. Swets & Zeitlinger, Lisse, pp 201–207

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Cavey MJ, Märkel K (1994) Echinoidea. In: Harrison FW, Chia FS (eds) Microscopic anatomy of invertebrates, Echinodermata, vol 14. Wiley-Liss Inc, New-York, pp 345–400

    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 

  • D’Andrea AF, Stancyk SE, Chandler GT (1996) Sublethal effects of cadmium on arm regeneration in the burrowing brittlestar, Microphiopholis gracillima. Ecotoxicol 5:115–133

    Article  Google Scholar 

  • Dashfield SL, Somerfield P, Widdicombe S, Austen MC, Nimmo M (2008) Impacts of ocean acidification and burrowing urchins on within-sediment pH profiles and subtidal nematode communities. J Exp Mar Biol Ecol 365:46–52

    Article  CAS  Google Scholar 

  • Davoult D, Migné A (2001) Respiration and excretion of a dense Ophiothrix fragilis population in the Bay of Seine (English Channel, France). In: Barker M (ed) Echinoderms 2000. Swets & Zeitlinger, Lisse, pp 243–248

    Google Scholar 

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

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

    Article  Google Scholar 

  • Dulvy NK, Sadovy Y, Reynolds JD (2003) Extinction and vulnerability in marine populations. Fish Fish 4:25–64

    Google Scholar 

  • Dupont S, Thorndyke MC (2006) Growth or differentiation? Adaptative regeneration in the brittlestar Amphiura filiformis. J Exp Biol 209:3873–3881

    Article  Google Scholar 

  • Dupont S, Thorndyke MC (2007) Bridging the regeneration gap: insights from echinoderm models. Nat Rev genetics 8. doi:10.1038/nrg1923-c1

  • Dupont S, Thorndyke MC (2009a) Ocean Acidification and its impact on the early life-history stages of marine animals. In: Briand F (ed) Impacts of acidification on biological, chemical and physical systems in the Mediterranean and Black Seas. N° 36 in CIESM Workshop Monographs. CIESM, Monaco., pp 89–98

    Google Scholar 

  • Dupont S, Thorndyke MC (2009b) Impact of CO2-driven ocean acidification on invertebrates early life-history–what we know, what we need to know and what we can do (Discussion paper). Biogeosciences 6:3109–3131

    Google Scholar 

  • Dupont S, Havenhand J, Thorndyke W, Peck L, Thorndyke M (2008) CO2-driven ocean acidification radically affect larval survival and development in the brittlestar Ophiothrix fragilis. Mar Ecol Prog Ser 373:285–294

    Article  CAS  Google Scholar 

  • Dupont S, Wren J, Ortega-Martinez O, Stumpp M, Melzner F, Thorndyke M (submitted) Impact of CO2-driven ocean acidification on echinoderm larval survival is species-specific and not easy to predict – to a working hypothesis. In: Proceedings of the 13th international echinoderm conference

  • Elkin C, Marshall SJ (2007) Desperate larvae : influence of deferred costs and habitat requirements on habitat selection. Mar Ecol Prog Ser 335:142–153

    Article  Google Scholar 

  • Filisto S, Roccheri M, Bonaventura R, Matranga V (2008) Environmentally relevant cadmium concentrations affect development and induce apoptosis of Paracentrotus lividus larvae cultured in vitro. Cell Biol Toxicol 24:603–610

    Article  CAS  Google Scholar 

  • Freedman B (1995) Environmental ecology: the ecological effects of pollution, disturbance and other stresses, 2nd edn. Academic Press, San Diego

    Google Scholar 

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

    Google Scholar 

  • Gooding RA, Harley CDG, Tang E (2009) Elevated water temperature and carbone dioxide concentration increase the growth of a keystone echinoderm. Proc Natl Acad Sci USA 106:9316–9321

    Article  CAS  Google Scholar 

  • Granberg ME (2004) Role of sediment organic matter quality and benthic organisms for the fate of organic contaminants on marine systems. PhD dissertation, Gothenburg University

  • Gunnarsson JS, Granberg ME, Nilsson HC, Rosenberg R, Hellman B (1999) Influence of sediment-organic matter quality on growth and polychlorobiphenil bioavailability in Echinodermata (Amphiura filiformis). Environ Toxicol Chem 18:1534–1543

    Article  CAS  Google Scholar 

  • 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 ecosysytem effects of ocean acidification. Nature 454:96–99

    Article  CAS  Google Scholar 

  • Hamdoun A, Epel D (2007) Embryo stability and vulnerability in an always changing world. Proc Natl Acad Sci USA 104:1745–1750

    Article  CAS  Google Scholar 

  • Havenhand J, 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 

  • Heinzeller T, Welsch U (1994) Crinoidea. In: Harrison FW, Chia FS (eds) Microscopic anatomy of invertebrates, Echinodermata, vol 14. Wiley-Liss Inc, New-York, pp 9–148

    Google Scholar 

  • Hendriks IE, Duarte CM, Alvarez M (2009) Vulnerability of marine biodiversity to ocean acidification: a meta-analysis. Estuar Coast Shelf Sci doi:10.1016/j.ecss.2009.11.022

  • Hernández OD, Gutièrrez AJ, Gonzàlez-Weller D, Lozano G, Melòn EG, Rubio C, Hardisson A (2009) Accumulation of toxic metals (Pb and Cd) in the sea urchin Diadema aff. antillarum Philippi, 1845, in an oceanic island (Tenerife, Canary Islands). Environ Toxicol doi:10.1002/tox.20487

  • Hyman LH (1955) The invertebrates. Vol IV Echinodermata, McGraw-Hill, New-York

    Google Scholar 

  • Iglesias-Rodrıguez MD, Halloran PR, Rickaby REM, Hall IR, Colmenero-Hidalgo E, Gittins JR, Green DRH, Tyrrell T, Gibbs SJ, von Dassow P, Rehm E, Armbrust EV, Boessenkool KP (2008) Phytoplankton calcification in a high CO2 world. Science 320:336–339

    Article  CAS  Google Scholar 

  • Kassahn KS, Crozier RH, Pörtner HO, Caley MJ (2009) Animal performance and stress: responses and tolerance limits at different levels of biological organization. Biol Rev 84:277–292

    Article  Google Scholar 

  • Kendall MA, Bowman RS, Williamson P, Lewis JR (1985) Annual recruitment of Semibalanus balanoides. Ecology 54:384–390

    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 (2004a) Effects of increased atmospheric CO2 on sea urchin early development. Mar Ecol Prog Ser 274:161–169

    Article  Google Scholar 

  • Kurihara H, Shirayama Y (2004b) Effects of increased atmospheric CO2 and decreased pH on sea urchin embryos and gametes. In: Heinzeller T, Nebelsick JH (eds) Echinoderms: München. Taylor & Francis group, London, pp 31–36

    Google Scholar 

  • Kurihara H, Shimode S, Shirayama Y (2004) Sub-lethal effects of elevated concentration of CO2 on planktonic copepods and sea urchins. J Oceanography 60:743–750

    Article  CAS  Google Scholar 

  • Laegdsgaard P, Byrne M, Anderson DT (1991) Reproduction of sympatric populations of Heliocidaris erythrogramma and H tuberculata (Echinoidea) in New South Wales. Mar Biol 110:359–374

    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 

  • Lefebvre A, Davoult D (1997) Recrutement d’Ophiothrix fragilis (Echinoderme: ophiuride) en Manche orientale: Etude biométrique. J Res Oceanogr 22:109–116

    Google Scholar 

  • Lesser MP, Krusse VA, Barry TM (2003) Exposure to ultraviolet radiation causes apoptosis in developing sea urchin embryos. J Exp Biol 206:4097–4103

    Article  Google Scholar 

  • Lisette Vega R, Epel D (2004) Stress-induced apoptosis in sea urchin embryogenesis. Mar Environ Res 58:799–802

    Article  CAS  Google Scholar 

  • Micael J, Alves MJ, Costa AC, Jones MB (2009) Exploitation and conservation of echinoderms. Oceanog Mar Biol 47:191–208

    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

    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 

  • Mucci A (1983) The solubility of calcite and aragonite in seawater at various salinities, temperatures, and one atmosphere total pressure. Am J Sci 283:780–799

    CAS  Google Scholar 

  • Muus K (1981) Density and growth of juvenile Amphiura filiformis (Ophiuroidea) in the Oresund. Ophelia 20:153–168

    Google Scholar 

  • Novelli AA, Argese E, Tagliapietre D, Bettiol C, Volpi Ghirardini A (2002) Toxicity of tributyltin and triphenyltin to early life-styles of Paracentrotus lividus (Echinodermata: Echinoidea). Environ Toxicol Chem 21:859–864

    Article  CAS  Google Scholar 

  • O’Donnell MJ, Hammond LM, Hofmann GF (2009) Predicted impact of ocean acidification on a marine invertebrate: elecated CO2 alters response to thermal stress in sea urchin larvae. Mar Biol 156:439–446

    Article  CAS  Google Scholar 

  • O’Neill P (1989) Structure and mechanics of starfish body wall. J Exp Biol 147:53–89

    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 

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

    Article  Google Scholar 

  • Pennington JT, Strathmann RR (1990) Consequences of the calcite skeletons of planktonic echinoderm larvae for orientation, swimming, and shape. Biol Bull 179:121–133

    Article  Google Scholar 

  • Politi Y, Arod T, Klein E, Weiner S, Addadi L (2004) Sea urchin spine calcite forms via a transient amorphous calcite carbonate phase. Science 306:1161–1164

    Article  CAS  Google Scholar 

  • Pörtner HO, Dupont S, Melzner F, Storch D, Thorndyke M (2010) Studies of metabolic and other characters across life stages. In: Guide for best practices in ocean acidification research and data reporting. Available via EPOCA. http://www.epoca-project.eu/

  • Riebesell U, Zondervan I, Rost B, Tortell PD, Zeebe RE, Morel FMM (2000) Reduced calcification of marine plankton in response to increased atmospheric CO2. Nature 407:364–367

    Article  CAS  Google Scholar 

  • Ries JB, Cohen AL, McCorkle DC (2009) Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 37:1131–1134

    Article  CAS  Google Scholar 

  • Royal Society (2005) Ocean acidification due to increasing atmospheric carbon dioxide. Policy Document 12/05, The Royal Scoety, London

  • Ruttimann J (2006) Sick seas. Nature 442:978–980

    Article  CAS  Google Scholar 

  • Selck H, Granberg ME, Forbes VE (2004) Impact of sediment organic matter quality on the fate and effects of fluoranthene in the infaunal brittle star Amphiura filiformis. Mar Environ Res 59:19–46

    Article  CAS  Google Scholar 

  • Serafy DK, Fell FJ (1985) Marine flora and fauna of the Northeastern United States. Echinodermata: Echinoidea. NOAA Technical Report NMFS 33

  • Shirayama Y, Thornton H (2005) Effect of increased atmospheric CO2 on shallow water marine benthos. J Geophys Res 110, doi:10.1029/2004JC002618

  • Sköld M, Rosenberg R (1996) Arm regeneration frequency in eight species of ophiuroidea (Echinodermata) from European sea areas. J Sea Res 35:353–362

    Article  Google Scholar 

  • Smiley S (1994) Holothuroidea. In: Harrison FW, Chia FS (eds) Microscopic anatomy of invertebrates, Echinodermata, vol 14. Wiley-Liss Inc, New-York, pp 410–471

    Google Scholar 

  • Sørensen JG, Kristensen TN, Loeschcke V (2003) The evolutionary and ecological role of heat shock proteins. Ecol Lett 6:1025–1037

    Article  Google Scholar 

  • Sugni M, Mozzi D, Barbaglio A, Bonasoro F, Candia Carnevali MD (2007) Endocrine disrupting compounds and echinoderms: new ecotoxicological sentinels for the marine ecosystem. Ecotoxicology 16:95–108

    Article  CAS  Google Scholar 

  • Taban IC, Bechmann RK, Torgrimsen S, Baussant T, Sanni S (2004) Detection of DNA damage in mussels and sea urchins exposed to crude oil using comet assay. Mar Environ Res 58:701–705

    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 

  • Van Straalen NM (2003) Ecotoxicology becomes stress ecology. Environ Sci Technol 324–330

  • Walsh GE, McLaughlin LL, Louie MK, Deans CH, Lores EM (1986) Inhibition of arm regeneration by Ophioderma brevispina (Echinodermata: Ophiuroidea) by tributyltin oxide and triphenyltin oxide. Ecotoxicol Environ Saf 12:95–100

    Article  CAS  Google Scholar 

  • Warner GF (1971) On the ecology of a dense bed of the brittlestar Ophiothrix fragilis. J Mar Biol Assoc UK 55:199–210

    Google Scholar 

  • Whooten JT, Pfister CA, Forester JD (2008) Dynamic patterns and ecological impacts of declining ocean pH in a high resolution multi-year dataset. Proc Natl Acad Sci USA 105:18848–18853

    Article  Google Scholar 

  • Widdicombe S, Dupont S, Thorndyke M (2010) Laboratory experiments and benthic mesocosm studies. In: Guide for best practices in ocean acidification research and data reporting. Available via EPOCA. http://www.epoca-project.eu/

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

    Article  Google Scholar 

  • Wood HL, Widdicombe S, Spicer JI (2009) The influence of hypercapnia and the infaunal brittlestar Amphiura filiformis on sediment nutrient flux–will ocean acidification affect nutrient exchange? Biogeosciences 6:2015–2024

    Article  CAS  Google Scholar 

  • Zalasiewicz J, Williams M, Smith A, Barry TL, Coe AL, Bown PR, Brenchley P, Cantrill D, Gale A, Gibbard P, Gregory FJ, Hounslow MW, Kerr AC, Pearson P, Knox R, Powell J, Waters C, Marshall J, Oates M, Rawson P, Stone P (2008) Are we now living in the Anthropocene. GSA Today 18:4–8

    Article  Google Scholar 

  • Zito F, Costa C, Sciarrino S, Cavalcante C, Poma V, Matranga V (2005) Cell adhesion and communication: a lesson from echinoderm embryos for the exploitation of new therapeutic tools. Prog Mol Subcell Biol 39:7–44

    Article  CAS  Google Scholar 

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Acknowledgments

This work was performed within the Linnaeus Centre for Marine Evolutionary Biology at the University of Gothenburg (http://www.cemeb.science.gu.se/), and supported by a Linnaeus-grant from the Swedish Research Councils VR and Formas and the Royal Swedish Academy of Sciences. This paper is a contribution to the “European Project on Ocean Acidification” (EPOCA) which received funding from the European Community’s Seventh Framework Programme (FP7/2007-2013) under grant agreement N211384. The authors also thank Knut & Alice Wallenbergs Stiftelsen, BAS Q4 BIOREACH/BIOFLAME core program for financial support and EMBO for a long term fellowship to OO.

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Dupont, S., Ortega-Martínez, O. & Thorndyke, M. Impact of near-future ocean acidification on echinoderms. Ecotoxicology 19, 449–462 (2010). https://doi.org/10.1007/s10646-010-0463-6

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