Abstract
Increased atmospheric CO2 emissions are inducing changes in seawater carbon chemistry, lowering its pH, decreasing carbonate ion availability and reducing calcium carbonate saturation state. This phenomenon, known as ocean acidification, is happening at a faster rate in cold regions, i.e., polar and sub-polar waters. The larval development of Arbacia dufresnei from a sub-Antarctic population was studied at high (8.0), medium (7.7) and low (7.4) pH waters. The results show that the offspring from sub-Antarctic populations of A. dufresnei are susceptible to a development delay at low pH, with no significant increase in abnormal forms. Larvae were isometric between pH treatments. Even at calcium carbonate (CaCO3) saturation states (of both calcite and aragonite, used as proxies of the magnesium calcite) <1, skeleton deposition occurred. Polar and sub-polar sea urchin larvae can show a certain degree of resilience to acidification, also emphasizing A. dufresnei potential to poleward migrate and further colonize southern regions.
References
Allen RM, Marshall DJ (2010) The larval legacy: cascading effects of recruit phenotype on post-recruitment interactions. Oikos 119:1977–1983
Andersson AJ, Mackenzie FT, Bates NR (2008) Life on the margin: implications of ocean acidification on Mg-calcite, high latitude and cold-water marine calcifiers. Mar Ecol Prog Ser 373:265–273
Balch T, Scheibling RE (2001) Larval supply, settlement and recruitment in echinoderms. In: Jangoux M, Lawrence JM (eds) Echinoderm Studies, vol 6. Balkema, The Netherlands, pp 1–83
Barnes DKA, Peck LS (2008) Vulnerability of antarctic shelf biodiversity to predicted regional warming. Clim Res 37:149–163
Bernasconi I (1953) Monografía de los equinoideos argentinos. An Mus Hist Nat, Montevideo, 2ªSerie, 6, pp 1–58
Brögger MI (2005) Biología reproductiva del erizo verde Arbacia dufresnii (Blainville, 1825) en costas del Golfo Nuevo, Patagonia. Tesis de Licenciatura. Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires. Buenos Aires, Argentina
Brögger MI, Martinez MI, Penchaszadeh PE (2004) Reproduction biology of Arbacia dufresnii in Golfo Nuevo, Argentina Sea. In: Lawrence JM, Guzmán O (eds) Sea urchins: Fisheries and ecology. Proceedings of international conference sea urchin fish aquaculture. DEStech Publications, Lancaster, USA, pp 165–169
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
Byrne M, Soars N, Selvakumaraswamy P, Dworjanyn SA, Davis AR (2009b) Sea urchin fertilization in a warm, acidified and high pCO2 ocean across a range of sperm densities. Mar Environ Res 69:234–239
Caldeira K, Wickett ME (2003) Anthropogenic carbon and ocean pH. Nature 425:365
Caldeira K, Wickett ME (2005) Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean. J Geophys Res. doi:10.1029/2004JC002671
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
David B, Choné T, Festeau A, De Ridder C (2005) Synopses of the Antarctic benthos, Vol. 10: Antarctic echinoidea. Koeltz Scientific Books, Königstein
Del Valls TA, Dickson AG (1998) The pH of buffers based on 2-amino-2- hydroxymethyl-1, 3-propanediol (“TRIS”) in synthetic sea water. Deep-Sea Res 1:1541–1554
Dickson AG (1990) Thermodynamics of the dissociation of boric acid in synthetic seawater from 273.15 to 318.15 K. Deep-Sea Res 37:755–766
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
Dickson AG, Sabine CL, Christian JR (2007) Guide to best practices for Ocean CO2 Measurements. PICES Special Publication 3
DOE (1994) Handbook of methods for the analysis of the various parameters of the carbon dioxide system in seawater. Department of Energy, ORNL/CDIAC-74, Version 2
Dubois Ph, Chen CP (1989) Calcification in echinoderms. In: Jangoux M, Lawrence JM (eds) Echinoderm studies, vol 3. A.A. Balkema, Rotterdam, pp 109–178
Dupont S, Olga-Martínez O, Thorndyke M (2010) Impact of near-future ocean acidification on echinoderms. Ecotoxicology 19:449–462
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 fertilization and embryonic development. Mar Biol 157:2689–2702
Fabry VJ, McClintock JB, Mathis JT, Grebmeier JM (2009) Ocean acidification at high latitudes: the bellwether. Oceanography 22:160–171
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
Giménez L (2010) Relationships between habitat conditions, larval traits, and juvenile performance in a marine invertebrate. Ecology 91:1401–1413
Gosselin L, Qian P (1997) Juvenile mortality in benthic marine invertebrates. Mar Ecol Prog Ser 146:265–282
Gran G (1952) Determination of the equivalence point in potentiometric titrages-Part II. Analyst 77:661–671
Hart MW, Strathmann RR (1994) Functional consequences of phenotypic plasticity in echinoid larvae. Biol Bull 186:291–299
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
Hofmann GE, Todgham AE (2010) Living in the now: physiological mechanisms to tolerate a rapidly changing environment. Annu Rev Physiol 72:127–145
Hofmann GE, Barry JP, Edmunds PJ, Gates RD, Hutchins DA, Klinger T, Sewell MA (2010) The effect of ocean acidification on calcifying organisms in marine ecosystems: an organism to ecosystem perspective. Annu Rev Physiol 41:127–147
Intergovernmental Panel on Climate Change (2007) Climate Change 2007: the fourth assessment report of the IPCC. Cambridge University Press, Cambridge
Jara F, Céspedes R (1994) An experimental evaluation of habitat enhancement on homogeneous marine bottoms in southern Chile. Bull Mar Sci 55:295–307
Kino S, Agatsuma Y (2007) Reproduction of the sea urchin Loxechinus albus in Chiloé Island, Chile. Fisheries Sci 73:1265–1273
Kurihara H (2008) Effects of CO2-driven ocean acidification on the early developmental stages of invertebrates. Mar Ecol Prog Ser 373:275–284
Kurihara H, Shirayama Y (2004) Effects of increased atmospheric CO2 on sea urchin early development. Mar Ecol Prog Ser 274:161–169
Lamare M, Barker M (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
Marsh AG, Leong PKK, Manahan DT (1999) Energy metabolism during embryonic development and larval growth of an antarctic sea urchin. J Exp Biol 202:2041–2050
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
Miner B (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
Morse JW, Mackenzie FT (1990) Geochemistry of sedimentary carbonates. Volume 48 Developments in Sedimentology. Elsevier, Amsterdam
Moulin L, Catarino AI, Claessens T, Dubois Ph (2011) Effects of seawater acidification on early development of the intertidal sea urchin Paracentrotus lividus (Lamarck 1816). Mar Pollut Bull 62:48–54
Mutschke E, Ríos C (2006) Distribución espacial y abundancia relativa de equinodermos en el Estrecho de Magallanes, Chile. Ciencia y Tecnología del Mar, Volume 29, número 001 Comité Oceanográfico Nacional Valparaíso, Chile, pp 91–102
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 G-K, Rodgers KB, Sabine CL, Sarmiento JL, Schlitzer R, Slater RD, Totterdell IJ, Weirig M-F, Yamanaka Y, Yool A (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437:681–686
Pechenik JA (2006) Larval experience and latent effects–metamorphosis is not a new beginning. Integr Comp Biol 46:323–333
Pedrotti ML (1993) Spatial and temporal distribution and recruitment of echinoderm larvae in the Ligurian Sea. J Mar Biol Assoc UK 73:513–530
Pedrotti ML, Fenaux L (1992) Dispersal of echinoderm larvae in a geographical area marked by upwelling (Ligurian Sea, NW Mediterranean). Mar Ecol Prog Ser 86:217–227
Penchaszadeh P, Lawrence JM (1999) Arbacia dufresnei (Echinodermata: Echinoidea): a carnivore in Argentinian waters. In: Candia Carnevali MD, Bonasoro F (eds) Echinoderm research. Balkema, Rotterdam, pp 526–530
Pierrot D, Lewis E, Wallace DWR (2006) MS excel program developed for CO2 system calculations. ORNL/CDIAC-105a. Carbon dioxide information analysis center, Oak Ridge National Laboratory. U.S. Department of Energy, Oak Ridge, Tennessee
Pörtner H-O (2008) Ecosystem effects of ocean acidification in times of ocean warming: a physiologist’s view. Mar Ecol Prog Ser 373:203–217
Pörtner H-O, Farrell AP (2008) Physiology and climate change. Science 322:690–692
Ridgwell A, Schmidt DN (2010) Past constraints on the vulnerability of marine calcifiers to massive carbon dioxide release. Nat Geosci 3:196–200
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. PloSone 5(6):e11372. doi:10.1371/journal.pone.0011372
Soars N, Prowse T, Byrne M (2009) Overview of phenotypic plasticity in echinoid larvae, ‘Echinopluteus transversus’ type vs. typical echinoplutei. Mar Ecol Prog Ser 383:113–125
Turley C, Blackford J, Widdicombe S, Lowe D, Nightingale PD, Rees AP (2006) Reviewing the impact of increased atmospheric CO2 on oceanic pH and the marine ecosystem. In: Schellnhuber HJ, Cramer W, Nakicenovic N, Wigley T, Yohe G (eds) Avoiding dangerous climate change 8. Cambridge University Press, UK, pp 65–70
Vaïtilingon D, Morgan R, Grosjean P, Gosselin P, Jangoux M (2001) Effects of delayed metamorphosis and food rations on the perimetamorphic events in the echinoid Paracentrotus lividus (Lamarck, 1816) (Echinodermata). J Exp Mar Biol Ecol 262:41–60
Valdenegro A, Silva N (2003) Physical and chemical oceanographic features of inlets and fjords of southern Chile, between Magellan Strait and Cape Horn (CIMAR 3 FIORDOS). Cienc Tecnol Mar 26:19–60
Vasquez JA, Castilla JC, Santelices B (1984) Distributional patterns and diets of four species of sea urchins in giant kelp forest (Macrocystis pyrifera) of Puerto Toro, Navarino Island, Chile. Mar Ecol Prog Ser 19:55–63
Warnau M, Pagano G (1994) Developmental toxicity of PbCl2 in the echinoid Paracentrotus lividus (Echinodermata). Bull Environ Contam Toxicol 53:434–441
Zaixso HE (2004) Bancos de cholga Aulacomya atra atra (Moulina) (Bivalvia: Mytilidae) del golfo San José (Chubut, Argentina): diversidad y relaciones con facies afines. Revista de Biología Marina y Oceanografía 39:61–78
Acknowledgments
A. I. Catarino holds a FCT grant (SFRH/BD/27947/2006, Portugal). Ph. Dubois is a Senior Research Associate of the NFSR (Belgium). Work supported by FRFC contract 2.4532.07 and Belspo contract SD/BA/02B. The authors are grateful to the Laredo Centre personnel for technical support, to E. Newcombe and C. Cardenas (INACH) for diving support and technical advice, to C. Gimpel and G. Asencio (INACH) for assistance, to P. Gosselin for technical advice. The authors are also thankful to N. Khatri, the reviewers S. Dupont and M. Thorndyke (Sven Lovén Centre for Marine Sciences) and to an anonymous reviewer for helping improving the quality of this work.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Catarino, A.I., De Ridder, C., Gonzalez, M. et al. Sea urchin Arbacia dufresnei (Blainville 1825) larvae response to ocean acidification. Polar Biol 35, 455–461 (2012). https://doi.org/10.1007/s00300-011-1074-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00300-011-1074-2