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Acid–base balance and metabolic response of the sea urchin Paracentrotus lividus to different seawater pH and temperatures

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Abstract

Purpose

In order to better understand if the metabolic responses of echinoids could be related to their acid–base status in an ocean acidification context, we studied the response of an intertidal sea urchin species, Paracentrotus lividus, submitted to low pH at two different temperatures.

Methods

Individuals were submitted to control (8.0) and low pH (7.7 and 7.4) at 10°C and 16°C (19 days). The relation between the coelomic fluid acid–base status, the RNA/DNA ratio of gonads and the individual oxygen uptake were studied.

Results

The coelomic fluid pH decreased with the aquarium seawater, independently of temperature, but this explained only 13% of the pH variation. The coelomic fluid showed though a partial buffer capacity that was not related to skeleton dissolution ([Mg2+] and [Ca2+] did not differ between pH treatments). There was an interaction between temperature and pH on the oxygen uptake (V O2) which was increased at pH 7.7 and 7.4 at 10°C in comparison with controls, but not at 16°C, indicating an upregulation of the metabolism at low temperature and pH. However, gonad RNA/DNA ratios did not differ according to pH and temperature treatments, indicating that even if maintenance of physiological activities has an elevated metabolic cost when individuals are exposed to stress, they are not directly affected during short-term exposure. Long-term studies are needed in order to verify if gonad production/growth will be affected by low pH seawaters exposure.

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References

  • Ahearn GA, Franco P (1991) Electrogenic 2Na+/H+ antiport in echinoderm gastrointestinal epithelium. J Exp Biol 158:495–507

    Google Scholar 

  • Ali F, Nakamura K (2000) Metabolic characteristics of the Japanese clam Ruditapes philippinarum (Adams and Reeve) during aerial exposure. Aquac Res 31:157–165

    Article  Google Scholar 

  • Bamford DR (1982) Epithelial absorption. In: Jangoux M, Lawrence JM (eds) Echinoderm nutrition. Balkema, Rotterdam

    Google Scholar 

  • Belchier M, Clemmesen D, Cortes D, Doan T, Folkvord A, Garcia A, Geffen AJ, Høie H, Johannessen A, Moksness E, de Pontual H, Rámirez T, Schnack D, Sveinsbø B (2004) Recruitment studies: manual on precision and accuracy of tools. International Council for the Exploration of the Sea Techniques in Marine Environmental Sciences Report Series ICES, Copenhagen

    Google Scholar 

  • Binyon J (1966) Salinity tolerance and ionic regulation. In: Boolootian R (ed) Physiology of Echinodermata. Interscience Publishers, New York

    Google Scholar 

  • Bishop CD, Lee KJ, Watts SA (1994) A comparison of osmolality and specific ion concentrations in the fluid compartments of the regular sea urchin Lytechinus variegatus Lamarck (Echinodermata: Echinoidea) in varying salinities. Comp Biochem Physiol 108A:497–502

    Article  CAS  Google Scholar 

  • Bookbinder LH, Shick JM (1986) Anaerobic and aerobic energy metabolism in ovaries of the sea urchin Strongylocentrotus droebachiensis. Mar Biol 93:103–110

    Article  CAS  Google Scholar 

  • Boudouresque CF, Verlaque M (2001) Ecology of Paracentrotus lividus. In: Lawrence JM (ed) Edible Sea Urchins: Biology and Ecology. Elsevier, Amsterdam

    Google Scholar 

  • Brockington S, Clarke A (2001) The relative influence of temperature and food on the metabolism of a marine invertebrate. J Exp Mar Biol Ecol 258:87–99

    Article  Google Scholar 

  • Burnett L, Terwilliger N, Carroll A, Jorgensen D, Scholnick D (2002) Respiratory and acid–base physiology of the purple sea urchin, Strongylocentrotus purpuratus, during air exposure: presence and function of a facultative lung. Biol Bull 203:42–50

    Article  Google Scholar 

  • Caldarone EM, Wagner M, Onge-Burns JS, Buckley LJ (2001) Protocol and guide for estimating nucleic acids in larval fish using a fluorescence microplate reader. Reference Document 01-11. Northeast Fisheries Science Center, Woods Hole

    Google Scholar 

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

    Article  CAS  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. doi:10.1029/2004JC002671

  • Catarino AI, Cabral HN, Peeters K, Pernet P, Punjabi U, Dubois Ph (2008) Metal concentrations, sperm motility, and RNA/DNA ratio in two echinoderm species from a highly contaminated fjord (the Sørfjord, Norway). Environ Toxicol Chem 27:1553–1560

    Article  CAS  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. doi:10.1016/j.jembe.2011.04.002

  • 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

    Google Scholar 

  • Dickson AG (1990) Thermodynamics of the dissociation of boric-acid in potassium-chloride solutions form 273.15 K to 318.15 K. J Chem Thermodynam 22:113–127

    Article  CAS  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

  • Diehl WJ (1986) Osmoregulation in echinoderms. Comp Biochem Physiol A 84:199–205

    Article  Google Scholar 

  • Dissanayake A, Clough R, Spicer JI, Jones MB (2010) Effects of hypercapnia on acid–base balance and osmo-iono-regulation in prawns (Decapoda: Palaemonidae). Bull Aquat Biol 11:27–36

    Article  Google Scholar 

  • 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

  • Doncaster CP, Davey AJH (2007) Analysis of variance and covariance, how to chose and construct models for the life sciences. Cambridge University Press, Cambridge

    Book  Google Scholar 

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

    Article  Google Scholar 

  • Dowben RM (1971) Cell biology. Herper & Row Publishers, New York

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Elligton WR (1982) Intermediary metabolism. In: Jangoux M, Lawrence JM (eds) Echinoderm nutrition. A. A. Balkema, Rotterdam

    Google Scholar 

  • Fabry VJ, Seibel BA, Feely RA, Orr JC (2008) Impacts of ocean acidification on marine fauna and ecosystem processes. ICES J Mar Sci 65:414–432

    Article  CAS  Google Scholar 

  • Farmanfarmaian A (1966) The respiratory physiology of the echinoderms. In: Boolootian RA (ed) Physiology of echinodermata. Interscience Publishers, USA

    Google Scholar 

  • Ferguson JC (1990) Hyperosmotic properties of the fluids of the perivisceral coelom and water vascular system of starfish kept under stable conditions. Comp Biochem Physiol A 95:245–248

    Article  Google Scholar 

  • Gellhorn E (1927) Vergleichend-physiologische Untersuchungen über die Pufferungspotenz von Blut und Körpersäften—I. Mitteilung. Pflügers Archiv für die Gesamte Physiologie des Menschen und der Tiere 216(1):253–266

    Article  CAS  Google Scholar 

  • Gooding RA, Harley CDG, Tang E (2009) Elevated water temperature and carbon dioxide concentration increase the growth of a keystone echinoderm. PNAS 106:9316–9321

    Article  CAS  Google Scholar 

  • Gran G (1952) Determination of the equivalence point in potentiometric titrages—part II. Analyst 77:661–671

    Article  CAS  Google Scholar 

  • Grosjean Ph, Spirlet C, Jangoux M (1996) Experimental study of growth in the echinoid Paracentrotus lividus (Lamarck, 1816) (Echinodermata). J Exp Mar Biol Ecol 201:173–184

    Article  Google Scholar 

  • Grosjean PH, Spirlet C, Gosselin P, Vaïtilingon D, Jangoux M (1998) Land-based, closed-cycle echiniculture of Paracentrotus lividus (Lamarck) (Echinoidea: Echinodermata): a long-term experiment at a pilot scale. J Shellfish Res 17:1523–1531

    Google Scholar 

  • Guppy M, Withers P (1999) Metabolic depression in animals: physiological perspectives and biochemical generalizations. Biol Rev 74:1–40

    Article  CAS  Google Scholar 

  • Harrison JF, Wong CJH, Phillips JE (1990) Haemolymph buffering in the locust Schistocerca gregaria. J Exp Biol 154:573–579

    Google Scholar 

  • Heisler N (1986) Buffering and transmembrane ion transfer processes. In: Heisler N (ed) Acid-base regulation in animal. Elsevier Science, Amsterdam

    Google Scholar 

  • Heisler M (1989) Interactions between gas exchange, metabolism, and ion transport in animals: an overview. Can J Zool 67:2923–2935

    Article  CAS  Google Scholar 

  • Hiestand W (1940) Oxygen consumption of Thyone briareus (Holothuroidea) as a function of oxygen tension and hydrogen ion concentration of surrounding medium. Trans Wis Acad Sci Arts Lett 32:167–174

    CAS  Google Scholar 

  • Himmelman JH, Guderley H, Vignault G, Drouin G, Wells PG (1984) Response of the sea urchin, Strongylocentrotus droebachiensis, to reduced salinities: importance of size, acclimation, and interpopulation differences. Can J Zool 62:1015–1021

    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  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Holland LZ, Giese AC, Phillips JH (1967) Studies on the perivisceral coelomic fluid protein concentration during seasonal and nutritional changes in the purple sea urchin. Comp Biochem Physiol 21:361–371

    Article  CAS  Google Scholar 

  • Hughes AD, Kelly MS, Barnes DK, Catarino AI, Black KD (2006) The dual functions of sea urchin gonads are reflected in the temporal variations of their biochemistry. Mar Biol 148:789–798

    Article  Google Scholar 

  • IPCC (2007) Climate Change 2007: the fourth assessment report of the IPCC. Cambridge University Press, Cambridge. ISBN 0521705975

    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 

  • Lawrence JM (1990) The effect of stress and disturbance on echinoderms. Zool Sci 7:17–28

    Google Scholar 

  • Lawrence JM, Lane JM (1982) The utilization of nutrients by postmetamorphic echinoderms. In: Jangoux M, Lawrence JM (eds) Echinoderm Nutrition. A. A. Balkema, Rotterdam

    Google Scholar 

  • Liyana-Pathirana C, Shahidi F, Whittick A, Hooper R (2002) Effect of season and artificial diet on amino acids and nucleic acids in gonads of green sea urchin Strongylocentrotus droebachiensis. Comp Biochem Physiol A 133:389–398

    Article  Google Scholar 

  • McPherson BC (1968) Feeding and oxygen uptake of the tropical sea urchin, Eucidari tribuloides (Lamarck). Bio Bull 132:308–321

    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 

  • Michaelidis B, Ouzounis C, Paleras A, Pörtner H (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

    Article  CAS  Google Scholar 

  • Moore HB (1966) Ecology of echinoids. In: Boolootian R (ed) Physiology of Echinodermata. Interscience Publishers, New York

    Google Scholar 

  • Morris S, Taylor AC (1983) Diurnal and seasonal variation in physico-chemical conditions within intertidal rock pools. Estuar Coast Shelf Sci 17:339–355

    Article  Google Scholar 

  • Pane E, Barry J (2007) Extracellular acid–base regulation during short-term hypercapnia is effective in a shallow-water crab, but ineffective in a deep-sea crab. Mar Ecol Prog Ser 334:1–9

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Reipschläger A, Pörtner H-O (1996) Metabolic depression during environmental stress: the role of extracellular versus intracellular pH in Sipunculus nudus. J Exp Biol 199:1801–1807

    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 

  • Sabourin TD, Stickle WB (1981) Effects of salinity on respiration and nitrogen excretion in two species of echinoderms. Mar Biol 65:91–99

    Article  CAS  Google Scholar 

  • Santos-Gouvea IA, Freire CA (2007) Effects of hypo- and hypersaline seawater on the microanatomy and ultrastructure of epithelial tissues of Echinometra lucunter (Echinodermata: Echinoidea) of intertidal and subtidal populations. Zool Stud 46:203–215

    Google Scholar 

  • Sarch MN (1932) Die Pufferung Der Körperflüssigkeiten Bei Echinodermen. J Comp Physiol A 14:525–545

    Google Scholar 

  • Schäfer S, Abele D, Weihe E, Köhler A (2011) Sex-specific biochemical and histological differences in gonads of sea urchins (Psammechinus miliaris) and their response to phenanthrene exposure. Mar Environ Res 71:70–78

    Article  Google Scholar 

  • Seibel BA, Walsh PJ (2003) Biological impacts of deep-sea carbon dioxide injection inferred from indices of physiological performance. J Exp Biol 206:641–650

    Article  CAS  Google Scholar 

  • Shick JM (1983) Respiratory gas exchange in echinoderms. In: Jangoux M, Lawrence JM (eds) Echinoderms studies 1. Balkema, Rotterdam

    Google Scholar 

  • Shirayama Y, Thornton H (2005) Effect of increased atmospheric CO2 on shallow water marine benthos. J Geophys Res C 110:1–7

    Article  Google Scholar 

  • Siikavuopio SI, Mortensen A (2008) Effects of body weight and temperature on feed intake, gonad growth and oxygen consumption in green sea urchin, Strongylocentrotus droebachiensis. Development 281:77–82

    Google Scholar 

  • Siikavuopio S, 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 

  • Spicer JI (1995) Oxygen and acid–base status of the sea urchin. Mar Biol 124:71–76

    Article  Google Scholar 

  • Spicer JI, Taylor AC, Hill AD (1988) Acid–base status in the sea urchins Psammechinus miliaris and Echinus esculentus (Echinodermata: Echinoidea) during emersion. Mar Biol 534:527–534

    Article  Google Scholar 

  • Stickle WB, Diehl WJ (1987) Effects of salinity on echinoderms. In: Jangoux M, Lawrence JM (eds) Echinoderm studies, vol 2. A.A. Balkema, Rotterdam

    Google Scholar 

  • Talbot T, Lawrence JM (2002) The effect of salinity on respiration, excretion, regeneration and production in Ophiophragmus filograneus (Echinodermata: Ophiuroidea). J Exp Mar Biol Ecol 275:1–14

    Article  Google Scholar 

  • Truchot JP (1988) Problems of acid–base balance in rapidly changing intertidal environments. Integr Comp Biol 28:55–64

    Article  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 

  • Ulbricht RJ, Pritchard AW (1972) Effect of temperature on the metabolic rate of sea urchins. Biol Bull Mar Biol Lab Woods Hole 142:178–185

    Article  Google Scholar 

  • Vidolin D, Santos-Gouvea IA, Freire CA (2007) Differences in ion regulation in the sea urchins Lytechinus variegatus and Arbacia lixula (Echinodermata: Echinoidea). J Mar Biol Ass UK 87:769–775

    Article  CAS  Google Scholar 

  • Whiteley NM, Scott JL, Breeze SJ, McCann L (2001) Effects of water salinity on acid–base balance in decapod crustaceans. J Exp Biol 204:1003–1011

    CAS  Google Scholar 

  • 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, 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 

  • Wood HL, Spicer JI, Kendall MA, Lowe DM, Widdicombe S (2011) Ocean warming and acidification; implications for the Arctic brittlestar Ophiocten sericeum. Polar Biol. doi:10.1007/s00300-011-0963-8

  • Zar JH (2005) Biostatistical analysis, 5th edn. Pearson Prentice-Hall, New Jersey

    Google Scholar 

  • Zhuang Z, Duerr JM, Ahearn GA (1995) Antiporter in echinoderm gastrointestinal epithelium. J Exp Biol 1217:1207–1217

    Google Scholar 

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Acknowledgements

A. I. Catarino holds a FCT grant (Fundação para a Ciência e Tecnologia, SFRH/BD/27947/2006, Portugal). Ph. Dubois is a Senior Research Associate of the NFSR (Belgium). Work supported by FRFC (Fonds pour la Recherche Fondamentale Collective de Belgique) contract 2.4532.07 and Belspo contract SD/BA/02B. The authors are grateful to A. Borges (ULG), for TRIS-AMP buffers supply, and to T. Dupont, S.M. Zoudi, Ph. Pernet and L. Geerts (ULB) for technical support. Further acknowledgements to N. Dahkani (MRAC) for IPC-AES analysis, C.P. Doncaster (University of Southampton) for statistical advice, and C. Moureaux, C. De Ridder, Prof. Jangoux (ULB), and Prof. Heisler (H-U Berlin) for theoretical advice.

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  1. Laboratoire de Biologie Marine, Université Libre de Bruxelles, CP 160/15, 1050, Brussels, Belgium

    Ana I. Catarino, Mathieu Bauwens & Philippe Dubois

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  1. Ana I. Catarino
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Correspondence to Ana I. Catarino.

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Catarino, A.I., Bauwens, M. & Dubois, P. Acid–base balance and metabolic response of the sea urchin Paracentrotus lividus to different seawater pH and temperatures. Environ Sci Pollut Res 19, 2344–2353 (2012). https://doi.org/10.1007/s11356-012-0743-1

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