Advertisement

Environmental Science and Pollution Research

, Volume 21, Issue 23, pp 13602–13614 | Cite as

Acid–base physiology response to ocean acidification of two ecologically and economically important holothuroids from contrasting habitats, Holothuria scabra and Holothuria parva

  • Marie CollardEmail author
  • Igor Eeckhaut
  • Frank Dehairs
  • Philippe Dubois
Research Article

Abstract

Sea cucumbers are dominant invertebrates in several ecosystems such as coral reefs, seagrass meadows and mangroves. As bioturbators, they have an important ecological role in making available calcium carbonate and nutrients to the rest of the community. However, due to their commercial value, they face overexploitation in the natural environment. On top of that, occurring ocean acidification could impact these organisms, considered sensitive as echinoderms are osmoconformers, high-magnesium calcite producers and have a low metabolism. As a first investigation of the impact of ocean acidification on sea cucumbers, we tested the impact of short-term (6 to 12 days) exposure to ocean acidification (seawater pH 7.7 and 7.4) on two sea cucumbers collected in SW Madagascar, Holothuria scabra, a high commercial value species living in the seagrass meadows, and H. parva, inhabiting the mangroves. The former lives in a habitat with moderate fluctuations of seawater chemistry (driven by day–night differences) while the second lives in a highly variable intertidal environment. In both species, pH of the coelomic fluid was significantly negatively affected by reduced seawater pH, with a pronounced extracellular acidosis in individuals maintained at pH 7.7 and 7.4. This acidosis was due to an increased dissolved inorganic carbon content and pCO2 of the coelomic fluid, indicating a limited diffusion of the CO2 towards the external medium. However, respiration and ammonium excretion rates were not affected. No evidence of accumulation of bicarbonate was observed to buffer the coelomic fluid pH. If this acidosis stays uncompensated for when facing long-term exposure, other processes could be affected in both species, eventually leading to impacts on their ecological role.

Keywords

Sea cucumbers Holothuria parva Holothuria scabra Ocean acidification Acid–base regulation Echinoderms 

Notes

Acknowledgments

M. Collard is holder of a Belgian FRIA grant. Ph. Dubois is a research director of the National Fund for Scientific Research (FRS-FNRS; Belgium). We thank the “Institut Halieutique et des Sciences Marines” of Toliara, Madagascar and the staff of the institution for their welcome and help, particularly, R. Rasoloforinina, G. Todinanahary and G. Tsiresy. We thank the FRS-FNRS for the travel grant to Madagascar. We would also like to thank Professor L. Chou for providing the TRIS and AMP buffers, C. Massin for determining the holothurian Holothuria parva, M. Schaltz for field measurements and G. Seghers, G. Caulier and B. Danis for their help and support during the experiments. Finally, we thank D. Verstraeten and N. Brion for their help with the analyses.

Supplementary material

11356_2014_3259_MOESM1_ESM.pdf (15 kb)
ESM 1 (PDF 15 kb)
11356_2014_3259_MOESM2_ESM.pdf (20 kb)
ESM 2 (PDF 19 kb)

References

  1. Anderson SC, Flemming JM, Watson R, Lotze HK (2011a) Serial exploitation of global sea cucumber fisheries. Fish Fish 12:317–339CrossRefGoogle Scholar
  2. Anderson SC, Flemming JM, Watson R, Lotze HK (2011b) Rapid global expansion of invertebrate fisheries: trends, drivers and ecosystem effects. PLoS One 6:e14735CrossRefGoogle Scholar
  3. Apostolaki ET, Vizzini S, Hendriks I, Olsen YS (2014) Seagrass ecosystem response to long-term high CO2 in a Mediterranean volcanic vent. Mar Environ Res. doi: 10.1016/j. marenvres.2014.05.008 Google Scholar
  4. Appelhans YS, Thomsen J, Pansch C, Melzner F, Wahl M (2012) Sour times: seawater acidification effects on growth, feeding behaviour and acid–base status of Asterias rubens and Carcinusmaenas. Mar EcolProgSer 459:85–97Google Scholar
  5. Caldeira K, Wickett M (2003) Anthropogenic carbon and ocean pH. Nature 425:365CrossRefGoogle Scholar
  6. Caldeira K, Wickett M (2005) Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean. J Geophys Res 110:C09S04Google Scholar
  7. Cherbonnier G (1988) Echinoderms: Holothuroids. Faune de Madagascar 70:1–292 (in French)Google Scholar
  8. 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 156:347–365CrossRefGoogle Scholar
  9. Clarke A (1998) Temperature and energetics: an introduction to cold ocean physiology. In: Pörtner HO, Playle RC (eds) Society for experimental biology, seminar series: 66, cold ocean physiology. Cambridge University Press, New York, pp 365–390Google Scholar
  10. Collard M, Laitat K, Moulin L, Catarino A, Grosjean P, Dubois P (2013a) Buffer capacity of the coelomic fluid in echinoderms. Comp Biochem Phys A 166:199–206CrossRefGoogle Scholar
  11. Collard M, Catarino A, Bonnet S, Flammang P, Dubois P (2013b) Effects of CO2-induced ocean acidification on physiological and mechanical properties of the starfish Asterias rubens. J Exp Mar Biol Ecol 446:355–362CrossRefGoogle Scholar
  12. Collard M, Dery A, Dehairs F, Dubois P (2014) Echinoidea and Cidaroidea respond differently to ocean acidification. Comp Biochem Phys A174:45–55CrossRefGoogle Scholar
  13. Conand C (2008) Population status, fisheries and trade of sea cucumbers in Africa and the Indian Ocean. In: Toral-Granda V, Lovatelli A, Vasconcellos M (eds) Sea cucumbers. A global review of fisheries and trade. FAO Fisheries and Aquaculture Technical Paper, No. 516. FAO, Rome, pp 143–193Google Scholar
  14. Delroisse J, Fourgon D, Eeckhaut I (2013) Reproductive cycles and recruitment in Ophiomastix venosa and Ophiocoma scolopendrina, two co-existing tropical ophiuroids from the barrier reef of Tolaria (Madagascar). Cah Biol Mar 54:593–603Google Scholar
  15. DelValls TA, Dickson AG (1998) The pH of buffers based on 2-amino-2-hydroxymethyl-1,3-propanediol (‘tris’) in synthetic seawater. Deep-Sea Res 45:1541–1554CrossRefGoogle Scholar
  16. Dickson AG (1990) Standard potential of the reaction AgCls + ½ H2 = Ags + HClAq and the standard acidity constant of the ion HSO4 in synthetic sea-water from 273.15-K to 318.15-K. J Chem Thermodyn 22:113–127CrossRefGoogle Scholar
  17. Dickson AG, Millero FJ (1987) A comparison of the equilibrium-constants for the dissociation of carbonic-acid in seawater media. Deep-Sea Res 34:1733–1743CrossRefGoogle Scholar
  18. Doncaster CP, Davey AJ (2007) Analysis of variance and covariance. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  19. Dupont S, Thorndyke M (2012) Relationship between CO2-driven changes in extracellular acid–base balance and cellular immune response in two polar echinoderm species. J Exp Mar Biol Ecol 424–425:32–37CrossRefGoogle Scholar
  20. Dupont S, Ortega-Martinez O, Thorndyke M (2010) Impact of near-future ocean acidification on echinoderms. Ecotoxicology 19:449–462CrossRefGoogle Scholar
  21. Eeckhaut I, Lavitra T, Rasoforinina R, Rabenevanana MW, Gildas P, Jangoux M (2008) Madagascar Holothurie SA: the first trade company based on sea cucumber aquaculture in Madagascar. SPC Beche-de-mer Information Bull 28:22–23Google Scholar
  22. Eriksson H, Robinson G, Slater M, Troell M (2012) Sea cucumber aquaculture in the Western Indian Ocean: Challenges for sustainable livelihood and stock improvement. AMBIO 41:103–121CrossRefGoogle Scholar
  23. Farmanfarmaian A (1966) The respiratory physiology of Echinoderms. In: Boolootian RA (ed) Physiology of echinodermata. Interscience, New York, pp 245–266Google Scholar
  24. Gillikin DP, Bouillon S (2007) Determination of δ18O of water and δ13C of dissolved inorganic carbon using a simple modification of an elemental analyzer-isotope ratio mass spectrometer (EA-IRMS): an evaluation. Rapid Commun Mass Spectrom 21:1475–1478CrossRefGoogle Scholar
  25. Gillikin DP, Lorrain A, Meng L, Dehairs F (2007) A large metabolic contribution to the δ13C record in marine aragonitic bivalve shells. Geochim Cosmochim Acta 71:2936–2946CrossRefGoogle Scholar
  26. Gran G (1952) Determination of the equivalence point in potentiometric titrations: Part II. Analyst 77:661–671CrossRefGoogle Scholar
  27. Hamel JF, Conand C, Pawson DL, Mercier A (2001) The sea cucumber Holothuria scabra (Holothuroidea: Echinodermata): its biology and exploitation as beche-de-mer. Adv Mar Biol 41:129–223CrossRefGoogle Scholar
  28. Hammond LS (1981) An analysis of grain size modification in biogenic carbonate sediments by deposit-feeding holothurians and echinoids (Echinodermata). Limnol Oceanogr 26:898–906CrossRefGoogle Scholar
  29. Hendriks IE, Olsen YS, Ramajo L, Basso L, Steckbauer A, Moore TS, Howard J, Duarte CM (2014) Photosynthetic activity buffers ocean acidification. Biogeosciences 11:333–346CrossRefGoogle Scholar
  30. Hofmann GE, Smith JE, Johnson KS et al (2011) High-frequency dynamics of ocean pH: a mutli-ecosystem comparison. PLoS One 6:e28983CrossRefGoogle Scholar
  31. Holtmann WC, Stumpp M, Gutowska M, Syré S, Himmerkus N, Melzner F, Bleich M (2013) Maintenance of coelomic fluid pH in sea urchins exposed to elevated CO2: the role of body cavity epithelia and stereom dissolution. Mar Biol 160:2631–2645CrossRefGoogle Scholar
  32. Invers O, Romero J, Perez M (1997) Effects of pH on seagrass photosynthesis: a laboratory and field assessment. Aquat Bot 59:185–194CrossRefGoogle Scholar
  33. Jansen H, Ahrens MJ (2004) Carbonate dissolution in the guts of benthic deposit feeders: a numerical model. Geochim Cosmochim Acta 68:4077–4092CrossRefGoogle Scholar
  34. Langenbuch M, Pörtner HO (2002) Changes in the metabolic rate and N excretion in the marine invertebrate Sipunculus nudus under conditions of environmental hypercapnia: identifying effective of acid–base variables. J Exp Biol 205:1153–1160Google Scholar
  35. Lavitra T, Vaïtilingon D, Rasolofonirina R, Eeckhaut I (2006) Seasonal abundance of sea cucumber larvae at Toliara Great Reef, Madagascar. SPC Beche-de-mer Information Bull 24:35–38Google Scholar
  36. Lawrence J (1987) A functional biology of Echinoderms. Croom Helm Ltd, BeckenhamGoogle Scholar
  37. Lovelock CE, Ellison J (2007) Vulnerability of mangroves and tidal wetlands of the Great Barrier Reef to climate change. In: Johnson J, Marshall P (eds) Climate change and the Great Barrier Reef: a vulnerability assessment. Great Barrier Reef Marine Park Authority and Australian Greenhouse Office, Townsville, pp 237–269Google Scholar
  38. Marba N, Holmer M, Gacia E, Barron C (2006) Seagrass beds and coastal biogeochemistry. In: Larkum AWD, Orth RJ, Duarte CM (eds) Seagrasses: biology, ecology and conservation. Springer, Dordrecht, pp 135–157Google Scholar
  39. McElroy DJ, Nguyen HD, Byrne M (2012) Respiratory response of the intertidal seastar Parvulastra exigua to contemporary and near-future pulses of warming and hypercapnia. J Exp Mar Biol Ecol 416–417:1–7CrossRefGoogle Scholar
  40. Mehrbach C, Culberso CH, Hawley JE, Pytkowic RM (1973) Measurement of apparent dissociation-constants of carbonic-acid in seawater at atmospheric-pressure. Limnol Oceanogr 18:897–907CrossRefGoogle Scholar
  41. 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 6:2313–2331CrossRefGoogle Scholar
  42. Mercier A, Battaglene SC, Hamel J-F (1999) Daily burrowing cycle and feeding activity of juvenile sea cucumbers Holothuria scabra in response to environmental factors. J Exp Mar Biol Ecol 239:125–156CrossRefGoogle Scholar
  43. Millero FJ, Huang F (2009) The density of seawaters as a function of salinity (5 to 70 g kg−1) and temperature (273.15 to 363.15 K). Ocean Sci 5:91–100CrossRefGoogle Scholar
  44. Millero FJ, Poisson A (1981) International one-atmosphere equation of state of seawater. Deep-Sea Res 28:625–629CrossRefGoogle Scholar
  45. Moulin L, Grosjean P, Leblud J, Batigny A, Dubois P (2014) Impact of elevated pCO2 on acid–base regulation of the sea urchin Echinometra mathaei and its relation to resistance to ocean acidification: a study in mesocosms. J Exp Mar Biol Ecol 467:97–104CrossRefGoogle Scholar
  46. Nguyen DH, Byrne M (2014) Early benthic juvenile Parvulastra exigua (Asteroidea) are tolerant to extreme acidification and warming in its intertidal habitat. J Exp Mar Biol Ecol 453:36–42CrossRefGoogle Scholar
  47. Orr JC (2011) Recent and future changes in ocean carbonate chemistry. In: Gattuso JP, Hansson L (eds) Ocean acidification. Oxford University Press, New York, pp 41–66Google Scholar
  48. Pierrot D, Lewis E, Wallace D (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, TennesseeGoogle Scholar
  49. Plotieau T, Baele J-M, Vaucher R, Hasler C-A, Koudad D, Eeckhaut I (2013) Analysis of the impact of Holothuria scabra intensive farming on sediment. Cah Biol Mar 54:703–711Google Scholar
  50. Przeslawski R, Ahyong S, Byrne M, Wörheide G, Hutchings P (2008) Beyond corals and fish: the effects of climate change on noncoral benthic invertebrates of tropical reefs. Glob Change Biol 14:2773–2795CrossRefGoogle Scholar
  51. Purcell SW, Mercier A, Conand C, Hamel JF, Toral-Granda MV, Lovatelli A, Uthicke S (2013) Sea cucumber fisheries: global analysis of stocks, management measures and drivers of overfishing. Fish Fish 14:34–59CrossRefGoogle Scholar
  52. Purcell SW, Polidoro BA, Hamel JF, Gamboa RU, Mercier A (2014) The cost of being valuable: predictors of extinction risk in marine invertebrates exploited as luxury seafood. P Roy Soc B 281:20133296CrossRefGoogle Scholar
  53. Rasolofonirina R, Mara E, Jangoux M (2004) Sea cucumber fishery and mariculture in Madagascar, a case study of Toliara, southwest Madagascar. In: Lovatelli A, Conand C, Purcell S, Uthicke S, Hamel JF, Mercier A (eds) Advances in sea cucumber aquaculture and management. FAO Fisheries Technical Paper No. 463. FAO, Rome, pp 133–149Google Scholar
  54. Rasolofonirina R, Vaïtilingon D, Eeckhaut I, Jangoux M (2005) Reproductive cycle of edible echinoderms from the Southwestern Indian Ocean II. The sandfish Holothuria scabra (Jaeger, 1833). WIOJMS 4:61–76Google Scholar
  55. Reipschläger A, Pörtner HO (1996) Metabolic depression during environmental stress: the role of extracellular versus intracellular pH in Sipunculus nudus. J Exp Biol 199:1801–1807Google Scholar
  56. Saderne V, Fietzek P, Herman PM (2013) Extreme variations of pCO2 and pH in a macrophyte meadow of the Baltic Sea in summer: evidence of the effect of photosynthesis and local upwelling. PLoS One 8:e62689CrossRefGoogle Scholar
  57. Santos IA, Castellano GC, Frier CA (2012) Direct relationship between osmotic and ionic conforming behavior and tissue water regulatory capacity in echinoids. Comp Biochem Phys A 164:466–476CrossRefGoogle Scholar
  58. Schneider K, Silverman J, Woolsey E, Eriksson H, Byrne M, Caldeira K (2011) Potential influence of sea cucumbers on coral reef CaCO3 budget: a case study at One Tree Reef. J Geophys Res 116:G04032Google Scholar
  59. Schneider K, Silverman J, Kravitz B, Rivlin T, Schneider-Mor A, Barbosa S, Byrne M, Caldeira K (2013) Inorganic carbon turnover caused by digestion of carbonate sands and metabolic activity of holothurians. Estuar Coast Shelf S133:217–223CrossRefGoogle Scholar
  60. Schram JB, McClintock JB, Angus RA, Lawrence JM (2011) Regenerative capacity and biochemical composition of the sea star Luidia clathrata (Say) (Echinodermata: Asteroidea) under conditions of near-future ocean acidification. J Exp Mar Biol Ecol 407:266–274CrossRefGoogle Scholar
  61. Seibel BA, Walsh PJ (2003) Biological impacts of deep-sea carbon dioxide injection inferred from indices of physiological performance. J Exp Biol 206:641–650CrossRefGoogle Scholar
  62. Stickle WB, Diehl WJ (1987) Effects of salinity on echinoderms. In: Jangoux M, Lawrence J (eds) Echinoderm studies, vol 2. A.A. Balkema, Rotterdam, pp 235–285Google Scholar
  63. Stumpp M, Trübenbach K, Brennecke D, Hu MY, Melzner F (2012) Resource allocation and extracellular acid–base status in the sea urchin Strongylocentrotus droebachiensis. Aquat Toxicol 110–111:194–207CrossRefGoogle Scholar
  64. Uthicke S (2001a) Nutrient regeneration by abundant coral reef holothurians. J Exp Mar Biol Ecol 265:153–170CrossRefGoogle Scholar
  65. Uthicke S (2001b) Interactions between sediment-feeders and microalgae on coral reefs: grazing losses versus production enhancement. Mar Ecol Prog Ser 210:125–138CrossRefGoogle Scholar
  66. Uthicke S, Klumpp DW (1998) Microphytobenthos community production at a near-shore coral reef: seasonal variation and response to ammonium recycled by holothurians. Mar Ecol Prog Ser 169:1–11CrossRefGoogle Scholar
  67. Vaïtilingon D, Rasolofonirina R, Jangoux M (2003) Feeding preferences, seasonal gut repletion indices, and diel feeding patterns of the sea urchin Tripneustes gratilla (Echinodermata: Echinoidea) on a coastal habitat off Toliara (Madagascar). Mar Biol 143:451–458CrossRefGoogle Scholar
  68. Vaïtilingon D, Eeckhaut I, Fourgon D, Jangoux M (2004) Population dynamics, infestation and host selection of Vexilla vexillum, an ectoparasitic muricid of echinoids, in Madagascar. Dis Aquat Org 61:241–255CrossRefGoogle Scholar
  69. Vaucher R (2012) Impact of holothuroids (Aspidochirotida) on carbonate sediments. Dissertation, University of Geneva, Switzerland (in French)Google Scholar
  70. Wolkenhauer SM, Uthicke S, Burridge C, Skewes T, Pitcher R (2010) The ecological role of Holothuria scabra (Echinodermata: Holothuroidea) within subtropical seagrass beds. J Mar Biol Assoc UK 90(2):215–223CrossRefGoogle Scholar
  71. Weber JN (1969) The incorporation of magnesium into the skeletal calcite of echinoderms. Am J Sci 267:537–566CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Marie Collard
    • 1
    • 2
    Email author
  • Igor Eeckhaut
    • 3
  • Frank Dehairs
    • 2
  • Philippe Dubois
    • 1
  1. 1.Laboratoire de Biologie MarineUniversité Libre de BruxellesBrusselsBelgium
  2. 2.Laboratory for Analytical, Environmental and Geo-Chemistry, Earth Systems Science research GroupVrije Universiteit BrusselBrusselsBelgium
  3. 3.Biology of Marine Organisms and BiomimeticsUniversity of MonsMonsBelgium

Personalised recommendations