Marine Biology

, Volume 161, Issue 11, pp 2531–2545 | Cite as

Tough as a rock-boring urchin: adult Echinometra sp. EE from the Red Sea show high resistance to ocean acidification over long-term exposures

Original Paper


Ocean acidification, a process caused by the continuous rise of atmospheric CO2 levels, is expected to have a profound impact on marine invertebrates. Findings of the numerous studies conducted in this field indicate high variability in species responses to future ocean conditions. This study aimed at understanding the effects of long-term exposure to elevated pCO2 conditions on the performance of adult Echinometra sp. EE from the Gulf of Aqaba (Red Sea). During an 11-month incubation under high pCO2 (1,433 μatm, pHNBS 7.7) and control (435 μatm, pHNBS 8.1) conditions, we examined the urchins’ somatic and gonadal growth, gametogenesis and skeletal microstructure. Somatic and gonadal growths were exhibited with no significant differences between the treatments. In addition, all urchins in the experiment completed a full reproductive cycle, typical of natural populations, with no detectable impact of increased pCO2 on the timing, duration or progression of the cycle. Furthermore, scanning electron microscopy imaging of urchin tests and spines revealed no signs of the usual observed effects of acidosis, such as skeletal dissolution, widened stereom pores or non-smoothed structures. Our results, which yielded no significant impact of the high pCO2 treatment on any of the examined processes in the urchins studied, suggest high resistance of adult Echinometra sp. EE to near future ocean acidification conditions. With respect to other findings in this area, the outcome of this study provides an example of the complicated and diverse responses of echinoids to the predicted environmental changes.

Supplementary material

227_2014_2525_MOESM1_ESM.docx (132 kb)
Supplementary material 1 (DOCX 132 kb)
227_2014_2525_MOESM2_ESM.docx (132 kb)
Supplementary material 2 (DOCX 132 kb)
227_2014_2525_MOESM3_ESM.doc (77 kb)
Supplementary material 3 (DOC 77 kb)
227_2014_2525_MOESM4_ESM.xlsx (16 kb)
Supplementary material 4 (XLSX 16 kb)


  1. Albright R, Bland C, Gillette P, Serafy JE, Langdon C, Capo TR (2012) Juvenile growth of the tropical sea urchin Lytechinus variegatus exposed to near-future ocean acidification scenarios. J Exp Mar Biol Ecol 426:12–17CrossRefGoogle Scholar
  2. 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 367:265–273CrossRefGoogle Scholar
  3. Arakaki Y, Uehara T (1999) Morphological comparison of black Echinometra individuals among those in the Indo-West Pacific. Zool Sci 16:551–558CrossRefGoogle Scholar
  4. Arakaki Y, Uehara T, Fagoonee I (1998) Comparative studies of the genus Echinometra from Okinawa and Mauritius. Zool Sci 15:159–168CrossRefGoogle Scholar
  5. Asnaghi V, Chiantore M, Mangialajo L, Gazeau F, Francour P, Alliouane S, Gattuso JP (2013) Cascading effects of ocean acidification in a rocky subtidal community. PLoS ONE 8:e61978CrossRefGoogle Scholar
  6. Asnaghi V, Mangialajo L, Gattuso JP, Francour P, Privitera D, Chiantore M (2014) Effects of ocean acidification and diet on thickness and carbonate elemental composition of the test of juvenile sea urchins. Mar Environ Res 93:1–7CrossRefGoogle Scholar
  7. Bak RPM (1994) Sea urchin bioerosion on coral reefs: place in the carbonate budget and relevant variables. Coral Reefs 13:99–103CrossRefGoogle Scholar
  8. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B 57:289–300Google Scholar
  9. Booth JG, Hall P, Wood ATA (1993) Balanced importance resampling for the bootstrap. Ann Stat 21:286–298CrossRefGoogle Scholar
  10. Bronstein O, Loya Y (2013) The Taxonomy and Phylogeny of Echinometra (Camarodonta: Echinometridae) from the Red Sea and Western Indian Ocean. PLoS ONE 8:e77374CrossRefGoogle Scholar
  11. Bruno JF, Sweatman H, Precht WF, Selig ER, Schutte VG (2009) Assessing evidence of phase shifts from coral to macroalgal dominance on coral reefs. Ecology 90:1478–1484CrossRefGoogle Scholar
  12. Byrne M (1990) Annual reproductive cycles of the commercial sea urchin Paracentrotus lividus from an exposed intertidal and a sheltered subtidal habitat on the west coast of Ireland. Mar Biol 104:275–289CrossRefGoogle Scholar
  13. 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 Annu Rev 49(1):42Google Scholar
  14. Byrne M, Przeslawski R (2013) Multistressor impacts of warming and acidification of the ocean on marine invertebrates’ life histories. Integr Comp Biol 53:582–596CrossRefGoogle Scholar
  15. Byrne M, Lamare M, Winter D, Dworjanyn SA, Uthicke S (2013) The stunting effect of a high CO2 ocean on calcification and development in sea urchin larvae, a synthesis from the tropics to the poles. Philos Trans R Soc London Ser B Biol Sci 368:20120439. doi:10.1098/rstb.2012.0439 CrossRefGoogle Scholar
  16. Caldeira K, Wickett ME (2003) Anthropogenic carbon and ocean pH. Nature 425:365CrossRefGoogle Scholar
  17. Caldeira K, Wickett ME (2005) Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean. J Geophys Res 110:C09S04Google Scholar
  18. Calosi P, Rastrick SP, Graziano M et al (2013) Distribution of sea urchins living near shallow water CO2 vents is dependent upon species acid–base and ion-regulatory abilities. Mar Poll Bull 73:470–484CrossRefGoogle Scholar
  19. Canty A, Ripley B (2009) Boot: Bootstrap R (S-Plus) functions. R package version 1.2-41.
  20. Collard M, Dery A, Dehairs F, Dubois F (2014) Euechinoidea and Cidaroidea respond differently to ocean acidification. Comp Biochem Physiol A 174:45–55CrossRefGoogle Scholar
  21. Connell SD, Kroeker KJ, Fabricius KE, Kline DI, Russell BD (2013) The other ocean acidification problem: CO2 as a resource among competitors for ecosystem dominance. Philos Trans R Soc London Ser B Biol Sci 368:20120442CrossRefGoogle Scholar
  22. Courtney T, Westfield I, Ries JB (2013) CO2-induced ocean acidification impairs calcification in the tropical urchin Echinometra viridis. J Exp Mar Biol Ecol 440:169–175CrossRefGoogle Scholar
  23. Diaz-Pulido G, Gouezo M, Tilbrook B, Dove S, Anthony K (2011) High CO2 enhances the competitive strength of seaweeds over corals. Ecol Lett 14:156–162CrossRefGoogle Scholar
  24. 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
  25. Doney SC, Fabry VJ, Feely RA, Kleypas JA (2009) Ocean acidification: the other CO2 problem. Annu Rev Mar Sci 1:169–192CrossRefGoogle Scholar
  26. Dorey N, Lancon P, Thorndyke M, Dupont S (2013) Assessing physiological tipping point of sea urchin larvae exposed to a broad range of pH. Glob Change Biol 19:3355–3367Google Scholar
  27. Downing N, El-Zahr CR (1987) Gut evacuation and filling rates in the rock-boring sea urchin, Echinometra mathaei. Bull Mar Sci 41:579–584Google Scholar
  28. Dupont S, Ortega-Martínez O, Thorndyke M (2010) Impact of near-future ocean acidification on echinoderms. Ecotoxicology 19:449–462CrossRefGoogle Scholar
  29. Dupont S, Dorey N, Stumpp M, Melzner F, Thorndyke M (2012) Long-term and trans-life-cycle effects of exposure to ocean acidification in the green sea urchin Strongylocentrotus droebachiensis. Mar Biol 160:1835–1843CrossRefGoogle Scholar
  30. Efron B (1987) Better bootstrap confidence intervals. J Am Stat Assoc 82:171–185CrossRefGoogle Scholar
  31. Fabry VJ, Seibel BA, Feely RA, Orr JC (2008) Impacts of ocean acidification on marine fauna and ecosystem processes. ICES J Mar Sci J Cons 65:414–432CrossRefGoogle Scholar
  32. Fernandez C, Caltagirone A (1994) Growth rate of adult sea urchins, Paracentrotus lividus, in a lagoon environment: the effect of different diet types. In: David B, Guille A, Feral J-P, Roux M (eds) Echinoderms through time. AA Balkema, Rotterdam, pp 655–660Google Scholar
  33. Ferrari R, Gonzalez-Rivero M, Ortiz JC, Mumby PJ (2012) Interaction of herbivory and seasonality on the dynamics of Caribbean macroalgae. Coral Reefs 31:683–692CrossRefGoogle Scholar
  34. Fuji A (1967) Ecological studies on the growth and food consumption of Japanese common littoral sea urchin, Strongylocentrotus intermedius (A. Agassiz). Mem Fac Fish Hokkaido Univ 15(2):83–160Google Scholar
  35. Gage JD (1992) Natural growth bands and growth variability in the sea urchin Echinus esculentus: results from tetracycline tagging. Mar Biol 114:607–616CrossRefGoogle Scholar
  36. Gonor JJ (1972) Gonad growth in the sea urchin, Strongylocentrotus purpuratus (Stimpson)(echinodermata: Echinoidea) and the assumptions of gonad index methods. J Exp Mar Biol Ecol 10:89–103CrossRefGoogle Scholar
  37. Heflin LE, Gibbs VK, Jones WT, Makowsky R, Lawrence AL, Watts SA (2013) Growth rates are related to production efficiencies in juveniles of the sea urchin Lytechinus variegatus. J Mar Biol Assoc UK 93:1673–1683CrossRefGoogle Scholar
  38. Hiratsuka Y, Uehara T (2007) Feeding ecology of four species of sea urchins (genus Echinometra) in Okinawa. Bull Mar Sci 81:85–100Google Scholar
  39. Holtmann WC, Stumpp M, Gutowska MA, 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
  40. IPCC (2013) Summary for policymakers. In: Stocker TF, Qin D, Plattner GK, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) Climate change 2013: the physical science basis. Cambridge University Press, Cambridge, Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate changeGoogle Scholar
  41. Kurihara H, Shirayama Y (2004) Effects of increased atmospheric CO2 on sea urchin early development. Mar Ecol Prog Ser 274:161–169CrossRefGoogle Scholar
  42. Kurihara H, Yin R, Nishihara GN, Soyano K, Ishimatsu A (2013) Effect of ocean acidification on growth, gonad development and physiology of the sea urchin Hemicentrotus pulcherrimus. Aquat Biol 18:281–292CrossRefGoogle Scholar
  43. Lebrato M, McClintock JB, Amsler MO, Ries JB, Egilsdottir H, Lamare M, Baker BJ (2013) From the Arctic to the Antarctic: the major, minor, and trace elemental composition of echinoderm skeletons: ecological archives E094-127. Ecology 94:1434CrossRefGoogle Scholar
  44. Levitan DR (1988) Density-dependent size regulation and negative growth in the sea urchin Diadema antillarum Philippi. Oecologia 76:627–629Google Scholar
  45. Lewis E, Wallace DWR (1998) CO2SYS—program developed for the CO2 system calculations. Carbon Dioxide Inf Anal Center Report ORNL/CDIAC-105Google Scholar
  46. Lozano J, Galera J, López S, Turon X, Palacin C, Morera G (1995) Biological cycles and recruitment of Paracentrotus lividus (Echinodermata: Echinoidea) in two contrasting habitats. Mar Ecol Prog Ser 122:179–191CrossRefGoogle Scholar
  47. McClanahan TR, Kurtis JD (1991) Population regulation of the rock-boring sea urchin Echinometra mathaei (de Blainville). J Exp Mar Biol Ecol 147:121–146CrossRefGoogle Scholar
  48. McClanahan TR, Muthiga NA (2007) Ecology of Echinometra. In: Lawrence JM (ed) Edible Sea Urchins: biology and ecology, vol 38. Elsevier science B.V., pp 297–317Google Scholar
  49. 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 18:897–907CrossRefGoogle Scholar
  50. Meidel SK, Scheibling RE (1998) Annual reproductive cycle of the green sea urchin, Strongylocentrotus droebachiensis, in differing habitats in Nova Scotia, Canada. Mar Biol 131:461–478CrossRefGoogle Scholar
  51. Meidel SK, Scheibling RE (1999) Effects of food type and ration on reproductive maturation and growth of the sea urchin Strongylocentrotus droebachiensis. Mar Biol 134:155–166CrossRefGoogle Scholar
  52. 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 Poll Bull 54:89–96CrossRefGoogle Scholar
  53. Minor MA, Scheibling RE (1997) Effects of food ration and feeding regime on growth and reproduction of the sea urchin Strongylocentrotus droebachiensis. Mar Biol 129:159–167CrossRefGoogle Scholar
  54. 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 457:97–104CrossRefGoogle Scholar
  55. Muthiga NA, Jaccarini V (2005) Effects of seasonality and population density on the reproduction of the Indo-Pacific echinoid Echinometra mathaei in Kenyan coral reef lagoons. Mar Biol 146:445–453CrossRefGoogle Scholar
  56. Orr JC, Fabry VJ, Aumont O et al (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437:681–686CrossRefGoogle Scholar
  57. Pearse JS (1969) Reproductive periodicities of Indo-Pacific invertebrates in the Gulf of Suez II. The echinoid Echinometra mathaei (de Blainville). Bull Mar Sci 19:580–613Google Scholar
  58. Pearse JS, Cameron RA (1991) Echinodermata: echinoidea. In: Giese AC, Pearse JS, Pearse VB (eds) Reproduction of marine invertebrates. Echinoderms and lophophorates, vol 6., Boxwood PressPacific Grove, CA, pp 513–662Google Scholar
  59. Pewsey A, Neuhäuser M, Ruxton GD (2013) Circular statistics in R. Oxford University Press, OxfordGoogle Scholar
  60. Pörtner HO (2008) Ecosystem effects of ocean acidification in times of ocean warming: a physiologist’s view. Mar Ecol Prog Ser 373:203–217CrossRefGoogle Scholar
  61. Prince J (1995) Limited effects of the sea urchin Echinometra mathaei (de Blainville) on the recruitment of benthic algae and macroinvertebrates into intertidal rock platforms at Rottnest Island, Western Australia. J Exp Mar Biol Ecol 186:237–258CrossRefGoogle Scholar
  62. Ries JB, Cohen AL, McCorkle DC (2009) Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 37:1131–1134CrossRefGoogle Scholar
  63. Robbins LL, Hansen ME, Kleypas JA, Meylan SC (2010) CO2calc: a user-friendly seawater carbon calculator for Windows, Max OS X, and iOS (iPhone). US Geological Survey Open-File Report, 1280 (17)Google Scholar
  64. Russell MP (1998) Resource allocation plasticity in sea urchins: rapid, diet induced, phenotypic changes in the green sea urchin, Strongylocentrotus droebachiensis (Müller). J Exp Mar Biol Ecol 220:1–14CrossRefGoogle Scholar
  65. Sammarco PW (1982) Echinoid grazing as a structuring force in coral communities: whole reef manipulations. J Exp Mar Biol Ecol 61:31–55CrossRefGoogle Scholar
  66. Shirayama Y, Thornton H (2005) Effect of increased atmospheric CO2 on shallow water marine benthos. J Geophys Res 110:C09–S08Google Scholar
  67. Siikavuopio SI, 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 266:97–101CrossRefGoogle Scholar
  68. Spirlet C, Grosjean P, Jangoux M (1998) Reproductive cycle of the echinoid Paracentrotus lividus: analysis by means of the maturity index. Invertebr Reprod Dev 34:69–81CrossRefGoogle Scholar
  69. Stumpp M, Dupont S, Thorndyke MC, Melzner F (2011) CO2 induced seawater acidification impacts sea urchin larval development II: gene expression patterns in pluteus larvae. Comp Biochem Physiol A Mol Int Physiol 60:320–330CrossRefGoogle Scholar
  70. Stumpp M, Trübenbach K, Brennecke D, Hu MY, Melzner F (2012) Resource allocation and extracellular acid–base status in the sea urchin Strongylocentrotus droebachiensis in response to CO2 induced seawater acidification. Aquat Toxicol 110:194–207CrossRefGoogle Scholar
  71. Uthicke S, Soars N, Foo S, Byrne M (2012) Effects of elevated pCO2 and the effect of parent acclimation on development in the tropical Pacific sea urchin Echinometra mathaei. Mar Biol 160:1913–1926CrossRefGoogle Scholar
  72. Uthicke S, Liddy M, Nguyen HD, Byrne M (2014) Interactive effects of near-future temperature increase and ocean acidification on physiology and gonad development in adult Pacific sea urchin, Echinometra sp. A. Coral Reefs 1–15Google Scholar
  73. Walker CW, Lesser MP (1998) Manipulation of food and photoperiod promotes out-of-season gametogenesis in the green sea urchin, Strongylocentrotus droebachiensis: implications for aquaculture. Mar Biol 132:663–676CrossRefGoogle Scholar
  74. Wangensteen OS, Dupont S, Casties I, Turon X, Palacín C (2013a) Some like it hot: temperature and pH modulate larval development and settlement of the sea urchin Arbacia lixula. J Exp Mar Biol Ecol 449:304–311CrossRefGoogle Scholar
  75. Wangensteen OS, Turon X, Casso M, Palacin C (2013b) The reproductive cycle of the sea urchin Arbacia lixula in Northwest Mediterranean: potential influence of temperature and photoperiod. Mar Biol 160:1–14CrossRefGoogle Scholar
  76. Wolfe K, Dworjanyn SA, Byrne M (2013) Effects of ocean warming and acidification on survival, growth and skeletal development in the early benthic juvenile sea urchin (Heliocidaris erythrogramma). Glob Change Biol 19:2698–2707CrossRefGoogle Scholar
  77. Zeebe RE, Wolf-Gladrow D (2001) CO2 in seawater: equilibrium, equilibrium, kinetics, isotopes. Elsevier Oceanography Series. Elsevier Science B.V, Amsterdam, pp 1–83Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.Ben Gurion University of the NegevBeer-ShevaIsrael
  2. 2.The Interuniversity Institute for Marine SciencesEilatIsrael
  3. 3.Department of Animal BiologyUniversity of BarcelonaBarcelonaSpain
  4. 4.The Mina and Everard Goodman Faculty of Life SciencesBar-Ilan UniversityRamat GanIsrael

Personalised recommendations