Skip to main content

Advertisement

Log in

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
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • 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 426:12–17

    Article  Google Scholar 

  • 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 367:265–273

    Article  Google Scholar 

  • Arakaki Y, Uehara T (1999) Morphological comparison of black Echinometra individuals among those in the Indo-West Pacific. Zool Sci 16:551–558

    Article  Google Scholar 

  • Arakaki Y, Uehara T, Fagoonee I (1998) Comparative studies of the genus Echinometra from Okinawa and Mauritius. Zool Sci 15:159–168

    Article  CAS  Google Scholar 

  • 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:e61978

    Article  CAS  Google Scholar 

  • 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 93:1–7

    Article  Google Scholar 

  • Bak RPM (1994) Sea urchin bioerosion on coral reefs: place in the carbonate budget and relevant variables. Coral Reefs 13:99–103

    Article  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B 57:289–300

    Google Scholar 

  • Booth JG, Hall P, Wood ATA (1993) Balanced importance resampling for the bootstrap. Ann Stat 21:286–298

    Article  Google Scholar 

  • Bronstein O, Loya Y (2013) The Taxonomy and Phylogeny of Echinometra (Camarodonta: Echinometridae) from the Red Sea and Western Indian Ocean. PLoS ONE 8:e77374

    Article  CAS  Google Scholar 

  • 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 90:1478–1484

    Article  Google Scholar 

  • 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 104:275–289

    Article  Google Scholar 

  • 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):42

    Google Scholar 

  • Byrne M, Przeslawski R (2013) Multistressor impacts of warming and acidification of the ocean on marine invertebrates’ life histories. Integr Comp Biol 53:582–596

    Article  CAS  Google Scholar 

  • 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

    Article  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 110:C09S04

    Google Scholar 

  • 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 73:470–484

    Article  CAS  Google Scholar 

  • Canty A, Ripley B (2009) Boot: Bootstrap R (S-Plus) functions. R package version 1.2-41. http://cran.r-project.org/web/packages/boot/index.html

  • Collard M, Dery A, Dehairs F, Dubois F (2014) Euechinoidea and Cidaroidea respond differently to ocean acidification. Comp Biochem Physiol A 174:45–55

    Article  CAS  Google Scholar 

  • 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 368:20120442

    Article  Google Scholar 

  • Courtney T, Westfield I, Ries JB (2013) CO2-induced ocean acidification impairs calcification in the tropical urchin Echinometra viridis. J Exp Mar Biol Ecol 440:169–175

    Article  CAS  Google Scholar 

  • Diaz-Pulido G, Gouezo M, Tilbrook B, Dove S, Anthony K (2011) High CO2 enhances the competitive strength of seaweeds over corals. Ecol Lett 14:156–162

    Article  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 

  • 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 

  • 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 19:3355–3367

    Google Scholar 

  • Downing N, El-Zahr CR (1987) Gut evacuation and filling rates in the rock-boring sea urchin, Echinometra mathaei. Bull Mar Sci 41:579–584

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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 160:1835–1843

    Article  Google Scholar 

  • Efron B (1987) Better bootstrap confidence intervals. J Am Stat Assoc 82:171–185

    Article  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 J Cons 65:414–432

    Article  CAS  Google Scholar 

  • 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 655–660

    Google Scholar 

  • Ferrari R, Gonzalez-Rivero M, Ortiz JC, Mumby PJ (2012) Interaction of herbivory and seasonality on the dynamics of Caribbean macroalgae. Coral Reefs 31:683–692

    Article  Google Scholar 

  • 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):83–160

    Google Scholar 

  • Gage JD (1992) Natural growth bands and growth variability in the sea urchin Echinus esculentus: results from tetracycline tagging. Mar Biol 114:607–616

    Article  Google Scholar 

  • 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 10:89–103

    Article  Google Scholar 

  • 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 93:1673–1683

    Article  Google Scholar 

  • Hiratsuka Y, Uehara T (2007) Feeding ecology of four species of sea urchins (genus Echinometra) in Okinawa. Bull Mar Sci 81:85–100

    Google Scholar 

  • 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 160:2631–2645

    Article  CAS  Google Scholar 

  • 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 change

    Google Scholar 

  • Kurihara H, Shirayama Y (2004) Effects of increased atmospheric CO2 on sea urchin early development. Mar Ecol Prog Ser 274:161–169

    Article  Google Scholar 

  • 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 18:281–292

    Article  Google Scholar 

  • 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 94:1434

    Article  Google Scholar 

  • Levitan DR (1988) Density-dependent size regulation and negative growth in the sea urchin Diadema antillarum Philippi. Oecologia 76:627–629

    Google Scholar 

  • Lewis E, Wallace DWR (1998) CO2SYS—program developed for the CO2 system calculations. Carbon Dioxide Inf Anal Center Report ORNL/CDIAC-105

  • 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 122:179–191

    Article  Google Scholar 

  • McClanahan TR, Kurtis JD (1991) Population regulation of the rock-boring sea urchin Echinometra mathaei (de Blainville). J Exp Mar Biol Ecol 147:121–146

    Article  Google Scholar 

  • 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 297–317

  • 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 

  • Meidel SK, Scheibling RE (1998) Annual reproductive cycle of the green sea urchin, Strongylocentrotus droebachiensis, in differing habitats in Nova Scotia, Canada. Mar Biol 131:461–478

    Article  Google Scholar 

  • Meidel SK, Scheibling RE (1999) Effects of food type and ration on reproductive maturation and growth of the sea urchin Strongylocentrotus droebachiensis. Mar Biol 134:155–166

    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 Poll Bull 54:89–96

    Article  CAS  Google Scholar 

  • Minor MA, Scheibling RE (1997) Effects of food ration and feeding regime on growth and reproduction of the sea urchin Strongylocentrotus droebachiensis. Mar Biol 129:159–167

    Article  Google Scholar 

  • 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 457:97–104

    Article  CAS  Google Scholar 

  • 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 146:445–453

    Article  Google Scholar 

  • Orr JC, Fabry VJ, Aumont O et al (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437:681–686

    Article  CAS  Google Scholar 

  • Pearse JS (1969) Reproductive periodicities of Indo-Pacific invertebrates in the Gulf of Suez II. The echinoid Echinometra mathaei (de Blainville). Bull Mar Sci 19:580–613

    Google Scholar 

  • 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 513–662

    Google Scholar 

  • Pewsey A, Neuhäuser M, Ruxton GD (2013) Circular statistics in R. Oxford University Press, Oxford

    Google Scholar 

  • Pörtner HO (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 

  • 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 186:237–258

    Article  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 

  • 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)

  • 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 220:1–14

    Article  Google Scholar 

  • Sammarco PW (1982) Echinoid grazing as a structuring force in coral communities: whole reef manipulations. J Exp Mar Biol Ecol 61:31–55

    Article  Google Scholar 

  • Shirayama Y, Thornton H (2005) Effect of increased atmospheric CO2 on shallow water marine benthos. J Geophys Res 110:C09–S08

  • 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 266:97–101

    Article  CAS  Google Scholar 

  • Spirlet C, Grosjean P, Jangoux M (1998) Reproductive cycle of the echinoid Paracentrotus lividus: analysis by means of the maturity index. Invertebr Reprod Dev 34:69–81

    Article  Google Scholar 

  • 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 60:320–330

    Article  Google Scholar 

  • 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 110:194–207

    Article  Google Scholar 

  • 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 160:1913–1926

    Article  Google Scholar 

  • 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 1–15

  • 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 132:663–676

    Article  Google Scholar 

  • 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 449:304–311

    Article  Google Scholar 

  • 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 160:1–14

    Article  Google Scholar 

  • 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 19:2698–2707

    Article  Google Scholar 

  • Zeebe RE, Wolf-Gladrow D (2001) CO2 in seawater: equilibrium, equilibrium, kinetics, isotopes. Elsevier Oceanography Series. Elsevier Science B.V, Amsterdam, pp 1–83

    Google Scholar 

Download references

Acknowledgments

We are grateful to the staff of the Interuniversity Institute (IUI) for Marine Sciences in Eilat, Israel, for logistic help. We also thank Dr. Hanna Rosenfeld, Dr. Hanit Ben Ari, Dr. Iris Meiri Ashkenazi, Ms. Barbara Colorni, Mr. David Ben Ezra and Prof. Muki Shpigel from the National Center for Mariculture (NCM) laboratory in Eilat, Israel, for their professional advice, assistance with preparation of histology sections and the supply of algal material. Many thanks to Ms. Gabriela Perna and Ms. Elizabeth Foran who assisted greatly with the urchins sampling and the ongoing maintenance of the experiment, and to Mr. Moty Ohavia, (IUI), for his priceless professional tips. We are also grateful to Ms. Roxana Golan from the Ben Gurion University of the Negev, Israel, for her guidance and assistance with SEM operation. This study was partially supported by an Israel Science Foundation grant to MF.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yael Hazan.

Additional information

Communicated by M. Byrne.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hazan, Y., Wangensteen, O.S. & Fine, M. Tough as a rock-boring urchin: adult Echinometra sp. EE from the Red Sea show high resistance to ocean acidification over long-term exposures. Mar Biol 161, 2531–2545 (2014). https://doi.org/10.1007/s00227-014-2525-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-014-2525-4

Keywords

Navigation