Marine Biology

, Volume 157, Issue 11, pp 2489–2502 | Cite as

Effects of ocean acidification on invertebrate settlement at volcanic CO2 vents

  • M. Cigliano
  • M. C. GambiEmail author
  • R. Rodolfo-Metalpa
  • F. P. Patti
  • J. M. Hall-Spencer
Original Paper


We present the first study of the effects of ocean acidification on settlement of benthic invertebrates and microfauna. Artificial collectors were placed for 1 month along pH gradients at CO2 vents off Ischia (Tyrrhenian Sea, Italy). Seventy-nine taxa were identified from six main taxonomic groups (foraminiferans, nematodes, polychaetes, molluscs, crustaceans and chaetognaths). Calcareous foraminiferans, serpulid polychaetes, gastropods and bivalves showed highly significant reductions in recruitment to the collectors as pCO2 rose from normal (336–341 ppm, pH 8.09–8.15) to high levels (886–5,148 ppm) causing acidified conditions near the vents (pH 7.08–7.79). Only the syllid polychaete Syllis prolifera had higher abundances at the most acidified station, although a wide range of polychaetes and small crustaceans was able to settle and survive under these conditions. A few taxa (Amphiglena mediterranea, Leptochelia dubia, Caprella acanthifera) were particularly abundant at stations acidified by intermediate amounts of CO2 (pH 7.41–7.99). These results show that increased levels of CO2 can profoundly affect the settlement of a wide range of benthic organisms.


Foraminifera Polychaete Ocean Acidification Crustose Coralline Alga Coccolithophores 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



Thanks are due to MC Buia and the staff of the benthic ecology group of the Stazione Zoologica Anton Dohrn, located at Villa Dohrn (Ischia), for support in the laboratory and at sea. We are also indebted to E Vecchi (foraminiferans), MB Scipione (amphipods) and M Lorenti (isopods and tanaids) for the identification of some of the benthic taxa. C Vasapollo helped with the statistical analyses. The captain V Rando and B Iacono supported the work at sea. We also thank two anonymous reviewers whose comments improved the Ms. This work is a contribution to the European Project on Ocean Acidification (EPOCA FP7/2007-2013 grant agreement no 211384) and was partly funded by the Save Our Seas Foundation.


  1. Augier H, Boudouresque C-F (1970) Végetation marine de l’ile de Port Cros. Le recif barrière de posidonies. Bull Mus Hist Nat Marseille 30:221–228Google Scholar
  2. Barry JP, Hall-Spencer JM, Tyrell T (2010) In situ perturbation experiments: natural venting sites, spatial/temporal gradients in ocean pH, manipulative in situ pCO2 perturbations. In: Riebesell U, Fabry VJ, Hansson L, Gattuso J-P (eds) Guide to best practices for ocean acidification research and data reporting. Publications Office of the European Union, LuxembourgGoogle Scholar
  3. Bellan G (1980) Relationship of pollution to rocky substratum polychaetes on the French Mediterranean coast. Mar Pollut Bull 11(11):318–321CrossRefGoogle Scholar
  4. Bijma J, Hönisch B, Zeebe RE (2002) Impact of the ocean carbonate chemistry on living foraminiferal shell weight: comment on ‘Carbonate ion concentration in glacial-age deep waters of the Caribbean Sea’ by Broecker WS, Clark E. Geochem Geophys Geosyst 3(11):1064. doi: 10.1029/2009GC000388 CrossRefGoogle Scholar
  5. Boudouresque CF, Cinelli F (1971) Le peuplement des biotopes sciaphiles superficiels de mode battu de l’île d’Ischia (Golfe de Naples, Italie). Pubbl St Zool Napoli 39:1–43Google Scholar
  6. Boudouresque CF, Cinelli F (1976) Les peuplement algal des biotopes sciaphiles superficiles de mode battu en Mediterranée occidentale. Pubbl St Zool Napoli 40:433–459Google Scholar
  7. Buia MC, Gambi MC, Lorenti M, Dappiano M, Zupo V (2003) Aggiornamento sulla distribuzione e sullo stato ambientale dei sistemi a fanerogame marine (Posidonia oceanica e Cymodocea nodosa) delle isole Flegree. Acc Sc Lett Arti Napoli, Mem Soc Sc Fis Mat 5:163–186Google Scholar
  8. Caldeira K, Wickett ME (2003) Anthropogenic carbon and ocean pH. Nature 425:365CrossRefPubMedGoogle Scholar
  9. Cozzolino GC, Scipione MB, Lorenti M, Zupo V (1992) Migrazioni nictemerali e struttura del popolamento a crostacei Peracaridi e Decapodi in una prateria a Posidonia oceanica dell’isola d’Ischia (Golfo di Napoli). Oebalia suppl 17:343–346Google Scholar
  10. Dashfield SL, Somerfield PJ, Widdicombe S, Austen MC, Nimmo M (2008) Impacts of ocean acidification and burrowing urchins on within-sediment profiles and subtidal nematode communities. J Exp Mar Biol Ecol 365(1):46–52CrossRefGoogle Scholar
  11. deFur PL, McMahon BR (1984) Physiological compensation to short term air exposure in red rock crabs, Cancer productus Randall, from littoral and sublittoral habitats: acid-base balance. Physiol Zool 57:151–160Google Scholar
  12. Dupont S, Havenhand J, Thorndyke W, Peck L, Thorndyke M (2008) Near-future level of CO2-driven ocean acidification radically affects larval survival and development in the brittlestar Ophiothrix fragilis. Mar Ecol Prog Ser 373:285–294CrossRefGoogle Scholar
  13. Ellis RP, Bersey J, Rundle SD, Hall-Spencer JM, Spicer JI (2009) Subtle but significant effects of CO2 acidified sea water on embryos of the intertidal snail, Littorina obtusata. Aquat Biol 5:41–48CrossRefGoogle Scholar
  14. Fabry VJ, Siebel BA, Feeley RA, Orr JC 2008. Impact of ocean acidification on marine fauna and ecosystem processes. International council for the exploration of the sea. Oxford Journal 414–432Google Scholar
  15. 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 305:362–366CrossRefPubMedGoogle Scholar
  16. Findlay HS, Kendall MA, Spicer JI, Widdicombe S (2009) Future high CO2 in the intertidal may compromise adult barnacle Semibalanus balanoides survival and embryonic development rate. Mar Ecol Prog Ser 389:193–202CrossRefGoogle Scholar
  17. Gambi MC, Cafiero G (2001) Functional diversity in the Posidonia oceanica ecosystem: an example with polychaete borers of the scales. In: Faranda FM, Guglielmo L, Spezie G (eds) Mediterranean Ecosystems: Structure and Processes. Springer-Verlag, Italy, pp 399–405Google Scholar
  18. Gambi MC, Ramella L, Sella G, Protto P, Aldieri E (1997) Variation in genome size in benthic polychaetes: systematic and ecological relationships. J Mar Biol Ass UK 77:1045–1057CrossRefGoogle Scholar
  19. Gambi MC, Zupo V, Buia MC, Mazzella L (2000) Feeding ecology of the polychaete Platynereis dumerilii (Audouin & Milne Edwards) (Nereididae) in the seagrass Posidonia oceanica system: role of the epiphytic flora. Ophelia 53(3):189–202Google Scholar
  20. Gambi MC, De Lauro M, Iannuzzi F (Eds) (2003) Ambiente marino costiero e territorio delle isole Flegree (Ischia Procida Vivara). Acc Sc Lett Arti Napoli. Mem Soc Sc Fis Mat 5:425Google Scholar
  21. Gattuso J-P, Frankignoulle M, Bourge I, Romaine S, Buddemeier RW (1998) Effect of calcium carbonate saturation of seawater in coral calcification. Glob Planet Chan 18:37–46CrossRefGoogle Scholar
  22. Gazeau F, Quiblier C, Jansen JM, Gattuso JP, Middelburg JJ, Heip CHR (2007) Impact of elevated CO2 on shellfish calcification. Geophys Res Lett 34:L07603CrossRefGoogle Scholar
  23. Gobin J, Warwick RM (2006) Geographical variation in species diversity: a comparison of marine polychaetes and nematodes. J Exp Mar Biol Ecol 330:234–244CrossRefGoogle Scholar
  24. Green MA, Jones ME, Boudreau CL, Moore RL, Westman BA (2004) Dissolution mortality of juvenile bivalves in coastal marine deposits. Limnol Oceanogr 49:727–734CrossRefGoogle Scholar
  25. Guidetti P, Bussotti S (1998) Juveniles of littoral fish species in shallow seagrass beds: preliminary quali-quantitative data. Biol Mar Mediter 5:347–350Google Scholar
  26. Hall-Spencer JM, Rodolfo-Metalpa R, Martin S, Ransome S, Fine M, Turner SM, Rowley SJ, Tedesco D, Buia MC (2008) Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 454:96–99CrossRefPubMedGoogle Scholar
  27. Houghton JT, Callander BA, Varney SK (1992) Climate Change: the supplementary report to the IPCC Scientific. Cambridge University Press, CambridgeGoogle Scholar
  28. Iglesias-Rodriguez D, Halloran PR, Rickaby REM, Hall IR, Colmenero-Hidalgo E, Gittins JR, Green DRH, Tyrrell T, Gibb S, von Dassow P, Rehm E, Armbrust EV, Boessenkool KP (2008) Phytoplankton calcification in a high-CO2 world. Science 320(5874):336–340CrossRefPubMedGoogle Scholar
  29. Jokiel PL, Rodgers KS, Kuffner IB, Andersson AJ, Cox EF, Mackenzie FT (2008) Ocean acidification and calcifying reef organisms: a mesocosm investigation. Coral Reefs 27:473–483CrossRefGoogle Scholar
  30. Jury C, Whitehead R, Szmant A (2009) Effects of variations in carbonate chemistry on the calcification rates of Madracis auretenra (=Madracis mirabilis sensu Wells, 1973): bicarbonate concentrations best predict calcification rates Global Chan Biol doi: 10.1111/j.1365-2486.2009.02057.x
  31. Keeling CD, Whorf TP (1994) Atmospheric CO2 records from sites in the SIO air sampling network. In: Boden TA, Kaiser DP, Sepanki RJ, Stoss FW (eds) Trends ‘93: a compendium of data on global change. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory. Oak Ridge, TN, pp 16–26Google Scholar
  32. Kendall MA, Widdicombe S, Davey JT, Somerfield PJ, Austen MCV, Warwick RM (1996) The biogeography of islands: preliminary results from a comparative study of the isles of Scilly and Cornwall. J Mar Biol Ass UK 76:219–222CrossRefGoogle Scholar
  33. Kleypas JA, Feely RA, Fabry VJ, Langdon C, Sabine CL, Robbins LL (2006) Impacts of Ocean Acidification on Coral Reefs and Other Marine Calcifiers: A Guide for Future Research. Report of a workshop held 18–20 April 2005, St. Petersburg, FLGoogle Scholar
  34. Kuffner IB, Andersson AJ, Jokiel PL, Rodgers KS, Mackenzie FT (2007) Decreased abundance of crustose coralline algae due to ocean acidification. Nat Geosci 1(2):114–117CrossRefGoogle Scholar
  35. Kurihara H, Ishimatsu A (2008) Effects of high CO2 seawater on the copepod (Acartia tsuensis) through all life stages and subsequent generations. Mar Pollut Bull 56:1086–1090CrossRefPubMedGoogle Scholar
  36. Kurihara H, Shirayama Y (2004) Effects of increased atmospheric CO2 on sea urchin early development. Mar Ecol Prog Ser 274:161–169CrossRefGoogle Scholar
  37. Kurihara H, Shimode S, Shirayama Y (2004) Sub-lethal effects of elevated concentration of CO2 on planktonic copepods and sea urchins. J Oceanogr 60:743–750CrossRefGoogle Scholar
  38. Kurihara H, Kato S, Ishimatsu A (2007) Effects of increased seawater pCO2 on early development of the oyster Crassostrea gigas. Aquat Biol 1:91–98CrossRefGoogle Scholar
  39. Lindinger MI, Lauren DJ, McDonald DG (1984) Acid–base balance in the sea mussel, Mytilus edulis. III. Effects of environmental hypercapnia on intra- and extracellular acid–base balance. Mar Biol Lett 5:371–381Google Scholar
  40. Lorenti M, Scipione MB (1990) Relationships between trophic structure and diel migrations of Isopods and Amphipods in a Posidonia oceanica bed of the island of Ischia (Gulf of Naples, Italy). Rapp Comm int Expl Mer Médit 32(1):17Google Scholar
  41. Martin S, Rodolfo-Metalpa R, Ransome E, Rowley S, Buia MC, Gattuso JP, Hall-Spencer JM (2008) Effects of naturally acidified seawater on seagrass calcareous epibionts. Biol Lett 4(6):689–692CrossRefPubMedGoogle Scholar
  42. Menge BA (1992) Community regulation: under what conditions are bottom-up factors important on rocky shores? Ecology 73:755–765CrossRefGoogle Scholar
  43. Michaelidis B, Ouzounis C, Paleras A, Portner HO (2005) Effects of long-term moderate hypercapnia on acid–base balance and growth rate in marine mussels Mytilus galloprovincialis. Mar Ecol Progr Ser 293:109–118CrossRefGoogle Scholar
  44. Porri F, McQuaid CD, Radloff S (2006) Spatio-temporal variability of larval abundances and settlement of Perna perna: differential delivery of mussels. Mar Ecol Progr Ser 315:141–150CrossRefGoogle Scholar
  45. Porzio L, Hall-Spencer J, Buia MC (2008) Macroalgal community response to increasing CO2. II International Symposium on the ocean in a high-CO2 world. Monaco, p 75 (abstract)Google Scholar
  46. Pulitzer Finali G (1970) Report on a collection of sponges from the Bay of Naples. I. Sclerospongiae, Lithistida, Tetractinellida, Epipolasida. Pubbl St Zool Napoli 38:328–354Google Scholar
  47. Pulitzer Finali G, Pronzato R (1976) Report on a collection of sponges from the Bay of Naples. II. Keratosa. Pubbl St Zool Napoli 40:83–104Google Scholar
  48. Raven J, Caldeira K, Elderfield H, Hoegh-Guldberg O, Liss P, Riebesell U, Shepherd J, Turley C, Watson A (2005) Ocean acidification due to increasing atmospheric carbon dioxide. The Royal Society policy document 12/05. The Clyvedon Press Ltd, CardiffGoogle Scholar
  49. Riebesell U (2008) Acid test for marine biodiversity. Nature 454:46–47CrossRefPubMedGoogle Scholar
  50. Riebesell U, Wolf-Gladrow DA, Smetacek V (1993) Carbon dioxide limitation of marine phytoplankton growth rates. Nature 361:249–251CrossRefGoogle Scholar
  51. Riebesell U, Zondervan I, Rost B, Tortell PD, Richard EZ, Morel FMM (2000) Reduced calcification of marine plankton in response to increased atmospheric CO2. Nature 407:364–367CrossRefPubMedGoogle Scholar
  52. Riebesell U, Schulz KG, Bellerby RGJ, Botros M, Fritsche P, Meyerhöfer M, Neill C, Nondal G, Oschlies A, Wohlers J, Zöllner E (2007) Enhanced biological carbon consumption in a high CO2 ocean. Nature 450:545–554CrossRefPubMedGoogle Scholar
  53. Ries JB, Cohen AL, McCorkle DC (2009) Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 37:1131–1134CrossRefGoogle Scholar
  54. Rittmann A, Gottini V (1981) L’Isola d’Ischia. Geologia. Boll Servizio Geol It 101:131–274Google Scholar
  55. Rodolfo-Metalpa R, Martin S, Ferrier-Pages C, Gattuso JP (2010a) Response of Mediterranean corals to ocean acidification. Biogeosci Discuss 6:7103–7131CrossRefGoogle Scholar
  56. Rodolfo-Metalpa R, Lombardi C, Cocito S, Hall-Spencer JM, Gambi MC (2010b) Effects of ocean acidification and high temperatures on the bryozoan Myriapora truncata at natural CO2 vents. Mar Ecol Evol Persp 31(3). doi: 10.1111/j.1439-0485.2009.00354.x
  57. Rouse GW, Gambi MC (1997) Cladistic relationships within Amphiglena Claparède (Polychaeta: Sabellidae) with a new species and a redescription of A. mediterranea (Leydig). J Nat Hist 31:999–1018CrossRefGoogle Scholar
  58. Russo GF, Fresi E, Vinci D, Chessa LA (1984a) Malacofauna di strato foliare delle praterie di Posidonia oceanica (L.) Delile intorno all’isola d’Ischia (Golfo di Napoli): analisi strutturale del popolamento estivo in rapporto alla profondità ed alla esposizione. Nova Thalassia 6:655–661Google Scholar
  59. Russo GF, Fresi E, Vinci D, Chessa LA (1984b) Mollusk syntaxon of foliar stratum along a depth gradient in a Posidonia oceanica (L.) Delile meadow: diel variability. In: Boudouresque C-F, Jeudy de Grissac A, Olivier J (Eds) GIS Posidonie publ Fr 1:303–310Google Scholar
  60. Sarà M (1959) Poriferi del litorale dell’isola d’Ischia e loro ripartizione per ambienti. Pubbl St Zool Napoli 31:421–472Google Scholar
  61. Scipione MB (1999) Amphipod biodiversity in the foliar stratum of shallow-water Posidonia oceanica beds in the Mediterranean Sea. In: Schram FR, van Vaupel Kelin JC (eds) Crustacean and the Biodiversity Crisis. Brill, Leiden, pp 649–662Google Scholar
  62. Seibel BA, Fabry VJ (2003) Marine biotic response to elevated carbon dioxide. Adv Appl Biodiv Sci 4:59–67Google Scholar
  63. Tedesco D (1996) Chemical and isotopic investigation of fumarolic gases from Ischia Island (Southern Italy): evidence of magmatic and crustal contribution. J Vulcanol Geother Res 74:233–242CrossRefGoogle Scholar
  64. Thornton H, Shirayama Y (2001) III-1 Effects on benthic organisms. In: CO2 ocean sequestration and its biological impacts. Bull Jpn Soc Sci Fish 67(4):756–757Google Scholar
  65. Vezina AF, Hoegh-Guldberg O (Coordinators) (2008) Effects of ocean acidification on marine ecosystems. Mar Ecol Prog Ser 373:199–309Google Scholar
  66. Widdicombe S, Needham HR (2007) Impact of CO2-induced seawater acidification on the burrowing activity of Nereis virens and sediment nutrient flux. Mar Ecol Prog Ser 341:111–122CrossRefGoogle Scholar
  67. Wood HL, Spicer JI, Widdicombe S (2008) Ocean acidification may increase calcification rates, but at a cost. Proc R Soc Lond 275B:1767–1773CrossRefGoogle Scholar
  68. Zeebe RE, Wolf-Gladrow D (2001) CO2 in seawater: equilibrium, kinetics, isotopes. In: Halpern D (ed) Elsevier oceanography series, Series 65. Elsevier, AmsterdamGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • M. Cigliano
    • 1
  • M. C. Gambi
    • 1
    Email author
  • R. Rodolfo-Metalpa
    • 2
    • 3
  • F. P. Patti
    • 1
  • J. M. Hall-Spencer
    • 2
  1. 1.Stazione Zoologica Anton Dohrn, Laboratory of Functional and Evolutionary EcologyNaplesItaly
  2. 2.Marine Institute, Marine Biology and Ecology Research CentreUniversity of PlymouthPlymouthUK
  3. 3.IAEA, Marine Environment LaboratoriesMonacoMonaco

Personalised recommendations