Persistent natural acidification drives major distribution shifts in marine benthic ecosystems

Proceedings of the Royal Society B: Biological Sciences

Volumn 282, Issue 1818, 2015, Pages

  Linares, C ^a   Vidal, M ^a   Canals, M ^a   Kersting, D K ^a   Amblas, D ^a   Aspillaga, E ^a   Cebrian E ^b,c   Delgado Huertas, A ^d   Diaz D ^e,f   Garrabou, J ^f   Hereu, B ^a   Navarro, L ^a   Teixido N ^g   Ballesteros, E ^b  

^a UNIVERSITY OF BARCELONA   (Spain)

^b CENTRE D ESTUDIS AVANÇATS DE BLANES CEAB CSIC   (Spain)

^c UNIVERSITY OF GIRONA   (Spain)

^d INSTITUTO ANDALUZ DE CIENCIAS DE LA TIERRA   (Spain)

^e INSTITUTO ESPAÑOL DE OCEANOGRAFÍA   (Spain)

^f INSTITUT DE CIÈNCIES DEL MAR   (Spain)

^g STAZIONE ZOOLOGICA ANTON DOHRN   (Italy)

Author keywords

Calcification; Climate change; CO2 vents; Ocean acidification; pH

Indexed keywords

ACIDIFICATION; ARAGONITE; BENTHOS; CALCIFICATION; CALCITE; CARBON DIOXIDE; CLIMATE CHANGE; DOMINANCE; KELP FOREST; MARINE ECOSYSTEM; PERSISTENCE; PH; SHALLOW WATER; SOCIOECONOMIC IMPACT; VENTING;

ALGAE; LAMINARIA RODRIGUEZII;

ACID; CARBON DIOXIDE; CARBONIC ACID DERIVATIVE; SEA WATER;

ANIMAL; ANTHOZOA; BRYOZOA; CHEMISTRY; ECOSYSTEM; LAMINARIA; MEDITERRANEAN SEA; PH; PHYSIOLOGY; RED ALGA;

ACIDS; ANIMALS; ANTHOZOA; BRYOZOA; CARBON DIOXIDE; CARBONATES; ECOSYSTEM; HYDROGEN-ION CONCENTRATION; LAMINARIA; MEDITERRANEAN SEA; RHODOPHYTA; SEAWATER;

EID: 84945934438     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2015.0587     Document Type: Article

References (44)

1. 3 system in the oceans. Science 305, 362-366. (doi:10.1126/science.1097329)
2. Pelejero C, Calvo E, Hoegh-Guldberg O. 2010 Paleoperspectives on ocean acidification. Trends Ecol. Evol. 25, 332-344. (doi:10.1016/j.tree.2010.02.002)
3. IPCC. 2013 Summary for policymakers. In Climate change 2013: the physical science basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change (eds TF Stocker et al.). Cambridge, UK: Cambridge University Press.
4. Penman DE, Hönisch B, Zeebe RE, Thomas E, Zachos JC. 2014 Rapid and sustained surface ocean acidification during the Paleocene-Eocene Thermal Maximum. Paleoceanography 29, 357-369. (doi:10. 1002/2014PA002621)
5. Gattuso JP, Mach KJ, Morgan GM. 2013 Ocean acidification and its impacts: an expert survey. Clim. Change 117, 725-738. (doi:10.1007/s10584-012- 0591-5)
6. 2 problem. Ann. Rev. Mar. Sci. 1, 169-192. (doi:10.1146/annurev. marine. 010908.163834)
7. 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, 419-1434. (doi:10.1111/j.1461-0248.2010. 01518.x)
8. Fabricius KE, De'ath G, Noonan S, Uthicke S. 2014 Ecological effects of ocean acidification and habitat complexity on reef-associated macroinvertebrate communities. Proc. R. Soc. B 281, 20132479. (doi:10.1098/rspb.2013.2479)
9. Hall-Spencer JM, Rodolfo-Metalpa R, Martin S, Ransome E, Fine M, Turner SM, Rowley SJ, Tedesco D, Buia MC. 2008 Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 454, 96-99. (doi:10.1038/ nature07051)
10. Fabricius KE et al. 2011 Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nat. Clim. Change 1, 1-5. (doi:10. 1038/NCLIMATE1122)
11. Inoue S, Kayanne H, Yamamoto S, Kurihara H. 2013 Spatial community shift from hard to soft corals in acidified water. Nat. Clim. Change 3, 683-687. (doi:10.1038/NCLIMATE1855)
12. Bianchi CN, Dando PR, Morri C. 2011 Increased diversity of sessile epibenthos at subtidal hydrothermal vents: seven hypotheses based on observations at Milos Island, Aegean Sea. Adv. Oceanogr. Limnol. 2, 1-31. (doi:10.1080/19475721. 2011.565804)
13. Pettit LR, Hart MB, Medina-Sánchez AN, Smart CW, Rodolfo-Metalpa R, Hall-Spencer JM, Prol- Ledesma RM. 2013 Benthic foraminifera show some resilience to ocean acidification in the northern Gulf of California, Mexico. Mar. Pollut. Bull. 73, 452-462. (doi:10.1016/j.marpolbul. 2013.02.011)
14. Kroeker KJ, Micheli F, Gambi MC, Martz TR. 2011 Divergent ecosystem responses within a benthic marine community to ocean acidification. Proc. Natl Acad. Sci. USA 108, 14 515-14 520. (doi:10.1073/ pnas.1107789108)
15. Canals M, Ballesteros E. 1997 Production of carbonate particles by phytobenthic communities on the Mallorca-Menorca shelf, northwestern Mediterranean Sea. Deep-Sea Res. II 44, 611-616. (doi:10.1016/S0967-0645(96)00095-1)
16. Ballesteros E. 2006 Mediterranean coralligenous assemblages: a synthesis of the present knowledge. Oceanogr. Mar. Biol. Annu. Rev. 44, 123-195.
17. Barbera C et al. 2003 Conservation and management of northeast Atlantic and Mediterranean maërl beds. Aquat. Conserv: Mar. Freshw. Ecosyst.13, S65-S76. (doi:10.1002/aqc.569)
18. Martin CS et al. 2013 Coralligenous and maërl habitats: predictive modelling to identify their spatial distributions across the Mediterranean Sea. Sci. Rep. 4, 5073. (doi:10.1038/srep05073)
19. Koch M, Bowes G, Ross C, Zhang XH. 2013 Climate change and ocean acidification effects on seagrasses and marine macroalgae. Glob. Change Biol. 19, 103-132. (doi:10.1111/j.1365-2486.2012.02791.x)
20. Maillard A, Mauffret A. 1993 Structure et volcanisme de la fosse de Valence (Méditerranée nord-occidentale). Bull. Soc. Géol. Fr. 164, 365-383.
21. Grasshoff K, Kremling K, Ehrhardt M. 1999 Methods of seawater analysis. Weinheim, Germany: Wiley-VCH.
22. 2 measurements. Sydney, Australia: North Pacific Marine Science Organization (PICES Special Publication, 3).
23. 2 system calculations. Oak Ridge, TN: Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, US Department of Energy.
24. Anderson MJ. 2001 A new method for nonparametric multivariate analysis of variance. Austral Ecol. 26, 32-46. (doi:10.1111/j.1442-9993.2001. 01070.pp.x)
25. Pinheiro JC, Bates D, DebRoy S, Sarkar D, R Core Team. 2014 Package 'nlme': linear and nonlinear mixed effects models. Version 3.1-117. See http:// CRAN.R-project.org/package=nlme.
26. Oksanen J, et al. 2013 Package 'vegan': community ecology package. Version 2.0-10.
27. Pinheiro JC, Bates D. 2000 Mixed-effects models in S and S-PLUS. New York, NY: Springer.
28. Chen IC, Hill JK, Ohlemüller R, Roy DB, Thomas CD. 2011 Rapid range shifts of species associated with high levels of climate warming. Science 333, 1024-1026. (doi:10.1126/science.1206432)
29. Zimmerman RC et al. 1997 Impacts of CO2 enrichment on productivity and light requirements of eelgrass. Plant Physiol. 115, 599-607. (doi:10. 1104/pp.115.2.599)
30. 2 enrichment: possible impacts of climate change and potential for remediation of coastal habitats. Mar. Ecol. Prog. Ser. 344, 1-13. (doi:10.3354/meps07084)
31. Bo M et al. 2012 Deep coral oases in the South Tyrrhenian Sea. PLoS ONE 7, e49870. (doi:10.1371/ journal.pone.0049870)
32. Joher S, Ballesteros E, Cebrián E, Sánchez N, Rodríguez-Prieto C. 2012 Deep-water macroalgaldominated coastal detritic assemblages on the continental shelf off Mallorca and Menorca (Balearic Islands, Western Mediterranean). Bot. Mar. 55, 485-497. (doi:10.1515/bot-2012-0113)
33. 2 enhances the competitive strength of seaweeds over corals. Ecol. Lett. 14, 156-162. (doi:10.1111/j.1461-0248.2010. 01565.x)
34. Doropoulos C, Ward S, Diaz-Pulido G, Hoegh- Guldberg O, Mumby PJ. 2012 Ocean acidification reduces coral recruitment by disrupting intimate larval-algal settlement interactions. Ecol. Lett. 15, 338-346. (doi:10.1111/j.1461-0248.2012.01743.x)
35. Porzio L, Buia MC, Hall-Spencer JM. 2011 Effects of ocean acidification on macroalgal communities. J. Exp. Mar. Biol. Ecol. 400, 278-287. (doi:10.1016/ j.jembe.2011.02.011)
36. Kuffner IB, Andersson AJ, Jokiel PL, Rodgers KS, Mackenzie FT. 2008 Decreased abundance of crustose coralline algae due to ocean acidification. Nat. Geosci. 1, 114-117. (doi:10. 1038/ngeo100)
37. Nash MC, Troitzsch U, Opdyke BN, Trafford JM, Russell BD, Kline DI. 2011 First discovery of dolomite and magnesite in living coralline algae and its geobiological implications. Biogeosciences 8, 3331-3340. (doi:10.5194/bg-8-3331-2011)
38. Nash MCE et al. 2013 Dolomite-rich coralline algae in reefs resist dissolution in acidified conditions. Nat. Clim. Change 3, 268-272. (doi:10.1038/ nclimate1760)
39. Hofmann GE et al. 2011 High-frequency dynamics of ocean pH: a multi-ecosystem comparison. PloS ONE 6, e28983. (doi:10.1371/journal.pone. 0028983)
40. Hofmann G, Kelley AL, Shaw EC, Martz TR, Hofmann GE. 2015 Near-shore Antarctic pH variability has implications for the design of ocean acidification experiments. Sci. Rep. 5, 9638. (doi:10.1038/ srep09638)
41. Hoegh-Guldberg O et al. 2007 Coral reefs under rapid climate change and ocean acidification. Science 318, 1737-1742. (doi:10.1126/science. 1152509)
42. Crain CM, Kroeker K, Halpern BS. 2008 Interactive and cumulative effects of multiple human stressors in marine systems. Ecol. Lett. 11, 1304-1315. (doi:0.1111/j.1461-0248.2008.01253.x)
43. Crowe TP et al. 2013 Large-scale variation in combined impacts of canopy loss and disturbance on community structure and ecosystem functioning. PLoS ONE 8, e66238. (doi:10.1371/journal.pone. 0066238)
44. Thibaut T, Pinedo S, Torras X, Ballesteros E. 2005 Long-term decline of the populations of Fucales (Cystoseira spp. and Sargassum spp.) in the Albères coast (France, Northwestern Mediterranean). Mar. Pollut. Bull. 50, 1472-1489. (doi:10.1016/j. marpolbul.2005.06.014)