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Coral Reefs

, Volume 34, Issue 3, pp 955–966 | Cite as

Effects of seawater acidification on a coral reef meiofauna community

  • V. C. Sarmento
  • T. P. Souza
  • A. M. Esteves
  • P. J. P. Santos
Report

Abstract

Despite the increasing risk that ocean acidification will modify benthic communities, great uncertainty remains about how this impact will affect the lower trophic levels, such as members of the meiofauna. A mesocosm experiment was conducted to investigate the effects of water acidification on a phytal meiofauna community from a coral reef. Community samples collected from the coral reef subtidal zone (Recife de Fora Municipal Marine Park, Porto Seguro, Bahia, Brazil), using artificial substrate units, were exposed to a control pH (ambient seawater) and to three levels of seawater acidification (pH reductions of 0.3, 0.6, and 0.9 units below ambient) and collected after 15 and 30 d. After 30 d of exposure, major changes in the structure of the meiofauna community were observed in response to reduced pH. The major meiofauna groups showed divergent responses to acidification. Harpacticoida and Polychaeta densities did not show significant differences due to pH. Nematoda, Ostracoda, Turbellaria, and Tardigrada exhibited their highest densities in low-pH treatments (especially at the pH reduction of 0.6 units, pH 7.5), while harpacticoid nauplii were strongly negatively affected by low pH. This community-based mesocosm study supports previous suggestions that ocean acidification induces important changes in the structure of marine benthic communities. Considering the importance of meiofauna in the food web of coral reef ecosystems, the results presented here demonstrate that the trophic functioning of coral reefs is seriously threatened by ocean acidification.

Keywords

Coral reefs Ocean acidification Climate change Benthos Marine Park 

Notes

Acknowledgments

VC Sarmento gratefully acknowledges a PhD scholarship from the Fundação de Amparo à Ciência e Tecnologia do Estado de Pernambuco (FACEPE), and PJP Santos (CNPq 305417/2011-8) and AM Esteves (CNPq 312143/2013-3) acknowledge research fellowships from the Conselho Nacional de Ciência e Tecnologia (CNPq). We thank Alex M. Silva for help with meiofauna extraction and Dr. Janet W. Reid for English language revision. Special thanks are also due to the ‘Rede de Pesquisas Coral Vivo,’ to Petrobras and to the Arraial d’Ajuda Eco Parque, for all logistical assistance provided. We are grateful to the reviewers for their incisive and helpful comments on the manuscript.

References

  1. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46Google Scholar
  2. Araújo-Castro CMV, Souza-Santos LP (2005) Are the diatoms Navicula sp. and Thalassiosira fluviatilis suitable to be fed to the benthic harpacticoid copepod Tisbe biminiensis? J Exp Mar Biol Ecol 327:58–69CrossRefGoogle Scholar
  3. Barry JP, Buck KR, Lovera CF, Kuhnz L, Whaling PJ, Peltzer ET, Walz P, Brewer PG (2004) Effects of direct ocean CO2 injection on deep-sea meiofauna. J Oceanogr 60:759–766CrossRefGoogle Scholar
  4. Berkström C, Jones GP, McCormick MI, Srinivasan M (2012) Ecological versatility and its importance for the distribution and abundance of coral reef wrasses. Mar Ecol Prog Ser 461:151–163CrossRefGoogle Scholar
  5. Bibby R, Cleall-Harding P, Rundle S, Widdicombe S, Spicer J (2007) Ocean acidification disrupts induced defences in the intertidal gastropod Littorina littorea. Biol Lett 3:699–701PubMedCentralPubMedCrossRefGoogle Scholar
  6. Birkeland C (1997) Life and death of coral reefs. Chapman and Hall, New YorkCrossRefGoogle Scholar
  7. Bishop MJ (2005) Artificial sampling units: a tool for increasing the sensitivity of tests for impact in soft sediments. Environ Monit Assess 107:203–220PubMedCrossRefGoogle Scholar
  8. Byrne M (2012) Global change ecotoxicology: Identification of early life history bottlenecks in marine invertebrates, variable species responses and variable experimental approaches. Mar Environ Res 76:3–15PubMedCrossRefGoogle Scholar
  9. 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 Lond B Biol Sci 368:20120439PubMedCentralPubMedCrossRefGoogle Scholar
  10. Caldeira K, Wickett M (2003) Anthropogenic carbon and ocean pH. Nature 425:365PubMedCrossRefGoogle Scholar
  11. Caldeira K, Wickett M (2005) Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean. J Geophys Res 110:1–12Google Scholar
  12. Calosi P, Rastrick SPS, Lombardi C, Guzman HJ, Davidson L, Jahnke M, Giangrande A, Hardege JD, Schulze A, Spicer JI, Gambi MC (2013) Adaptation and acclimatization to ocean acidification in marine ectotherms: an in situ transplant experiment with polychaetes at a shallow CO2 vent system. Proc R Soc Lond B Biol Sci 368:20120444CrossRefGoogle Scholar
  13. Carman KR, Thistle D, Fleeger JW, Barry JP (2004) Influence of introduced CO2 on deep-sea metazoan meiofauna. J Oceanogr 60:767–772CrossRefGoogle Scholar
  14. Castro P, Huber ME (2010) Marine Biology, 8th edn. The McGraw-Hill Companies, New YorkGoogle Scholar
  15. Ceballos-Osuna L, Carter HA, Miller NA, Stillman JH (2013) Effects of ocean acidification on early life-history stages of the intertidal porcelain crab Petrolisthes cinctipes. J Exp Biol 216:1405–1411PubMedCrossRefGoogle Scholar
  16. Christen N, Calosi P, McNeill CL, Widdicombe S (2013) Structural and functional vulnerability to elevated pCO2 in marine benthic communities. Mar Biol 160:2113–2128CrossRefGoogle Scholar
  17. Cigliano M, Gambi MC, Rodolfo-Metalpa R, Patti FP, Hall-Spencer JM (2010) Effects of ocean acidification on invertebrate settlement at volcanic CO2 vents. Mar Biol 157:2489–2502CrossRefGoogle Scholar
  18. Cumbo VR, Fan TY, Edmunds PJ (2013) Effects of exposure duration on the response of Pocillopora damicornis larvae to elevated temperature and high pCO2. J Exp Mar Bio Ecol 439:100–107CrossRefGoogle Scholar
  19. Dahl U, Lind CR, Gorokhova E, Eklund B, Breitholtz M (2009) Food quality effects on copepod growth and development: Implications for bioassays in ecotoxicological testing. Ecotoxicol Environ Saf 72:351–357PubMedCrossRefGoogle Scholar
  20. Danovaro R, Scopa M, Gambi C, Franschetti S (2007) Trophic importance of subtidal metazoan meiofauna: evidence from in situ exclusion experiments on soft and rocky substrates. Mar Biol 152:339–350CrossRefGoogle Scholar
  21. Dashfield SL, Somerfield PJ, Widdicombe S, Austen MC, Nimmo M (2008) Impacts of ocean acidification and burrowing urchins on within-sediment pH profiles and subtidal nematode communities. J Exp Mar Bio Ecol 365:46–52CrossRefGoogle Scholar
  22. De Troch M, Vandepitte L, Raes M, Suárez-Morales E, Vincx M (2005) A field colonization experiment with meiofauna and seagrass mimics: effect of time, distance and leaf surface area. Mar Biol 148:73–86CrossRefGoogle Scholar
  23. De’ath G, Fabricius K, Lough J (2013) Yes – Coral calcification rates have decreased in the last twenty-five years! Mar Geol 346:400–402CrossRefGoogle Scholar
  24. Dickson AG, Sabine CL, Christian JR (2007) Guide to best practices for ocean CO2 measurements. PICES Special Publication 3, SidneyGoogle Scholar
  25. Dupont S, Thorndyke MC (2009) Impact of CO2-driven ocean acidification on invertebrates early life-history – What we know, what we need to know and what we can do. Biogeosci Discuss 6:3109–3131CrossRefGoogle Scholar
  26. Dupont S, Dorey N, Thorndyke MC (2010) What meta-analysis can tell us about vulnerability of marine biodiversity to ocean acidification? Estuar Coast Shelf Sci 89:182–185CrossRefGoogle Scholar
  27. Ellis RP, Bersey J, Rundle SD, Hall-Spencer JM, Spicer JI (2009) Subtle but significant effects of CO2 acidified seawater on embryos of the intertidal snail, Littorina obtusata. Aquat Biol 5:41–48CrossRefGoogle Scholar
  28. Fabricius K, De’ath G (2001) Environmental factors associated with the spatial distribution of crustose coralline algae on the Great Barrier Reef. Coral Reefs 19:303–309CrossRefGoogle Scholar
  29. 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 Lond B Biol Sci 281:20132479CrossRefGoogle Scholar
  30. Fabricius KE, Langdon C, Uthicke S, Humphrey C, Noonan S, De’ath G, Okazaki R, Muehllehner N, Glas MS, Lough JM (2011) Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nat Clim Chang 1:165–169CrossRefGoogle Scholar
  31. Feely RA, Doney SC, Cooley SR (2009) Ocean acidification: present conditions and future changes in a high-CO2 world. Oceanography 22:36–47CrossRefGoogle Scholar
  32. 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 305:362–366PubMedCrossRefGoogle Scholar
  33. Findlay HS, Kendall MA, Spicer JI, Widdicombe S (2010) Post-larval development of two intertidal barnacles at elevated CO2 and temperature. Mar Biol 157:725–735CrossRefGoogle Scholar
  34. Fitzer SC, Caldwell GS, Clare AS, Upstill-Goddard RC, Bentley MG (2013) Response of copepods to elevated pCO2 and environmental copper as co-stressors – A multigenerational study. PLoS One 8:e71257PubMedCentralPubMedCrossRefGoogle Scholar
  35. Fitzer SC, Caldwell GS, Close AJ, Clare AS, Upstill-Goddard RC, Bentley MG (2012) Ocean acidification induces multi-generational decline in copepod naupliar production with possible conflict for reproductive resource allocation. J Exp Mar Bio Ecol 418–419:30–36CrossRefGoogle Scholar
  36. Fleeger JW, Johnson DS, Carman KR, Weisenhorn PB, Gabriele A, Thistle D, Barry JP (2010) The response of nematodes to deep-sea CO2 sequestration: A quantile regression approach. Deep Sea Res Part I Oceanogr Res Pap 57:696–707CrossRefGoogle Scholar
  37. Gaylord B, Kroeker KJ, Sunday JM, Anderson KM, Barry JP, Brown NE, Connell SD, Dupont S, Fabricius KE, Hall-Spencer JM, Klinger T, Milazzo M, Munday PI, Russell BD, Sanford E, Schreiber SJ, Thiyagarajan V, Vaughan MLH, Widdicombe S, Harley CDG (2015) Ocean acidification through the lens of ecological theory. Ecology 96:3–15PubMedCrossRefGoogle Scholar
  38. Gibbons MJ, Griffiths CL (1986) A comparison of macrofaunal and meiofaunal distribution and standing stock across a rocky shore, with an estimate of their productivities. Mar Biol 3:181–188CrossRefGoogle Scholar
  39. Giere O (2009) Meiobenthology: The microscopic motile fauna of aquatic sediments, 2nd edn. Springer-Verlag, BerlinGoogle Scholar
  40. Gobin JF, Warwick RM (2006) Geographical variation in species diversity: A comparison of marine polychaetes and nematodes. J Exp Mar Bio Ecol 330:234–244CrossRefGoogle Scholar
  41. Gutiérrez JL, Jones CG, Byers JE, Arkema KK, Berkenbusch K, Commito JA, Duarte CM, Hacker SD, Lambrinos JG, Hendriks IE, Hogarth PJ, Palomo MG, Wild C (2011) Physical ecosystem engineers and the functioning of estuaries and coasts. In: Wolanski E, McLusky DS (eds) Treatise on estuarine and coastal science. Waltham: Academic 7:53–81Google Scholar
  42. Hale R, Calosi P, McNeill L, Mieszkowska N, Widdicombe S (2011) Predicted levels of future ocean acidification and temperature rise could alter community structure and biodiversity in marine benthic communities. Oikos 120:661–674CrossRefGoogle Scholar
  43. 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 454:96–99PubMedCrossRefGoogle Scholar
  44. Hargrave CW, Gary KP, Rosado SK (2009) Potential effects of elevated atmospheric carbon dioxide on benthic autotrophs and consumers in stream ecosystems: a test using experimental stream mesocosms. Glob Chang Biol 15:2779–2790CrossRefGoogle Scholar
  45. Hendriks IE, Duarte CM (2010) Ocean acidification: Separating evidence from judgment – A reply to Dupont et al. Estuar Coast Shelf Sci 89:186–190CrossRefGoogle Scholar
  46. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742PubMedCrossRefGoogle Scholar
  47. Hoey AS, Bellwood DR (2010) Cross-shelf variation in browsing intensity on the Great Barrier Reef. Coral Reefs 29:499–508CrossRefGoogle Scholar
  48. IPCC (2013) Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, New York, NY, USAGoogle Scholar
  49. IPCC (2014) Climate Change 2014: Impacts, Adaptation, and Vulnerability. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, New York, NY, USAGoogle Scholar
  50. Ishida H, Watanabe Y, Fukuhara T, Kaneko S, Furusawa K, Shirayama Y (2005) In situ enclosure experiment using a benthic chamber system to assess the effect of high concentration of CO2 on deep-sea benthic communities. J Oceanogr 61:835–843CrossRefGoogle Scholar
  51. Ishida H, Golmen LG, West J, Krüger M, Coombs P, Berge JA, Fukuhara T, Magi M, Kita J (2013) Effects of CO2 on benthic biota: An in situ benthic chamber experiment in Storfjorden (Norway). Mar Pollut Bull 73:443–451PubMedCrossRefGoogle Scholar
  52. Johnson VR, Brownlee C, Rickaby REM, Graziano M, Milazzo M, Hall-Spencer JM (2013) Responses of marine benthic microalgae to elevated CO2. Mar Biol 160:1813–1824CrossRefGoogle Scholar
  53. 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
  54. Kelaher BP (2003) Changes in habitat complexity negatively affect diverse gastropod assemblages in coralline algal turf. Oecologia 135:431–441PubMedCrossRefGoogle Scholar
  55. Kennedy A, Jacoby C (1999) Biological indicators of marine environmental health: meiofauna–a neglected benthic component? Environ Monit Assess 54:47–68CrossRefGoogle Scholar
  56. Kleypas JA, Yates KK (2009) Coral reefs and ocean acidification. Oceanography 22:108–117CrossRefGoogle Scholar
  57. Kramer MJ, Bellwood O, Bellwood DR (2012) Cryptofauna of the epilithic algal matrix on an inshore coral reef, Great Barrier Reef. Coral Reefs 31:1007–1015CrossRefGoogle Scholar
  58. Kramer MJ, Bellwood O, Bellwood DR (2013) The trophic importance of algal turfs for coral reef fishes: the crustacean link. Coral Reefs 32:575–583CrossRefGoogle Scholar
  59. 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 108:14515–14520PubMedCentralPubMedCrossRefGoogle Scholar
  60. Kurihara H (2008) Effects of CO2-driven ocean acidification on the early developmental stages of invertebrates. Mar Ecol Prog Ser 373:275–284CrossRefGoogle Scholar
  61. 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 56:1086–1090PubMedCrossRefGoogle Scholar
  62. 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
  63. Kurihara H, Ishimatsu A, Shirayama Y (2007) Effects of elevated seawater CO2 concentration on the meiofauna. J Mar Sci Technol Special Issue:17–22Google Scholar
  64. Leão ZMAN, Dominguez JML (2000) Tropical coast of Brazil. Mar Pollut Bull 41:112–122CrossRefGoogle Scholar
  65. Li W, Gao K (2012) A marine secondary producer respires and feeds more in a high CO2 ocean. Mar Pollut Bull 64:699–703PubMedCrossRefGoogle Scholar
  66. Lidbury I, Johnson V, Hall-Spencer JM, Munn CB, Cunliffe M (2012) Community-level response of coastal microbial biofilms to ocean acidification in a natural carbon dioxide vent ecosystem. Mar Pollut Bull 64:1063–1066PubMedCrossRefGoogle Scholar
  67. Maida M, Ferreira BP (1997) Coral reefs of Brazil: an overview. Proc 8th Int Coral Reef Symp 1:263–274Google Scholar
  68. Matias MG, Underwood AJ, Coleman RA (2007) Interactions of components of habitat alter composition and variability of assemblages. J Anim Ecol 76:986–994PubMedCrossRefGoogle Scholar
  69. Mayor DJ, Matthews C, Cook K, Zuur AF, Hay S (2007) CO2-induced acidification affects hatching success in Calanus finmarchicus. Mar Ecol Prog Ser 350:91–97CrossRefGoogle Scholar
  70. McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance based redundancy analysis. Ecology 82:290–297CrossRefGoogle Scholar
  71. Mirto S, Danovaro R (2004) Meiofaunal colonisation on artificial substrates: a tool for biomonitoring the environmental quality on coastal marine systems. Mar Pollut Bull 48:919–926PubMedCrossRefGoogle Scholar
  72. Morita M, Suwa R, Iguchi A, Nakamura M, Shimada K, Sakai K, Suzuki A (2009) Ocean acidification reduces sperm flagellar motility in broadcast spawning reef invertebrates. Zygote 18:103–107CrossRefGoogle Scholar
  73. Pascal PY, Fleeger JW, Galvez F, Carman KR (2010) The toxicological interaction between ocean acidity and metals in coastal meiobenthic copepods. Mar Pollut Bull 60:2201–2208PubMedCrossRefGoogle Scholar
  74. Pörtner HO, Langenbuch M, Reipschläger A (2004) Biological impact of elevated ocean CO2 concentrations: lessons from animal physiology and earth history. J Oceanogr 60:705–718CrossRefGoogle Scholar
  75. Porzio L, Buia MC, Hall-Spencer JM (2011) Effects of ocean acidification on macroalgal communities. J Exp Mar Bio Ecol 400:278–287CrossRefGoogle Scholar
  76. Riebesell U, Fabry VJ, Hansson L, Gattuso JP (2010) Guide to best practices for ocean acidification research and data reporting. Publications Office of the European Union, Luxembourg, p 260Google Scholar
  77. Robbins LL, Hansen ME, Kleypas JA, Meylan SC (2010) CO2calc—A user-friendly seawater carbon calculator for Windows, Max OS X, and iOS (iPhone): U.S. Geological Survey Open-File Report 2010–1280Google Scholar
  78. Roberts CM, McClean CJ, Veron JEN, Hawkins JP, Allen GR, McAllister DE, Mittermeier CG, Schueler FW, Spalding M, Wells F, Vynne C, Werner TB (2002) Marine biodiversity hotspots and conservation priorities for tropical reefs. Science 295:1280–1284PubMedCrossRefGoogle Scholar
  79. Rossoll D, Bermúdez R, Hauss H, Schulz KG, Riebesell U, Sommer U, Winder M (2012) Ocean acidification-induced food quality deterioration constrains trophic transfer. PLoS One 7:e34737PubMedCentralPubMedCrossRefGoogle Scholar
  80. Ruppert EE, Fox RS, Barnes RD (2004) Invertebrate zoology: A functional evolutionary approach, 7th edn. Brooks/Cole, Thomson Learning, BelmontGoogle Scholar
  81. Sabine CL, Feely RA, Gruber N, Key RM, Lee K, Bullister JL, Wanninkhof R, Wong CS, Wallace DWR, Tilbrook B, Millero FJ, Peng TH, Kozyr A, Ono T, Rios AF (2004) The oceanic sink for anthropogenic CO2. Science 305:367–371PubMedCrossRefGoogle Scholar
  82. Santos HF, Carmo FL, Duarte G, Dini-Andreote F, Castro CB, Rosado AS, Elsas JD, Peixoto RS (2014) Climate change affects key nitrogen-fixing bacterial populations on coral reefs. ISME J 8:2272–2279PubMedCrossRefGoogle Scholar
  83. Sarmento VC, Santos PJP (2012) Trampling on coral reefs: tourism effects on harpacticoid copepods. Coral Reefs 31:135–146CrossRefGoogle Scholar
  84. Snelgrove PVR, Butman CA (1994) Animal–sediment relationships revisited: cause versus effect. Oceanogr Mar Biol 32:111–177Google Scholar
  85. Sung CG, Kim TW, Park YG, Kang SG, Inaba K, Shiba K, Choi TS, Moon SD, Litvin S, Lee KT, Lee JS (2014) Species and gamete-specific fertilization success of two sea urchins under near future levels of pCO2. J Mar Syst 137:67–73CrossRefGoogle Scholar
  86. Takeuchi K, Fujioka Y, Kawasaki Y, Shirayama Y (1997) Impacts of high concentration of CO2 on marine organisms; a modification of CO2 ocean sequestration. Energy Convers Manag 38:337–341CrossRefGoogle Scholar
  87. Thistle D, Carman KR, Sedlacek L, Brewer PG, Fleeger JW, Barry JP (2005) Deep-ocean, sediment-dwelling animals are sensitive to sequestered carbon dioxide. Mar Ecol Prog Ser 289:1–4CrossRefGoogle Scholar
  88. Underwood AJ, Chapman MG (1996) Scales of spatial patterns of distribution of intertidal invertebrates. Oecologia 107:212–224CrossRefGoogle Scholar
  89. Underwood AJ, Chapman MG (2006) Early development of subtidal macrofaunal assemblages: relationships to period and timing of colonization. J Exp Mar Bio Ecol 330:221–233CrossRefGoogle Scholar
  90. 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 33:831–845CrossRefGoogle Scholar
  91. van Hooidonk R, Maynard JA, Manzello D, Planes S (2014) Opposite latitudinal gradients in projected ocean acidification and bleaching impacts on coral reefs. Glob Chang Biol 20:103–112PubMedCrossRefGoogle Scholar
  92. Webster NS, Negri AP, Flores F, Humphrey C, Soo R, Botté ES, Vogel N, Uthicke S (2013) Near-future ocean acidification causes differences in microbial associations within diverse coral reef taxa. Environ Microbiol Rep 5:243–251PubMedCrossRefGoogle Scholar
  93. White AT, Vogt HP, Arin T (2000) Philippine coral reefs under threat: the economic losses caused by reef destruction. Mar Pollut Bull 40:598–605CrossRefGoogle Scholar
  94. Widdicombe S, Dashfield SL, McNeill CL, Needham HR, Beesley A, McEvoy A, Øxnevad S, Clarke KR, Berge JA (2009) Effects of CO2 induced seawater acidification on infaunal diversity and sediment nutrient fluxes. Mar Ecol Prog Ser 379:59–75CrossRefGoogle Scholar
  95. Wieser W, Ott J, Schiemer F, Gnaiger E (1974) An ecophysiological study of some meiofauna species inhabiting a sandy beach at Bermuda. Mar Biol 26:235–248CrossRefGoogle Scholar
  96. Wilkinson CR (1996) Global change and coral reefs: impacts on reefs, economies and human cultures. Glob Chang Biol 2:547–558CrossRefGoogle Scholar
  97. Wismer S, Hoey AS, Bellwood DR (2009) Cross-shelf benthic community structure on the Great Barrier Reef: relationships between macroalgal cover and herbivore biomass. Mar Ecol Prog Ser 376:45–54CrossRefGoogle Scholar
  98. Witt V, Wild C, Anthony KRN, Diaz-Pulido G, Uthicke S (2011) Effects of ocean acidification on microbial community composition of, and oxygen fluxes through, biofilms from the Great Barrier Reef. Environ Microbiol 13:2976–2989PubMedCrossRefGoogle Scholar
  99. Wyckmans M, Chepurnov VA, Vanreusel A, De Troch M (2007) Effects of food diversity on diatom selection by harpacticoid copepods. J Exp Mar Bio Ecol 345:119–128CrossRefGoogle Scholar
  100. Zar JH (1996) Biostatistical Analysis, 3rd edn. Prentice-Hall, New JerseyGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • V. C. Sarmento
    • 1
  • T. P. Souza
    • 1
  • A. M. Esteves
    • 1
  • P. J. P. Santos
    • 1
  1. 1.Departamento Zoologia, Centro de Ciências BiológicasUniversidade Federal de PernambucoRecifeBrazil

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