in

A high biodiversity mitigates the impact of ocean acidification on hard-bottom ecosystems

  • 1.

    Doney, S. C., Fabry, V. J., Feely, R. A. & Kleypas, J. A. Ocean Acidification: The Other CO2 Problem. Annu. Rev. Mar. Sci. 1, 169–92 (2009).

  • 2.

    Cerrano, C. et al. Red coral extinction risk enhanced by ocean acidification. Sci. Rep. 3, 1457 (2013).

  • 3.

    Bramanti, L. et al. Detrimental effects of ocean acidification on the economically important Mediterranean red coral (Corallium rubrum). Glob. Change Biol. 19, 1897–1908 (2013).

  • 4.

    Pörtner, H. O. et al. Ocean systems. In: Climate Change 2014: Impacts, Adaptation, and Vulnerability. Part A: Global and Sectoral Aspects. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change (eds: Field, C. B. et al.). Cambridge University Press, Cambridge, United Kingdom and New York, USA, pp. 411–484. (2014).

  • 5.

    Gattuso, J. P. et al. Contrasting futures for ocean and society from different anthropogenic CO2 emissions scenarios. Science 349, aac4722 (2015).

  • 6.

    Kroeker, K. J., Kordas, R. L., Crim, R. N. & Singh, G. G. Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecol. Lett. 13, 1419–1434 (2010).

  • 7.

    Goodwin, C., Rodolfo-Metalpa, R., Picton, B. & Hall-Spencer, J. M. Effects of ocean acidification on sponge communities. Mar. Ecol.-Evol. Persp. 35, 41–49 (2014).

  • 8.

    Martin, S., & Hall-Spencer, J. M. Effects of Ocean Warming and Acidification on Rhodolith/Maërl Beds. In Rhodolith/Maërl Beds: A Global Perspective Springer. International Publishing, pp. 55–85 (2017).

  • 9.

    Wernberg, T., Smale, D. A. & Thomsen, M. S. A decade of climate change experiments on marine organisms: procedures, patterns and problems. Glob. Change Biol. 18, 1491–1498 (2012).

  • 10.

    Kroeker, K. J., Gambi, M. C. & Micheli, F. Community dynamics and ecosystem simplification in a high-CO2 ocean. Proc. Natl. Acad. Sci. USA 110, 12721–12726 (2013).

  • 11.

    Foster, T., Falter, J. L., McCulloch, M. T. & Clode, P. L. Ocean acidification causes structural deformities in juvenile coral skeletons. Sci. Adv. 2, e1501130 (2016).

  • 12.

    Loreau, M. et al. Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294, 804–808 (2001).

  • 13.

    Naeem, S., Bunker, D. E., Hector, A., Loreau, M. & Perrings, C. Biodiversity, Ecosystem-Functioning, and Human Wellbeing. Oxford University Press, New York. (2009).

  • 14.

    Duffy, J. E. Why biodiversity is important to the functioning of real‐world ecosystems. Front. Ecol. Environ. 7, 437–444 (2009).

    • Article
    • Google Scholar
  • 15.

    Worm, B. et al. Impacts of biodiversity loss on ocean ecosystem services. Science 314, 787–790 (2006).

  • 16.

    Cardinale, B. J. et al. Biodiversity loss and its impact on humanity. Nature 486, 59 (2012).

  • 17.

    Tilman, D., Isbell, F. & Cowles, J. M. Biodiversity and ecosystem functioning. Annu. Rev. Ecol. Evol. Syst. 45, 471–493 (2014).

    • Article
    • Google Scholar
  • 18.

    Tilman, D., Reich, P. B. & Isbell, F. Biodiversity impacts ecosystem productivity as much as resources, disturbance, or herbivory. Proc. Natl. Acad. Sci. USA 109, 10394–10397 (2012).

  • 19.

    Hooper, D. U. et al. A global synthesis reveals biodiversity loss as a major driver of ecosystem change. Nature 486, 105–108 (2012).

  • 20.

    Paine, R. T. A note on trophic complexity and community stability. Am. Nat. 103, 91–93 (1969).

    • Article
    • Google Scholar
  • 21.

    Smith, C., et al. Report on identification of keystone species and processes across regional seas. Deliverable 6.1, DEVOTES Project. 105 pp. https://hal.archives-ouvertes.fr/hal-01790558 (2015).

  • 22.

    Coleman, F. C. & Williams, S. L. Overexploiting marine ecosystem engineers: potential consequences for biodiversity. Trends Ecol. Evol. 17, 40–44 (2002).

    • Article
    • Google Scholar
  • 23.

    Heithaus, M. R., Frid, A., Wirsing, A. J. & Worm, B. Predicting ecological consequences of marine top predator declines. Trends Ecol. Evol. 23, 202–210 (2008).

  • 24.

    Linares, C. et al. Immediate and delayed effects of a mass mortality event on gorgonian population dynamics and benthic community structure in the NW Mediterranean Sea. Mar. Ecol. Progr. Ser. 305, 127–137 (2005).

  • 25.

    Ponti, M. et al. Ecological shifts in Mediterranean coralligenous assemblages related to gorgonian forest loss. PLoS One 9, e102782 (2014).

  • 26.

    Yachi, S. & Loreau, M. Biodiversity and ecosystem productivity in a fluctuating environment: The insurance hypothesis. Proc. Natl Acad. Sci. USA 96, 1463–1468 (1999).

  • 27.

    Hector, A. & Bagchi, R. Biodiversity and ecosystem multifunctionality. Nature 448, 188–90 (2007).

  • 28.

    Loreau, M. & de Mazancourt, C. Biodiversity and ecosystem stability: a synthesis of underlying mechanisms. Ecol. Lett. 16, 106–115 (2013).

  • 29.

    Mori, A. S., Furukawa, T. & Sasaki, T. Response diversity determines the resilience of ecosystems to environmental change. Biol. Rev. 88, 349–364 (2013).

  • 30.

    Nagelkerken, I. & Connell, S. D. Global alteration of ocean ecosystem functioning due to increasing human CO2 emissions. Proc. Natl. Acad. Sci. USA 112, 13272–13277 (2015).

  • 31.

    Gilman, S. E., Urban, M. C., Tewksbury, J., Gilchrist, G. W. & Holt, R. D. A framework for community interactions under climate change. Trends Ecol. Evol. 25, 325–331 (2010).

  • 32.

    Tylianakis, J. M., Didham, R. K., Bascompte, J. & Wardle, D. A. Global change and species interactions in terrestrial ecosystems. Ecol. Lett. 11, 1351–1363 (2008).

  • 33.

    Davis, A. J., Jenkinson, L. S., Lawton, J. H., Shorrocks, B. & Wood, S. Making mistakes when predicting shifts in species range in response to global warming. Nature 391, 783–786 (1998).

  • 34.

    González-Megías, A. & Menéndez, R. Climate change effects on above- and below-ground interactions in a dryland ecosystem. Philos. T. R. Soc. B. 367, 3115–3124 (2012).

    • Article
    • Google Scholar
  • 35.

    Liancourt, P. et al. Plant response to climate change varies with topography, interactions with neighbors, and ecotype. Ecology 94, 444–453 (2013).

  • 36.

    Suttle, K. B., Thomsen, M. A. & Power, M. E. Species interactions reverse grassland responses to changing climate. Science 315, 640–642 (2007).

  • 37.

    Falkowski, P. G., Fenchel, T. & Delong, E. F. The microbial engines that drive earth’s biogeochemical cycles. Science 320, 1034–1039 (2008).

  • 38.

    Gasol, J. M., & Kirchman, D. L. Microbial ecology of the oceans. John Wiley & Sons. 528 pp. (2018).

  • 39.

    Danovaro, R. et al. Marine viruses and global climate change. FEMS Microbiol. Rev. 35, 993–1034 (2011).

  • 40.

    Ribes, M. et al. Restructuring of the sponge microbiome favors tolerance to ocean acidification. Environ. Microbiol. Rep. 8, 536–544 (2016).

  • 41.

    Torda, G. et al. Rapid adaptive responses to climate change in corals. Nat. Clim. Change 7, 627–636 (2017).

  • 42.

    Bourne, D. G., Morrow, K. M. & Webster, N. S. Insights into the coral microbiome: underpinning the health and resilience of reef ecosystems. Annu. Rev. Microbiol. 70, 317–340 (2016).

  • 43.

    Casas-Güell, E. et al. Structure and biodiversity of coralligenous assemblages dominated by the precious red coral Corallium rubrum over broad spatial scales. Sci. Rep. 6, 36535 (2016).

  • 44.

    Ballesteros, E. Mediterranean coralligenous assemblages: A synthesis of present knowledge. Oceanography and Marine Biology – An Annual Review 44, 123–195 (2006).

    • Google Scholar
  • 45.

    Kipson, S. et al. Preliminary list of typical/indicator species within Croatian Coralligenous Monitoring Protocol. In Second Mediterranean Symposium on the conservation of Coralligenous and other Calcareous Bio-Concretions (pp. 219-220) RAC/SPA publ. (2014).

  • 46.

    Garrabou, J., Ballesteros, E. & Zabala, M. Structure and dynamics of north-western Mediterranean rocky benthic communities along a depth gradient. Estuar. Coast. Shelf S. 55, 493–508 (2002).

    • Article
    • Google Scholar
  • 47.

    Cornwall, C. E. et al. Diurnal fluctuations in seawater pH influence the response of a calcifying macroalga to ocean acidification. P. Roy. Soc. B-Biol. Sci. 280, 20132201 (2013).

  • 48.

    Rivest, E. B., Comeau, S. & Cornwall, C. E. The role of natural variability in shaping the response of coral reef organisms to climate change. Curr. Clim. Change Rep. 3, 271–281 (2017).

    • Article
    • Google Scholar
  • 49.

    Vargas, C. A. et al. Species-specific responses to ocean acidification should account for local adaptation and adaptive plasticity. Nat. Ecol. Evol. 1, 0084 (2017).

    • Article
    • Google Scholar
  • 50.

    Anthony, K. R. N., Kleypas, J. A. & Gattuso, J. P. Coral reefs modify their seawater carbon chemistry-implications for impacts of ocean acidification. Glob. Change Biol. 17, 3655–3666 (2011).

  • 51.

    Cornwall, C. E. et al. Resistance of corals and coralline algae to ocean acidification: physiological control of calcification under natural pH variability. P. Roy. Soc. B-Biol. Sci. 285, 20181168 (2018).

  • 52.

    Kroeker, K. J. et al. Ecological change in dynamic environments: Accounting for temporal environmental variability in studies of ocean change biology. Glob. Change Biol. (2019).

  • 53.

    Bevilacqua, S., Guarnieri, G., Farella, G., Terlizzi, A. & Fraschetti, S. A regional assessment of cumulative impact mapping on Mediterranean coralligenous outcrops. Sci. Rep. 8, 1757 (2018).

  • 54.

    Zunino, S., Canu, D. M., Zupo, V. & Solidoro, C. Direct and indirect impacts of marine acidification on the ecosystem services provided by coralligenous reefs and seagrass systems. Glob. Ecol. Conserv. 18, e00625 (2019).

    • Article
    • Google Scholar
  • 55.

    Dickson, A. G., Sabine, C. L., & Christian, J. R. Guide to Best Practices for Ocean CO2 Measurements. PICES Special Publication. 3, 191 pp. (2007).

  • 56.

    Pelletier, G. J., Lewis, E., Wallace, D. W. R. CO2SYS.XLS: a Calculator for the CO2 System in Seawater for Microsoft Excel/VBA. Version 16. Washington State Department of Ecology, http://www.ecy.wa.gov/programs/eap/models.html (2011).

  • 57.

    Danovaro, R. Methods for the Study of Deep-sea Sediments, Their Functioning and Biodiversity. CRC Press, BocaRaton, FL, pp. 414 (2010).

  • 58.

    Pusceddu, A., Dell’Anno, A., Fabiano, M. & Danovaro, R. Quantity and bioavailability of sediment organic matter as signatures of benthic trophic status. Mar. Ecol. Progr. Ser. 375, 41–52 (2009).

  • 59.

    Trygonis, V. & Sini, M. photoQuad: A dedicated seabed image processing software, and a comparative error analysis of four photoquadrat methods. J. Exp. Mar. Biol. Ecol. 424, 99–108 (2012).

    • Article
    • Google Scholar
  • 60.

    Cabioc’h, J. et al. Guide des algues des mers d’Europe. Manche et Atlantique. Méditerranée Ed.: Delachaux et Niestlé, Paris. 272 pp. (2006).

  • 61.

    Calcinai, B. et al. Comparison between the sponge fauna living outside and inside the coralligenous bioconstruction. A quantitative approach. Mediterr. Mar. Sci. 16, 413–418 (2015).

    • Article
    • Google Scholar
  • 62.

    Form, A. U. & Riebesell, U. Acclimation to ocean acidification during long-term CO2 exposure in the cold-water coral Lophelia pertusa. Glob. Change Biol. 18, 843–853 (2012).

  • 63.

    Jokiel, P. L., Maragos, J. E., & Franzisket, L. Coral growth: buoyant weight technique. Coral reefs: research methods. UNESCO, Paris, 529–541 (1978).

  • 64.

    Tsounis, G., Rossi, S., Gili, J. M. & Arntz, W. E. Red coral fishery at the Costa Brava (NW Mediterranean): case study of an overharvested precious coral. Ecosystems 10, 975–986 (2007).

    • Article
    • Google Scholar
  • 65.

    Ries, J. B., Cohen, A. L. & McCorkle, D. C. Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 37, 1131–1134 (2009).

  • 66.

    Manzello, D. P. Coral growth with thermal stress and ocean acidification: lessons from the eastern tropical Pacific. Coral Reefs 29, 749–758 (2010).

  • 67.

    Debreuil, J. et al. Comparative analysis of the soluble organic matrix of axial skeleton and sclerites of Corallium rubrum: Insights for biomineralization. Comp. Biochem. Phys. B 159, 40–48 (2011).

  • 68.

    Gabay, Y., Fine, M., Barkay, Z. & Benayahu, Y. Octocoral tissue provides protection from declining oceanic pH. PloS One 9, e91553 (2014).

  • 69.

    Patel, A. et al. Virus and prokaryote enumeration from planktonic aquatic environments by epifluorescence microscopy with SYBR Green I. Nat. Protoc. 2, 269–276 (2007).

  • 70.

    Garate, L., Blanquer, A. & Uriz, M. J. Calcareous spherules produced by intracellular symbiotic bacteria protect the sponge Hemimycale columella from predation better than secondary metabolites. Mar. Ecol. Progr. Ser. 523, 81–92 (2015).

  • 71.

    Uriz, M. J., Agell, G., Blanquer, A., Turon, X. & Casamayor, E. O. Endosymbiotic calcifying bacteria: a new cue to the origin of calcification in metazoa? Evolution 66, 2993–299 (2012).

  • 72.

    Pernthaler, A., Pernthaler, J. & Amann, R. Fluorescence in situ hybridization and catalyzed reporter deposition for the identification of marine bacteria. Appl. Environ. Microbiol. 68, 3094–3101 (2002).

  • 73.

    Barone, G. et al. Benthic deep-sea fungi in submarine canyons of the Mediterranean Sea. Progr. Oceanogr. 168, 57–64 (2018).

  • 74.

    Anderson, M. J. Permutational multivariate analysis of variance (PERMANOVA). Wiley StatsRef: Statistics Reference Online, 1–15 (2014).

  • 75.

    R Core Team R. A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/ (2014).

  • 76.

    Anderson, M. J., Gorley, R. N. & Clarke, K. R. Permanova+ for Primer: Guide to Software and Statistical Methods. Primer-E, Plymouth, UK. (2008).

  • 77.

    Regione Liguria online portal. http://rgetrasweb.regione.liguria.it/qpg/Tree.do?codNodo=3282.

  • 78.

    Flecha, S. et al. Trends of pH decrease in the Mediterranean Sea through high frequency observational data: indication of ocean acidification in the basin. Sci. Rep. 5, 16770 (2015).

  • 79.

    Hassoun, A. E. R. et al. Acidification of the Mediterranean Sea from anthropogenic carbon penetration. Deep-Sea Res. Pt. I 102, 1–15 (2015).

  • 80.

    Bradassi, F., Cumani, F., Bressan, G. & Dupont, S. Early reproductive stages in the crustose coralline alga Phymatolithon lenormandii are strongly affected by mild ocean acidification. Mar. Biol. 160, 2261–2269 (2013).

  • 81.

    Noisette, F., Egilsdottir, H., Davoult, D. & Martin, S. Physiological responses of three temperate coralline algae from contrasting habitats to near-future ocean acidification. J. Exp. Mar. Biol. Ecol. 448, 179–187 (2013).

  • 82.

    Le Goff, C. et al. In vivo pH measurement at the site of calcification in an octocoral. Sci. Rep. 7, 11210 (2017).

  • 83.

    Previati, M., Scinto, A., Cerrano, C. & Osinga, R. Oxygen consumption in Mediterranean octocorals under different temperatures. J. Exp. Mar. Biol. Ecol. 390, 39–48 (2010).

    • Article
    • Google Scholar
  • 84.

    Cohen, A. L. & Holcomb, M. Why corals care about ocean acidification: uncovering the mechanism. Oceanography 22, 118–127 (2009).

    • Article
    • Google Scholar
  • 85.

    Andersson, A. J. & Gledhill, D. Ocean acidification and coral reefs: effects on breakdown, dissolution, and net ecosystem calcification. Annu. Rev. Mar Sci. 5, 321–348 (2013).

    • Article
    • Google Scholar
  • 86.

    Blackford, J. et al. Detection and impacts of leakage from sub-seafloor deep geological carbon dioxide storage. Nat. Clim. Change 4, 1011–1016 (2014).

  • 87.

    Cerrano, C. et al. Gold coral (Savalia savaglia) and gorgonian forests enhance benthic biodiversity and ecosystem functioning in the mesophotic zone. Biodiv. Conserv. 19, 153–167 (2010).

    • Article
    • Google Scholar
  • 88.

    Bianchelli, S., Pusceddu, A., Canese, S., Greco, S. & Danovaro, R. High meiofaunal and nematodes diversity around mesophotic coral oases in the Mediterranean Sea. PloS One 8, e66553 (2013).

  • 89.

    Bianchelli, S., Buschi, E., Danovaro, R. & Pusceddu, A. Biodiversity loss and turnover in alternative states in the Mediterranean Sea: a case study on meiofauna. Sci. Rep. 6, 34544 (2016).

  • 90.

    Tsounis, G. et al. Diet and seasonal prey capture rates in the Mediterranean red coral (Corallium rubrum L.) Mar. Biol. 149, 313–325 (2006).

    • Google Scholar
  • 91.

    Anthony, K. R. & Fabricius, K. E. Shifting roles of heterotrophy and autotrophy in coral energetics under varying turbidity. J. Exp. Mar. Biol. Ecol. 252, 221–253 (2000).

  • 92.

    De Goeij, J. M. et al. Surviving in a marine desert: the sponge loop retains resources within coral reefs. Science 342, 108–110 (2013).

  • 93.

    Rix, L. et al. Reef sponges facilitate the transfer of coral-derived organic matter to their associated fauna via the sponge loop. Mar. Ecol. Progr. Ser. 589, 85–96 (2018).

  • 94.

    Bayer, K., Kamke, J. & Hentschel, U. Quantification of bacterial and archaeal symbionts in high and low microbial abundance sponges using real-time PCR. FEMS Microbiol. Ecol. 89, 679–690 (2014).

  • 95.

    Bordenstein, S. R. & Theis, K. R. Host biology in light of the microbiome: ten principles of holobionts and hologenomes. PLoS Biol. 13, e1002226 (2015).

  • 96.

    Hester, E. R., Barott, K. L., Nulton, J., Vermeij, M. J. & Rohwer, F. L. Stable and sporadic symbiotic communities of coral and algal holobionts. ISME J. 10, 1157–1169 (2016).

  • 97.

    Williams, G. J. et al. Ocean warming and acidification have complex interactive effects on the dynamics of a marine fungal disease. Proc. R. Soc. B-Biol. Sci. 281, 20133069 (2014).

  • 98.

    Krause, E., Wichels, A., Giménez, L. & Gerdts, G. Marine fungi may benefit from ocean acidification. Aquat. Microb. Ecol. 69, 59–67 (2013).

    • Article
    • Google Scholar
  • 99.

    Krause, E., Wichels, A., Erler, R. & Gerdts, G. Study on the effects of near-future ocean acidification on marine yeasts: a microcosm approach. Helgoland Mar. Res. 67, 607 (2013).

  • 100.

    Peters, E. C. Diseases of coral reef organisms. In Coral Reefs in the Anthropocene. Springer Netherlands, pp. 147–178 (2015).

    • Google Scholar
  • 101.

    Jephcott, T. G. et al. Ecological impacts of parasitic chytrids, syndiniales and perkinsids on populations of marine photosynthetic dinoflagellates. Fungal Ecol. 19, 47–58 (2016).

    • Article
    • Google Scholar
  • 102.

    Toledo-Hernández, C. et al. The role of sclerites in the defense against pathogens of the sea fan Gorgonia ventalina (Octocorallia). J. Exp. Mar. Biol. Ecol. 483, 20–24 (2016).

    • Article
    • Google Scholar
  • 103.

    Tribollet, A., Godinot, C., Atkinson, M. & Langdon, C. Effects of elevated pCO2 on dissolution of coral carbonates by microbial euendoliths. Global Biogeochem. Cy. 23, GB3008 (2009).

  • 104.

    Tribollet, A. Dissolution of dead corals by euendolithic microorganisms across the northern Great Barrier Reef (Australia). Microb. Ecol. 55, 569–580 (2008).

    • Article
    • Google Scholar
  • 105.

    Cadotte, M. W., Dinnage, R. & Tilman, D. Phylogenetic diversity promotes ecosystem stability. Ecology 93, S223–S233 (2012).

    • Article
    • Google Scholar
  • 106.

    Louca, S. et al. Function and functional redundancy in microbial systems. Nat. Ecol. Evol. 2, 936–943 (2018).

  • 107.

    Konopka, A., Lindemann, S. & Fredrickson, J. Dynamics in microbial communities: unraveling mechanisms to identify principles. ISME J. 9, 1488–1495 (2015).

  • 108.

    Micheli, F. et al. Evidence that marine reserves enhance resilience to climatic impacts. PloS one 7, e40832 (2012).

  • 109.

    Roberts, C. M. et al. Marine reserves can mitigate and promote adaptation to climate change. Proc. Natl. Acad. Sci. USA 114, 6167–6175 (2017).

  • 110.

    Hisano, M., Searle, E. B. & Chen, H. Y. Biodiversity as a solution to mitigate climate change impacts on the functioning of forest ecosystems. Biol. Rev. 93, 439–456 (2018).

  • 111.

    Hisano, M., Chen, H. Y., Searle, E. B. & Reich, P. B. Species-rich boreal forests grew more and suffered less mortality than species-poor forests under the environmental change of the past half-century. Ecol. Lett. 22, 999–1008 (2019).

  • 112.

    Duffy, J. E., Lefcheck, J. S., Stuart-Smith, R. D., Navarrete, S. A. & Edgar, G. J. Biodiversity enhances reef fish biomass and resistance to climate change. Proc. Natl. Acad. Sci. USA 113, 6230–6235 (2016).

  • 113.

    Mellin, C., Aaron MacNeil, M., Cheal, A. J., Emslie, M. J. & Julian Caley, M. Marine protected areas increase resilience among coral reef communities. Ecol. Lett. 19, 629–637 (2016).


  • Source: Ecology - nature.com

    Combined influence of soil moisture and atmospheric evaporative demand is important for accurately predicting US maize yields

    Meta-analysis of honey bee neurogenomic response links Deformed wing virus type A to precocious behavioral maturation