References

Biogeosciences

1726-4189

Copernicus Publications

Göttingen, Germany

10.5194/bg-10-5671-2013

Respiration of Mediterranean cold-water corals is not affected by ocean acidification as projected for the end of the century

Maier

¹ ² Bils

¹ ² ³ Weinbauer

M. G.

¹ ² Watremez

⁴ Peck

M. A.

³ Gattuso

J.-P.

https://orcid.org/0000-0002-4533-4114

¹ ²

Laboratoire d'Océanographie de Villefranche, UMR7093, CNRS-INSU, BP 28, 06234 Villefranche-sur-mer, France

Université Pierre et Marie Curie-Paris 6, Observatoire Océanologique de Villefranche, 06230 Villefranche-sur-mer, France

University of Hamburg, Institute for Hydrobiology and Fisheries Science, Olbersweg 24, 22767 Hamburg, Germany

Agence des Aires Marines Protégées, 16 quai de la Douane, 29229 Brest, France

27 08 2013

10 8 5671 5680

2013

This work is licensed under the Creative Commons Attribution 3.0 Unported License. To view a copy of this licence, visit https://creativecommons.org/licenses/by/3.0/

This article is available from https://bg.copernicus.org/articles/10/5671/2013/bg-10-5671-2013.html

The full text article is available as a PDF file from https://bg.copernicus.org/articles/10/5671/2013/bg-10-5671-2013.pdf

The rise of CO2 has been identified as a major threat to life in the ocean. About one-third of the anthropogenic CO2 produced in the last 200 yr has been taken up by the ocean, leading to ocean acidification. Surface seawater pH is projected to decrease by about 0.4 units between the pre-industrial revolution and 2100. The branching cold-water corals Madrepora oculata and Lophelia pertusa are important, habitat-forming species in the deep Mediterranean Sea. Although previous research has investigated the abundance and distribution of these species, little is known regarding their ecophysiology and potential responses to global environmental change. A previous study indicated that the rate of calcification of these two species remained constant up to 1000 μatm CO2, a value that is at the upper end of changes projected to occur by 2100. We examined whether the ability to maintain calcification rates in the face of rising pCO2 affected the energetic requirements of these corals. Over the course of three months, rates of respiration were measured at a pCO2 ranging between 350 and 1100 μatm to distinguish between short-term response and longer-term acclimation. Respiration rates ranged from 0.074 to 0.266 μmol O2 (g skeletal dry weight)−1 h−1 and 0.095 to 0.725 μmol O2 (g skeletal dry weight)−1 h−1 for L. pertusa and M. oculata, respectively, and were independent of pCO2. Respiration increased with time likely due to regular feeding, which may have provided an increased energy supply to sustain coral metabolism. Future studies are needed to confirm whether the insensitivity of respiration to increasing pCO2 is a general feature of deep-sea corals in other regions.

References 1

Al-Horani, F. A., Al-Moghrabi, S. M., and de Beer. D.: The mechanism of calcification and its relation to photosynthesis and respiration in the scleractinian coral Galaxea fascicularis, Mar. Biol., 142, 419–426, 2003.

Allemand, D., Ferrier-Pagès, C., Furla, P., Houlbrèque, F., Puverel, S., Reynaud, S., Tambutté, É., Tambutté, S., and Zoccola, D.: Biomineralisation in reef-building corals: from molecular mechanisms to environmental control, C. R. Palevol. 3, 453–467, 2004.

Barnes, R. S. K.: The invertebrates: a synthesis, Blackwell Science Ltd, Oxford, 2001.

Caldeira, K. and Wickett, M. E.: Anthropogenic carbon and ocean pH, Nature, 425, 365–365, <a href="http://dx.doi.org/10.1038/425365a">https://doi.org/10.1038/425365a</a>, 2003

Cao, L., Caldeira, K., and Jain, A. K.: Effects of carbon dioxide and climate change on ocean acidification and carbonate mineral saturation, Geophys. Res. Lett., 34, L05607, <a href="http://dx.doi.org/10.1029/2006GL028605">https://doi.org/10.1029/2006GL028605</a>, 2007.

Davies, A. J., Wisshak, M., Orr, J. C., and Roberts, J. M. Predicting suitable habitat for the cold-water coral Lophelia pertusa (Scleractinia), Deep-Sea Res. Pt. I, 55, 1048–1062, 2008.

Delibrias, G. and Taviani, M.: Dating the death of Mediterranean deep-sea scleractinian corals, Mar. Geol., 62, 175–180, 1985.

Dodds, L. A., Roberts, J. M., Taylor, A. C., and Marubini, F.: Metabolic tolerance of the cold-water coral Lophelia pertusa (Scleractinia) to temperature and dissolved oxygen change, J. Exp. Mar. Biol. Ecol., 349, 205–214, 2007.

Feely, R. A., Sabine, C. L., Lee, K., Berelson, W., Kleypas, J., Fabry, V. J., and Millero, F. J.: Impact of anthropogenic CO2 on the CaCO3 system in the oceans, Science, 305, 362–366, 2004.

Ferrier-Pagès, C., Gattuso, J.-P., and Jaubert, J.: Effect of small variations in salinity on the rates of photosynthesis and respiration of the zooxanthellate coral Stylophora pistillata, Mar. Ecol.-Prog. Ser., 181, 309–314, 1999.

Ferrier-Pagès, C., Witting, J., Tambutté, E., and Sebens, K. P.: Effect of natural zooplankton feeding on the tissue and skeletal growth of the scleractinian coral Stylophora pistillata, Coral Reefs, 22, 229–240, 2003.

Form, A. U. and Riebesell, U.: Acclimation to ocean acidification during long-term CO2 exposure in the cold-water coral Lophelia pertusa, Glob. Change Biol., 18, 843–853, <a href="http://dx.doi.org/10.1111/j.1365-2486.2011.02583.x">https://doi.org/10.1111/j.1365-2486.2011.02583.x</a>, 2012.

Freiwald, A., Beuck, L., Rüggeberg, A., Taviani, M., and Hebbeln, D.: The white coral community in the central Mediterranean Sea revealed by ROV surveys, Oceanography, 22, 36–52, 2009.

Gattuso, J.-P., Allemand, D., and Frankignoulle, M.: Photosynthesis and calcification at cellular, organismal and community levels in coral reefs: A review on interactions and control by carbonate chemistry, Amer. Zool., 39, 160–183, 1999.

Goreau, T. F.: The physiology of skeleton formation in corals. I. A method for measuring the rate of calcium deposition by corals under different conditions, Biol. Bull. 116, 59–75, 1959.

Gori, A., Orejas, C., Madurell, T., Bramanti, L., Martins, M., Quintanilla, E., Marti-Puig, P., Lo Iacono, C., Puig, P., Requena, S., Greenacre, M., and Gili, J. M.: Bathymetrical distribution and size structure of cold-water coral populations in the Cap de Creus and Lacaze-Duthiers canyons (northwestern Mediterranean), Biogeosciences, 10, 2049–2060, <a href="http://dx.doi.org/10.5194/bg-10-2049-2013">https://doi.org/10.5194/bg-10-2049-2013</a>, 2013.

Guinotte, J. M., Orr, J., Cairns, S., Freiwald, A., Morgan, L., and George, R.: Will human-induced changes in seawater chemistry alter the distribution of deep-sea scleractinian corals?, Front. Ecol. Environ., 4, 141–146, 2006.

Hochachka, P. W. and Somero, G. N.: Biochemical adaptation: mechanism and process in physiological evolution, Oxford University Press, New York, New York, USA, 2002.

Houlbrèque, F., Tambutté, E., and Ferrier-Pagès, C.: Effect of zooplankton availability on the rates of photosynthesis, and tissue and skeletal growth in the scleractinian coral Stylophora pistillata, J. Exp. Mar. Biol. Ecol., 296, 145–166, 2003.

IPPC: Climate change 2007: the physical science basis, Cambridge University Press, Cambridge, UK, New York, NY, USA, 2007.

Kaniewska, P., Campbell, P. R., Kline, D. I., Rodriguez-Lanetty, M., Miller, D. J., Dove, S., and Hoegh-Guldberg, O.: Major cellular and physiological impacts of ocean acidification on a reef building coral, PLOS One, 7, e34659, <a href="http://dx.doi.org/10.1371/journal.pone.0034659">https://doi.org/10.1371/journal.pone.0034659</a>, 2012.

Khatiwala, S., Primeau, F., and Hall, T.: Reconstruction of the history of anthropogenic CO2 concentrations in the ocean, Nature, 462, 346–349, 2009.

Kleypas, J. A., McMacus, J. W., and Meñez, L. A. B.: Environmental limits to coral reef development: Where do we draw the line?, Amer. Zool., 39, 146–159, 1999.

Lavigne, H. and Gattuso, J.-P.: seacarb: seawater carbonate chemistry with R. R package version 2.4., <a href="http://CRAN.R-project.org/package=seacarb">http://CRAN.R-project.org/package=seacarb</a>, (last access: 22 February 2013), 2011.

Maier, C., Hegeman, J., Weinbauer, M. G., and Gattuso, J.-P.: Calcification of the cold-water coral Lophelia pertusa, under ambient and reduced pH, Biogeosciences, 6, 1671–1680, <a href="http://dx.doi.org/10.5194/bg-6-1671-2009">https://doi.org/10.5194/bg-6-1671-2009</a>, 2009.

Maier, C., de Kluijver, A., Agis, M., Brussaard, C. P. D., van Duyl, F. C., and Weinbauer, M. G.: Dynamics of nutrients, total organic carbon, prokaryotes and viruses in onboard incubations of cold-water corals, Biogeosciences, 8, 2609–2620, <a href="http://dx.doi.org/10.5194/bg-8-2609-2011">https://doi.org/10.5194/bg-8-2609-2011</a>, 2011.

Maier, C., Watremez, P., Taviani, M., Weinbauer, M. G., and Gattuso, J.-P.: Calcification rates and the effect of ocean acidification on Mediterranean cold-water corals, P. Roy. Soc. Lond., B, 279, 1713–1723, <a href="http://dx.doi.org/10.1098/rspb.2011.1763">https://doi.org/10.1098/rspb.2011.1763</a>, 2012.

Maier, C., Schubert, A., Berzunza Sanchez, M. M., Weinbauer, M. G., Watremez, P., and Gattuso, J.-P.: End of the century pCO2 levels do not impact calcification in Mediterranean cold-water corals, PLoS ONE, 8, e62655, <a href="http://dx.doi.org/10.1371/journal.pone.0062655">https://doi.org/10.1371/journal.pone.0062655</a>, 2013.

McConnaughey, T. A. and Whelan, J. F.: Calcification generates protons for nutrient and bicarbonate uptake, Earth Sci. Rev., 42, 95–117, 1997.

McCulloch, M., Trotter, J., Montagna, P., Falter, J., Dunbar, R., Freiwald, A., Fösterra, G., Lopez Correa, M., Maier, C., Rüggeberg, A., and Taviani, M.: Resilience of cold-water scleractinian corals to ocean acidification: Boron isotopic systematics of pH and saturation state up-regulation, Geochim. Cosmochim. Ac., 87, 21–34, <a href="http://dx.doi.org/10.1016/j.gca.2012.03.027">https://doi.org/10.1016/j.gca.2012.03.027</a>, 2012.

Moya, A., Huisman, L., Ball, E. E., Hayward, D. C., Grasso, L. C., Chua, C. M., Woo, H. N., Gattuso, J.-P., Forêt, S., and Miller, D. J.: Whole transcriptome analysis of the coral Acropora millepora reveals complex responses to CO2-driven acidification during the initiation of calcification, Mol. Ecol., 21, 2440–2454, 2012.

Naumann, M. S., Orejas, C., Wild, C., and Ferrier-Pagès, C.: First evidence for zooplankton feeding sustaining key physiological processes in a scleractinian cold water coral, J. Exp. Mar. Biol. Ecol., 214, 3570–3576, 2011.

Orejas, C., Gori, A., Iacono, C. L., Puig, P., Gili, J.-M., and Dale, M. R. T.: Cold-water corals in the Cap de Creus canyon, northwestern Mediterranean: spatial distribution, density and anthropogenic impact, Mar. Ecol.-Prog. Ser., 397, 37–51, 2009.

Orr, J. C., Fabry, V. J., Aumont, O., Bopp, L., Doney, S. C., Feely, R. A., Gnanadesikan, A., Gruber, N., Ishida, A., Joos, F., Key, R. M., Lindsay, K., Maier-Reimer, E., Matear, R., Monfray, P., Mouchet, A., Najjar, R. G., Plattner, G.-K., Rodgers, K.B., Sabine, C.L., Sarmiento, J. L., Schlitzer, R., Slater, R. D., Totterdell, I. J., Weirig, M.-F., Yamanaka, Y., and Yool, A.: Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms, Nature, 437, 681–686, 2005.

Roberts, J. M., Wheeler, A. J., and Freiwald, A.: Reefs of the deep: The biology and geology of cold-water coral ecosystems, Science, 312, 543–547, 2006.

Rodolfo-Metalpa, R., Peirano, A., Houlbrèque, F., Abbate, M., and Ferrier-Pagès, C.: Effects of temperature, light and heterotrophy on the growth rate and budding of the temperate coral Cladocora caespitosa, Coral Reefs, 27, 17–25, 2008.

Sabine, C. L., Feely, R. A., Gruber, N., Key, R. M., Lee, K., Bullister, J. L., Wanninkhof, R., Wong, C. S., Wallace, D. W. R., Tilbrook, B., Millero, F. J., Peng, T.-H., Kozyr, A., Ono, T., and Rios, A. F.: The oceanic sink for anthropogenic CO2, Science, 305, 367–371, 2004.

Taviani, M., Freiwald, A., and Zibrowius, H.: Deep coral growth in the Mediterranean Sea: an overview. In: Cold-water corals and ecosystems, edited by: Freiwald, A. and Roberts, J. M., Springer-Verlag, Berlin Heidelberg, 137–156, 2005a.

Taviani, M., Remia, A., Corselli, C., Freiwald, A., Malinverno, E., Mastrototaro, F., Savini, A., and Tursi, A.: First geo-marine survey of living cold-water Lophelia reefs in the Ionian Sea (Mediterranean basin), Facies, 50, 409–417, 2005b.

Thomsen, J., Casties, I., Pansch, C.Körtzinger, A., and Melzner, F.: Food availability outweighs ocean acidification effects in juvenile Mytilus edulis: laboratory and field experiments, Glob. Change Biol., 19, 1017–1027, <a href="http://dx.doi.org/10.1111/gcb.12109">https://doi.org/10.1111/gcb.12109</a>, 2013

Thresher, R. E., Tilbrook, B., Fallon, S., Wilson, N. C., and Adkins, J.: Effects of chronic low carbonate saturation levels on the distribution, growth and skeletal chemistry of deep-sea corals and other seamount megabenthos, Mar. Ecol.-Prog. Ser., 442, 87–99, 2011.

Tsounis, G., Orejas, C., Reynaud, S., Gili, J.-M., Allemand, D., and Ferrier-Pagès, C.: Prey-capture rates in four Mediterranean cold-water corals, Mar. Ecol.-Prog. Ser., 398, 140–155, 2010.

Tursi, A., Mastrototaro, F., Matarrese, A., Maiorano, P., and D'Onghia, G.: Biodiversity of the white coral reefs in the Ionian Sea (Central Mediterranean), Chem. Ecol., 20, 107–116, 2004.

Zoccola, D., Tambutté, E., Kulhanek, E., Puverel, S., Scimeca, J.-C., Allemand, D., and Tambutté, S.: Molecular cloning and localization of a PMCA P-type calcium ATPase from the coral Stylophora pistillata, Biochim. Biophys. Acta, 1663, 117–126, 2004.