Cidaroids spines facing ocean acidification

Benthos; Epibionts; Magnesium concentration; Minerals; Ocean acidification; Sea urchin; Spine; Acidification; Biofilms; Calcium carbonate; Dissolution; Facings; Magnesium; Mammals; Shellfish; Magnesium concentrations; Ocean acidifications; Seawater corrosion; Article; Cidaroida; Echinoidea; Euechinoidea; Adaptation, Physiological; Animals; Hydrogen-Ion Concentration; Oceans and Seas; Sea Urchins; Seawater; Temperature; Water Pollutants

Abstract :

[en] When facing seawater undersaturated towards calcium carbonates, spines of classical sea urchins (euechinoids) show traces of corrosion although they are covered by an epidermis. Cidaroids (a sister clade of euechinoids) are provided with mature spines devoid of epidermis, which makes them, at first sight, more sensitive to dissolution when facing undersaturated seawater. A recent study showed that spines of a tropical cidaroid are resistant to dissolution due to the high density and the low magnesium concentration of the peculiar external spine layer, the cortex. The biofilm and epibionts covering the spines was also suggested to take part in the spine protection. Here, we investigate the protective role of these factors in different cidaroid species from a broad range of latitude, temperature and depth. The high density of the cortical layer and the cover of biofilm and epibionts were confirmed as key protection against dissolution. The low magnesium concentration of cidaroid spines compared to that of euechinoid ones makes them less soluble in general. © 2018 Elsevier Ltd

Disciplines :

Aquatic sciences & oceanology

Author, co-author :

Dery, A.; Laboratoire de Biologie Marine, Université Libre de Bruxelles, avenue F.D. Roosevelt 50, Brussels, B-1050, Belgium

Tran, P. D.; Laboratoire de Biologie Marine, Université Libre de Bruxelles, avenue F.D. Roosevelt 50, Brussels, B-1050, Belgium

Compère, Philippe ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Morphologie fonctionnelle et évolutive

Dubois, Philippe; Université Libre de Bruxelles - ULB > Laboratoire de Biologie Marine

Language :

English

Title :

Cidaroids spines facing ocean acidification

Publication date :

2018

Journal title :

Marine Environmental Research

ISSN :

0141-1136

Publisher :

Elsevier Ltd

Volume :

138

Pages :

9-18

Peer reviewed :

Peer Reviewed verified by ORBi

Funders :

U600415FUniversité de BourgogneNational Council for Scientific Research, NCSRFonds De La Recherche Scientifique - FNRS, FNRS

Available on ORBi :

since 13 June 2019

Statistics

Number of views

71 (2 by ULiège)

Number of downloads

0 (0 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

Bibliography

Aizenberg, J., Hanson, J., Koetzle, T.F., Weiner, F., Addadi, L., Control of macromolecule distribution within synthetic and biogenic single calcite crystals. J. Am. Chem. Soc. 119 (1997), 881-886.
Andersson, A., Mackenzie, F., Bates, N., Life on the margin: implications of ocean acidification on Mg-calcite, high latitude and cold-water marine calcifiers. Mar. Ecol. Prog. Ser. 373 (2008), 265-273.
Calosi, P., Rastrick, S.P.S., Graziano, M., Thomas, S.C., Baggini, C., Carter, H.A., Hall-Spencer, J.M., Milazzo, M., Spicer, J.I., Distribution of sea urchins living near shallow water CO2 vents is dependent upon species acid-base and ion-regulatory abilities. Mar. Pollut. Bull. 73:2 (2013), 470-484.
Catarino, A.I., Guibourt, V., Moureaux, C., De Ridder, C., Compère, P., Dubois, P., Antarctic urchin Ctenocidaris speciosa spines: lessons from the deep. Cah. Biol. Mar., 54, 2013 659-655.
Chave, K.E., Aspects of the biogeochemistry of magnesium 1. Calcareous marine organisms. J. Geol., 62, 1954, 3.
Clarke, F.W., Wheeler, W.C., The Inorganic Constituents of Marine Invertebrates. 1922, Washington Government Printing Office 62.
Collard, M., Laitat, K., Moulin, L., Catarino, A., Grosjean, P., Dubois, P., Buffer capacity of the coelomic fluid in echinoderms. Comp. Biochem. Physiol. A 166 (2013), 199-206.
Collard, M., De Ridder, C., David, B., Dehairs, F., Dubois, P., Could Antarctic sea urchins be more resilient to near-future ocean acidification than expected?. Global Change Biol. 21 (2015), 605-617.
Collard, M., Rastrick, S.P.S., Calosi, P., Demolder, Y., Dille, J., Hall-Spencer, J.M., Milazzo, M., Moulin, L., Widdicombe, S., Dehairs, F., Dubois, P., The impact of ocean acidification and warming on the skeletal mechanical properties of the sea urchin Paracentrotus lividus from laboratory and field observations. ICES J. Mar. Sci. 73 (2016), 727-738.
David, B., Stock, R.S., De Carlo, F., Hétérier, V., De Ridder, C., Microstructures of Antarctic cidaroid spines: diversity of shapes and ectosymbiont attachments. Mar. Biol. 156:8 (2009), 1559-1572.
Dery, A., Guibourt, V., Catarino, A.I., Compère, P., Dubois, P., Properties, morphogenesis, and effect of acidification on spines of the cidaroid sea urchin Phyllacanthus imperialis. Invertebr. Biol. 133 (2014), 188-199.
Dery, A., Collard, M., Dubois, P., Ocean acidification reduces spine mechanical strength in euechinoid but not in cidaroid sea urchins. Environ. Sci. Technol. 51:7 (2017), 3640-3648.
Doncaster, C.P., Davey, A.J., Analysis of Variance and Covariance. 2007, Cambridge University Press, UK 288.
Dubois, P., The skeleton of postmetamorphic echinoderms in a changing world. Biol. Bull., 226, 2014, 3.
Gorzelak, P., Stolarski, J., Dery, A., Dubois, P., Escrig, S., Meibom, A., Ultrascale and microscale growth dynamics of the cidaroid spine of Phyllacanthus imperialis revealed by 26Mg labeling and NanoSIMS isotopic imaging. J. Morphol. 275 (2014), 788-796.
Gorzelak, P., Dery, A., Dubois, P., Stolarski, J., Sea urchin growth dynamics at microstructural length scale revealed by Mn-labeling and cathodoluminescence imaging. Front. Zool., 2017, 14-42.
Gran, G., Determination of the equivalence point in potentiometric titrations. Part II. Analyst 77 (1952), 661-671.
Hazan, Y., Wangensteen, O.S., Fine, M., Tough as a rock-boring urchin: adult Echinometra sp. EE from the Red Sea show high resistance to ocean acidification over long-term exposures. Mar. Biol. 161:11 (2014), 2531-2545.
Heatfield, B.M., Growth of the calcareous skeleton during regeneration of spines of the sea urchin, Strongylocentrotus purpuratus (stimpson): a light and scanning electron microscopic study. J. Morphol. 134 (1971), 57-89.
Hermans, J., André L., Navez, J., Pernet, P., Dubois, P., Relative influences of solution composition and presence of intracrystalline proteins on magnesium incorporation in calcium carbonate minerals: insight into vital effects. J. Geophys. Res., 116, 2011.
Lebrato, M., Andersson, A.J., Ries, J.B., Aronson, R.B., Lamare, L.B., Koeve, W., Oschlies, A., Iglesias-Rodriguez, M.D., Thatje, S., Amsler, M., Vos, S.C., Jones, D.A.B., Ruhl, H.A., Gates, A.R., McClintock, J.B., Benthic marine calcifiers coexist with CaCO3-undersaturated seawater worldwide. Global Biogeochem. Cycles 30:7 (2016), 1038-1053.
Loste, E., Wilson, M., Seshadri, R., Meldrum, F.C., The role of magnesium in stabilising amorphous calcium carbonate and controlling calcite morphologies. J. Cryst. Growth 254 (2003), 206-218.
Magdans, U., Gies, H., Systematic investigations of the Ca/Mg distribution as a function of habitat of the sea urchin and the sample location in the spine. Eur. J. Mineral 16:2 (2004), 261-268.
Märkel, K., Kubanek, F., Willgallis, A., Polykristal- liner Calcit bei Seeigeln (Echinodermata, Echinoidea). Z. Zellforsch 119 (1971), 355-377.
Märkel, K., Röser, U., The spine tissues in the echinoid Eucidaris tribuloides. Zoomorphology 103 (1983), 25-41.
McClintock, J.B., Amsler, M.O., Angus, R.A., Challener, R.C., Schram, J.B., Amsler, C.D., Mah, C.L., Cuce, J., Baker, B.J., The Mg-calcite composition of Antarctic echinoderms: important implications for predicting the impacts of ocean acidification. J. Geol. 119 (2011), 457-466.
Moulin, L., Grosjean, P., Leblud, J., Batigny, A., Collard, M., Dubois, P., Long-term mesocosms study of the effects of ocean acidification on growth and physiology of the sea urchin Echinometra mathaei. Mar. Environ. Res. 103 (2015), 103-114.
Moureaux, C., Perez-Huerta, A., Compere, P., Zhu, W., LeLoup, T., Cusack, M., Dubois, P., Structure, composition and mechanical relations to function in sea urchin spine. J. Struct. Biol. 170 (2010), 41-49.
Morse, J.W., Mackenzie, F.T., Geochemistry of Sedimentary Carbonates. 1990, Elsevier science publishers B.V., Amsterdam 707.
Morse, J.W., Andersson, A.J., Mackenzie, F.T., Initial responses of carbonate-rich shelf sediments to rising atmospheric pCO2 and “ocean acidification”: role of high Mg-calcites. Geochem. Cosmochim. Acta 70 (2006), 5814-5830.
Peck, V.L., Tarling, G.A., Manno, C., Harper, E.M., Tynan, E., Outer organic layer and internal repair mechanism protects pteropod Limacina helicina from ocean acidification. Deep Sea Res. Part II Top. Stud. Oceanogr. 127 (2016), 41-52.
Plummer, L.N., Mackenzie, F.T., Predicting mineral solubility from rate data; application to the dissolution of magnesian calcites. Am. J. Sci. 274 (1974), 61-83.
Politi, Y., Sea Urchin spine calcite forms via a transient amorphous calcium carbonate phase. Science 306 (2004), 1161-1164.
Raz, S., Hamilton, P.C., Wilt, F.H., Weiner, S., Addadi, L., The transient phase of amorphous calcium carbonate in sea urchin larval spicules: the involvement of proteins and magnesium ions in its formation and stabilization. Adv. Funct. Mater. 13 (2003), 480-486.
Sewell, M.A., Hofmann, G.E., Antarctic echinoids and climate change: a major impact on the brooding forms. Global Change Biol. 17 (2010), 734-744.
Smith, A.M., Clark, D.E., Lamare, M.D., Winter, D.J., Byrne, M., Risk and resilience: variations in magnesium in echinoid skeletal calcite. Mar. Ecol. Prog. Ser. 561 (2016), 1-16.
Thomsen, J., Gutowska, M.A., Saphörster, J., Heinemann, A., Trübenbach, K., Fietzke, J., Hiebenthal, C., Eisenhauer, A., Körtzinger, A., Wahl, M., Melzner, F., Calcifying invertebrates succeed in a naturally CO2-rich coastal habitat but are threatened by high levels of future acidification. Biogeosciences 7 (2010), 3879-3891.
Tunnicliffe, V., Davies, K.T.A., Butterfield, D.A., Embley, R.W., Rose, J.M., Chadwick, W.W. Jr., Survival of mussels in extremely acidic waters on a submarine volcano. Nat. Geosci. 2 (2009), 344-348.
Twitchett, R.J., Oji, T., Early Triassic recovery of echinoderms. C. R. Palevol 4 (2005), 531-542.
Uthicke, S., Liddy, M., Nguyen, H.D., Byrne, M., 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 33:3 (2014), 831-845.
Weber, J.N., The incorporation of magnesium into the skeletal calcites of echinoderms. Am. J. Sci. 267 (1969), 537-566.