Structural and Elemental Analysis of the Freshwater, Low-Mg Calcite Coralline Alga Pneophyllum cetinaensis
Abstract
:1. Introduction
2. Results
2.1. XRD Analysis
2.2. Mechanical Properties
2.3. Elements Composition
3. Discussion
4. Materials and Methods
4.1. Sample Collection
4.2. SEM Analysis
4.3. XRD/Phase Identification
4.4. Mechanical Properties
4.5. Element Analysis
Instrumentation, Operating Conditions and Data Reduction
4.6. Statistical Analysis
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Brodie, J.; Zuccarello, G.C. Systematics of the species rich algae: Red algal classification, phylogeny and speciation. In Reconstructing the Tree of Life: Taxonomy and Systematics of Species Rich Taxa; Trevor, R., Hodkinson, J.A.N.P., Eds.; CRC Press: New York, NY, USA, 2006; pp. 323–336. ISBN 9781420009538. [Google Scholar]
- Teichert, S.; Woelkerling, W.; Rüggeberg, A.; Wisshak, M.; Piepenburg, D.; Meyerhöfer, M.; Form, A.; Freiwald, A. Arctic rhodolith beds and their environmental controls (Spitsbergen, Norway). Facies 2014, 60, 15–37. [Google Scholar] [CrossRef]
- Foster, M.S. Rhodoliths: Between rocks and soft places. J. Phycol. 2001, 37, 659–667. [Google Scholar] [CrossRef]
- Teichert, S. Hollow rhodoliths increase Svalbard’s shelf biodiversity. Sci. Rep. 2014, 4, 6972. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Adey, W.; Halfar, J.; Humphreys, A.; Suskiewicz, T.; Belanger, D.; Gagnon, P.; Fox, M. Subarctic rhodolith beds promote longevity of crustose coralline algal buildups and their climate archiving potential. Palaios 2015, 30, 281–293. [Google Scholar] [CrossRef]
- McCoy, S.J.; Kamenos, N.A. Coralline algae (Rhodophyta) in a changing world: Integrating ecological, physiological, and geochemical responses to global change. J. Phycol. 2015, 51, 6–24. [Google Scholar] [CrossRef]
- Ballesteros, E. Mediterranean coralligenous assemblages: A synthesis of present knowledge. In Oceanography and Marine Biology: An Annual Review; Gibson, R.N., Gordon, J.D., Atkinson, R.J.A., Eds.; Taylor & Francis: New York, NY, USA, 2006. [Google Scholar]
- Basso, D.; Babbini, L.; Kaleb, S.; Bracchi, V.A.; Falace, A. Monitoring deep Mediterranean rhodolith beds. Aquat. Conserv. Mar. Freshw. Ecosyst. 2016, 26, 549–561. [Google Scholar] [CrossRef] [Green Version]
- Van der Heijden, L.H.; Kamenos, N.A. Reviews and syntheses: Calculating the global contribution of coralline algae to total carbon burial. Biogeosciences 2015, 12, 6429–6441. [Google Scholar] [CrossRef] [Green Version]
- Guiry, M.D.; Guiry, G.M. AlgaeBase. World-Wide Electronic Publication, National University of Ireland, Galway. Available online: https://www.algaebase.org/ (accessed on 3 April 2020).
- Žuljević, A.; Kaleb, S.; Peña, V.; Despalatović, M.; Cvitković, I.; De Clerck, O.; Le Gall, L.; Falace, A.; Vita, F.; Braga, J.C.; et al. First freshwater coralline alga and the role of local features in a major biome transition. Sci. Rep. 2016, 6, 19642. [Google Scholar] [CrossRef] [Green Version]
- Johansen, H.W. Coralline Algae: A First Synthesis; CRC: Boca Raton, FL, USA, 1981. [Google Scholar]
- Stanley, S.M.; Ries, J.B.; Hardie, L.A. From the Cover: Low-magnesium calcite produced by coralline algae in seawater of Late Cretaceous composition. Proc. Natl. Acad. Sci. USA 2002, 99, 15323–15326. [Google Scholar] [CrossRef] [Green Version]
- Ries, J.B. Mg fractionation in crustose coralline algae: Geochemical, biological, and sedimentological implications of secular variation in the Mg/Ca ratio of seawater. Geochim. Cosmochim. Acta 2006, 70, 891–900. [Google Scholar] [CrossRef]
- Azmy, K.; Brand, U.; Sylvester, P.; Gleeson, S.A.; Logan, A.; Bitner, M.A. Biogenic and abiogenic low-Mg calcite (bLMC and aLMC): Evaluation of seawater-REE composition, water masses and carbonate diagenesis. Chem. Geol. 2011, 280, 180–190. [Google Scholar] [CrossRef] [Green Version]
- Andersson, A.J.; Mackenzie, F.T.; Bates, N.R. Life on the margin: Implications of ocean acidification on Mg-calcite, high latitude and cold-water marine calcifiers. Mar. Ecol. Prog. Ser. 2008, 373, 265–273. [Google Scholar] [CrossRef]
- Smith, A.M.; Sutherland, J.E.; Kregting, L.; Farr, T.J.; Winter, D.J. Phylomineralogy of the Coralline red algae: Correlation of skeletal mineralogy with molecular phylogeny. Phytochemistry 2012, 81, 97–108. [Google Scholar] [CrossRef] [PubMed]
- Ries, J.B.; Stanley, S.M.; Hardie, L.A. Scleractinian corals produce calcite, and grow more slowly, in artificial Cretaceous seawater. Geology 2006, 34, 525–528. [Google Scholar] [CrossRef]
- Ragazzola, F.; Foster, L.C.; Jones, C.J.; Scott, T.B.; Fietzke, J.; Kilburn, M.R.; Schmidt, D.N. Impact of high CO2 on the geochemistry of the coralline algae Lithothamnion glaciale. Sci. Rep. 2016, 6, 20572. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mucci, A. Influence of temperature on the composition of magnesian calcite overgrowths precipitated from seawater. Geochim. Cosmochim. Acta 1987, 51, 1977–1984. [Google Scholar] [CrossRef]
- Lea, D.W.; Bijma, J.; Spero, H.J.; Archer, D. Implications of a carbonate ion effect on shell carbon and oxygen isotopes for glacial ocean conditions. In Use of Proxies in Paleoceanography; Examples from the South Atlantic; Fischer, G., Wefer, G., Eds.; Springer: Berlin, Germany, 1999; pp. 513–522. [Google Scholar]
- Bentov, S.; Erez, J. Novel observations on biomineralization processes in foraminifera and implications for Mg/Ca ratio in the shells. Geology 2005, 33, 841–844. [Google Scholar] [CrossRef]
- Maeda, A.; Fujita, K.; Horikawa, K.; Suzuki, A.; Yoshimura, T.; Tamenori, Y.; Kawahata, H. Evaluation of oxygen isotope and Mg/Ca ratios in high-magnesium calcite from benthic foraminifera as a proxy for water temperature. J. Geophys. Res. Biogeosci. 2017, 122, 185–199. [Google Scholar] [CrossRef]
- Kamenos, N.A.; Cusack, M.; Moore, P.G. Coralline algae are global palaeothermometers with bi-weekly resolution. Geochim. Cosmochim. Acta 2008, 72, 771–779. [Google Scholar] [CrossRef]
- Hetzinger, S.; Halfar, J.; Kronz, A.; Steneck, R.; Adey, W.H.; Philipp, A.L.; Schöne, B. High-resolution Mg/Ca ratios in a coralline red alga as a proxy for Bering Sea temperature variations from 1902–1967. Palaois 2009, 24, 406–412. [Google Scholar] [CrossRef]
- Adey, W.H.; Halfar, J.; Williams, B. The Coralline Genus Clathromorphum foslie Emend. Adey: Biological, Physiological, and Ecological Factors Controlling Carbonate Production in an Arctic-Subarctic Climate Archive; Smithonian Institution Scholarly Press: Washington DC, USA, 2013; ISBN 0196-0768. [Google Scholar]
- Fietzke, J.; Ragazzola, F.; Halfar, J.; Dietze, H.; Foster, L.C.; Hansteen, T.H.; Eisenhauer, A.; Steneck, R.S. Century-scale trends and seasonality in pH and temperature for shallow zones of the Bering Sea. Proc. Natl. Acad. Sci. USA 2015, 112, 2960–2965. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ragazzola, F.; Caragnano, A.; Basso, D.; Schmidt, D.N.; Fietzke, J. Establishing temperate crustose early Holocene coralline algae as archives for palaeoenvironmental reconstructions of the shallow water habitats of the Mediterranean Sea. Palaeontology 2020, 63, 155–170. [Google Scholar] [CrossRef] [Green Version]
- Caragnano, A.; Basso, D.; Storz, D.; Jacob, D.E.; Ragazzola, F.; Benzoni, F.; Dutrieux, E. Elemental variability in the coralline alga Lithophyllum yemenense as an archive of past climate in the Gulf of Aden (NW Indian Ocean). J. Phycol. 2017, 53, 381–395. [Google Scholar] [CrossRef] [Green Version]
- Kastner, M. Oceanic minerals: Their origin, nature of their environment, and significance. Proc. Natl. Acad. Sci. USA 1999, 96, 3380–3387. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Caragnano, A.; Basso, D.; Jacob, D.E.; Storz, D.; Rodondi, G.; Benzoni, F.; Dutrieux, E. The coralline red alga Lithophyllum kotschyanum f. affine as proxy of climate variability in the Yemen coast, Gulf of Aden (NW Indian Ocean). Geochim. Cosmochim. Acta 2014, 124, 1–17. [Google Scholar] [CrossRef]
- Halfar, J.; Hetzinger, S.; Adey, W.; Zack, T.; Gamboa, G.; Kunz, B.; Williams, B.; Jacob, D.E. Coralline algal growth-increment widths archive North Atlantic climate variability. Palaeogeogr. Palaeoclimatol. Palaeoecol. 2011, 302, 71–80. [Google Scholar] [CrossRef]
- Freitas, P.; Clarke, L.J.; Kennedy, H.; Richardson, C.; Abrantes, F. Mg/Ca, Sr/Ca, and stable-isotope (δ18O and δ13C) ratio profiles from the fan mussel Pinna nobilis: Seasonal records and temperature relationships. Geochem. Geophys. Geosyst. 2005, 6. [Google Scholar] [CrossRef]
- Halfar, J.; Adey, W.H.; Kronz, A.; Hetzinger, S.; Edinger, E.; Fitzhugh, W.W. Arctic sea-ice decline archived by multicentury annual-resolution record from crustose coralline algal proxy. Proc. Natl. Acad. Sci. USA 2013, 110, 19737–19741. [Google Scholar] [CrossRef] [Green Version]
- Chan, P.; Halfar, J.; Williams, B.; Hetzinger, S.; Steneck, R.; Zack, T.; Jacob, D.E. Freshening of the Alaska Coastal Current recorded by coralline algal Ba/Ca ratios. J. Geophys. Res. Biogeosci. 2011, 116, G01032. [Google Scholar] [CrossRef] [Green Version]
- Martin, J.M.; Meybeck, M. Elemental mass-balance of material carried by major world rivers. Mar. Chem. 1979, 7, 173–206. [Google Scholar] [CrossRef]
- Clarke, F.W.; Wheeler, W.C. The Inorganic Constituents of Marine Invertebrates; US Government Printing Office: Washington, DC, USA, 1922.
- Fragoso, D.; Ramírez-Cahero, F.; Rodríguez-Galván, A.; Hernández-Reyes, R.; Heredia, A.; Rodríguez, D.; Aguilar-Franco, M.; Bucio, L.B.V.A. Characterization of the CaCO3 biomineral in coralline red algae (Corallinales) from the Pacific coast of Mexico. Ciencias Mar. 2010, 36, 41–58. [Google Scholar] [CrossRef]
- Long, X.; Ma, Y.; Qi, L. Biogenic and synthetic high magnesium calcite—A review. J. Struct. Biol. 2014, 185, 1–14. [Google Scholar] [CrossRef] [PubMed]
- Kunitake, M.E.; Baker, S.P.; Estroff, L.A. The effect of magnesium substitution on the hardness of synthetic and biogenic calcite. MRS Commun. 2012, 2, 113–116. [Google Scholar] [CrossRef] [Green Version]
- Chave, K.E.; Wheeler, B.D. Mineralogic Changes during Growth in the Red Alga. Clathromorphum Compactum. Sci. 1965, 147, 621. [Google Scholar] [CrossRef]
- Moberly, R., Jr. Composition of magnesian calcites of algae and pelecypods by electron microprobe analysis 1. Sedimentology 1968, 11, 61–82. [Google Scholar] [CrossRef]
- Halfar, J.; Steneck, R.; Joachimski, M.; Kronz, A.; Wanamaker, A.D., Jr. Coralline red algae as high-resolution climate recorders. Geology 2008, 36, 463–466. [Google Scholar] [CrossRef]
- Given, R.K.; Wilkinson, B.H. Kinetic control of morphology, composition, and mineralogy of abiotic sedimentary carbonates. J. Sediment. Res. 1985, 55, 109–119. [Google Scholar] [CrossRef]
- Marchini, A.; Ragazzola, F.; Vasapollo, C.; Castelli, A.; Cerrati, G.; Gazzola, F.; Jiang, C.; Langeneck, J.; Manauzzi, M.C.; Musco, L.; et al. Intertidal mediterranean coralline algae habitat is expecting a shift toward a reduced growth and a simplified associated fauna under climate change. Front. Mar. Sci. 2019, 6, 106. [Google Scholar] [CrossRef] [Green Version]
- Melbourne, L.A.; Griffin, J.; Schmidt, D.N.; Rayfield, E.J. Potential and limitations of finite element modelling in assessing structural integrity of coralline algae under future global change. Biogeosciences 2015, 12, 5871–5883. [Google Scholar] [CrossRef] [Green Version]
- Merkel, C.; Deuschle, J.; Griesshaber, E.; Enders, S.; Steinhauser, E.; Hochleitner, R.; Brand, U.; Schmahl, W.W. Mechanical properties of modern calcite—(Mergerlia truncata) and phosphate-shelled brachiopods (Discradisca stella and Lingula anatina) determined by nanoindentation. J. Struct. Biol. 2009, 168, 396–408. [Google Scholar] [CrossRef]
- Chen, J.Y.; Bottjer, D.J.; Oliveri, P.; Dornbos, S.Q.; Gao, F.; Ruffins, S.; Chi, H.; Li, C.W.; Davidson, E.H. Small Bilaterian Fossils from 40 to 55 Million Years Before the Cambrian. Science 2004, 305, 218–222. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fitzer, S.C.; Zhu, W.; Tanner, K.E.; Phoenix, V.R.; Kamenos, N.A.; Cusack, M. Ocean acidification alters the material properties of Mytilus edulis shells. J. R. Soc. Interface 2015, 12, 20141227. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Côté, A.S.; Darkins, R.; Duffy, D.M. Deformation twinning and the role of amino acids and magnesium in calcite hardness from molecular simulation. Phys. Chem. Chem. Phys. 2015, 17, 20178–20184. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Stanley, S.M.; Powell, M.G. Depressed rates of origination and extinction during the late Paleozoic ice age: A new state for the global marine ecosystem. Geology 2003, 31, 877–880. [Google Scholar] [CrossRef]
- Stanley, G.D., Jr. The evolution of modern corals and their early history. Earth Sci. Rev. 2003, 60, 195–225. [Google Scholar] [CrossRef]
- Lebrato, M.; Andersson, A.J.; Ries, J.B.; Aronson, R.B.; Lamare, M.D.; Koeve, W.; Oschlies, A.; Iglesias-Rodriguez, M.D.; Thatje, S.; Amsler, M.; et al. Benthic marine calcifiers coexist with CaCO3-undersaturated seawater worldwide. Glob. Biogeochem. Cycles 2016, 30, 1038–1053. [Google Scholar] [CrossRef] [Green Version]
- Hetzinger, S.; Halfar, J.; Zack, T.; Gamboa, G.; Jacob, D.E.; Kunz, B.E.; Kronz, A.; Adey, W.; Lebednik, P.A.; Steneck, R.S. High-resolution analysis of trace elements in crustose coralline algae from the North Atlantic and North Pacific by laser ablation ICP-MS. Palaeogeogr. Palaeoclimatol. Palaeoecol. 2011, 302, 81–94. [Google Scholar] [CrossRef]
- Burton, J.H.; Price, T.D. The ratio of barium to strontium as a paleodietary indicator of consumption of marine resources. J. Archaeol. Sci. 1990, 17, 547–557. [Google Scholar] [CrossRef]
- Hetzinger, S.; Halfar, J.; Zack, T.; Mecking, J.V.; Kunz, B.E.; Jacob, D.E.; Adey, W.H. Coralline algal barium as indicator for 20th century northwestern North Atlantic surface ocean freshwater variability. Sci. Rep. 2013, 3, 1761. [Google Scholar] [CrossRef] [Green Version]
- Monnin, C.; Jeandel, C.; Cattaldo, T.; Dehairs, F. The marine barite saturation state of the world’s oceans. Mar. Chem. 1999, 65, 253–261. [Google Scholar] [CrossRef]
- Maslen, E.N.; Streltsov, V.A.; Streltsova, N.R.; Ishizawa, N. Electron density and optical anisotropy in rhombohedral carbonates. III. Synchrotron X-ray studies of CaCO3, MgCO3 and MnCO3. Acta Crystallogr. Sect. B 1995, 51, 929–939. [Google Scholar] [CrossRef] [Green Version]
- Beake, B.D.; Leggett, G.J. Nanoindentation and nanoscratch testing of uniaxially and biaxially drawn poly(ethylene terephthalate) film. Polymer 2002, 43, 319–327. [Google Scholar] [CrossRef]
- Beake, B.D.; Leggett, G.J.; Alexander, M.R. Characterisation of the mechanical properties of plasma-polymerised coatings by nanoindentation and nanotribology. J. Mater. Sci. 2002, 37, 4919–4927. [Google Scholar] [CrossRef]
- Oliver, W.C.; Pharr, G.M. An improved technique for determining hardness and elastic modulus using load and displacement sensing indentation experiments. J. Mater. Res. 1992, 7, 1564–1583. [Google Scholar] [CrossRef]
- Guillong, M.; Meier, D.L.; Allan, M.M.; Heinrich, C.A.; Yardley, B.W.D. Appendix A6: SILLS: A MATLAB-based program for the reduction of laser ablation ICP-MS data of homogeneous materials and inclusions. Mineral. Assoc. Can. Short Course 2008, 40, 328–333. [Google Scholar]
- Paton, C.; Hellstrom, J.; Paul, B.; Woodhead, J.; Hergt, J. Iolite: Freeware for the visualisation and processing of mass spectrometric data. J. Anal. At. Spectrom. 2011, 26, 2508–2518. [Google Scholar] [CrossRef]
- Longerich, H.P.; Jackson, S.E.; Gunther, D. Laser ablation inductively coupled plasma mass spectrometric transient signal data acquisition and analyte concentration calculation (vol 11, pg 899, 1996). J. Anal. At. Spectrom. 1997, 12, 391. [Google Scholar]
© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Ragazzola, F.; Kolzenburg, R.; Zekonyte, J.; Teichert, S.; Jiang, C.; Žuljević, A.; Caragnano, A.; Falace, A. Structural and Elemental Analysis of the Freshwater, Low-Mg Calcite Coralline Alga Pneophyllum cetinaensis. Plants 2020, 9, 1089. https://doi.org/10.3390/plants9091089
Ragazzola F, Kolzenburg R, Zekonyte J, Teichert S, Jiang C, Žuljević A, Caragnano A, Falace A. Structural and Elemental Analysis of the Freshwater, Low-Mg Calcite Coralline Alga Pneophyllum cetinaensis. Plants. 2020; 9(9):1089. https://doi.org/10.3390/plants9091089
Chicago/Turabian StyleRagazzola, Federica, Regina Kolzenburg, Jurgita Zekonyte, Sebastian Teichert, Chulin Jiang, Ante Žuljević, Annalisa Caragnano, and Annalisa Falace. 2020. "Structural and Elemental Analysis of the Freshwater, Low-Mg Calcite Coralline Alga Pneophyllum cetinaensis" Plants 9, no. 9: 1089. https://doi.org/10.3390/plants9091089