Hostname: page-component-848d4c4894-8kt4b Total loading time: 0 Render date: 2024-07-05T02:03:42.877Z Has data issue: false hasContentIssue false

Aragonite production in calcite seas: effect of seawater Mg/Ca ratio on the calcification and growth of the calcareous alga Penicillus capitatus

Published online by Cambridge University Press:  08 April 2016

Justin B. Ries*
Affiliation:
Department of Earth and Planetary Sciences, Johns Hopkins University, 301 Olin Hall, Baltimore, Maryland 21218. E-mail: [email protected]

Abstract

Previous studies have shown that secular variation in the Mg/Ca ratio of seawater throughout the Phanerozoic would have subjected the aragonite-producing codiacean algae to at least three transitions between the low-Mg calcite (molar Mg/Ca <2) and aragonite + high-Mg calcite (molar Mg/Ca >2) nucleation fields in the oceans, since their origin in the Ordovician. These studies have asserted that major sediment production by codiacean algae in Recent tropical seas is permitted by the Mg/Ca ratio of modern seawater (molar Mg/Ca ∼5.2) remaining within the aragonitic/high-Mg calcite nucleation field (molar Mg/Ca >2). Here I present the results of experiments conducted to determine the effects of ambient Mg/Ca on the mineralogy, growth rate, primary productivity, calcification rate, and biomechanics of the codiacean alga Penicillus capitatus.

P. capitatus specimens were grown in three artificial seawater treatments that mimic ancient seawater of differing Mg/Ca ratios, corresponding to the low-Mg calcite nucleation field (molar Mg/Ca ∼1.0), a “boundary field” (molar Mg/Ca ∼2.5), and the aragonite + high-Mg calcite nucleation field (molar Mg/Ca ∼5.2). Significantly, P. capitatus specimens maintained a mostly aragonitic mineralogy in all three seawater treatments. However, linear growth rates, primary productivity, calcification, and thallus stiffness decreased with reductions in ambient Mg/Ca. That P. capitatus precipitates approximately three-quarters of its CaCO3 as aragonite in the seawater treatment that favors the inorganic precipitation of low-Mg calcite suggests that the alga dictates the precipitation of that polymorph, either by pumping cations to create an internal aragonite nucleation field (molar Mg/Ca >2) or by employing organic templates that specify the nucleation of the aragonite polymorph (Borowitzka 1984). However, the alga's precipitation of one-quarter of its CaCO3 as low-Mg calcite suggests that its mineralogical control is limited and can be partially overridden by the Mg/Ca ratio of ambient seawater. The reduced calcification of P. capitatus specimens grown in the low-Mg calcite and boundary nucleation fields is probably due to the inherent difficulty of precipitating aragonite from seawater which does not naturally support its nucleation. The decreased rates of linear growth and primary production are probably caused by reductions in CO2 available for photosynthesis due to the reduction in calcification (Borowitzka and Larkum 1977). The observed decrease in thallus stiffness is probably due to the reductions in calcification and primary productivity observed in P. capitatus specimens grown in the low-Mg calcite and boundary nucleation fields.

The present study suggests that aragonitic algae would have been handicapped in oceans characterized by Mg/Ca ratios that did not support their inherent mineralogy. Producing aragonite in seawater outside of the aragonite + high-Mg calcite nucleation field would probably have reduced the competitiveness of these algae, made them more susceptible to predation, and reduced their contribution to carbonate sedimentation. These findings support earlier assertions that the dominant ecological and sedimentological roles of codiacean algae in Recent tropical seas is permitted by a Mg/Ca ratio of seawater that supports the algae's aragonitic mineralogy during this time.

Type
Articles
Copyright
Copyright © The Paleontological Society 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature Cited

Bathurst, R. G. C. 1975. Carbonate sediments and their diagenesis. Elsevier, Amsterdam.Google Scholar
Baumiller, T. K., and Ausich, W. I. 1996. Crinoid stalk flexibility: theoretical predictions and fossil stalk postures. Lethaia 29:4759.Google Scholar
Bidwell, J. P., and Spotte, S. 1985. Artificial seawaters: formulas and methods. Jones and Bartlett, Boston.Google Scholar
Böhm, L., and Fütterer, D. 1978. Algal calcification in some Codiaceae (Chlorophyta): ultrastructure and location of skeletal deposits. Journal of Phycology 14:486493.CrossRefGoogle Scholar
Borowitzka, M. A. 1977. Algal calcification. Oceanography and Marine Biology Annual Review 15:189223.Google Scholar
Borowitzka, M. A. 1984. Calcification in aquatic plants. Plant, Cell and Environment 7:457466.Google Scholar
Borowitzka, M. A., and Larkum, A. W. D. 1976. Calcification in the green alga Halimeda. III. The sources of inorganic carbon for photosynthesis and calcification and a model of the mechanism of calcification. Journal of Experimental Biology 27:879893.Google Scholar
Borowitzka, M. A., and Larkum, A. W. D. 1977. Calcification in the green alga Halimeda. I. An ultrastructure study of thallus development. Journal of Phycology 13:616.Google Scholar
Borowitzka, M. A., Larkum, W. D., and Nockolds, C. E. 1974. A scanning electron microscope study of the structure and organization of the calcium carbonate deposits of algae. Phycologia 13:195203.Google Scholar
Chuvashov, B., and Riding, R. 1984. Principal floras of Paleozoic marine calcareous algae. Palaeontology 27:487500.Google Scholar
Cloud, P. E. Jr. 1962. Environment of calcium carbonate deposition west of Andros Island, Bahamas. U.S. Geological Survey Professional Paper 350.Google Scholar
Dickson, J. A. D. 2002. Fossil echinoderms as monitor of the Mg/Ca ratio of Phanerozoic oceans. Science 298:12221224.Google Scholar
Dickson, J. A. D. 2004. Echinoderm skeletal preservation: calcite-aragonite seas and the Mg/Ca ratio of Phanerozoic oceans. Journal of Sedimentary Research 74:355365.Google Scholar
Drew, E. A. 1983. Halimeda biomass growth rate and sediment generation on reefs in the Central Great Barrier Reef Province. Coral Reefs 2:101110.CrossRefGoogle Scholar
Drew, E. A., and Abel, K. M. 1988. Studies on Halimeda. 1. The distribution and species composition of Halimeda meadows throughout the Great Barrier Reef Province. Coral Reefs 6:195205.Google Scholar
Elliot, G. F. 1978. Ecological significance of post-Paleozoic green calcareous algae. Geological Magazine 115:437442.Google Scholar
Flajs, G. 1977. Skeletal structures of some calcifying algae. Pp. 225231in Flugel, E., ed. Fossil algae. Springer, Berlin.Google Scholar
Flügel, E. 1988. Halimeda: paleontological record and palaeoenvironmental significance. Coral Reefs 6:123130.Google Scholar
Flügel, E. 1991. Triassic and Jurassic marine calcareous algae: a critical review. Pp. 481503in Riding, 1991.Google Scholar
Folk, R. L. 1974. The natural history of crystalline calcium carbonate: effect of magnesium content and salinity. Journal of Sedimentary Petrology 44:4053.Google Scholar
Friedman, E. I., Roth, W. C., Turner, J. B., and McEwin, R. S. 1972. Calcium oxalate crystals in the aragonite-producing green alga Penicillus and related genera. Science 177:891893.Google Scholar
Füchtbauer, H., and Hardie, L. A. 1976. Experimentally determined homogeneous distribution coefficients for precipitated magnesian calcites: application to marine carbonate cements. Geological Society of America Abstracts with Program 8:877.Google Scholar
Füchtbauer, H., and Hardie, L. A. 1980. Comparison of experimental and natural magnesian calcites. International Association of Sedimentologists Meeting, Bochum, Germany, Abstracts, pp. 167169.Google Scholar
Gaylord, E. H., and Gaylord, C. N. 1990. Structural engineering handbook. McGraw-Hill, New York.Google Scholar
Hardie, L. A. 1996. Secular variation in seawater chemistry: an explanation for the coupled secular variation in the mineralogies of marine limestones and potash evaporites over the past 600 m.y. Geology 24:279283.2.3.CO;2>CrossRefGoogle Scholar
Hillis, L. 1991. Recent calcified Halimedaceae. Pp. 167188in Riding 1991.Google Scholar
Hillis-Colinvaux, L. 1980. Ecology and taxonomy of Halimeda: primary producer of coral reefs. Advances in Marine Biology No. 17. Academic Press, London.Google Scholar
Hine, A. C., Hallock, P., Harris, M. W., Mullins, H. T., Belknap, D. F., and Jaap, W. C. 1988. Halimeda bioherms along an open seaway: Miskito Channel, Nicaraguan Rise, SW Carribbean Sea. Coral Reefs 6:173178.Google Scholar
H⊘eg, O. A. 1927. Preliminary note on a new Codiaceae from the Ordovician of Norway. Avh Norske Videnskaps Akademi i Oslo, Mat. Naturviss. 4:115.Google Scholar
Hudson, J. H. 1985. Growth rate and carbonate production in Halimeda opuntia: Marquesas Keys, Florida. Pp. 257263In Toomey, D. F. and Nitecki, M. H., eds. Paleoalgology. Springer, Berlin.Google Scholar
Johnson, J. H. 1961. Limestone-building algae and algal limestones. Colorado School of Mines.Google Scholar
Jux, U. 1966. Palaeoporella in Boda-Kalk von Dalarne. Palaeontographica 118:153165.Google Scholar
Leitmeier, H. 1910. Zur kenntnis der carbonate, die dimorphie des Kohlensauren Kalkes. I. Teil. Neues Jahrbuch für Mineralogie, Heft 1:4974.Google Scholar
Leitmeier, H. 1915. Zur kenntnis der carbonate. II. Teil. Neues Jahrbuch für Mineralogie, Beilageband 40:655700.Google Scholar
Lippman, F. 1960. Versuche zur Aufklarung der Bildungsbedingungen von Calcit und Aragonit. Fortschritte der Mineralogie 38:156161.Google Scholar
Lowenstam, H. A. 1955. Aragonite needles secreted by algae and some sedimentary implications. Journal of Sedimentary Petrology 25:270272.Google Scholar
Lowenstam, H. A., and Epstein, S. 1957. On the origin of sedimentary aragonite needles of the Great Bahama Bank. Journal of Geology 65:364375.CrossRefGoogle Scholar
Lowenstein, T. K., Timofeeff, M. N., Brennan, S. T., Hardie, L. A., and Demicco, R. V. 2001. Oscillations in Phanerozoic seawater chemistry: evidence from fluid inclusions. Science 294:10861088.CrossRefGoogle ScholarPubMed
Lowenstein, T. K., Hardie, L. A., Timofeeff, M. N., and Demicco, R. V. 2003. Secular variation in seawater chemistry and the origin of calcium chloride basinal brines. Geology 31:857860.Google Scholar
Mamet, B. 1991. Carbonifereous calcareous algae. Pp. 370451in Riding 1991.Google Scholar
Mankiewicz, C. 1988. Occurrence and paleoecologic significance of Halimeda in late Miocene reefs, southeastern Spain. Coral Reefs 6:271279.Google Scholar
Marshall, J. F., and Davies, P. J. 1988. Halimeda bioherms of the Great Barrier Reef. Coral Reefs 6:139148.Google Scholar
Matthews, R. K. 1966. Genesis of Recent lime mud in southern British Honduras. Journal of Sedimentary Petrology 36:428454.Google Scholar
Milliman, J. D. 1974. Marine carbonates. Springer, Berlin.Google Scholar
Milliman, J. D. 1977. Role of calcareous algae in Atlantic continental margin sedimentation. Pp. 232247in Flugel, E., ed. Fossil algae. Springer, Berlin.Google Scholar
Montañez, I. P. 2002. Biological skeletal carbonate records changes in major-ion chemistry of paleo-oceans. Proceedings of the National Academy of Sciences USA 99:1585215854.Google Scholar
Mu, X. 1991. Fossil Udoteaceae and Gymnocodiaceae. Pp. 146166in Riding 1991.Google Scholar
Müller, G., Irion, G., and Förstner, U. 1972. Formation and diagenesis of inorganic Ca-Mg carbonates in the lacustrine environment. Naturwissenschaften 59:158164.Google Scholar
Multer, H. G. 1988. Growth rate, ultrastructure and sediment contribution of Halimeda incrassata and Halimeda monile, Nonsuch and Falmouth Bays, Antiqua, W. I. Coral Reefs 6:179186.Google Scholar
Neumann, A. C., and Land, L. S. 1975. Lime mud deposition and calcareous algae in the Bight of Abaco, Bahamas: a budget. Journal of Sedimentary Petrology 45:763786.Google Scholar
Orme, G. R., and Salama, M. S. 1988. Form and seismic stratigraphy of Halimeda banks in part of the northern Great Barrier Reef Province. Coral Reefs 6:131137.Google Scholar
Paasche, E. 1968. Biology and physiology of coccolithophorids. Annual Review of Microbiology 22:7786.Google Scholar
Paul, V. J., and Van Alstyne, K. L. 1988. Chemical defense and chemical variation in some tropical Pacific species of Halimeda (Halimedaceae; Chlorophyta). Coral Reefs 6:263269.Google Scholar
Payri, C. E. 1988. Halimeda contribution to organic and inorganic production in a Tahitian reef system. Coral Reefs 6:251262.CrossRefGoogle Scholar
Phipps, C. V. G., and Roberts, H. H. 1988. Seismic characteristics and accretion history of Halimeda bioherms on Kalukalukuang Bank, eastern Java Sea (Indonesia). Coral Reefs 6:149159.Google Scholar
Reiskind, J. B., Seamon, P. T., and Bowes, G. 1988. Alternative methods of photosynthetic carbon assimilation in marine macroalgae. Plant Physiology 87:686692.Google Scholar
Reiskind, J. B., Seamon, P. T., and Bowes, G. 1989. Photosynthetic responses and anatomical features of two marine macroalgae with different CO2 compensation points. Aquatic Botany 33:7186.Google Scholar
Riding, R., ed. 1991. Calcareous algae and stromatolites. Springer, Berlin.Google Scholar
Riding, R., and Guo, L. 1991. Permian marine calcareous algae. Pp. 452480in Riding 1991.Google Scholar
Ries, J. B. 2004. Effect of ambient Mg/Ca on Mg fractionation in calcareous marine invertebrates: a record of the oceanic Mg/Ca ratio over the Phanerozoic. Geology 32:981984.Google Scholar
Roberts, H. H., Aharon, P., and Phipps, C. V. 1988. Morphology and sedimentology of Halimeda bioherms from the eastern Java Sea (Indonesia). Coral Reefs 6:161172.Google Scholar
Roux, A. 1991. Ordovician algae and global tectonics. Pp. 335348in Riding 1991.Google Scholar
Sandberg, P. A. 1983. An oscillating trend in Phanerozoic non-skeletal carbonate mineralogy. Nature 305:1922.Google Scholar
Schupp, P. J., and Paul, V. J. 1994. Calcium carbonate and secondary metabolites in tropical seaweeds: variable effects on herbivorous fishes. Ecology 75:11721185.Google Scholar
Segonzak, G. 1986. Aspects concernant les algues de type Halimeda (Chlorophycées), actuelles et fossiles. Bulletin de la Société de la Histoire Naturelle de Toulouse 122:125129.Google Scholar
Siemann, M. G. 2003. Extensive and rapid changes in seawater chemistry during the Phanerozoic: evidence from Br contents in basal halite. Terra Nova 15:243248.Google Scholar
Sikes, C. S., Roer, R. D., and Wilbur, K. M. 1980. Photosynthesis and coccolith formation: inorganic carbon sources and net inorganic reaction of deposition. Limnology and Oceanography 25:248261.Google Scholar
Spotte, S. H. 1979. Seawater aquariums: the captive environment. Wiley, New York.Google Scholar
Stanley, S. M., and Hardie, L. A. 1998. Secular oscillations in carbonate mineralogy of reef-building and sediment-producing organisms driven by tectonically forced shifts in seawater chemistry. Palaeogeography, Palaeoclimatology, Palaeoecology 144:319.Google Scholar
Stanley, S. M., and Hardie, L. A. 1999. Hypercalcification: paleontology links plate tectonics and geochemistry to sedimentology. GSA Today 9:27.Google Scholar
Stanley, S. M., Ries, J. B., and Hardie, L. A. 2002. Low-magnesium calcite produced by coralline algae in seawater of Late Cretaceous composition. Proceedings of the National Academy of Sciences USA 99:1532315326.Google Scholar
Stanley, S. M., Ries, J. B., and Hardie, L. A.In press. Seawater chemistry, coccolithophore population growth, and the origin of Cretaceous chalk. Geology.Google Scholar
Stockman, K. W., Ginsburg, R. N., and Shinn, E. A. 1967. The production of lime mud by algae in south Florida. Journal of Sedimentary Petrology 37:633648.Google Scholar
Van den Hoek, C. 1981. Chlorophyta: morphology and classification. Pp. 86132in Lobban, C. S., and Wynne, M. J., eds. The biology of seaweeds. University of California Press, Berkeley.Google Scholar
Wainwright, S. A., Biggs, W. D., Currey, J. D., and Gosline, J. M. 1976. Mechanical design in organisms. Edward Arnold, London.Google Scholar
Wefer, G. 1980. Carbonate production by algae Halimeda, Penicillus and Padina. Nature 285:323324.Google Scholar
Wray, J. L. 1977. Calcareous algae. Elsevier, Amsterdam.Google Scholar