Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-27T10:22:22.110Z Has data issue: false hasContentIssue false
  • English
  • Français

Macroevolutionary trends in silicoflagellate skeletal morphology: the costs and benefits of silicification

Published online by Cambridge University Press:  08 February 2016

Helena M. van Tol ,
Andrew J. Irwin  and
Zoe V. Finkel
Helena M. van Tol
Affiliation:
Environmental Science Program, Mount Allison University, Sackville, New Brunswick, Canada E4L 1A7. E-mail: hmvantol@mta.ca, zfinkel@mta.ca
Andrew J. Irwin
Affiliation:
Mathematics and Computer Science, Mount Allison University, Sackville, New Brunswick, Canada E4L 1E6. E-mail: airwin@mta.ca
Zoe V. Finkel*
Affiliation:
Environmental Science Program, Mount Allison University, Sackville, New Brunswick, Canada E4L 1A7. E-mail: hmvantol@mta.ca, zfinkel@mta.ca
*
∗∗Corresponding author
Get access Rights & Permissions [Opens in a new window]

Abstract

The silicoflagellates are a class of enigmatic chrysophytes characterized by netlike skeletons composed of opaline silica. Other major groups of siliceous plankton—the diatoms and radiolarians—exhibit evidence of decreasing size or silicification over the Cenozoic. We investigated trends in the silicoflagellate fossil record by constructing a species-level database of diversity and morphological metrics. This new database reveals a proliferation of silicoflagellate species with spined skeletons along with an increase in the mean number of spines per species over the Cenozoic. Although there is little change in skeleton size or silicification among species with spines, those without spines are larger than species with spines and exhibit a decrease in size toward the present. Increased grazing pressure combined with declining surface silicate availability may have shifted the costs and benefits of silicification, causing divergent responses in skeletal morphology between these different morphological lineages of silicoflagellates over time. We postulate that diminishing Cenozoic surface silicic acid availability may have predisposed large spineless silicoflagellate species to extinction, whereas increased grazing pressure may have contributed to the extinction of all remaining spineless species within the edible size range of grazers.

Type
Articles
Information
Paleobiology , Volume 38 , Issue 3 , Summer 2012 , pp. 391 - 402
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

Aksnes, D. L., and Egge, J. K. 1991. A theoretical model for nutrient uptake in phytoplankton. Marine Ecology Progress Series 70:65–72.CrossRefGoogle Scholar
Allen, J. T., Brown, L., Sanders, R., Moore, C. M., Mustard, A., Fielding, S., Lucas, M., Rixen, M., Savidge, G., Henson, S., and Mayor, D. 2005. Diatom carbon export enhanced by silicate upwelling in the northeast Atlantic. Nature 437:728–732.CrossRefGoogle ScholarPubMed
Bell, G. R. 1961. Penetration of spines from a marine diatom into the gill tissue of Lingcod (Ophiodon elongatus). Nature 192:279–280.CrossRefGoogle Scholar
Berner, R. A., Lasaga, A. C., and Garrels, R. M. 1983. The carbonate-silicate geochemical cycle and its effect on atmospheric carbon dioxide over the past 100 million years. Science 283:641–683.Google Scholar
Boney, A. D. 1981. Distephanus speculum: double skeletons with one aberrant partner. Journal of the Marine Biological Association of the U.K. 61:1027–1029.CrossRefGoogle Scholar
Brzezinski, M. A. 1992. Cell-cycle effects on the kinetics of silicic acid uptake and resource competition among diatoms. Journal of Plankton Research 14:1511–1539.CrossRefGoogle Scholar
Bukry, D. 1981. Synthesis of silicoflagellate stratigraphy for Maestrichtian to Quaternary marine sediment. Society of Economic Paleontologists and Minerologists Special Publication 32:433–444.Google Scholar
Chase, J. M. 1999. Food web effects of prey size refugia: variable interactions and alternative stable equilibria. American Naturalist 154:559–570.CrossRefGoogle ScholarPubMed
Cushing, D. H. 1989. A difference in structure between ecosystems in strongly stratified waters and in those that are only weakly stratified. Journal of Plankton Research 11:1–13.CrossRefGoogle Scholar
Daugbjerg, N., and Henriksen, P. 2001. Pigment composition and rbcL sequence data from the silicoflagellate Dictyocha speculum: a heterokont alga with pigments similar to some haptophytes. Journal of Phycology 37:1110–1120.CrossRefGoogle Scholar
Dawkins, R., and Krebs, J. R. 1979. Arms race within and between species. Proceedings of the Royal Society of London B 205:489–511.Google Scholar
Desikachary, T. V., and Prema, P. 1996. Silicoflagellates (Dictyochophyceae). InKies, L. and Schnetter, R., eds. Bibliotheca Phycologica, Vol. 100. J. Cramer, Berlin.Google Scholar
Dove, P. M. 2010. The rise of skeletal biominerals. Elements 6:37–42.CrossRefGoogle Scholar
Dugdale, R. C., and Wilkerson, F. P. 1998. Silicate regulation of new production in the equatorial Pacific upwelling. Nature 391:270–273.CrossRefGoogle Scholar
Fanuko, N. 1989. Possible relation between a bloom of Distephanus speculum (Silicoflagellata) and anoxia in bottom waters in the Northern Adriatic, 1983. Journal of Plankton Research 11:75–84.CrossRefGoogle Scholar
Finkel, Z. V., and Kotrc, B. 2010. Silica use through time: Macroevolutionary changes in the morphology of the diatom frustule. Geomicrobiology Journal 27:596–608.CrossRefGoogle Scholar
Finkel, Z. V., Katz, M. E., Wright, J. D., Schofield, O. M., and Falkowski, P. G. 2005. Climatically driven macroevolutionary patterns in the size of marine diatoms over the Cenozoic. Proceedings of the National Academy of Sciences USA 102:8928–8932.CrossRefGoogle ScholarPubMed
Finkel, Z. V., Beardall, J., Flynn, K. J., Quigg, A., Rees, T. A. V., and Raven, J. A. 2010a. Phytoplankton in a changing world: cell size and elemental stoichiometry. Journal of Plankton Research 32:119–137.CrossRefGoogle Scholar
Finkel, Z. V., Matheson, K. A., Regan, K. S., and Irwin, A. J. 2010b. Genotypic and phenotypic variation in diatom silicification under paleo-oceanographic conditions. Geobiology 8:433–445.CrossRefGoogle ScholarPubMed
Gowen, R. J., McCullough, G., Kleppel, G. S., Houchin, L., and Elliot, P. 1999. Are copepods important grazers of the spring phytoplankton bloom in the Irish Sea? Journal of Plankton Research 21:465–483.CrossRefGoogle Scholar
Guex, J. 2006. Reinitialization of evolutionary clocks during sublethal environmental stress in some invertebrates. Earth and Planetary Science Letters 242:240–253.CrossRefGoogle Scholar
Hamm, C. E., and Smetacek, V. 2007. Armor: why, when, and how. Pp. 311–332inFalkowski, P. G., and Knoll, A. H., eds. Evolution of primary producers in the sea. Elsevier, Amsterdam.CrossRefGoogle Scholar
Hamm, C. E., Merkel, R., Springer, O., Jurkojc, P., Maier, C., Prechtel, K., and Smetacek, V. 2003. Architecture and material properties of diatom shells provide effective mechanical protection. Nature 421:841–843.CrossRefGoogle ScholarPubMed
Hansen, B., Bjornsen, P. K., and Hansen, P. J. 1994. The size ratio between planktonic predators and their prey. Limnology and Oceanography 39:395–403.CrossRefGoogle Scholar
Hargraves, P. E., and Maranda, L. 2002. Potentially toxic or harmful microalgae from the Northeast coast. Northeastern Naturalist 9:81–120.CrossRefGoogle Scholar
Harper, H. E. Jr., and Knoll, A. H. 1975. Silica, diatoms, and Cenozoic radiolarian evolution. Geology 3:175–177.2.0.CO;2>CrossRefGoogle Scholar
Harrison, K. G. 2000. Role of increased marine silica input on paleo-pCO2 levels. Paleoceanography 15:292–298.CrossRefGoogle Scholar
Henriksen, P., Knipschildt, F., Moestrup, O., and Thomsen, H. A. 1993. Autoecology, life history and toxicology of the silicoflagellate Dictyocha speculum (Silicoflagellata, Dictyochophyceae). Phycologia 32:29–39.CrossRefGoogle Scholar
Hurd, D. C. 1973. Interactions of biogenic opal, sediment and seawater in the central equatorial Pacific. Geochimica et cosmochimica acta 37:2257–2282.CrossRefGoogle Scholar
Jochem, F., and Babenerd, B. 1989. Naked Dictyocha speculum—a new type of phytoplankton bloon in the Western Baltic. Marine Biology 103:373–379.CrossRefGoogle Scholar
Knoll, A. H. 2003. Biomineralization and evolutionary history. Reviews in Mineralogy and Geochemistry 54:329–356.CrossRefGoogle Scholar
Lazarus, D. B., Kotrc, B., Wulf, G., and Schmidt, D. N. 2009. Radiolarians decreased silicification as an evolutionary response to reduced Cenozoic ocean silica availability. Proceedings of the National Academy of Sciences USA 106:9333–9338.CrossRefGoogle ScholarPubMed
Ling, H. Y., and Takahashi, K. 1985. The silicoflagellate genus Octactis Schiller 1925: a synonym of the genus Distephanus. Micropaleontology 31:76–81.CrossRefGoogle Scholar
Lipps, J. H. 1970. Ecology and evolution of silicoflagellates. InYochelson, E., ed. Proceedings of the North American Paleontological Convention. Chicago 2:965–993.Google Scholar
Loeblich, A. R. III, Loeblich, L. A., Tappan, H., and Loeblich, A. R. Jr. 1968. Annotated index of fossil and recent silicoflagellates and ebridians with descriptions and illustrations of validly proposed taxa. Geological Society of America, Boulder, Colorado.CrossRefGoogle Scholar
Maldonado, M., Carmona, M. C., Uriz, M. J., and Cruzado, A. 1999. Decline in Mesozoic reef-building sponges explained by silicon limitation. Nature 401:785–788.CrossRefGoogle Scholar
Maldonado, M., Carmona, M. C., Velásquez, Z., Puig, A., Cruzado, A., López, A., and Young, C. M. 2005. Siliceous sponges as a silicon sink: an overlooked aspect of benthopelagic coupling in the marine silicon cycle. Limnology and Oceanography 50:799–809.CrossRefGoogle Scholar
Maldonado, M., Riesgo, A., Bucci, A., and Rützler, K. 2010. Revisiting silicon budgets at a tropical continental shelf: silica standing stocks in sponges surpass those in diatoms. Limnology and Oceanography 55:2001–2010.CrossRefGoogle Scholar
Maliva, R. G., Knoll, A. H., and Siever, R. 1989. Secular change in chert distribution: a reflection of evolving biological participation in the silica cycle. Palaios 4:519–532.CrossRefGoogle ScholarPubMed
Martin-Jézéquel, V., Hildebrand, M., and Brzeziski, M. A. 2000. Silicon metabolism in diatoms: implications for growth. Journal of Phycology 36:821–840.CrossRefGoogle Scholar
McCartney, K. 1987. Silicoflagellates, ebridians and archaeomonads. InBroadhead, T. W., ed. Fossil prokaryotes and protists: notes for a short course (J. Lipps, organizer). Studies in Geology 18:146–168. University of Tennessee, Dept. of Geological Sciences, Knoxville.Google Scholar
McCartney, K., and Loper, D. E. 1989. Optimized skeletal morphologies of silicoflagellate genera Dictyocha and Distephanus. Paleobiology 15:283–298.CrossRefGoogle Scholar
McCartney, K., and Loper, D. E. 1992. Optimal models of skeletal morphology for the silicoflagellate genus Corbisema. Micropaleontology 38:87–93.CrossRefGoogle Scholar
McCartney, K., and Wise, S. W. Jr. 1990. Cenozoic silicoflagellates and ebridians from ODP leg 113: biostratigraphy and notes on morphologic variability. Proceedings of the Ocean Drilling Program, Scientific Results 113:729–760.Google Scholar
McCartney, K., Wise, S. W. Jr, Harwood, D. M., and Gersonde, R. 1990. Enigmatic lower Albian silicoflagellates from ODP site 193: progenitors of the Order Silicoflagellata? Proceedings of the Ocean Drilling Program, Scientific Results 113:427–442.Google Scholar
McCartney, K., Witkowski, J., and Harwood, D. M. 2010. Early evolution of the silicoflagellates during the Cretaceous. Marine Micropaleontology 77:83–100.CrossRefGoogle Scholar
Padisák, J., Soróczki-Pintér, E., and Rezner, Z. 2003. Sinking properties of some phytoplankton shapes and the relation of form resistance to morphological diversity of plankton—an experimental study. Martens, K., ed. Hydrobiologia 500:243–257.CrossRefGoogle Scholar
Perch-Nielsen, K. 1985. Silicoflagellates. Pp. 811–846inM Bolli, H., Saunders, J. B., and Perch-Nielsen, K., eds. Plankton stratigraphy. Cambridge University Press, New York.Google Scholar
Perissinotto, R. 1992. Mesozooplankton size-selectivity and grazing impact on the phytoplankton community of the Prince Edward Archipelago (Southern Ocean). Marine Ecology Progress Series 79:243–258.CrossRefGoogle Scholar
Pondaven, P., Gallinari, M., Chollet, S., Bucciarelli, E., Sarthou, G., Schultes, S., and Jean, F. 2007. Grazing-induced changes in cell wall silicification in a marine diatom. Protist 158:21–28.CrossRefGoogle Scholar
R Development Core Team. 2010. R: a language and environment for statistical computing, Version 2.11.1. R Foundation for Statistical Computing, Vienna.Google Scholar
Ragueneau, O., Tréguer, P., Leynaert, A., Anderson, R. F., Brzezinski, M. A., DeMaster, D. J., Dugdale, R. C., Dymond, J., Fischer, G., François, R., Heinze, C., Maier-Reimer, E., Martin-Jézéquel, V., Nelson, D. M., and Quéguiner, B. 2000. A review of the Si cycle in the modern ocean: recent progress and missing gaps in the application of biogenic opal as a paleoprofuctivity proxy. Global and Planetary Change 26:317–365.CrossRefGoogle Scholar
Raven, J. A., and Waite, A. M. 2004. The evolution of silicification in diatoms: inescapable sinking or sinking as escape? New Phytologist 162:45–61.CrossRefGoogle Scholar
Reynolds, C. S. 1984. The ecology of freshwater plankton. Cambridge University Press, Cambridge.Google Scholar
Sarjeant, W. A., Lacalli, T., and Gaines, G. 1987. The cysts and skeletal elements of dinoflagellates: speculations on the ecological causes for their morphology and development. Micropaleontology 33:1–36.CrossRefGoogle Scholar
Smetacek, V. 1985. Role of sinking in diatom life-history cycles: ecological, evolutionary and geological significance. Marine Biology 3:239–251.CrossRefGoogle Scholar
Smetacek, V. 2001. A watery arms race. Nature 411:745.CrossRefGoogle ScholarPubMed
Sommer, U. 1998. Silicate and the functional geometry of marine phytoplankton. Journal of Plankton Research 20:1853–1859.CrossRefGoogle Scholar
Thomas, W. H., Hollibaugh, J. T., and Seibert, D. L. R. 1980. Effects of heavy metals on the morphology of some marine phytoplankton. Phycologia 19:202–209.CrossRefGoogle Scholar
Thomsen, H. A., and Moestrup, O. 1985. Is Distephanus speculum a fish-killer? A report of an unusual algal bloom from Danish coastal waters. Bulletin of Marine Science 37:778.Google Scholar
Tréguer, P., Nelson, D. M., Van Bennekom, A. J., DeMaster, D. J., Leynaert, A., and Quéguiner, B. 1995. The Silica Balance in the World Ocean: A Reestimate. Science 268:375–379.CrossRefGoogle Scholar
Van Valkenburg, S. D., and Norris, R. E. 1970. The growth and morphology of the silicoflagellate Dictyocha fibula Ehrenburg in culture. Journal of Phycology 6:48–54.CrossRefGoogle Scholar
Wallace, A. F., DeYoreo, J. J., and Dove, P. M. 2009. Kinetics of silica nucleation on carboxyl- and amine-terminated surfaces: insights for biomineralization. Journal of the American Chemical Society 131:5244–5250.CrossRefGoogle ScholarPubMed
Yool, A., and Tyrrell, T. 2003. Role of diatoms in regulating the ocean's silicon cycle. Global Biogeochemical Cycles 17:1–21.CrossRefGoogle Scholar