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Functional morphology and evolution of early Paleozoic dasycladalean algae (Chlorophyta)

Published online by Cambridge University Press:  08 April 2016

Steven T. LoDuca  and
Ernest R. Behringer
Steven T. LoDuca
Affiliation:
Department of Geography and Geology, Eastern Michigan University, Ypsilanti, Michigan 48197. E-mail: [email protected]
Ernest R. Behringer
Affiliation:
Department of Physics and Astronomy, Eastern Michigan University, Ypsilanti, Michigan 48197
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Abstract

Biophysical modeling and morphologic data from the fossil record were used to investigate the functional significance of changes in thallus morphology during the early evolutionary history of dasycladalean algae (dasyclads), a clade of benthic marine macroalgae. Modeling results indicate that the addition of cylindrical appendages (laterals) to an upright main axis, a key morphological innovation in the evolution of dasyclad thallus form, can provide for large gains in light interception efficiency, near-maximum gains in this regard being achieved when the ratio of total lateral surface area to main axis surface area is 4 or greater. Among the 13 early Paleozoic study taxa, all but one was found to exceed this value. Modeling of surface area to volume ratios for early Paleozoic dasyclads indicates that laterals for these forms conveyed only modest gains in this regard and, therefore, likely played little role in improving nutrient uptake. For survivorship, it appears that increasing thallus complexity by developing laterals conveyed important benefits by imparting both compartmentalization and redundancy, thereby increasing the likelihood that lateral-bearing forms would survive attacks by early mesograzers. Trends and patterns in the fossil record support such a survival-enhancing role for laterals and are consistent with the initial evolution of these structures as an early manifestation of an evolutionary arms race between macroalgae and herbivores initiated near the Proterozoic/Phanerozoic boundary.

Type
Articles
Information
Paleobiology , Volume 35 , Issue 1 , Winter 2009 , pp. 63 - 76
Copyright
Copyright © The Paleontological Society 

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References

Literature Cited

Adamich, M., Gibor, A., and Sweeney, B. M. 1975. Effects of low nitrogen levels and various nitrogen sources on growth and whorl development in Acetabularia (Chlorophyta). Journal of Phycology 11:364–367.Google Scholar
Anderson, S. M., and Charters, A. C. 1982. A fluid mechanics study of seawater flow through Gelidium nudifrons . Limnology and Oceanography 27:399–412.Google Scholar
Barattolo, F. 1990. Mesozoic and Cenozoic marine benthic calcareous algae with particular regard to Mesozoic Dasycladaleans. Pp. 504–540 in Riding, R., ed. Calcareous algae and stromatolites. Springer, Berlin.Google Scholar
Beadle, S. C. 1988. Dasyclads, cyclocrinitids and receptaculitids: comparative morphology and paleoecology. Lethaia 21:1–12.Google Scholar
Beadle, S. C., and Johnson, M. E. 1986. Palaeoecology of Silurian cyclocrinitid algae. Palaeontology 29:585–602.Google Scholar
Berger, S., and Kaever, M. J. 1992. Dasycladales: an illustrated monograph of a fascinating algal order. Georg Thieme, Stuttgart.Google Scholar
Bock, W. J., and von Wahlert, G. 1965. Adaptation and the form-function complex. Evolution 19:269–299.Google Scholar
Bonotto, S. 1969. Quelques observations sur les verticilles d'Acetabularia mediterranea . Bulletin de la Société Royale de Botanique de Belgique 102:165–179.Google Scholar
Bucur, I. I. 1999. Stratigraphic significance of some skeletal algae (Dasycladales, Caulerpales) of the Phanerozoic. In Farinacci, A. and Lord, A. R., eds. Depositional episodes and bioevents. Palaeopelagos Special Publication 2:53–104. Università La Sapienza, Rome.Google Scholar
Butterfield, N. J. 2001. Plankton ecology and the Proterozoic-Phanerozoic transition. Paleobiology 23:247–262.Google Scholar
Butterfield, N. J. 2004. A vaucheriacean alga from the middle Neoproterozoic of Spitsbergen: implications for the evolution of Proterozoic eukaryotes and the Cambrian explosion 30:231–252.Google Scholar
Carpenter, R. C. 1986. Partitioning herbivory and its effects on coral reef algal communities. Ecological Monographs 56:245–363.CrossRefGoogle Scholar
Chen, J., and Erdtmann, B.-D. 1991. Lower Cambrian fossil Lagerstätte from Chengjiang, Yunnan, China: insights for reconstructing early metazoan life. Pp. 57–76 in Simonetta, A. M. and Morris, S. Conway, eds. The early evolution of Metazoa and the significance of problematic taxa. Cambridge University Press, Cambridge.Google Scholar
Morris, S. Conway, and Peel, J. S. 1995. Articulated halkieriids from the Lower Cambrian of North Greenland and their role in early protostome evolution. Philosophical Transactions of the Royal Society of London B 347:305–358.Google Scholar
DeBoer, J. A., and Whoriskey, F. 1983. Production and role of hyaline hairs in Ceramium rubrum . Marine Biology 77:229–234.Google Scholar
Declève, A., Van Gorp, U., Boloukhère, M., and Bonotto, S. 1972. Biochemical and ultrastructural investigations on the whorls of Acetabularia mediterranea . Pp. 259–293 in Bonotto, S., Goutier, R., Kirchmann, R., and Maisin, J. R., eds. Biology and radiobiology of anucleate systems. II. Plant cells. Academic Press, New York.Google Scholar
Duffy, J. E., and Hay, M. E. 1990. Seaweed adaptations to herbivory. BioScience 40:368–375.CrossRefGoogle Scholar
Dumais, J., and Harrison, L. G. 2000. Whorl morphogenesis in the dasycladalean algae: the pattern formation viewpoint. Philosophical Transactions of the Royal Society of London B 355:281–305.Google Scholar
Fauchald, K., and Jumars, P. A. 1979. The diet of worms: a study of polychaete feeding guilds. Oceanography and Marine Biology Annual Review 17:193–284.Google Scholar
Gibor, A. 1973a. Observations on the sterile whorls of Acetabularia . Protoplasma 78:195–202.CrossRefGoogle Scholar
Gibor, A. 1973b. Acetabularia: physiological role of their deciduous organelles. Protoplasma 78:461–465.CrossRefGoogle Scholar
Gómez-Poot, J. M., Espinoza-Avalos, J., and Jiménez-Flores, S. G. 2002. Vegetative and reproductive characteristics of two species of Batophora (Chlorophyta, Dasycladaceae) from Chetumal Bay, Quintana Roo, Mexico. Botanica Marina 45:189–195.CrossRefGoogle Scholar
Goodwin, B. C., Skelton, J. C., and Kirk-Bell, S. M. 1983. Control of regeneration and morphogenesis by divalent actions in Acetabularia mediterranea . Planta 157:1–7.Google Scholar
Graham, L. E., and Wilcox, L. W. 2000. Algae. Prentice Hall, Upper Saddle River, N.J. Google Scholar
Hamm, C., and Smetacek, V. 2007. Armor: why, when, and how. Pp. 312–333 in Falkowski, P. G. and Knoll, A. H., eds. Evolution of primary producers in the sea. Elsevier, Burlington, Mass. Google Scholar
Han, T.-M., and Runnegar, B. 1992. Megascopic eukaryotic algae from the 2.1 billion-year-old Negaunee Iron-Formation, Michigan. Science 257:232–235.Google Scholar
Hay, M. E. 1981a. Herbivory, algal distribution, and the maintenance of between-habitat diversity on a tropical fringing reef. American Naturalist 118:520–540.CrossRefGoogle Scholar
Hay, M. E. 1981b. The functional morphology of turf-forming seaweeds: persistence in stressful marine habitats. Ecology 62:739–750.CrossRefGoogle Scholar
Hay, M. E. 1986. Functional geometry of seaweeds: ecological consequences of thallus layering and shape. Pp. 635–66 in Givnish, T. J., ed. On the economy of plant form and function. Cambridge University Press, Cambridge.Google Scholar
Hein, M., Pedersen, M. F., and Sand-Jensen, K. 1995. Size-dependent nitrogen uptake in micro- and macroalgae. Marine Ecology Progress Series 118:247–253.Google Scholar
H⊘eg, O. A. 1926. Description of the fossil plants. In H⊘eg, O. and Kiær, J., eds. A new plant-bearing horizon in the marine Ludlow of Ringerike. Avhandlinger utgitt av det Norske Videnskaps-Akademi. I. Matematisk-Naturvidenskapelig Klasse 1:1–12.Google Scholar
Kenrick, P., and Vinther, J. 2006. Chaetocladus gracilis n. sp., a non-calcified Dasycladales from the Upper Silurian of Skåne, Sweden. Review of Palaeobotany and Palynology 142:153–160.CrossRefGoogle Scholar
Kirk, J. T. O. 1994. Light and photosynthesis in aquatic ecosystems. Cambridge University Press, Cambridge.Google Scholar
Lewis, S. M., Norris, J. N., and Searles, R. B. 1987. The regulation of morphological plasticity in tropical reef algae by herbivory. Ecology 68:636–641.CrossRefGoogle Scholar
Littler, M. M., and Arnold, K. E. 1982. Primary productivity of marine macroalgal functional-form groups from southwestern North America. Journal of Phycology 18:307–311.Google Scholar
Littler, M. M., and Littler, D. S. 1980. The evolution of thallus form and survival strategies in benthic marine macroalgae: field and laboratory tests of a functional form model. American Naturalist 116:25–44.CrossRefGoogle Scholar
Littler, M. M., Littler, D. S., and Taylor, P. R. 1983. Evolutionary strategies in a tropical barrier reef system: functional-form groups of marine macroalgae. Journal of Phycology 19:229–237.Google Scholar
Lobban, C. S., and Harrison, P. J. 1994. Seaweed ecology and physiology. Cambridge University Press, Cambridge.Google Scholar
LoDuca, S. T., Kluessendorf, J., and Mikulic, D. G. 2003. A new noncalcified dasycladalean alga from the Silurian of Wisconsin. Journal of Paleontology 77:956–962.Google Scholar
Menzel, D. 1980. Plug formation and peroxidase accumulation in two orders of siphonous green algae (Caulerpales and Dasycladales) in relation to fertilization and injury. Phycologia 19:37–48.CrossRefGoogle Scholar
Menzel, D. 1994. Cell differentiation and the cytoskeleton in Acetabularia . New Phytologist 128:369–393.Google Scholar
Ngo, D. A., Garland, P. A., and Mandoli, D. F. 2005. Development and organization of the central vacuole of Acetabularia acetabulum . New Phytologist 165:731–746.CrossRefGoogle ScholarPubMed
Nielsen, S. L., and Sand-Jensen, K. 1990. Allometric scaling of maximal photosynthetic growth rate to surface/volume ratio. Limnology and Oceanography 35:177–181.CrossRefGoogle Scholar
Niklas, K. J. 1988. The role of phyllotactic pattern as a “developmental constraint” on the interception of light by leaf surfaces. Evolution 42:1–16.Google Scholar
Niklas, K. J. 1997. The evolutionary biology of plants. University of Chicago Press, Chicago.Google Scholar
Niklas, K. J. 2000. Modeling fossil plant form-function relationships: a critique. In Erwin, D. H. and Wing, S. L., eds. Deep time: Paleobiology's perspective Paleobiology 26(Suppl. to No. 4):289–304.Google Scholar
Niklas, K. J., and Kerchner, V. 1984. Mechanical and photosynthetic constraints on the evolution of plant shape. Paleobiology 10:79–101.CrossRefGoogle Scholar
Nishimura, N. J., and Mandoli, D. 1992a. Vegetative growth of Acetabularia acetabulum (Chlorophyta): structural evidence for juvenile and adult phases in development. Journal of Phycology 28:669–677.Google Scholar
Nishimura, N. J., and Mandoli, D. 1992b. Population analysis of reproductive cell structures of Acetabularia acetabulum (Chlorophyta). Phycologia 31:351–358.Google Scholar
Nitecki, M. H. 1970. North American cyclocrinitid algae. Fieldiana (Geology) 21:1–182.Google Scholar
Peterson, K. J., and Butterfield, N. J. 2005. Origin of the Eumetazoa: testing ecological predictions of molecular clocks against the Proterozoic fossil record. Proceedings of the National Academy of Sciences USA 102:9547–9552.Google Scholar
Pia, J. 1920. Die Siphoneae Verticillatae vom Karbon bis zur Kreide. Abhandlungen Zoologisch-Botanische Gesellschaftin Wien 11:3–263.Google Scholar
Plotnick, R., and Baumiller, T. K. 2000. Invention by evolution: functional analysis in paleobiology. In Erwin, D. H. and Wing, S. L., eds. Deep time: Paleobiology's perspective Paleobiology 26(Suppl. to No. 4):305–323.Google Scholar
Prandtl, L. 1935. The mechanics of viscous fluids. Pp. 34–207 in Durand, W. F., ed. Aerodynamic theory. Springer, Berlin.Google Scholar
Ramus, J. 1978. Seaweed anatomy and photosynthetic performance: the ecological significance of light guides, heterogeneous absorption and multiple scatter. Journal of Phycology 14:352–362.Google Scholar
Riding, R. 1994. Evolution of algal and cyanobacterial calcification. Pp. 426–438 in Bengtson, S., ed. Early life on Earth. Columbia University Press, New York.Google Scholar
Riding, R. 2001. Calcified algae and cyanobacteria. Pp. 445–473 in Zhuravlev, A. and Riding, R., eds. The ecology of the Cambrian radiation. Columbia University Press, New York.Google Scholar
Runnegar, B. 1994. Proterozoic eukaryotes: evidence from biology and geology. Pp. 287–297 in Bengtson, S., ed. Early life on Earth. Columbia University Press, New York.Google Scholar
Schweiger, H. G., Berger, S., Kloppstech, K., Apel, K., and Schweiger, M. 1974. Some fine structural and biochemical features of Acetabularia major (Chlorophyta, Dasycladaceae) grown in the laboratory. Phycologia 13:11–20.CrossRefGoogle Scholar
Serikawa, K. A., Porterfield, D. M., Smith, P. J. S., and Mandoli, D. F. 2000. Calcification and measurements of net proton and oxygen flux reveal subcellular domains in Acetabularia acetabulum . Planta 211:474–483.Google Scholar
Shihira-Ishikawa, I., Yano, D. M. Y., and Imahori, K. 1985. Morphological variability and plasticity in cultured cells of Acetabularia calyculus (Chlorophyceae). Pp. 245–256 in Hara, H., ed. Origin and evolution of diversity in plants and plant communities. Academia Scientific Book, Tokyo.Google Scholar
Steneck, R. S. 1983. Escalating herbivory and resulting adaptive trends in calcareous algal crusts. Paleobiology 9:44–61.Google Scholar
Steneck, R. S., and Dethier, M. N. 1994. A functional group approach to the structure of algal-dominated communities. Oikos 69:476–498.Google Scholar
Taylor, W. R. 1960. Marine algae of the eastern tropical and subtropical coasts of the Americas. University of Michigan Press, Ann Arbor.Google Scholar
Thompson, D. 1942. On growth and form. Cambridge University Press, Cambridge.Google Scholar
Vogel, S. 1994. Life in moving fluids: the physical biology of flow. Princeton University Press, Princeton, N.J. Google Scholar
von Dassow, M., Odell, G. M., and Mandoli, D. F. 2000. Relationships between growth, morphology and wall stress in the stalk of Acetabularia acetabulum . Planta 213:659–666.Google Scholar
Walter, M. R., Rulin, Du, and Horodyski, R. J. 1990. Coiled carbonaceous megafossils from the Middle Proterozoic of Jixian (Tianjin) and Montana. American Journal of Science 290-A:133–148.Google Scholar
Wheeler, W. N. 1988. Algal productivity and hydrodynamics: a synthesis. Progress in Phycological Research 6:23–58.Google Scholar
Xiao, S., and Dong, L. 2006. On the morphology and ecological history of Proterozoic macroalgae. Pp. 57–90 in Xiao, S. and Kaufman, A. J., eds. Neoproterozoic geology and paleobiology. Springer, Dordrecht.Google Scholar
Xiao, S., Yuan, X., Steiner, M., and Knoll, A. 2002. Macroscopic carbonaceous compressions in a terminal Proterozoic Shale: a systematic reassessment of the Miaohe biota, South China. Journal of Paleontology 76:347–376.Google Scholar
Zechman, F. W., Theriot, E. C., Zimmer, E. A., and Chapman, R. L. 1990. Phylogeny of the Ulvophyceae (Chlorophyta): cladistic analysis of nuclear-encoded rRNA sequence data. Journal of Phycology 26:700–710.Google Scholar