Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-28T16:54:38.487Z Has data issue: false hasContentIssue false

How green was Cooksonia? The importance of size in understanding the early evolution of physiology in the vascular plant lineage

Published online by Cambridge University Press:  08 April 2016

C. Kevin Boyce*
Affiliation:
Department of the Geophysical Sciences, University of Chicago, 5734 South Ellis Avenue, Chicago, Illinois 60637. E-mail: ckboyce@uchicago.edu

Abstract

Because of the fragmentary preservation of the earliest Cooksonia-like terrestrial plant macrofossils, younger Devonian fossils with complete anatomical preservation and documented gametophytes often have received greater attention concerning the early evolution of vascular plants and the alternation of generations. Despite preservational deficits, however, possible physiologies of Cooksonia-like fossils can be constrained by considering the overall axis size in conjunction with the potential range of cell types and sizes, because their lack of organ differentiation requires that all plant functions be performed by the same axis. Once desiccation resistance, support, and transport functions are taken into account, smaller fossils do not have volume enough left over for an extensive aerated photosynthetic tissue, thus arguing for physiological dependence on an unpreserved gametophyte. As in many mosses, axial anatomy is more likely to have ensured continued spore dispersal despite desiccation of the sporophyte than to have provided photosynthetic independence. Suppositions concerning size constraints on physiology are supported by size comparisons with fossils of demonstrable physiological independence, by preserved anatomical detail, and by size correlations between axis, sporangia, and sporangial stalk in Silurian and Early Devonian taxa. Several Cooksonia-like taxa lump fossils with axial widths spanning over an order of magnitude—from necessary physiological dependence to potential photosynthetic competence—informing understanding of the evolution of an independent sporophyte and the phylogenetic relationships of early vascular plants.

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

Armacost, R. R. 1944. The structure and function of the border parenchyma and vein-ribs of certain dicotyledon leaves. Proceedings of the Iowa Academy of Science 51:157169.Google Scholar
Banks, H. P. 1981. Time of appearance of some plant biocharacters during Siluro-Devonian time. Canadian Journal of Botany 59:12921296.Google Scholar
Bateman, R. M., Crane, P. R., DiMichele, W. A., Kenrick, P. R., Rowe, N. P., Speck, T., and Stein, W. E. 1998. Early evolution of land plants: phylogeny, physiology, and ecology of the primary terrestrial radiation. Annual Review of Ecology and Systematics 29:263292.Google Scholar
Bold, H. C. 1940. The nutrition of the sporophyte in mosses. American Journal of Botany 27:318322.Google Scholar
Bower, F. O. 1908. The origin of a land flora. Macmillan, London.Google Scholar
Boyce, C. K. 2005. The evolutionary history of roots and leaves. Pp. 479499 in Zwieniecki, M. A. and Holbrook, N. M., eds. Vascular transport in plants. Elsevier, Amsterdam.Google Scholar
Boyce, C. K., Cody, G. D., Fogel, M. L., Hazen, R. M., Alexander, C. M. O. D., and Knoll, A. H. 2003. Chemical evidence for cell wall lignification and the evolution of tracheids in Early Devonian plants. International Journal of Plant Science 164:691702.Google Scholar
Church, A. H. 1919. Thallasiophyta and the subaerial transmigration. Oxford University Press, Oxford.Google Scholar
Crandall-Stotler, B. 1980. Morphogenetic designs and a theory of bryophyte origins and divergence. BioScience 30:580585.Google Scholar
Crum, H. A. 2001. Structural diversity of bryophytes. University of Michigan Herbarium, Ann Arbor.Google Scholar
Edwards, D. 1970. Fertile Rhyniophytina from the Lower Devonian of Britain. Palaeontology 13:451461.Google Scholar
Edwards, D. 1973. Devonian floras. Pp. 105116 in Hallam, A., ed. Atlas of paleobiogeography. Elsevier, Amsterdam.Google Scholar
Edwards, D. 1979a. The early history of vascular plants based on Late Silurian and Early Devonian floras of the British Isles. In Harris, A. L., Holland, C. H., and Leake, Bernard E., eds. The Caledonides of the British Isles—reviewed. Geological Society of London Special Publication 8:405410.Google Scholar
Edwards, D. 1979b. A late Silurian flora from the Lower Old Red Sandstone of south-west Dyfed. Palaeontology 22:2352.Google Scholar
Edwards, D. 1993. Cells and tissues in the vegetative sporophytes of early land plants. New Phytologist 125:225247.Google Scholar
Edwards, D. 1996. New insights into early land ecosystems: a glimpse of a Lilliputian world. Review of Palaeobotany and Palynology 90:159174.Google Scholar
Edwards, D. 2000. The role of Mid-Paleozoic mesofossils in the detection of early bryophytes. Philosophical Transactions of the Royal Society of London B 355:733755.CrossRefGoogle Scholar
Edwards, D. 2003. Xylem in early tracheophytes. Plant, Cell and Environment 26:5772.Google Scholar
Edwards, D., and Axe, L. 2000. Novel conducting tissues in Lower Devonian plants. Botanical Journal of the Linnean Society 134:383399.Google Scholar
Edwards, D., and Fanning, U. 1985. Evolution and environment in the Late Silurian-Early Devonian: the rise of the pteridophytes. Philosophical Transactions of the Royal Society of London B 309:147165.Google Scholar
Edwards, D., and Feehan, J. 1980. Records of Cooksonia-type sporangia from late Wenlock strata in Ireland. Nature 287:4142.Google Scholar
Edwards, D., and Wellman, C. H. 2001. Embryophytes on land: the Ordovician to Lochkovian (Lower Devonian) Record. Pp. 328 in Gensel, and Edwards, 2001.Google Scholar
Edwards, D., Feehan, J., and Smith, D. G. 1983. A late Wenlock flora from Co. Tipperary, Ireland. Botanical Journal of the Linnean Society 86:1936.CrossRefGoogle Scholar
Edwards, D., Fanning, U., and Richardson, J. B. 1986. Stomata and stereome in early land plants. Nature 323:438440.Google Scholar
Edwards, D., Davies, K. L., and Axe, L. 1992. A vascular conducting strand in the early land plant Cooksonia . Nature 357:683685.Google Scholar
Edwards, D., Fanning, U., and Richardson, J. B. 1994. Lower Devonian coalified sporangia from Shropshire: Salopella Edwards & Richards and Tortilicaulis Edwards. Botanical Journal of the Linnean Society 116:89110.Google Scholar
Edwards, D., Abbott, G. D., and Raven, J. A. 1996. Cuticles of early land plants: a palaeoecophysiological evaluation. Pp. 131 in Kerstiens, G., ed. Plant cuticles. BIOS Scientific Publishers, Oxford.Google Scholar
Edwards, D., Ewbank, G., and Abbott, G. D. 1997. Flash pyrolysis of the outer cortical tissues in Lower Devonian Psilophyton dawsonii . Botanical Journal of the Linnean Society 124:345360.Google Scholar
Edwards, D., Kerp, H., and Hass, H. 1998. Stomata in early land plants: an anatomical and ecophysiological approach. Journal of Experimental Botany 49:255278.Google Scholar
Edwards, D., Morel, E. M., Paredes, F., Ganuza, D. G., and Zúñiga, A. 2001. Plant assemblages from the Silurian of southern Bolivia and their palaeogeographic significance. Botanical Journal of the Linnean Society 135:229250.Google Scholar
Edwards, D., Banks, H. P., Ciurca, S. J. Jr., and Laub, R. S. 2004. New Silurian Cooksonias from dolostones of north-eastern North America. Botanical Journal of the Linnean Society 146:399413.Google Scholar
Edwards, D., Li, C.-S., and Raven, J. A. 2006. Tracheids in an early vascular plant: a tale of two branches. Botanical Journal of the Linnean Society 150:115130.Google Scholar
Edwards, D. S. 1980. Evidence for the sporophytic status of the Lower Devonian plant Rhynia gwynne-vaughanii Kidston. Review of Palaeobotany and Palynology 29:177188.CrossRefGoogle Scholar
Edwards, D. S. 1986. Aglaophyton major, a non-vascular plant from the Devonian Rhynie Chert. Botanical Journal of the Linnean Society 93:173204.Google Scholar
Esau, K. 1953. Plant anatomy. Wiley, New York.Google Scholar
Fanning, U., Edwards, D., and Richardson, J. B. 1992. A diverse assemblage of early land plants from the Lower Devonian of the Welsh Borderland. Botanical Journal of the Linnean Society 109:161188.Google Scholar
Gensel, P. G. 1992. Phylogenetic relationships of the Zosterophylls and Lycopsids: evidence from morphology, paleoecology, and cladistic methods of inference. Annals of the Missouri Botanical Gardens 79:450473.Google Scholar
Gensel, P. G., and Edwards, D., eds. 2001. Plants invade the land: evolutionary and environmental perspectives. Columbia University Press, New York.CrossRefGoogle Scholar
Gensel, P. G., Kotyk, M. E., and Basinger, J. F. 2001. Morphology of above- and below-ground structures in Early Devonian (Pragian-Emsian) plants. Pp. 83102 in Gensel, and Edwards, 2001.Google Scholar
Gerrienne, P., Dilcher, D. L., Bergamaschi, S., Milagres, I., Pereira, E., and Rodrigues, M.-A. C. 2006. An exceptional specimen of the early land plant Cooksonia paranensis, and a hypothesis on the life cycle of the earliest eutracheophytes. Review of Palaeobotany and Palynology 142:123130.Google Scholar
Glasspool, I., Edwards, D., and Axe, L. 2006. Charcoal in the Early Devonian: a wildfire-derived Konservat-Lagerstätte. Review of Palaeobotany and Palynology 142:131136.Google Scholar
Habgood, K. S., Edwards, D., and Axe, L. 2002. New perspectives on Cooksonia from the Lower Devonian of the Welsh Borderland. Botanical Journal of the Linnean Society 139:339359.Google Scholar
Hébant, C. 1977. The conducting tissue of bryophytes. Cramer, Vaduz, Germany.Google Scholar
Hemsley, A. R. 1994. The origin of the land plant sporophyte: an interpolation scenario. Biological Review 69:263273.Google Scholar
Kenrick, P. 1994. Alternation of generation in land plants: new phylogenetic and palaeobotanical evidence. Biological Review 69:293330.CrossRefGoogle Scholar
Kenrick, P. 2000. The relationships of vascular plants. Philosophical Transactions of the Royal Society of London B 355:847855.Google Scholar
Kenrick, P. 2002. The origin of roots. Pp. 113 in Waisel, Y., Eshel, A., and Kafkafi, U., eds. Plant roots: the hidden half. Marcel Dekker, New York.Google Scholar
Kenrick, P., and Crane, P. R. 1991. Water-conducting cells in early fossil land plants: implications for the early evolution of tracheophytes. Botanical Gazette 152:335356.Google Scholar
Kenrick, P., and Crane, P. R. 1997. The origin and early diversification of land plants. Smithsonian Institution Press, Washington, D.C. Google Scholar
Kenrick, P., and Davis, P. 2004. Fossil plants. Smithsonian Books, Washington, D.C. Google Scholar
Kerp, H., Hass, H., and Mosbrugger, V. 2001. New data on Nothia aphylla Lyon 1964 ex El-Saadawy et Lacey 1979, a poorly known plant from the Lower Devonian Rhynie Chert. Pp. 5282 in Gensel, and Edwards, 2001.Google Scholar
Kerp, H., Trewin, N. H., and Hass, H. 2004. New gametophytes from the Early Devonian Rhynie Chert. Transactions of the Royal Society of Edinburgh (Earth Sciences) 94:411428.Google Scholar
Kidston, R., and Lang, W. H. 1917. On Old Red Sandstone plants showing structure, from the Rhynie Chert Bed, Aberdeenshire, Part I. Rhynia gwynne-vaughanii, Kidston and Lang. Transactions of the Royal Society of Edinburgh 51:761784.Google Scholar
Kidston, R., and Lang, W. H. 1920a. On Old Red Sandstone plants showing structure, from the Rhynie Chert Bed, Aberdeenshire, Part II. Additional note on Rhynia gwynne-vaughanii, Kidston and Lang; with descriptions of Rhynia major, n.sp., and Hornea lignieri n.g., n.sp. Transactions of the Royal Society of Edinburgh 52:603627.CrossRefGoogle Scholar
Kidston, R., and Lang, W. H. 1920b. On Old Red Sandstone plants showing structure, from the Rhynie Chert Bed, Aberdeenshire, Part III. Asteroxylon mackiei, Kidston and Lang. Transactions of the Royal Society of Edinburgh 52:643680.Google Scholar
Knoll, A. H., Niklas, K. J., Gensel, P. G., and Tiffney, B. H. 1984. Character diversification and patterns of evolution in early vascular plants. Paleobiology 10:3447.Google Scholar
Konrad, W., Roth-Nebelsick, A., Kerp, H., and Hass, H. 2000. Transpiration and assimilation of Early Devonian land plants with axially symmetric telomes—simulations on the tissue level. Journal of Theoretical Biology 206:91107.Google Scholar
Lupia, R. 1995. Paleobotanical data from fossil charcoal: an actualistic study of seed plant reproductive structures. Palaios 10:465477.Google Scholar
Lyon, A. G., and Edwards, D. 1991. The first zosterophyll from the Lower Devonian Rhynie Chert, Aberdeenshire. Transactions of the Royal Society of Edinburgh (Earth Sciences) 82:323332.Google Scholar
McElwain, J. C., and Chaloner, W. G. 1995. Stomatal density and index of fossil plants track atmospheric carbon dioxide in the Paleozoic. Annals of Botany 76:389395.Google Scholar
Mishler, B. D. 2001. The biology of bryophytes—bryophytes aren't just small tracheophytes. American Journal of Botany 88:21292131.Google Scholar
Mishler, B. D., and Churchill, S. P. 1984. A cladistic approach to the phylogeny of the “bryophytes.” Brittonia 36:406424.Google Scholar
Mishler, B. D., and Churchill, S. P. 1985. Transition to a land flora: phylogenetic relationships of the green algae and bryophytes. Cladistics 1:305328.Google Scholar
Niklas, K. J. 1976. The role of morphological biochemical reciprocity in early land plant evolution. Annals of Botany 40:12391254.Google Scholar
Niklas, K. J. 1985. The evolution of tracheid diameter in early vascular plants and its implications on the hydraulic conductance of the primary xylem strand. Evolution 39:11101122.Google Scholar
Niklas, K. J. 1997. The evolutionary biology of plants. University of Chicago Press, Chicago.Google Scholar
Niklas, K. J., Tiffney, B. H., and Knoll, A. H. 1980. Apparent changes in the diversity of fossil plants: a preliminary assessment. Evolutionary Biology 12:189.Google Scholar
Ogura, Y. 1972. Comparative anatomy of vegetative organs of the pteridophytes. Gebrüder Borntraeger, Berlin.Google Scholar
Paolillo, D. J. Jr., and Bazzaz, F. A. 1968. Photosynthesis in sporophytes of Polytrichum and Funaria . The Bryologist 71:335343.Google Scholar
Powell, C. L., Edwards, D., and Trewin, N. 2000. A new vascular plant from the Lower Devonian Windyfield chert, Rhynie, NE Scotland. Transactions of the Royal Society of Edinburgh (Earth Sciences) 90:331349.Google Scholar
Proctor, M. C. F. 1980. Evidence on the carbon nutrition of moss sporophytes from 14CO2 and the subsequent movement of labeled assimilate. Journal of Bryology 9:375386.Google Scholar
Raven, J. A. 1984. Physiological correlates of the morphology of early vascular plants. Botanical Journal of the Linnean Society 88:105126.CrossRefGoogle Scholar
Raven, J. A. 1993. The evolution of vascular plants in relation to quantitative functioning of dead water-conducting cells and stomata. Biological Review 68:337363.Google Scholar
Raven, J. A. 1996. Into the voids: the distribution, function, development and maintenance of gas spaces in plants. Annals of Botany 78:137142.Google Scholar
Raven, J. A. 1999. The minimum size of seeds and spores in relation to the ontogeny of homoiohydric plants. Functional Ecology 13:514.CrossRefGoogle Scholar
Raven, J. A. 2000. Land plant biochemistry. Philosophical Transactions of the Royal Society of London B 355:833846.CrossRefGoogle ScholarPubMed
Raven, J. A., and Edwards, D. 2001. Roots: evolutionary origins and biogeochemical significance. Journal of Experimental Botany 52:381401.CrossRefGoogle ScholarPubMed
Remy, W. 1982. Lower Devonian gametophytes: relation to the phylogeny of land plants. Science 215:16251627.Google Scholar
Remy, W., Remy, R., Hass, H., Schultka, S., and Franzmeyer, F. 1980. Sciadophyton Steinmann: ein gametophyt aus dem Siegen. Argumenta Palaeobotanica 8:119140.Google Scholar
Remy, W., Gensel, P. G., and Hass, H. 1993. The gametophyte generation of some Early Devonian land plants. International Journal of Plant Science 154:3558.Google Scholar
Renzaglia, K. S., Duff, R. J., Nickrent, D. L., and Garbary, D. J. 2000. Vegetative and reproductive innovations of early land plants: implications for a unified phylogeny. Philosophical Transactions of the Royal Society of London B 355:769793.Google Scholar
Roth-Nebelsick, A. 2001. Heat transfer of rhyniophytic plant axes. Review of Palaeobotany and Palynology 116:109122.CrossRefGoogle Scholar
Roth-Nebelsick, A., and Konrad, W. 2003. Assimilation and transpiration capabilities of rhyniophytic plants from the Lower Devonian and their implications for paleoatmospheric CO2 concentration. Palaeogeography, Palaeoclimatology, Palaeoecology 202:153178.Google Scholar
Rothwell, G. W. 1995. The fossil history of branching: implications for the phylogeny of land plants. Pp. 7186 in Hoch, P. C. and Stephenson, A. G., eds. Experimental and molecular approaches to plant biosystematics. Missouri Botanical Garden, St. Louis.Google Scholar
Shute, C. H., and Edwards, D. 1989. A new rhyniopsid with novel sporangium organization from the Lower Devonian of South Wales. Botanical Journal of the Linnean Society 100:111137.Google Scholar
Tafforeau, P., Boistel, R., Boiler, E., Bravin, A., Brunet, M., Chaimanee, Y., Cloetens, P., Feist, M., Hoszowska, J., Jaeger, J.-J., Kay, R. F., Lazzari, V., Marivaux, L., Nel, A., Nemoz, C., Thibault, X., Vignaud, P., Zabler, S. 2006. Applications of X-ray synchrotron microtomography for non-destructive 3D studies of paleontological specimens. Applied Physics A 83:195202.Google Scholar
Taylor, T. N. 1988. The origin of land plants: some answers, more questions. Taxon 37:805833.Google Scholar
Taylor, T. N., Remy, W., Hass, H., Kerp, H. 1995. Fossil arbuscular mycorrhizae from the Early Devonian. Mycologia 87:560573.Google Scholar
Taylor, T. N., Klavins, S. D., Krings, M., Taylor, E. L., Kerp, H., and Hass, H. 2004. Fungi from the Rhynie Chert: a view from the dark side. Transaction of the Royal Society of Edinburgh (Earth Sciences) 94:457473.Google Scholar
Taylor, T. N., Kerp, H., and Hass, H. 2005. Life history biology of early land plants: deciphering the gametophyte phase. Proceedings of the National Academy of Sciences USA 102:58925897.Google Scholar
Tomescu, A. M. F., and Rothwell, G. W. 2006. Wetlands before tracheophytes: thalloid terrestrial communities of the Early Silurian Passage Creek biota (Virginia). In Greb, S. F. and DiMichele, W. A., eds. Wetlands through time. Geological Society of America Special Paper 399:4156.Google Scholar
Zwieniecki, M. A., Boyce, C. K., and Holbrook, N. M. 2004. Functional design space of single veined leaves: role of tissue hydraulic properties in constraining leaf size and shape. Annals of Botany 94:507513.Google Scholar
Zwieniecki, M. A., Stone, H. A., Leigh, A., Boyce, C. K., and Holbrook, N. M. 2006. Hydraulic design of pine needles: one-dimensional optimization for single-vein leaves. Plant, Cell and Environment 29:803809.Google Scholar
Supplementary material: File

Boyce supplementary material

Appendices

Download Boyce supplementary material(File)
File 508.4 KB