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Modeling fluid flow in Medullosa, an anatomically unusual Carboniferous seed plant

Published online by Cambridge University Press:  08 April 2016

Jonathan P. Wilson ,
Andrew H. Knoll ,
N. Michele Holbrook  and
Charles R. Marshall
Jonathan P. Wilson
Affiliation:
Department of Earth and Planetary Sciences, Harvard University Cambridge, Massachusetts 02138. E-mail: [email protected]
Andrew H. Knoll
Affiliation:
Department of Organismic and Evolutionary Biology, Harvard University Cambridge, Massachusetts 02138
N. Michele Holbrook
Affiliation:
Department of Organismic and Evolutionary Biology, Harvard University Cambridge, Massachusetts 02138
Charles R. Marshall
Affiliation:
Department of Organismic and Evolutionary Biology, Harvard University Cambridge, Massachusetts 02138
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Abstract

Medullosa stands apart from most Paleozoic seed plants in its combination of large leaf area, complex vascular structure, and extremely large water-conducting cells. To investigate the hydraulic consequences of these anatomical features and to compare them with other seed plants, we have adapted a model of water transport in xylem cells that accounts for resistance to flow from the lumen, pits, and pit membranes, and that can be used to compare extinct and extant plants in a quantitative way. Application of this model to Medullosa, the Paleozoic coniferophyte Cordaites, and the extant conifer Pinus shows that medullosan tracheids had the capacity to transport water at volume flow rates more comparable to those of angiosperm vessels than to those characteristic of ancient and modern coniferophyte tracheids. Tracheid structure in Medullosa, including the large pit membrane area per tracheid and the high ratio of tracheid diameter to wall thickness, suggests that its xylem cells operated at significant risk of embolism and implosion, making this plant unlikely to survive significant water stress These features further suggest that tracheids could not have furnished significant structural support, requiring either that other tissues supported these plants or that at least some medullosans were vines. In combination with high tracheid conductivity, distinctive anatomical characters of Medullosa such as the anomalous growth of vascular cambium and the large number of leaf traces that enter each petiole base suggest vascular adaptations to meet the evapotranspiration demands of its large leaves. The evolution of highly efficient conducting cells dictates a need to supply structural support via other tissues, both in tracheid-based stem seed plants and in vessel-bearing angiosperms.

Type
Articles
Information
Paleobiology , Volume 34 , Issue 4 , Fall 2008 , pp. 472 - 493
Copyright
Copyright © The Paleontological Society 

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References

Literature Cited

Andrews, H. N. Jr. 1940. On the stelar anatomy of the pteridosperms with particular reference to the secondary wood. Annals of the Missouri Botanical Garden 27:51–118.Google Scholar
Andrews, H. N., and Mamay, S. H. 1953. Some American medullosas. Annals of the Missouri Botanical Garden 40:183–209.CrossRefGoogle Scholar
Arens, N. C. 1997. Responses of leaf anatomy to light environment in the tree fern Cyathea caracasana (Cyatheaceae) and its application to some ancient seed ferns. Palaios 12:84–94.Google Scholar
Axelrod, D. I. 1986. Cenozoic history of some western American pines. Annals of the Missouri Botanical Garden 73:565–641.Google Scholar
Bailey, I. W. 1953. Evolution of the tracheary tissue of land plants. American Journal of Botany 40:4–8.Google Scholar
Bannan, M. W. 1965. Length tangential diameter and length/width ratio of conifer tracheids. Canadian Journal of Botany 43:967–984 Google Scholar
Basinger, J. F., Rothwell, G. W., and Stewart, W. N. 1974. Cauline vasculature and leaf trace production in medullosan pteridosperms. American Journal of Botany 61:1002–1015.CrossRefGoogle Scholar
Batham, E. 1943. Vascular anatomy of New Zealand species of Gunnera . Transactions of the Royal Society of New Zealand 73:7.Google Scholar
Bauch, J., Schultze, R., and Liese, W. 1972. Morphological variability of bordered pit membranes in gymnosperms. Wood Science and Technology 6:165–184.Google Scholar
Becker, P. 2000. Competition in the regeneration niche between conifers and angiosperms: Bond's slow seedling hypothesis. Functional Ecology 14:401–412.CrossRefGoogle Scholar
Beeler, H. E. 1983. Anatomy and frond architecture of Neuropteris ovata and Neuropteris scheuchzeri from the Upper Pennsylvanian of the Appalachian Basin. Canadian Journal of Botany-Revue Canadienne de Botanique 61:2352–2368.Google Scholar
Boyce, C. K., Zwieniecki, M. A., Cody, G. D., Jacobsen, C., Wirick, S., Knoll, A. H., and Holbrook, N. M. 2004. Evolution of xylem lignification and hydrogel transport regulation. Proceedings of the National Academy of Sciences USA 101:17555–17558.Google Scholar
Brodribb, T. J., and Holbrook, N. M. 2003. Stomatal closure during leaf dehydration, correlation with other leaf physiological traits. Plant Physiology 132:2166–2173.Google Scholar
Brodribb, T. J., and Holbrook, N. M. 2004. Stomatal protection against hydraulic failure: a comparison of coexisting ferns and angiosperms. New Phytologist 162:663–670.Google Scholar
Brodribb, T. J., Holbrook, N. M., Edwards, E. J., and Gutierrez, M. V. 2003. Relations between stomatal closure, leaf turgor and xylem vulnerability in eight tropical dry forest trees. Plant, Cell and Environment 26:443–450.Google Scholar
Brodribb, T. J., Holbrook, N. M., and Hill, R. S. 2005. Seedling growth in conifers and angiosperms: impacts of contrasting xylem structure. Australian Journal of Botany 53:749–755.CrossRefGoogle Scholar
Brongniart, A. 1849. Tableau des genres des végétaux fossiles. Dictionnaire universel d'Histoire Naturelle 13:1–127.Google Scholar
Buckley, T. N., Mott, K. A., and Farquhar, G. D. 2003. A hydromechanical and biochemical model of stomatal conductance. Plant, Cell and Environment 26:1767–1785.Google Scholar
Carlquist, S. 2001. Comparative wood anatomy. Springer, Berlin.Google Scholar
Choat, B., Ball, M., Luly, J., and Holtum, J. 2003. Pit membrane porosity and water stress-induced cavitation in four co-existing dry rainforest tree species. Plant Physiology 131:41–48.CrossRefGoogle ScholarPubMed
Choat, B., Brodie, T. W., Cobb, A. R., Zwieniecki, M. A., and Holbrook, N. M. 2006. Direct measurements of intervessel pit membrane hydraulic resistance in two angiosperm tree species. American Journal of Botany 93:993–1000.Google Scholar
Choat, B., Jansen, S., Zwieniecki, M. A., Smets, E., and Holbrook, N. M. 2004. Changes in pit membrane porosity due to deflection and stretching: the role of vestured pits. Journal of Experimental Botany 55:1569–1575.Google Scholar
Cichan, M. A. 1986a. Conductance in the wood of selected Carboniferous plants. Paleobiology 12:302–310.Google Scholar
Cichan, M. A. 1986b. Vascular cambium and wood development in Carboniferous plants. 4. Seed plants. Botanical Gazette 147:227–235.Google Scholar
Cleal, C. J., James, R. M., and Zodrow, E. L. 1999. Variation in stomatal density in the Late Carboniferous gymnosperm frond Neuropteris ovata . Palaios 14:180–185.Google Scholar
Comstock, J. P., and Sperry, J. S. 2000. Theoretical considerations of optimal conduit length for water transport in vascular plants. New Phytologist 148:195–218.Google Scholar
Cotta, B. 1832. Die Dendrolithen in Beziehung auf ihren inneren Bau. Arnold Buch, Dresden and Leipzig.Google Scholar
Crane, P. R. 1985. Phylogenetic analysis of seed plants and the origin of angiosperms. Annals of the Missouri Botanical Garden 72:716–793.Google Scholar
Crane, P. R., Herendeen, P., and Friis, E. M. 2004. Fossils and plant phylogeny. American Journal of Botany 91:1683–1699.Google Scholar
Delevoryas, T. 1955. The Medullosae: structure and relationships. Palaeontographica, Abteilung B 97(3–6):114–167.Google Scholar
DiMichele, W. A., Pfefferkorn, H. W., and Gastaldo, R. A. 2001. Response of Late Carboniferous and Early Permian plant communities to climate change. Annual Review of Earth and Planetary Sciences 29:461–487.Google Scholar
DiMichele, W. A., Phillips, T. L., and Pfefferkorn, H. W. 2006. Paleoecology of Late Paleozoic pteridosperms from tropical Euramerica. Journal of the Torrey Botanical Society 133:83–118.Google Scholar
Dunn, M. T., Krings, M., Mapes, G., Rothwell, G. W., Mapes, R. H., and Keqin, S. 2003. Medullosa steinii sp. nov., a seed fern vine from the Upper Mississippian. Review of Palaeobotany and Palynology 124(3–4):307–324.Google Scholar
Esau, K. 1977. Anatomy of seed plants. Wiley, New York.Google Scholar
Falcon-Lang, H. J., and Scott, A. C. 2000. Upland ecology of some Late Carboniferous cordaitalean trees from Nova Scotia and England. Palaeogeography, Palaeoclimatology, Palaeoecology 156(3–4):225–242.Google Scholar
Florin, R. 1950. Upper Carboniferous and Lower Permian conifers. Botanical Review 16:258–282.Google Scholar
Florin, R. 1951. Evolution in cordaites and conifers. Acta Horti Bergiani 15:285–388.Google Scholar
Galtier, J. 1997. Coal-ball floras of the Namurian-Westphalian of Europe. Review of Palaeobotany and Palynology 95(1–4):51–72.Google Scholar
Galtier, J., Phillips, T. L., and Chalotprat, F. 1986. Euramerican coal-swamp plants in Midcarboniferous of Morocco. Review of Palaeobotany and Palynology 49(1–2):93–98.CrossRefGoogle Scholar
Greguss, P., and Balkay, B. 1972. Xylotomy of the living conifers. Akademiai Kiado, Budapest.Google Scholar
Hacke, U. G., and Sperry, J. S. 2001. Functional and ecological xylem anatomy. Perspectives in Plant Ecology Evolution and Systematics 4:97–115.CrossRefGoogle Scholar
Hacke, U. G., Sperry, J. S., and Pittermann, J. 2004. Analysis of circular bordered pit function. II. Gymnosperm tracheids with torus-margo pit membranes. American Journal of Botany 91:386–400.Google Scholar
Hacke, U. G., Sperry, J. S., Pockman, W. T., Davis, S. D., and McCulloch, K. A. 2001. Trends in wood density and structure are linked to prevention of xylem implosion by negative pressure. Oecologia 126:457–461.CrossRefGoogle ScholarPubMed
Hacke, U. G., Sperry, J. S., Feild, T. S., Sano, Y., Sikkema, E. H., and Pittermann, J. 2007. Water transport in vesselless angiosperms: conducting efficiency and cavitation safety. International Journal of Plant Sciences 168:1113–1126.Google Scholar
Hamer, J. J., and Rothwell, G. W. 1988. The vegetative structure of Medullosa endocentrica (Pteridospermopsida). Canadian Journal of Botany-Revue Canadienne de Botanique 66:375–387.Google Scholar
Holbrook, N. M., Ahrens, E. T., Burns, M. J., and Zwieniecki, M. A. 2001. In vivo observation of cavitation and embolism repair using magnetic resonance imaging. Plant Physiology 126:27–31.Google Scholar
Judd, W. S., Campbell, C. S., Kellogg, E. A., Stevens, P. F., and Donoghue, M. J. 2007. Plant systematics: a phylogenetic approach. Sinauer, Sunderland, Mass. Google Scholar
Kramer, P., and Boyer, J. 1995. Water relations of plants and soils. Academic Press, San Diego.Google Scholar
Krings, M., and Kerp, H. 2000. A contribution to the knowledge of the pteridosperm genera Pseudomariopteris Danze-Corsin nov. emend., and Helenopteris nov. gen. Review of Palaeobotany and Palynology 111(3–4):145–195.Google Scholar
Krings, M., Kerp, H., Taylor, T. N., and Taylor, E. L. 2003. How Paleozoic vines and lianas got off the ground: on scrambling and climbing Carboniferous-early Permian pteridosperms. Botanical Review 69:204–224.Google Scholar
Lancashire, J. R., and Ennos, A. R. 2002. Modelling the hydrodynamic resistance of bordered pits. Journal of Experimental Botany 53(373):1485–1493.Google Scholar
Li, H., and Taylor, D. W. 1998. Aculeovinea yunguiensis gen. et sp. nov. (Gigantopteridales), a new taxon of gigantopterid stem from the Upper Permian of Guizhou Province, China. International Journal of Plant Sciences 159:1023–1033.Google Scholar
Loepfe, L., Martinez-Vilalta, J., Piñol, J., and Mencuccini, M. 2007. The relevance of xylem network structure for plant hydraulic efficiency and safety. Journal of Theoretical Biology 247:788–803.CrossRefGoogle ScholarPubMed
Mapes, G., and Rothwell, G. W. 1980. Quaestora amplecta gen. et sp. n., a structurally simple medullosan stem from the Upper Mississippian of Arkansas. American Journal of Botany 67:636–647.CrossRefGoogle Scholar
Masselter, T., Speck, T., and Rowe, N. P. 2006. Ontogenetic reconstruction of the carboniferous seed plant Lyginopteris oldhamia . International Journal of Plant Sciences 167:147–166.CrossRefGoogle Scholar
Mickle, J. E., and Rothwell, G. W. 1982. Permineralized Alethopteris from the Upper Pennsylvanian of Ohio and Illinois. Journal of Paleontology 56:392–402.Google Scholar
Millar, C. I. 1993. Impact of the Eocene on the evolution of Pinus L. Annals of the Missouri Botanical Garden 80:471–498.CrossRefGoogle Scholar
Mosbrugger, V. 1990. The tree habit in land plants: a functional comparison of trunk constructions with a brief introduction into the biomechanics of trees. Springer, Berlin.Google Scholar
Norstog, K. J., and Nichols, T. J. 1997. The biology of the cycads. Cornell University Press, Ithaca, N.Y. Google Scholar
Pesacreta, T. C., Groom, L. H., and Rials, T. G. 2005. Atomic force microscopy of the intervessel pit membrane in the stem of Sapium sebiferum (Euphorbiaceae). IAWA Journal 26:397–426.Google Scholar
Pfefferkorn, H., Gillespie, W. H., Resnick, D. A., and Scheihing, M. H. 1984. Reconstruction and architecture of medullosan pteridosperms (Pennsylvanian): Mosasaur 2:1–8.Google Scholar
Phillips, T. L. 1981. Stratigraphic occurrences and vegetational patterns of Pennsylvanian pteridosperms in Euramerican coal swamps. Review of Palaeobotany and Palynology 32:5–26.Google Scholar
Phillips, T. L., Peppers, R. A., Avcin, M. J., and Laughnan, P. F. 1974. Fossil plants and coal: patterns of change in Pennsylvanian coal swamps of the Illinois Basin. Science 184:1367–1369.Google Scholar
Pittermann, J., and Sperry, J. S. 2006. Analysis of freeze-thaw embolism in conifers: the interaction between cavitation pressure and tracheid size. Plant Physiology 140:374–382.Google Scholar
Pittermann, J., Sperry, J. S., Hacke, U. G., Wheeler, J. K., and Sikkema, E. H. 2005. Torus-margo pits help conifers compete with angiosperms. Science 310:1924.Google Scholar
Wheeler, J. K., and Sikkema, E. H. 2006. Inter-tracheid pitting and the hydraulic efficiency of conifer wood: the role of tracheid allometry and cavitation protection. American Journal of Botany 93:1265–1273.Google Scholar
Pockman, W. T., Sperry, J. S., and O'Leary, J. W. 1995. Sustained and significant negative water-pressure in xylem. Nature 378:715–716.Google Scholar
Pryor, J. S. 1987. Delimiting species among permineralized medullosan fronds: an Upper Pennsylvanian Alethopteris myeloxylon . American Journal of Botany 74:687.Google Scholar
Pryor, J. S. 1990. Delimiting species among permineralized medullosan pteridosperms: a plant bearing Alethopteris fronds from the Upper Pennsylvanian of the Appalachian Basin. Canadian Journal of Botany-Revue Canadienne de Botanique 68:184–192.Google Scholar
Raven, P. H., Evert, R. F., and Eichhorn, S. E. 1999. Biology of plants, 6th ed. W. H. Freeman, N.Y. Google 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(1–2):153–178.Google Scholar
Roth-Nebelsick, A., Grimm, G., Mosbrugger, V., Hass, H., and Kerp, H. 2000. Morphometric analysis of Rhynia and Asteroxylon: testing functional aspects of early land plant evolution. Paleobiology 26:405–418.Google Scholar
Rowe, N. P., and Speck, T. 2004. Hydraulics and mechanics of plants: novelty, innovation, and evolution. Pp. 297–326 in Helmsley, A. R. and Poole, I., eds. The evolution of plant physiology. Elsevier, London.Google Scholar
Rowe, N. P., Speck, T., and Galtier, J. 1993. Biomechanical analysis of a Paleozoic gymnosperm stem. Proceedings of the Royal Society of London B 252:19–28.Google Scholar
Schopf, J. M. 1939. Medullosa distelica, a new species of the Anglica group of Medullosa . American Journal of Botany 26:196–207.CrossRefGoogle Scholar
Scott, D. H. 1899. On the structure and affinities of fossil plants from the Palaeozoic rocks. III. On Medullosa anglica, a new representative of the Cycadofilices. Philosophical Transactions of the Royal Society of London, Series B, Containing Papers of a Biological Character 191:81–126.Google Scholar
Smith, F. A., and Freeman, K. H. 2006. Influence of physiology and climate on delta D of leaf wax n-alkanes from C-3 and C-4 grasses. Geochimica et Cosmochimica Acta 70:1172–1187.CrossRefGoogle Scholar
Solms-Laubach, H. 1891. Fossil botany. Oxford University Press, London.Google Scholar
Sperry, J. S. 2003. Evolution of water transport and xylem structure. International Journal of Plant Sciences 164:S115–S127.CrossRefGoogle Scholar
Sperry, J. S., and Hacke, U. G. 2004. Analysis of circular bordered pit function. I. Angiosperm vessels with homogenous pit membranes. American Journal of Botany 91:369–385.Google Scholar
Sperry, J. S., and Tyree, M. T. 1990. Water-stress-induced xylem embolism in 3 species of conifers. Plant, Cell and Environment 13:427–436.Google Scholar
Sperry, J. S., Hacke, U. G., and Pittermann, J. 2006. Size and function in conifer tracheids and angiosperm vessels. American Journal of Botany 93:1490–1500.Google Scholar
Sperry, J. S., Hacke, U. G., and Wheeler, J. K. 2005. Comparative analysis of end wall resistivity in xylem conduits. Plant, Cell and Environment 28:456–465.Google Scholar
Stewart, W., and Delevoryas, T. 1952. Bases for determining relationships among the Medullosaceae. American Journal of Botany 39:505–516.Google Scholar
Stewart, W., and Rothwell, G. W. 1993. Paleobotany and the evolution of plants. Cambridge University Press, Cambridge.Google Scholar
Stidd, B. M. 1981. The current status of medullosan seed ferns. Review of Palaeobotany and Palynology 32:63–101.Google Scholar
Taiz, L., and Zeiger, E. 2002. Plant physiology. Sinauer, Sunderland, Mass. Google Scholar
Taylor, T. N., and Taylor, E. L. 1993. The biology and evolution of fossil plants. Prentice Hall, Upper Saddle River, N.J. Google Scholar
Thompson, M. V., and Holbrook, N. M. 2003. Scaling phloem transport: water potential equilibrium and osmoregulatory flow. Plant, Cell and Environment 26:1561–1577.Google Scholar
Tomlinson, P. B. 1990. The structural biology of palms. Clarendon, Oxford.Google Scholar
Tyree, M. T., and Ewers, F. W. 1991. The hydraulic architecture of trees and other woody plants (Tansley Review No. 34). New Phytologist 119:345–360.Google Scholar
Tyree, M. T., and Sperry, J. S. 1989. Vulnerability of xylem to cavitation and embolism. Annual Review of Plant Physiology and Plant Molecular Biology 40:19–38.Google Scholar
van den Honert, T. H. 1948. Water transport in plants as a catenary process. Discussions of the Faraday Society 3:146–153.Google Scholar
Veres, J. S. 1990. Xylem Anatomy and hydraulic conductance of Costa Rican Blechnum ferns. American Journal of Botany 77:1610–1625.Google Scholar
Vogel, S. 1994. Life in moving fluids. Princeton University Press, Princeton, N.J. Google Scholar
Wheeler, J. K., Sperry, J. S., Hacke, U. G., and Hoang, N. 2005. Inter-vessel pitting and cavitation in woody Rosaceae and other vesselled plants: a basis for a safety versus efficiency trade-off in xylem transport. Plant, Cell and Environment 28:800–812.Google Scholar
Wnuk, C., and Pfefferkorn, H. W. 1984. The life habits and paleoecology of Middle Pennsylvanian medullosan pteridosperms based on an in situ assemblage from the Bernice Basin (Sullivan County, Pennsylvania, USA). Review of Palaeobotany and Palynology 41(3–4):329–351.Google Scholar
Woodward, A. W., and Bartel, B. 2005. Auxin: regulation, action, and interaction. Annals of Botany 95:707–735.Google Scholar
Zimmermann, M. H. 1983. Xylem structure and the ascent of sap. Springer, Berlin.Google Scholar
Zwieniecki, M. A., Melcher, P. J., and Holbrook, N. M. 2001. Hydrogel control of xylem hydraulic resistance in plants. Science 291:1059–1062.Google Scholar