Hostname: page-component-78c5997874-94fs2 Total loading time: 0 Render date: 2024-11-19T09:37:42.123Z Has data issue: false hasContentIssue false

A physiologically explicit morphospace for tracheid-based water transport in modern and extinct seed plants

Published online by Cambridge University Press:  08 April 2016

Jonathan P. Wilson
Affiliation:
Department of Earth and Planetary Sciences, Harvard University, Cambridge, Massachusetts 02138
Andrew H. Knoll
Affiliation:
Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts 02138

Abstract

We present a morphometric analysis of water transport cells within a physiologically explicit three-dimensional space. Previous work has shown that cell length, diameter, and pit resistance govern the hydraulic resistance of individual conducting cells; thus, we use these three parameters as axes for our morphospace. We compare living and extinct plants within this space to investigate how patterns of plant conductivity have changed over evolutionary time. Extinct coniferophytes fall within the range of living conifers, despite differences in tracheid-level anatomy. Living cycads, Ginkgo biloba, the Miocene fossil Ginkgo beckii, and extinct cycadeoids overlap with both conifers and vesselless angiosperms. Three Paleozoic seed plants, however, occur in a portion of the morphospace that no living seed plant occupies. Lyginopteris, Callistophyton, and, especially, Medullosa evolved tracheids with high conductivities similar to those of some vessel-bearing angiosperms. Such fossils indicate that extinct seed plants evolved a structural and functional diversity of xylem architectures broader, in some ways, than the range observable in living seed 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

Anderson, J. M., Anderson, H. M., and Cruickshank, A. R. I. 1998. Late Triassic ecosystems of the Molteno Lower Elliot biome of southern Africa. Palaeontology 41:387421.Google Scholar
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 27:51118.CrossRefGoogle Scholar
Bailey, I. W., and Thompson, W. P. 1918. Additional notes upon the angiosperms Tetracentron, Trochodendron, and Drimys, in which vessels are absent from the Wood. Annals of Botany (old series) 32:503512.Google Scholar
Bailey, I. W., and Tupper, W. W. 1918. Size variation in tracheary cells. I. A comparison between the secondary xylems of vascular cryptogams, gymnosperms, and angiosperms. Proceedings of the American Academy of Arts and Sciences 54:149204.Google Scholar
Ball, M. C., Wolfe, J., Canny, M., Hofmann, M., Nicotra, A. B., and Hughes, D. 2002. Space and time dependence of temperature and freezing in evergreen leaves. Functional Plant Biology 29:12591272.Google Scholar
Ball, M. C., Canny, M. J., Huang, C. X., Egerton, J. J. G., and Wolfe, J. 2006. Freeze/thaw-induced embolism depends on nadir temperature: the heterogeneous hydration hypothesis. Plant, Cell and Environment 29:729745.CrossRefGoogle ScholarPubMed
Barman, M. W. 1965. Length tangential diameter and length/width ratio of conifer tracheids. Canadian Journal of Botany 43:967984.Google Scholar
Bateman, R. M., Hilton, J., and Rudall, P. J. 2006. Morphological and molecular phylogenetic context of the angiosperms: contrasting the ‘top-down’ and ‘bottom-up’ approaches used to infer the likely characteristics of the first flowers. Journal of Experimental Botany 57:34713503.Google Scholar
Batham, E. 1943. Vascular anatomy of New Zealand species of Gunnera . Transactions of the Royal Society of New Zealand 73:7.Google Scholar
Beck, A. L., and Labandeira, C. C. 1998. Early Permian insect folivory on a gigantopterid-dominated riparian flora from north-central Texas. Palaeogeography, Palaeoclimatology, Palaeoecology 142:139173.Google Scholar
Beck, C. B. 1960. Connection between Archaeopteris and Callixylon . Science 131:15241525.CrossRefGoogle ScholarPubMed
Beck, C. B. 1962. Reconstructions of Archaeopteris, and further consideration of its phylogenetic position. American Journal of Botany 49:373382.Google Scholar
Beck, C. B. 1970. The appearance of gymnospermous structure. Biological Reviews 45:379399.Google Scholar
Beck, C. B., and Wight, D. C. 1988. Progymnosperms. Pp. 185 in Beck, C., ed. Origin and evolution of gymnosperms. Columbia University Press, New York.Google Scholar
Beck, C., Schmid, R., and Rothwell, G. 1982. Stelar morphology and the primary vascular system of seed plants. Botanical Review 48:691815.CrossRefGoogle Scholar
Bond, W. J. 1989. The tortoise and the hare: ecology of angiosperm dominance and gymnosperm persistence. Biological Journal of the Linnean Society 36:227249.Google Scholar
Boyce, C. K., and Knoll, A. H. 2002. Evolution of developmental potential and the multiple independent origins of leaves in Paleozoic vascular plants. Paleobiology 28:70100.Google Scholar
Buckley, T. N. 2005. The control of stomata by water balance. New Phytologist 168:275291.CrossRefGoogle ScholarPubMed
Burleigh, J. G., and Mathews, S. 2004. Phylogenetic signal in nucleotide data from seed plants: implications for resolving the seed plant tree of life. American Journal of Botany 91:15991613.Google Scholar
Carlquist, S. 1996. Wood, bark and stem anatomy of Gnetales: a summary. International Journal of Plant Sciences 157:S58.Google Scholar
Carlquist, S. 1988. Wood anatomy of Drimys s.s. (Winteraceae) Aliso 12:8195.CrossRefGoogle 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 131:4148.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 55:15691575.Google Scholar
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 93:9931000.Google Scholar
Choat, B., Cobb, A. R., and Jansen, S. 2008. Structure and function of bordered pits: new discoveries and impacts on whole-plant hydraulic function. New Phytologist 177:608626.CrossRefGoogle ScholarPubMed
Chrysler, M. A. 1926. Vascular tissues of Microcycas calocoma . Botanical Gazette 82:233252.CrossRefGoogle Scholar
Cichan, M. A. 1985. Vascular cambium and wood development in Carboniferous plants. 2. Sphenophyllum-Plurifoliatum Williamson and Scott (Sphenophyllales). Botanical Gazette 146:395403.CrossRefGoogle Scholar
Cichan, M. A. 1986. Vascular cambium and wood development in Carboniferous plants. 4. Seed plants. Botanical Gazette 147:227235.Google Scholar
Cichan, M. A., and Taylor, T. N. 1984. A method for determining tracheid lengths in petrified wood by analysis of cross-sections. Annals of Botany 53:219226.Google Scholar
Comstock, J. P., and Sperry, J. S. 2000. Theoretical considerations of optimal conduit length for water transport in vascular plants. New Phytologist 148:195218.Google Scholar
Crane, P. R. 1985. Phylogenetic analysis of seed plants and the origin of angiosperms. Annals of the Missouri Botanical Garden 72:716793.Google Scholar
Davis, S. D., Sperry, J. S., and Hacke, U. G. 1999. The relationship between xylem conduit diameter and cavitation caused by freezing. American Journal of Botany 86:13671372.Google Scholar
Delevoryas, T. 1955. The Medullosae: structure and relationships. Palaeontographica, Abteilung B 97:114167.Google Scholar
DiMichele, W. A. 1979. Arborescent lycopods of Pennsylvanian age coals. Palaeontographica, Abteilung B 171:5777.Google Scholar
DiMichele, W. A., and DeMaris, P. J. 1987. Structure and dynamics of a Pennsylvanian-age Lepidodendron forest; colonizers of a disturbed swamp habitat in the Herrin (No. 6) Coal of Illinois. Palaios 2:146157.CrossRefGoogle Scholar
DiMichele, W. A., and Gastaldo, R. A. 2008. Plant paleoecology in deep time. Annals of the Missouri Botanical Garden 95:144198.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 133:83118.Google Scholar
Dixon, H. H. 1909. Transpiration and the ascent of sap. Progressus Rei Botanicae 3:166.Google Scholar
Dixon, H. H. 1914. Transpiration and the ascent of sap in plants. Macmillan, London.Google Scholar
Doyle, J. A. 2006. Seed ferns and the origin of angiosperms. Journal of the Torrey Botanical Society 133:169209.Google Scholar
Doyle, J. A. 2008. Integrating molecular phylogenetic and paleobotanical evidence on origin of the flower. International Journal of Plant Sciences 169:816843.Google Scholar
Edwards, D. 2003. Xylem in early tracheophytes. Plant, Cell and Environment 26:5772.Google Scholar
Ellerby, D., and Ennos, A. 1998. Resistances to fluid flow of model xylem vessels with simple and scalariform perforation plates. Journal of Experimental Botany 49:979985.CrossRefGoogle Scholar
Erasmus, T. 1976. On the anatomy of Dadoxylon arberi Seward with some remarks on the phylogenetical tendencies of its tracheid pits. Palaeontologia Africana 19:127133.Google Scholar
Esau, K. 1977. Anatomy of seed plants. Wiley, New York.Google Scholar
Feild, T. S., and Balun, L. 2008. Xylem hydraulic and photo-synthetic function of Gnetum (Gnetales) species from Papua New Guinea. New Phytologist 177:665675.CrossRefGoogle Scholar
Feild, T. S., Zwieniecki, M. A., and Holbrook, N. M. 2000. Winteraceae evolution: an ecophysiological perspective. Annals of the Missouri Botanical Garden 87:323334.Google Scholar
Feild, T. S., Brodribb, T., and Holbrook, M. 2002. Hardly a relict: freezing and the evolution of vesselless wood in Winteraceae. Evolution 56:464478.Google Scholar
Feng, Z., Wang, J., and Shen, G.-L. 2008. Zalesskioxylon xiaheyanense sp. nov., a gymnospermous wood of the Stephanian (Late Pennsylvanian) from Ningxia, northwestern China. Journal of Asian Earth Sciences 33:219228.Google Scholar
Florin, R. 1949. The morphology of Trichopitys heteromorpha Saporta, a seed plant of Paleozoic age, and the evolution of the female flowers in the Ginkgoinae. Acta Horti Bergiani 15:79109.Google Scholar
Florin, R. 1950. Upper Carboniferous and Lower Permian conifers. Botanical Review 16:258282.Google Scholar
Florin, R. 1951. Evolution in Cordaites and conifers. Acta Horti Bergiani 15:285388.Google Scholar
Galtier, J. 1988. Morphology and phylogenetic relationships of early pteridosperms. Pp. 135177 in Beck, C., ed. Origin and evolution of gymnosperms. Columbia University Press, New York.Google Scholar
Galtier, J., and Meyer-Berthaud, B. 2006. The diversification of early arborescent seed ferns. Journal of the Torrey Botanical Society 133:719.Google Scholar
Glasspool, I., Hilton, J., Collinson, M. E., and Shi-Jun, W. 2004a. Defining the gigantopterid concept: a reinvestigation of Gigantopteris (Megalopteris) nicotianaefolia Schenck and its taxonomic implications. Palaeontology 47:13391361.Google Scholar
Glasspool, I. J., Hilton, J., Collinson, M. E., Wang, S.-J., and Cheng, S. Li 2004b. Foliar physiognomy in Cathaysian gigantopterids and the potential to track Palaeozoic climates using an extinct plant group. Palaeogeography, Palaeoclimatology, Palaeoecology 205:69110.Google Scholar
Greguss, P. 1968. Xylotomy of the living cycads. Akademiai Kiado, Budapest, Hungary. Google Scholar
Greguss, P., and Balkay, B. 1972. Xylotomy of the living conifers. Akademiai Kiado, Budapest, Hungary. Google Scholar
Hacke, U. G., and Sperry, J. S. 2001. Functional and ecological xylem anatomy. Perspectives in Plant Ecology, Evolution and Systematics 4:97115.Google Scholar
Hacke, U. G., Sperry, J. S., Pockman, W. T., Davis, S. D., and McCulloch, K. A. 2001a. Trends in wood density and structure are linked to prevention of xylem implosion by negative pressure. Oecologia 126:457461.Google Scholar
Hacke, U. G., Stiller, V., Sperry, J. S., Pittermann, J., and McCulloh, K. A. 2001b. Cavitation fatigue: embolism and refilling cycles can weaken the cavitation resistance of xylem. Plant Physiology 125:779786.Google 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 91:386400.CrossRefGoogle ScholarPubMed
Hacke, U. G., Sperry, J. S., Wheeler, J. K., and Castro, L. 2006. Scaling of angiosperm xylem structure with safety and efficiency. Tree Physiology 26:689701.Google Scholar
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 168:11131126.Google Scholar
Hammel, H. T. 1967. Freezing of xylem sap without cavitation. Plant Physiology 42:5566.Google Scholar
Jagels, R., and Visscher, G. E. 2006. A synchronous increase in hydraulic conductive capacity and mechanical support in conifers with relatively uniform xylem structure. American Journal of Botany 93:179187.Google Scholar
Jansen, S., Sano, Y., Choat, B., Rabaey, D., Lens, F., and Dute, R. R. 2007. Pit membranes in tracheary elements of Rosaceae and related families: new records of tori and pseudotori. American Journal of Botany 94:503514.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
Lancashire, J. R., and Ennos, A. R. 2002. Modelling the hydrodynamic resistance of bordered pits. Journal of Experimental Botany 53:14851493.Google Scholar
Langdon, L. M. 1920. Stem anatomy of Dioon spinulosum . Botanical Gazette 70:110125.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 159:10231033.Google Scholar
Li, H., Taylor, E. L., and Taylor, T. N. 1996. Permian vessel elements. Science 271:188189.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 247:788803.Google Scholar
Maheshwari, H. K. 1972. Permian wood from Antarctica and revision of some Lower Gondwana wood taxa. Palaeontographica, Abteilung B 138:143.Google Scholar
Mamay, S. H., Miller, J. M., Rohr, D. M., and Stein, W. E. Jr. 1988. Foliar morphology and anatomy of the gigantopterid plant Delnortea abbottiae, from the Lower Permian of West Texas. American Journal of Botany 75:14091433.Google Scholar
McGhee, G. R. 1999. Theoretical morphology: the concept and its applications. Columbia University Press, New York.Google 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
Namboodiri, K. K., and Beck, C. B. 1968. A comparative study of the primary vascular system of conifers. III. Stelar evolution in gymnosperms. American Journal of Botany 55:464–72.Google Scholar
Niklas, K. J. 1992. Plant biomechanics. University of Chicago Press, Chicago.Google Scholar
Niklas, K. J. 1997. The evolutionary biology of plants. University of Chicago Press, Chicago.Google Scholar
Niklas, K. J., and Spatz, H. C. 2004. Growth and hydraulic (not mechanical) constraints govern the scaling of tree height and mass. Proceedings of the National Academy of Sciences USA 101:1566115663.Google Scholar
Pearce, R. S. 2001. Plant freezing and damage. Annals of Botany 87:417424.Google Scholar
Philippe, M., and Bamford, M. K. 2008. A key to morphogenera used for Mesozoic conifer-like woods. Review of Palaeobotany and Palynology 148:184207.Google Scholar
Philippe, M., Gomez, B., Girard, V., Coiffard, C., Daviero-Gomez, V., Thevenard, F., Billon-Bruyat, J.-P., Guiomar, M., Latil, J.-L., Le Loeuff, J., Néraudeau, D., Olivero, D., and Schlögl, J. 2008. Woody or not woody? Evidence for early angiosperm habit from the Early Cretaceous fossil wood record of Europe. Palaeoworld 17:142152.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 310:19241924.CrossRefGoogle ScholarPubMed
Pittermann, J., Sperry, J. S., Hacke, U. G., Wheeler, J. K., and Sikkema, E. H. 2006a. Inter-tracheid pitting and the hydraulic efficiency of conifer wood: the role of tracheid allometry and cavitation protection. American Journal of Botany 93:12651273.CrossRefGoogle ScholarPubMed
Pittermann, J., Sperry, J. S., Wheeler, J. K., Hacke, U. G., and Sikkema, E. H. 2006b. Mechanical reinforcement of tracheids compromises the hydraulic efficiency of conifer xylem. Plant, Cell and Environment 29:16181628.Google Scholar
Rabaey, D., Lens, F., Smets, E., and Jansen, S. 2006. The micromorphology of pit membranes in tracheary elements of Ericales: new records of Tori or Pseudo-tori? Annals of Botany 98:943951.Google Scholar
Raup, D. M. 1966. Geometric analysis of shell coiling; general problems. Journal of Paleontology 40:11781190.Google Scholar
Raup, D. M. 1967. Geometric analysis of shell coiling: coiling in ammonoids. Journal of Paleontology 41:4365.Google Scholar
Rothwell, G. W. 1975. The Callistophytaceae (Pteridospermopsida). I. Vegetative structures. Palaeontographica, Abteilung B 151:171196.Google Scholar
Rothwell, G. W. 1982. New interpretations of the earliest conifers. Review of Palaeobotany and Palynology 37:728.CrossRefGoogle Scholar
Rothwell, G. W., Mapes, G., and Mapes, M. R. H. 1997. Late Paleozoic conifers of North America: structure, diversity and occurrences. Review of Palaeobotany and Palynology 95:95113.Google Scholar
Rowe, N. P., and Speck, T. 2004. Hydraulics and mechanics of plants: novelty, innovation, and evolution. Pp. 297326 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 252:1928.Google Scholar
Ryberg, P. E., Taylor, E. L., and Taylor, T. N. 2007. Secondary phloem anatomy of Cycadeoidea (Bennettitales). American Journal of Botany 94:791798.Google Scholar
Sano, Y., and Jansen, S. 2006. Perforated pit membranes in imperforate tracheary elements of some angiosperms. Annals of Botany 97:10451053.Google Scholar
Schulte, P. J., Gibson, A. C., and Nobel, P. S. 1987. Xylem anatomy and hydraulic conductance of Psilotum nudum . American Journal of Botany 74:14381445.Google Scholar
Scott, D. H. 1902. On the primary structure of certain Palaeozoic stems with the Dadoxylon type of wood. Transactions of the Royal Society of Edinburgh 40:331365.Google Scholar
Scott, R. A., Barghoorn, E. S., and Prakash, U. 1962. Wood of Ginkgo in the Tertiary of western North America. American Journal of Botany 49:10951101.Google Scholar
Serbet, R., and Rothwell, G. W. 1992. Characterizing the most primitive seed ferns. I. A reconstruction of Elkinsia polymorpha . International Journal of Plant Sciences 153:602.Google 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 91:369385.Google Scholar
Sperry, J. S., and Ikeda, T. 1997. Xylem cavitation in roots and stems of Douglas-fir and white fir. Tree Physiology 17:275280.Google Scholar
Sperry, J. S., and Sullivan, J. E. M. 1992. Xylem embolism in response to freeze-thaw cycles and water stress in ring-porous, diffuse-porous, and conifer species. Plant Physiology 100:605613.Google Scholar
Sperry, J. S., and Tyree, M. T. 1988. Mechanism of water stress-induced xylem embolism. Plant Physiology 88:581587.Google Scholar
Sperry, J. S., and Tyree, M. T. 1990. Water-stress-induced xylem embolism in 3 species of conifers. Plant, Cell and Environment 13:427436.Google Scholar
Sperry, J. S., Nichols, K. L., Sullivan, J. E. M., and Eastlack, S. E. 1994. Xylem embolism in ring-porous, diffuse-porous, and coniferous trees of northern Utah and interior Alaska. Ecology 75:17361752.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 28:456465.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(10):14901500.Google Scholar
Sperry, J. S., Hacke, U. G., Feild, T. S., Sano, Y., and Sikkema, E. H. 2007. Hydraulic consequences of vessel evolution in angiosperms. International Journal of Plant Sciences 168:11271139.Google Scholar
Steponkus, P. L. 1984. Role of the plasma membrane in freezing injury and cold acclimation. Annual Review of Plant Physiology 35:543584.Google Scholar
Stewart, W., and Rothwell, G. W. 1993. Paleobotany and the evolution of plants. Cambridge University Press, Cambridge.Google Scholar
Sucoff, E. 1969. Freezing of conifer xylem sap and the cohesion-tension theory. Physiologia Plantarum 22:424431.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
Taylor, T. N., Taylor, E. L., and Krings, M. 2008. Paleobotany: the biology and evolution of fossil plants. Academic Press, San Diego.Google Scholar
Terrazas, T. 1991. Origin and activity of successive cambia in Cycas (Cycadales). American Journal of Botany 78:13351344.Google Scholar
Tomlinson, P. B. 1990. The structural biology of palms. Clarendon, Oxford.Google Scholar
Tyree, M. T., and Ewers, F. W. 1991. Tansley Review No. 34. The hydraulic architecture of trees and other woody plants. New Phytologist 119:345360.Google Scholar
Tyree, M. T., and Sperry, J. S. 1988. Do woody-plants operate near the point of catastrophic xylem dysfunction caused by dynamic water-stress? Answers from a model. Plant Physiology 88:574580.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 40:1938.Google Scholar
Tyree, M. T., Salleo, S., Nardini, A., Lo Gullo, M. A., and Mosca, R. 1999. Refilling of embolized vessels in young stems of laurel. Do we need a new paradigm? Plant Physiology 120:1121.Google Scholar
van den Honert, T. H. 1948. Water transport in plants as a catenary process. Discussions of the Faraday Society 3:146153.Google Scholar
Veres, J. S. 1990. Xylem anatomy and hydraulic conductance of Costa Rican Blechnum ferns. American Journal of Botany 77:16101625.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 28:800812.Google Scholar
Wilkinson, H. P. 2000. A revision of the anatomy of Gunneraceae. Botanical Journal of the Linnean Society 134:233266.Google Scholar
Wilson, J. P., Knoll, A. H., Holbrook, N. M., and Marshall, C. R. 2008. Modeling fluid flow in Medullosa, an anatomically unusual Carboniferous seed plant. Paleobiology 34:472493.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 41:329351.Google Scholar
Zimmermann, M. H. 1983. Xylem structure and the ascent of sap. Springer, Berlin.Google Scholar