On the hydraulic conductance of three woody Devonian plants

In: IAWA Journal

ABSTRACT

Most evolutionary innovations in plant vascular tissues, including secondary growth, occurred during the Devonian period (~420 to 360 million years ago). Such innovations had a major impact on land colonisation by plants and on their biodiversity. Here, we show the hydraulic conductance of the secondary xylem of three shrubby or arborescent plant fossils (a probably new genus of Cladoxylopsida, the archaeopteridalean genus Callixylon and the stenokolean genus Brabantophyton). Evidences come from the Ronquières fossil site (Belgium). This site is considered mid-late Givetian/earliest Frasnian in age. Results reveal that hydraulic conductivity of these early woody plants is more or less similar to that of modern gymnosperms, meaning that water transport was already as efficient in Devonian plants as it is in living plants. Our results further suggest that tracheids with features helping for optimised water transport were quickly selected in the evolutionary history of vascular plants.

  • ArnoldCA. 1940. Structure and relationships of some Middle Devonian plants from Western New York. Am. J. Bot.27: 5763. https://doi.org/10.1002/j.1537-2197.1940.tb14215.x.

    • Search Google Scholar
    • Export Citation
  • BaasPEwersFWDavisSDWheelerEA. 2004. Evolution of xylem physiology. In: HemsleyARPooleI (eds.) The evolution of plant physiology: 273–295. Elsevier Academic PressOxford. https://doi.org/10.1016/B978-012339552-8/50016-0.

    • Search Google Scholar
    • Export Citation
  • BeckCBSteinWE. 1993. Crossia virginiana gen. et sp. nov., a new member of the Stenokoleales from the Middle Devonian of southwestern Virginia. Palaeontogr. B229: 115134.

    • Search Google Scholar
    • Export Citation
  • BerryCM. 2008. The Middle Devonian plant collections of François Stockmans reconsidered. Geol. Belg.12: 2530.

  • ChoatBCobbARJansenS. 2008. Structure and function of bordered pits: new discoveries and impacts on whole-plant hydraulic function. New Phytol.177: 608626. https://doi.org/10.1111/j.1469-8137.2007.02317.x.

    • Search Google Scholar
    • Export Citation
  • CichanMA. 1986. Conductance in the wood of selected Carboniferous plants. Paleobiology12: 302310. https://www.jstor.org/stable/2400436.

    • Search Google Scholar
    • Export Citation
  • CornetLGerriennePMeyer-BerthaudBPrestianniC. 2012. A Middle Devonian Callixylon (Archaeopteridales) from RonquièresBelgium. Rev. Palaeobot. Palynol.183: 18. https://doi.org/10.1016/j.revpalbo.2012.07.004.

    • Search Google Scholar
    • Export Citation
  • DunnMTKringsMMapesGRothwellGWMapesRHKeqinS. 2003. Medullosa steinii sp. nov., a seed fern vine from the Upper Mississippian. Rev. Palaeobot. Palynol.124: 307324. https://doi.org/10.1016/S0034-6667(02)00254-3.

    • Search Google Scholar
    • Export Citation
  • Fairon-DemaretM.1981. Le genre Leclercqia Banks, H.P., Bonamo, P.M. et Grierson, J.D., 1972 dans le Dévonien moyen de Belgique. Bull. Inst. Roy. Sci. Nat. Belg.53: 1013.

    • Search Google Scholar
    • Export Citation
  • GaltierJMeyer-BerthaudB. 1996. The early seed plant Tristichia tripos (Unger) comb. nov. from the Lower Carboniferous of SaalfeldThuringia. Rev. Palaeobot. Palynol.93: 299315. https://doi.org/10.1016/0034-6667(95)00131-X.

    • Search Google Scholar
    • Export Citation
  • GaltierJPhillipsTL. 1999. The acetate peel technique. In: JonesTPRoweNP (eds.) Fossil plants and spores: modern techniques: 67–70. Geological SocietyLondon.

    • Search Google Scholar
    • Export Citation
  • GerriennePGenselPG. 2016. New data about anatomy, branching, and inferred growth patterns in the Early Devonian plant Armoricaphyton chateaupannense, Montjean-sur-LoireFrance. Rev. Palaeobot. Palynol.224: 3853. https://doi.org/10.1016/j.revpalbo.2015.07.014.

    • Search Google Scholar
    • Export Citation
  • GerriennePGenselPGStrullu-DerrienCLardeuxHSteemansPPrestianniC. 2011. A simple type of wood in two Early Devonian plants. Science333: 837. DOI: .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • GerriennePMeyer-BerthaudB. 2007. The proto-ovule Runcaria heinzeliniiStockmans 1968 emend. Gerrienne et al., 2004 (mid-Givetian, Belgium): concept and epitypification. Rev. Palaeobot. Palynol.145: 321323. https://doi.org/10.1016/j.revpalbo.2006.12.003.

    • Search Google Scholar
    • Export Citation
  • GerriennePMeyer-BerthaudBFairon-DemaretMStreelMSteemansP. 2004. Runcaria, a Middle Devonian seed plant precursor. Science306: 856858. DOI: .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • HackeUGSperryJS. 2001. Functional and ecological xylem anatomy. Perspec. plant Ecol. Evol. Syst.4: 97115. https://doi.org/10.1007/s004420100628.

    • Search Google Scholar
    • Export Citation
  • HackeUGSperryJSPittermannJ. 2004. Analysis of circular bordered pit function II. Gymnosperm tracheids with torus-margo pit membranes. Am. J. Bot.91: 386400. https://doi.org/10.3732/ajb.91.3.386.

    • Search Google Scholar
    • Export Citation
  • HackeUGSperryJSPittermannJ. 2005. Efficiency versus safety tradeoffs for water conduction in angiosperm vessels versus gymnosperm tracheids. In: HolbrookNMZwienieckiMA (eds.) Vascular transport in plants: 333–353. Elsevier Academic PressLondon. https://doi.org/10.1016/B978-012088457-5/50018-6.

    • Search Google Scholar
    • Export Citation
  • HackeUGSperryJSPockmanWTDavisSDMcCullohKA. 2001. Trends in wood density and structure are linked to prevention of xylem implosion by negative pressure. Oecologia126: 457461. https://link.springer.com/article/10.1007/s004420100628.

    • Search Google Scholar
    • Export Citation
  • HassHRoweNP. 1999. Thin sections and wafering. In: JonesTPRoweNP (eds.) Fossil plants and spores: modern techniques: 7681. Geological SocietyLondon.

    • Search Google Scholar
    • Export Citation
  • HoffmanLATomescuAM. 2013. An early origin of secondary growth: Franhueberia gerriennei gen. et sp. nov. from the Lower Devonian of Gaspé (Quebec, Canada). Am. J. Bot.100: 754763. https://doi.org/10.3732/ajb.1300024.

    • Search Google Scholar
    • Export Citation
  • JoyKWWillisAJLaceyWS. 1956. A rapid cellulose peel technique in palaeobotany. Ann. Bot.20: 635637.

  • KenrickP.1999. Opaque petrifaction techniques. In: JonesTPRoweNP (eds.) Fossil plants and spores: modern techniques: 8791. Geological SocietyLondon.

    • Search Google Scholar
    • Export Citation
  • KenrickPCranePR. 1997. The origin and early diversification of land plants. A cladistic study. Smithsonian Institute PressWashington DC.

    • Search Google Scholar
    • Export Citation
  • MattenLC. 1973. Preparation of pyritized plant petrifications. Rev. Palaeobot. Palynol.16: 165173. https://doi.org/10.1016/0034-6667(73)90044-4.

    • Search Google Scholar
    • Export Citation
  • MattenLC. 1992. Studies on Devonian plants from New York State: Stenokoleos holmesii n. sp. from the Cairo flora (Givetian) with an alternative model for lyginopterid seed fern evolution. Cour. Forsch. Senck.147: 7585.

    • Search Google Scholar
    • Export Citation
  • Meyer-BerthaudBDecombeixAL. 2007. A tree without leaves. Nature446: 861862. DOI: .

  • Meyer-BerthaudDecombeix AL. 2009. Evolution of earliest trees: The Devonian strategies. C. R. Palevol8: 155165. DOI: .

  • Meyer-BerthaudBSoriaADecombeixAL. 2010. The land plant cover in the Devonian: a reassessment of the evolution of the tree habit. Geol. Soc., LondonSpec. Pub.339: 5970. https://doi.org/10.1144/SP339.6.

    • Search Google Scholar
    • Export Citation
  • MomontNDecombeixALGerriennePPrestianniC. 2016a. New information, including anatomy of the secondary xylem, on the genus Brabantophyton (Stenokoleales) from Ronquières (Middle Devonian, Belgium). Rev. Palaeobot. Palynol.234: 4460. https://doi.org/10.1016/j.revpalbo.2016.08.009.

    • Search Google Scholar
    • Export Citation
  • MomontNGerriennePPrestianniC. 2016b. Brabantophyton, a new genus with stenokolealean affinities from a Middle to earliest Upper Devonian locality from Belgium. Rev. Palaeobot. Palynol.227: 7796. https://doi.org/10.1016/j.revpalbo.2015.10.009.

    • Search Google Scholar
    • Export Citation
  • MustafaH.1980. Beiträge zur Devonflora IV. Arg. Palaeobot.6: 115132.

  • NiklasKJ. 1985. The evolution of tracheid diameter in early vascular plants and its implications on the hydraulic conductance of the primary xylem strand. Evolution39: 11101122. https://doi.org/10.1111/j.1558-5646.1985.tb00451.x.

    • Search Google Scholar
    • Export Citation
  • PittermannJSperryJSHackeUGWheelerJKSikkemaEH. 2005. Torus-margo pits help conifers compete with angiosperms. Science310: 1924. DOI: .

  • PittermannJSperryJSWheelerJKHackeUGSikkemaEH. 2006. Mechanical reinforcement of tracheids compromises the hydraulic efficiency of conifer xylem. Plant Cell Environ.29: 16181628. https://doi.org/10.1111/j.1365-3040.2006.01539.x.

    • Search Google Scholar
    • Export Citation
  • RothwellGWNixonKC. 2006. How does the inclusion of fossil data change our conclusions about the phylogenetic history of euphyllophytes?Int. J. Plant Sci.167: 737749. https://doi.org/10.1086/503298.

    • Search Google Scholar
    • Export Citation
  • RoweNPSpeckT. 2003. Hydraulics and mechanics of plants: novelty, innovation and evolution. In: HemsleyARPooleI (eds.) The evolution of plant physiology: 301329. Acad. PressLondon. https://doi.org/10.1016/B978-012339552-8/50017-2.

    • Search Google Scholar
    • Export Citation
  • SchecklerSESkogJEBanksHP. 2006. Langoxylon asterochlaenoideum Stockmans: anatomy and relationships of a fern-like plant from the Middle Devonian of Belgium. Rev. Palaeobot. Palynol.142: 193217. https://doi.org/10.1016/j.revpalbo.2015.10.009.

    • Search Google Scholar
    • Export Citation
  • SpeckTRoweNP. 2003. Modelling primary and secondary growth processes in plants: a summary of the methodology and new data from an early lignophyte. Phil. Trans. Roy. Soc. Lond. BBiol. Sci.358: 14731485. DOI: .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • SperryJS. 2003. Evolution of water transport and xylem structure. Int. J. Plant Sci.164: S115S127. https://doi.org/10.1086/368398.

  • SperryJSHackeUG. 2004. Analysis of circular bordered pit function I. Angiosperm vessels with homogeneous pit membranes. Am. J. Bot.91: 369385. https://doi.org/10.3732/ajb.91.3.369

    • Search Google Scholar
    • Export Citation
  • SperryJSHackeUGPittermannJ. 2006. Size and function in conifer tracheids and angiosperm vessels. Am. J. Bot.93: 14901500. https://doi.org/10.3732/ajb.93.10.1490.

    • Search Google Scholar
    • Export Citation
  • SteinW.1993. Modeling the evolution of stelar architecture in vascular plants. Int. J. Plant Sci.154: 229263. https://doi.org/10.1086/297106.

    • Search Google Scholar
    • Export Citation
  • StockmansF.1968. Végétaux mésodévoniens récoltés aux confins du massif du Brabant (Belgique). Mem. Inst. Roy. Sci. Nat. Belg.159: 149.

    • Search Google Scholar
    • Export Citation
  • StreelMHiggsKLoboziakSRiegelWSteemansP. 1987. Spore stratigraphy and correlation with faunas and floras in the type marine Devonian of the Ardenne-Rhenish regions. Rev. Palaeobot. Palynol.50: 211229. https://doi.org/10.1016/0034-6667(87)90001-7.

    • Search Google Scholar
    • Export Citation
  • Strullu-DerrienCKenrickPBadelECochardHTafforeauP. 2013. An overview of the hydraulic systems in early land plants. IAWA J.34: 333351. DOI: .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Strullu-DerrienCKenrickPTafforeauPCochardHBonnemainJLLe HérisséALardeuxHBadelE. 2014. The earliest wood and its hydraulic properties documented in c. 407-million-year-old fossils using synchrotron microtomography. Bot. J. Linn. Soc.175: 423437. https://doi.org/10.1111/boj.12175.

    • Search Google Scholar
    • Export Citation
  • van den HonertTH. 1948. Water transport in plants as a catenary process. Disc. Faraday Soc.3: 146153. DOI: .

  • WilsonJP. 2013. Modeling 400 million years of plant hydraulics. Paleont. Soc. Papers19: 175194. https://doi.org/10.1017/S1089332600002734.

    • Search Google Scholar
    • Export Citation
  • WilsonJP. 2016. Hydraulics of Psilophyton and evolutionary trends in plant water transport after terrestrialization. Rev. Palaeobot. Palynol.227: 6576. https://doi.org/10.1016/j.revpalbo.2015.11.010.

    • Search Google Scholar
    • Export Citation
  • WilsonJPFischerWW. 2011. Hydraulics of Asteroxylon mackei, an early Devonian vascular plant, and the early evolution of water transport tissue in terrestrial plants. Geobiology9: 121130. https://doi.org/10.1111/j.1472-4669.2010.00269.x.

    • Search Google Scholar
    • Export Citation
  • WilsonJPKnollAH. 2010. A physiologically explicit morphospace for tracheid-based water transport in modern and extinct seed plants. Paleobiology36: 335355. https://doi.org/10.1666/08071.1.

    • Search Google Scholar
    • Export Citation
  • WilsonJPKnollAHHolbrookNMMarshallCR. 2008. Modeling fluid flow in Medullosa, an anatomically unusual Carboniferous seed plant. Paleobiology34: 472493. https://doi.org/10.1666/07076.1.

    • Search Google Scholar
    • Export Citation
  • WoodruffDRMeinzerFCLachenbruchB. 2008. Height-related trends in leaf xylem anatomy and shoot hydraulic characteristics in a tall conifer: safety versus efficiency in water transport. New Phytol.180: 9099. https://doi.org/10.1111/j.1469-8137.2008.02551.x.

    • Search Google Scholar
    • Export Citation
  • XuHHBerryCMSteinWEWangYTangPFuQ. 2017. Unique growth strategy in the Earth’s first trees revealed in silicified fossil trunks from China. PNAS114: 1200912014. https://doi.org/10.1073/pnas.1708241114.

    • Search Google Scholar
    • Export Citation
  • ZalesskyMD. 1911. Etude sur l’anatomie du Dadoxylon tchihatcheffi Goeppert. Mem. Com. Geol. Russ.68: 129.

Content Metrics

All Time Past Year Past 30 Days
Abstract Views 92 92 10
Full Text Views 23 23 6
PDF Downloads 14 14 1