Skip to main content
Log in

Paedomorphosis, Secondary Woodiness, and Insular Woodiness in Plants

  • Published:
The Botanical Review Aims and scope Submit manuscript

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13

Notes

  1. The term heraceous is treated more fully in the Discussion.

  2. For the purposes of this discussion we have amended our definition of wood as fibrous secondary xylem to include the highly parenchymatized secondary xylem of Coreopsis gigantea. We return to this issue in the last section of the Discussion.

VIII. Literature Cited

  • Andersson, L. & J. H. E. Rova. 1999. The rps16 intron and the phylogeny of the Rubioideae (Rubiaceae). Plant Systematics and Evolution 214: 161–186.

    Article  Google Scholar 

  • Archibald, J. K., M. E. Mort, D. J. Crawford & J. K. Kelly. 2005. Life history affects the evolution of reproductive isolation among species of Coreopsis (Asteraceae). Evolution 59: 2362–2369.

    PubMed  Google Scholar 

  • Arnold, D. H. & J. D. Mauseth. 1999. Effects of environmental factors on development of wood. American Journal of Botany 86: 367–371.

    Article  PubMed  Google Scholar 

  • Baas, P. & E. A. Wheeler. 1996. Parallelism and reversibility in xylem evolution—A review. IAWA Journal 17: 351–364.

    Google Scholar 

  • Bailey, I. W. 1944. The development of vessels in angiosperms and its significance in morphological research. American Journal of Botany 31: 421–428.

    Article  Google Scholar 

  • ——— & W. W. Tupper. 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: 149–204.

    Article  Google Scholar 

  • Baldwin, B. G. & M. J. Sanderson. 1998. Age and rate of diversification of the Hawaiian silversword alliance (Compositae). Proceedings of the National Academy of Sciences 95: 9402–9406.

    Article  CAS  Google Scholar 

  • ———, B. L. Wessa & J. L. Panero. 2002. Nuclear rDNA evidence for major lineages of helenioid Heliantheae (Compositae). Systematic Botany 27: 161–198.

    Google Scholar 

  • Balfour, I. B. & W. W. Smith. 1914. Kingonia uniflora. In: Diagnoses specierum novarum LI-CII (Species Chinenses). Notes of the Royal Botanical Garden, Edinburgh 8: 191–192.

    Google Scholar 

  • Bancroft, H. 1930. Arborescent habit in angiosperms. A review (continued). New Phytologist 29: 227–275.

    Article  Google Scholar 

  • Barber, J. C., J. Francisco-Ortega, A. Santos-Guerra, K. G. Turner & R. K. Jansen. 2002. Origin of Macaronesian Sideritis L. (Lamioideae: Lamiaceae) inferred from nuclear and chloroplast sequence datasets. Molecular Phylogenetics and Evolution 23: 293–306.

    Article  CAS  PubMed  Google Scholar 

  • Barghoorn, E. S., Jr. 1940. The ontogenetic development and phylogenetic specialization of rays in the xylem of dicotyledons. I. The primitive ray structure. American Journal of Botany 27: 918–928.

    Article  Google Scholar 

  • ———. 1941a. The ontogenetic development and phylogenetic specialization of rays in the xylem of dicotyledons. II. Modification of the multiseriate and uniseriate rays. American Journal of Botany 28: 273–282.

    Article  Google Scholar 

  • ———. 1941b. The ontogenetic development and phylogenetic specialization of rays in the xylem of dicotyledons. III. The elimination of rays. Bulletin of the Torrey Botanical Club 68: 317–325.

    Article  Google Scholar 

  • Baskin, J. M. & C. C. Baskin. 1989. Seed-germination ecophysiology of Jeffersonia diphylla, a perennial herb of mesic deciduous forests. American Journal of Botany 76: 1073–1080.

    Article  Google Scholar 

  • Berlyn, G. P. & J. Miksche. 1976. Botanical microtechnique and cytochemistry. Iowa State University Press, Ames, IA.

    Google Scholar 

  • Bissing, D. R. 1982. Variation in quantitative anatomical features of the xylem of selected dicotyledon woods in relation to water availability. Bulletin of the Torrey Botanical Club 189: 371–384.

    Article  Google Scholar 

  • Bohle, U. R., H. H. Hilger & W. F. Martin. 1996. Island colonization and evolution of the insular woody habit in Echium L. (Boraginaceae). Proceedings of the National Academy of Sciences 93: 11740–11745.

    Article  CAS  Google Scholar 

  • Bowers, B. G. 1996. A color atlas of plant structure. Iowa State University Press, Ames, IA.

    Google Scholar 

  • ———. & J. D. Mauseth. 2008. Plant structure: A color guide. Jones and Bartlett, Sudbury, MA.

    Google Scholar 

  • Bratton, S. P. 1976. Response of understory herbs to soil depth gradients in high and low diversity communities. Bulletin of the Torrey Botanical Club 103: 165–172.

    Article  Google Scholar 

  • Bremer, B. 1996. Phylogenetic studies within Rubiaceae and relationships to other families based on molecular data. Opera Botanica Belgica 7: 33–50.

    Google Scholar 

  • Carine, M. A., S. J. Russell, A. Santos-Guerra & J. Francisco-Ortega. 2004. Relationships of the Macaronesian and Mediterranean floras: Molecular evidence for multiple colonizations into Macaronesia and back-colonization of the continent in Convolvulus (Convolvulaceae). American Journal of Botany 91: 1070–1085.

    Article  Google Scholar 

  • Carlquist, S. 1962. A theory of paedomorphosis in dicotyledonous woods. Phytomorphology 12: 30–45.

    Google Scholar 

  • ———. 1966. Wood anatomy of Compositae: A summary, with comments on factors controlling wood evolution. Aliso 6: 25–44.

    Google Scholar 

  • ———. 1970. Wood anatomy of insular species of Plantago and the problem of raylessness. Bulletin of the Torrey Botanical Club 97: 353–361.

    Article  Google Scholar 

  • ———. 1974. Island biology. Columbia University Press, New York, NY.

    Google Scholar 

  • ———. 1983. Woody anatomy of Calyceraceae and Valerianaceae, with comments on aberrant perforation plates in predominately hebacous groups of dicotyledons. Aliso 10: 413–425.

    Google Scholar 

  • ———. 1985. Ecological wood anatomy of the woody southern California flora. IAWA Journal 6: 319–347.

    Google Scholar 

  • ———. 1989. Wood and bark anatomy of Empetraceae: Comments on paedomorphosis in woods of certain small shrubs. Aliso 12: 497–515.

    Google Scholar 

  • ———. 1992. Wood anatomy of sympetalous dicotyledon families—A summary, with comments on systematic relationships and evolution of the woody habit. Annals of the Missouri Botanical Garden 79: 303–332.

    Article  Google Scholar 

  • ———. 1995a. Wood anatomy of Berberidaceae: Ecological and phylogenetic considerations. Aliso 14: 85–103.

    Google Scholar 

  • ———. 1995b. Wood and bark anatomy of Ranunculaceae (including Hydrastis) and Glaucidiaceae. Aliso 14: 65–84.

    Google Scholar 

  • ———. 1997. Pentaphragma: A unique wood and its significance. IAWA Journal 18: 3–12.

    Google Scholar 

  • ———. 2001. Comparative wood anatomy. Springer, Berlin.

    Google Scholar 

  • ———. 2003. Wood anatomy of Polygonaceae: Analysis of a family with exceptional wood diversity. Botanical Journal of the Linnean Society 141: 25–51.

    Article  Google Scholar 

  • ———. 2007. Successive cambia revisited: Ontogeny, histology, diversity, and functional significance. The Journal of the Torrey Botanical Society 134: 301–332.

    Article  Google Scholar 

  • ———. 2009. Xylem heterochrony: An unappreciated key to angiosperm origin and diversifications. Botanical Journal of the Linnean Society 161: 25–65.

    Google Scholar 

  • Chaffey, N., E. Cholewa, S. Regan & B. Sundberg. 2002. Secondary xylem development in Arabidopsis: A model for wood formation. Physiologia Plantarum 114: 594–600.

    Article  CAS  PubMed  Google Scholar 

  • Chalk, L. 1937. The phylogenetic value of certain anatomical features of docotyledonous woods. Annals of Botany 1: 409–428.

    Google Scholar 

  • Chrysler, M. A. 1937. Persistent juveniles among the cycads. Botanical Gazette 98: 696–710.

    Article  Google Scholar 

  • Cleveland, W. S. 1979. Robust locally weighted regression and smoothing scatterplots. Journal of the American Statistical Association 74: 829–836.

    Article  Google Scholar 

  • ———. 1981. LOWESS: A program for smoothing scatterplots by robust locally weighted regression. The American Statistician 35: 54.

    Article  Google Scholar 

  • Consortium of California Herbaria. 2008. Distribution of Coreopsis gigantea. Consortium of California Herbaria. Berkeley, CA. Available from http://ucjeps.berkeley.edu/cgi-bin/get_smasch_county.pl?taxon_id=2331 [Accessed: August 28, 2009].

  • Crawford, D. J. 1976. Taxonomy of Coreopsis sect Pseudo-Agarista (Compositae) in Mexico with additional comments on sectional relationships in Mexican Coreopsis. Brittonia 28: 329–336.

    Article  Google Scholar 

  • ———. 1982. Chromosome numbers and taxonomic notes for Mexican Coreopsis, sections Electra and Pseudoagarista (Compositae, Heliantheae). Brittonia 34: 384–387.

    Article  Google Scholar 

  • ———. & R. Whitkus. 1988. Allozyme divergence and the mode of speciation for Coreopsis gigantea and Coreopsis maritima (Compositae). Systematic Botany 13: 256–264.

    Article  Google Scholar 

  • Cronquist, A. 1955. Phylogeny and taxonomy of the Compositae. American Midland Naturalist 53: 478–511.

    Article  Google Scholar 

  • Darwin, C. 1939. Journal of researches into the geology and natural history of the various countries visited by H.M.S. Beagle. Henry Colburn, London.

  • Darwin, C. 1859. The origin of species. John Murray, London, U.K.

    Google Scholar 

  • de Beer, G. R. 1930. Embryos and ancestors. Clarendon, Oxford, U.K.

    Google Scholar 

  • Dietz, H. & I. Ullmann. 1997. Age determination of dicotyledonous herbaceous perennials by means of annual rings: Exception or rule? Annals of Botany 80: 377–379.

    Article  Google Scholar 

  • ———. & F. H. Schweingruber. 2002. Annual rings in native and introduced forbs of lower Michigan, USA. Canadian Journal of Botany 80: 642–649.

    Article  Google Scholar 

  • Dormer, K. J. 1954. The Acacia type of vascular system and some of its derivatives. Introduction: Menispermaceae, Lardizabalaceae, and Berberidaceae. New Phytologist 53: 301–311.

    Article  Google Scholar 

  • Edwards, E. J., R. Nyffeler & M. J. Donoghue. 2005. Basal cactus phylogeny: Implications of Pereskia (Cactaceae) paraphyly for the transition to the cactus life form. American Journal of Botany 92: 1177–1188.

    Article  Google Scholar 

  • eFloras. 2008. Published on the Internet. Missouri Botanical Garden & Harvard University Herbaria. St. Louis, Missouri & Cambridge, MA. Available from http://www.efloras.org [Accessed: 15 September, 2009].

  • Ellenberg, H. & D. Mueller-Dombois. 1967. A key to Raunkiaer plant life forms with revised subdivisions. Berichte des Geobotanischen Institutes der Eidgenössischen Technischen Hochschule 37: 56–73.

    Google Scholar 

  • Endress, P. K., P. Baas & M. Gregory. 2000. Systematic plant morphology and anatomy—50 years of progress. Taxon 49: 401–434.

    Article  Google Scholar 

  • Esau, K. 1977. Anatomy of seed plants. John Wiley & Sons, Inc., New York, New York.

    Google Scholar 

  • Evert, R. F. 2006. Esau's plant anatomy. Wiley, Hoboken, NJ.

    Book  Google Scholar 

  • Fairfield, K. N., M. E. Mort & A. Santos-Guerra. 2004. Phylogenetics and evolution of the Macaronesian members of the genus Aichryson (Crassulaceae) inferred from nuclear and chloroplast sequence. Plant Systematics and Evolution 248: 71–83.

    Article  CAS  Google Scholar 

  • Feild, T. S., N. C. Arens, J. A. Doyle, T. E. Dawson & M. J. Donoghue. 2004. Dark and disturbed: A new image of early angiosperm ecology. Paleobiology 30: 82–107.

    Article  Google Scholar 

  • Fern, K. 1997–2003. Plants for a future database. Plants for a Future. Cornwall, UK. Available from http://pfaf.org [Accessed: 25 September, 2009].

  • Florida Exotic Pest Plant Council. 2008. Nandina domestica. Florida Exotic Pest Plant Council. Available from http://www.fleppc.org/ID_book/Nandina%20domestica.pdf [Accessed: October 15, 2008].

  • Floridata's Plant Encyclopedia. 2008. Nadina domestica. Available from http://www.floridata.com/ref/N/nand_dom.cfm [Accessed: October 15, 2008].

  • Foreman, L. L. 1988. A synopsis of Thai Menispermaceae. Kew Bulletin 43: 369–407.

    Article  Google Scholar 

  • Frost, F. H. 1930a. Specialization in secondary xylem of dicotyledons. I. Origin of vessel. Botanical Gazette 89: 67–94.

    Article  Google Scholar 

  • ———. 1930b. Specialization in secondary xylem of dicotyledons. II. Evolution of end wall of vessel segment. Botanical Gazette 90: 198–212.

    Article  Google Scholar 

  • ———. 1931. Specialization in secondary xylem of dicotyledons. III. Specialization of lateral wall of vessel segment. Botanical Gazette 91: 88–96.

    Article  Google Scholar 

  • Fuertes-Aguilar, J., M. F. Ray, J. Francisco-Ortega, A. Santos-Guerra & R. K. Jansen. 2002. Molecular evidence from chloroplast and nuclear markers for multiple colonizations of Lavatera (Malvaceae) in the Canary Islands. Systematic Botany 27: 74–83.

    Google Scholar 

  • Fukada, I. 1967. The biosystematics of Achlys. Taxon 16: 308–316.

    Article  Google Scholar 

  • ———. & H. Baker. 1970. Achlys californica (Berberidaceae): A new species. Taxon 19: 341–344.

    Article  Google Scholar 

  • Garrison, R. 1949. Origin and development of axillary buds: Betula papyrifera Marsh and Euptelea polyandra Sieb. et Zucc. American Journal of Botany 36: 379–389.

    Article  Google Scholar 

  • Gianoli, E. 2004. Evolution of a climbing habit promotes diversification in flowering plants. Proceedings of the Royal Society of London Series B-Biological Sciences 271: 2011–2015.

    Article  Google Scholar 

  • Gilbert, S. G. 1940. Evolutionary significance of ring porosity in woody angiosperms. Botanical Gazette 102: 105–120.

    Article  Google Scholar 

  • Givnish, T. J. 1982. On the adaptive significance of leaf height in forest herbs. The American Naturalist 120: 353–381.

    Article  Google Scholar 

  • ———. 1998. Adaptive plant evolution on islands: Classical patterns, molecular data, new insights. Pp 281–304. In: P. R. Grant (ed). Evolution on islands. Oxford University Press, Oxford.

    Google Scholar 

  • Goodson, B. E., A. Santos-Guerra & R. K. Jansen. 2006. Molecular systematics of Descurainia (Brassicaceae) in the Canary Islands: Biogeographic and taxonomic implications. Taxon 55: 671–682.

    Article  Google Scholar 

  • Gould, S. J. 1977. Ontogeny and phylogeny. Belknap, Cambridge, MA.

    Google Scholar 

  • Groover, A. T. 2005. What genes make a tree a tree? Trends in Plant Science 10: 210–214.

    Article  CAS  PubMed  Google Scholar 

  • Hacke, U. G. & J. S. Sperry. 2001. Functional and ecological xylem anatomy. Perspectives in Plant Ecology Evolution and Systematics 4: 97–115.

    Article  Google Scholar 

  • ———, ———, J. K. Wheeler & L. Castro. 2006. Scaling of angiosperm xylem structure with safety and efficiency. Tree Physiology 26: 689–701.

    PubMed  Google Scholar 

  • Halpern, C. B. 1989. Early successional patterns of forest species—Interactions of life-history traits and disturbance. Ecology 70: 704–720.

    Article  Google Scholar 

  • Harris, A. 2008. Red dahlia (Dahlia coccinea). Chihuahuan Desert Plants. University of Texas at El Paso. El Paso, TX. Available from http://museum.utep.edu/chih/gardens/plants/DtoF/Dahliacoccinea.htm [Accessed: November 7, 2008].

  • Heywood, V. H., J. B. Harborne & B. L. Turner (eds). 1977. The biology and chemistry of the Compositae. Academic, London, UK.

    Google Scholar 

  • Hoot, S. B. 1991. Phylogeny of the Ranunculaceae based on epidermal microcharacters and macromorphology. Systematic Botany 16: 741–755.

    Article  Google Scholar 

  • ———, S. Magallon & P. R. Crane. 1999. Phylogeny of basal eudicots based on three molecular data sets: atpB, rbcL, and 18S nuclear ribosomal DNA sequences. Annals of the Missouri Botanical Garden 86: 1–32.

    Article  Google Scholar 

  • Hubbell, T. H. 1968. Biology of islands. Proceedings of the National Academy of Sciences 60: 22–32.

    Article  CAS  Google Scholar 

  • InsideWood. 2004-onwards. Published on the Internet. Raleigh, NC. Available from http://insidewood.lib.ncsu.edu [Accessed: 27 January, 2009].

  • Isnard, S., T. Speck & N. P. Rowe. 2003. Mechanical architecture and development in Clematis: Implications for canalised evolution of growth forms. New Phytologist 158: 543–559.

    Article  Google Scholar 

  • Jansen, R. K., E. B. Smith & D. J. Crawford. 1987. A cladistic study of North-American Coreopsis (Asteraceae, Heliantheae). Plant Systematics and Evolution 157: 73–84.

    Article  Google Scholar 

  • Jones, C. S. & M. A. Watson. 2001. Heteroblasty and preformation in mayapple, Podophyllum peltatum (Berberidaceae): Developmental flexibility and morphological constraint. American Journal of Botany 88: 1340–1358.

    Article  Google Scholar 

  • Jorgensen, T. H. & J. M. Olesen. 2001. Adaptive radiation of island plants: Evidence from Aeonium (Crassulaceae) of the Canary Islands. Perspectives in Plant Ecology Evolution and Systematics 4: 29–42.

    Article  Google Scholar 

  • Judd, W. S., C. S. Campbell, E. A. Kellog, P. F. Stevens & M. J. Donoghue. 2002. Plant systematics: A phylogenetic approach. Sinauer Associates, Sunderland, MA.

    Google Scholar 

  • Kadereit, J. W., F. R. Blattner, K. B. Jork & A. Schwarzbach. 1995. The phylogeny of the Papaveraceae sensu lato: Morphological, geographical and ecological implications. Plant Systematics and Evolution 133–145.

  • Kang, S. S. 1990. Medicinal plants in the Republic of Korea. Korean Journal of Pharmacology 21: 56–111.

    CAS  Google Scholar 

  • Keil, D. J. 1993. Coreopsis gigantea (Kellogg) H.M. Hall. Jepson Flora Project: Jepson Interchange. Berkeley, CA. Available from http://ucjeps.berkeley.edu/cgi-bin/get_JM_treatment.pl?609,1008,1013 [Accessed: August 28, 2009].

  • Kemper Center for Home Gardening. 2001–2009. Plant Finder. Missouri Botanical Garden. St. Louis, MO. Available from http://www.mobot.org/gardeninghelp/plantfinder/serviceplantfinder.shtml [Accessed: 24 September, 2009].

  • Kim, S., D. E. Soltis, P. S. Soltis, M. J. Zanis & Y. Suh. 2004a. Phylogenetic relationships among early-diverging eudicots based on four genes: Were the eudicots ancestrally woody? Molecular Phylogenetics and Evolution 31: 16–30.

    Article  CAS  PubMed  Google Scholar 

  • Kim, S. C., D. J. Crawford, J. Francisco-Ortega & A. Santos-Guerra. 1996. A common origin for woody Sonchus and five related genera in the Macaronesian islands: Molecular evidence for extensive radiation. Proceedings of the National Academy of Sciences 93: 7743–7748.

    Article  CAS  Google Scholar 

  • ———, ———, M. Tadesse, M. Berbee, F. R. Ganders, M. Pirseyedi & E. J. Esselman. 1999. ITS sequences and phylogenetic relationships in Bidens and Coreopsis (Asteraceae). Systematic Botany 24: 480–493.

    Article  Google Scholar 

  • Kim, Y. -D. & R. K. Jansen. 1996. Phylogenetic implications of rbcL and ITS sequence variation in the Berberidaceae. Systematic Botany 21: 381–396.

    Article  Google Scholar 

  • ——— & ———. 1998. Chloroplast DNA restriction site variation and phylogeny of the Berberidaceae. American Journal of Botany 85: 1766–1778.

    Article  CAS  Google Scholar 

  • ———, S. -H. Kim, C. H. Kim & R. K. Jansen. 2004b. Phylogeny of Berberidaceae based on sequences of the chloroplast gene ndhF. Biochemical Systematics and Ecology 32: 291–301.

    Article  CAS  Google Scholar 

  • Kitin, P., Y. Sano & R. Funada. 2002. Fusiform cells in the cambium of Kalopanax pictus are exclusively mononucleate. Journal of Experimental Botany 53: 483–488.

    Article  CAS  PubMed  Google Scholar 

  • ———, R. Funada, Y. Sano & J. Ohtani. 2000. Analysis by confocal microscopy of the structure of cambium in the hardwood Kalopanax pictus. Annals of Botany 86: 1109–1117.

    Article  Google Scholar 

  • Kling, G. J., C. P. Lindsey, M. E. Zampardo, G. D. By & L. L. Hayden. 2008. Mahonia bealei (leatherleaf mahonia). UIPlants: Woody Ornamentals. University of Illinois at Urbana-Campaign. Urbana-Campaign, IL. Available from http://woodyplants.nres.uiuc.edu [Accessed: September 24, 2008].

  • Knox, E. B. & J. D. Palmer. 1995. The origin of Dendrosenecio within the Senecioneae (Asteraceae) based on chloroplast DNA evidence. American Journal of Botany 82: 1567–1573.

    Article  Google Scholar 

  • Kribs, D. A. 1935. Salient lines of structural specialization in the wood rays of dicotyledons. Botanical Gazette 96: 547–557.

    Article  Google Scholar 

  • ——— 1937. Salient lines of structural specialization in the wood parenchyma of dicotyledons. Bulletin of the Torrey Botanical Club 64: 177–187.

    Article  Google Scholar 

  • Kron, K., W. Judd, P. Stevens, D. Crayn, A. Anderberg, P. Gadek, C. Quinn & J. Luteyn. 2002. Phylogenetic classification of Ericaceae: Molecular and morphological evidence. The Botanical Review 68: 335–423.

    Article  Google Scholar 

  • Krumbiegel, A. & A. Kästner. 1993. Sekundäres Dickenwachstum von Sproß und Wurzel bei annuellen dicotylen. Österreichische Akademie der Wissenschaften, Biosystematics and Ecology Series 4: 1–49.

    Google Scholar 

  • Kumazawa, M. 1930. Morphology and biology of Glaucidium palmatum Sieb. et Zucc. with notes of affinities to the allied genera Hydrastis, Podophyllum, and Diphylleia. Journal of the Faculty of Science, University of Tokyo. Botany 2: 345–380.

    Google Scholar 

  • Landman, N. 1988. Heterochrony in ammonites. Pp 159–182. In: M. L. McKinney (ed). Heterochrony in evolution: A multidisciplinary approach. Plenum Press, New York, NY.

    Google Scholar 

  • Lens, F., I. Groeninckx, E. Smets & S. Dessein. 2009. Woodiness within the Spermacoceae-Knoxieae alliance (Rubiaceae): Retention of the basal woody condition in Rubiaceae or recent innovation? Annals of Botany 103: 1049–1064.

    Article  PubMed  Google Scholar 

  • ———, S. Dressler, S. Jansen, L. van Evelghem & E. Smets. 2005a. Relationships within balsaminoid Ericales: A wood anatomical approach. American Journal of Botany 92: 941–953.

    Article  Google Scholar 

  • ———, S. Jansen, P. Caris, L. Serlet & E. Smets. 2005b. Comparative wood anatomy of the primuloid clade (Ericales s.l.). Systematic Botany 30: 163–183.

    Article  Google Scholar 

  • ———, J. Schonenberger, P. Baas, S. Jansen & E. Smets. 2007. The role of wood anatomy in phylogeny reconstruction of Ericales. Cladistics 23: 229–254.

    Article  Google Scholar 

  • Linberg, D. 1988. Heterochrony in gastropods: A neontological view. Pp 197–216. In: M. L. McKinney (ed). Heterochrony in evolution: A multidisciplinary approach. Plenum Press, London.

    Google Scholar 

  • Liu, Y. B. & Q. B. Zhang. 2007. Growth rings of roots in perennial forbs in Duolun grassland, Inner Mongolia, China. Journal of Integrative Plant Biology 49: 144–149.

    Article  Google Scholar 

  • Loconte, H. & J. R. Estes. 1989. Phylogenetic systematics of Berberidaceae and Ranunculales (Magnoliidae). Systematic Botany 14: 565–579.

    Article  Google Scholar 

  • Mabberley, D. J. 1974. Pauchycauly, vessel-elements, islands and the evolution of arborescence in 'herbacous' families. New Phytologist 73: 977–984.

    Article  Google Scholar 

  • Maddison, W. P. & D. R. Maddison. 2009. Mesquite: A modular system for evolutionary analysis.

  • Mauseth, J. D. 1988. Plant anatomy. Benjamin Cummings, Meno Park, CA, USA. Version 2.0 http://mesquiteproject.org.

    Google Scholar 

  • ———. 2004. Wide-band tracheids are present in almost all species of Cactaceae. Journal of Plant Research 117: 69–76.

    Article  PubMed  Google Scholar 

  • ———. 2006a. Wood in the cactus subfamily Opuntioideae has extremely diverse structure. Bradleya 24: 93–106.

    Google Scholar 

  • ———. 2006b. Structure-function relationships in highly modified shoots of Cactaceae. Annals of Botany 98: 901–926.

    Article  PubMed  Google Scholar 

  • ——— & B. J. Plemons. 1995. Developmentally variable, polymorphic woods in Cacti. American Journal of Botany 82: 1199–1205.

    Article  Google Scholar 

  • ——— & B. J. Plemons-Rodriguez. 1998. Evolution of extreme xeromorphic characters in wood: A study of nine evolutionary lines in Cactaceae. American Journal of Botany 85: 209–218.

    Article  Google Scholar 

  • ——— & M. E. Stone-Palmquist. 2001. Root wood differs strongly from shoot wood within individual plants of many Cactaceae. International Journal of Plant Sciences 162: 767–776.

    Article  Google Scholar 

  • McKinney, M. L. 1988. Classifying heterochrony allometry, size, and time. Pp 17–34. In: M. L. McKinney (ed). Heterochrony in evolution: A multidisciplinary approach. Plenum Press, London.

    Google Scholar 

  • McNamara, K. J. 1986. A guide to the nomenclature of heterochrony. Journal of Paleontology 60: 4–13.

    Google Scholar 

  • ——— & M. L. McKinney. 2005. Heterochrony, disparity, and macroevolution. Paleobiology 31: 17–26.

    Article  Google Scholar 

  • Meacham, C. A. 1980. Phylogeny of the Berberidaceae with an evaluation of classifications. Systematic Botany 5: 149–172.

    Article  Google Scholar 

  • Melzer, S., F. Lens, J. Gennen, S. Vanneste, A. Rohde & T. Beeckman. 2008. Flowering-time genes modulate meristem determinacy and growth form in Arabidopsis thaliana. Nature Genetics 40: 1489–1492.

    Article  CAS  PubMed  Google Scholar 

  • Metcalfe, C. R. & L. Chalk. 1950. Anatomy of the dicotyledons. Oxford University Press, London.

    Google Scholar 

  • Meylan, B. A. & B. G. Butterfield. 1978. The structure of New Zealand woods. Science Information Division, New Zealand Department of Scientific and Industrial Research, Wellington, NZ.

    Google Scholar 

  • Miller, S. 2003. NAPPO—PRA/Grains Panel Pest Fact Sheet—Ranunculus repens L. North American Plant Protection Organization, Ottawa. http://www.nappo.org/PRA-sheets/Ranunculusrepens.pdf.

    Google Scholar 

  • Minitab Inc. 2006. Minitab statistical software. Minitab, State College, PA.

  • Moore, M. J., J. Francisco-Ortega, A. Santos-Guerra & R. K. Jansen. 2002. Chloroplast DNA evidence for the roles of island colonization and extinction in Tolpis (Asteraceae: Lactuceae). American Journal of Botany 89: 518–526.

    Article  Google Scholar 

  • Mort, M. E., D. J. Crawford & K. N. Fairfield. 2004. Phylogeny and character evolution in California Coreopsis (Asteraceae): Insights from morphology and from sequences of the nuclear and plastid genomes. Systematic Botany 29: 781–789.

    Article  Google Scholar 

  • ———, D. E. Soltis, P. S. Soltis, J. Francisco-Ortega & A. Santos-Guerra. 2002. Phylogenetics and evolution of the Macaronesian clade of Crassulaceae inferred from nuclear and chloroplast sequence data. Systematic Botany 27: 271–288.

    Google Scholar 

  • Munz, P. A. 1974. A flora of southern California. University of California Press, Berkeley, CA.

    Google Scholar 

  • Myers, L. 1924. Tyloses in Menispermum. Botanical Gazette 78: 453–457.

    Article  Google Scholar 

  • Nieminen, K. M., L. Kauppinen & Y. Helariutta. 2004. A weed for wood? Arabidopsis as a genetic model for xylem development. Plant Physiology 135: 653–659.

    Article  CAS  PubMed  Google Scholar 

  • Novak, J. & C. Lemmon. 2005. Blue cohosh (Caulophylum thalictroides), goldthread (Coptis trifolia). Connecticut Wildflowers. Available from http://www.ct-botanicalsociety.org [Accessed: October 15, 2008].

  • Oh, S., S. Park & K. H. Han. 2003. Transcriptional regulation of secondary growth in Arabidopsis thaliana. Journal of Experimental Botany 54: 2709–2722.

    Article  CAS  PubMed  Google Scholar 

  • Olson, M. E. 2003. Stem and leaf anatomy of the arborescent Cucurbitaceae Dendrosicyos socotrana with comments on the evolution of pachycauls from lianas. Plant Systematics and Evolution 239: 199–214.

    Article  Google Scholar 

  • ———. 2007. Wood ontogeny as a model for studying heterochrony, with an example of paedomorphosis in Moringa (Moringaceae). Systematics and Biodiversity 5: 145–158.

    Article  Google Scholar 

  • Panshin, A. J. & C. de Zeeuw. 1970. Textbook of wood technology. McGraw Hill, New York, NY.

    Google Scholar 

  • Qiu, Y. L., M. W. Chase, D. H. Les & C. R. Parks. 1993. Molecular phylogenetics of the Magnoliidae—Cladistic analyses of nucleotide-sequences of the plastid gene rbcL. Annals of the Missouri Botanical Garden 80: 587–606.

    Article  Google Scholar 

  • Radford, A. E., H. E. Ahles & C. R. Bell. 1968. Manual of the vascular flora of the Carolinas. University of North Carolina Press, Chapel Hill, NC.

    Google Scholar 

  • Rajput, K. S. & K. S. Rao. 1998. Cambial anatomy and absence of rays in the stem of Boerhaavia species (Nyctaginaceae). Annales Botanici Fennici 35: 131–135.

    Google Scholar 

  • ——— & ———. 1999. Structural and development studies on cambial variant in Pupalia lappacea (Amaranthaceae). Annals of Botany Fennici 36: 137–141.

    Google Scholar 

  • Ramsey, F. L. & D. W. Schafer. 2002. The statistical sleuth: A course in methods of data analysis. Duxbury Press, Pacific Grove, CA.

    Google Scholar 

  • Raunkiær, C. 1904. Om biologiske Typer, med Hensyn til Planternes Tilpasninger til at overleve ugunstige Aarstide. Botanisk Tidsskrift 26: 14.

    Google Scholar 

  • ——— 1934. Life forms of plants and statistical plant geography. Clarendon, Oxford.

    Google Scholar 

  • Reed, D. 2004. Yellowroot (Xanthorhiza simplicissima). Wildflowers of the Southeastern United States. Available from http://2bnthewild.com/index2.shtml [Accessed: September 24, 2008].

  • Rehder, A. 2001. Manual of cultivated trees and shrubs. The Blackburn Press, Caldwell, NJ.

    Google Scholar 

  • Ritter, M. E. 2006. The physical environment: An introduction to physical geography. Available from http://www.uwsp.edu/geo101/textbook/title_page.html [Accessed: August 23, 2009].

  • Rowe, N., S. Isnard & T. Speck. 2004. Diversity of mechanical architectures in climbing plants: An evolutionary perspective. Journal of Plant Growth Regulation 23: 108–128.

    Article  CAS  Google Scholar 

  • Ruzin, S. E. 1999. Plant microtechnique and microscopy. Oxford University Press, Cambridge.

    Google Scholar 

  • Sakai, A., T. Ohsawa & M. Ohsawa. 1995. Adaptive significance of sprouting of Euptelea polyandra, a deciduous tree growing on steep slopes with shallow soil. Journal of Plant Research 108: 377–386.

    Article  Google Scholar 

  • Saylor, J. 2008. Dahlia coccinea. MSUplants.com. Michigan State University. East Lansing, MI. Available from http://msuplants.com/pd.asp?pid=618 [Accessed: November 7, 2008].

  • Schmid, W. G. 2002. An encyclopedia of shade perennials. Timber Press, Portland, OR.

  • Schweingruber, F. H. 2006. Anatomical characteristics and ecological trends in the xylem and phloem of Brassicaceae and Resedacae. IAWA Journal 27: 419–442.

    Google Scholar 

  • ———. 2007a. Stem anatomy of Caryophyllaceae. Flora 202: 281–292.

    Google Scholar 

  • ———. 2007b. Wood structure and environment. Springer, Berlin.

    Google Scholar 

  • ——— & P. Poschlod. 2005. Growth rings in herbs and shrubs: Life span, age determination and stem anatomy. Forest Snow and Landscape 79: 165–415.

    Google Scholar 

  • ——— & W. Landolt. 2005–2008. The xylem database. Swiss Federal Institute for Forest, Snow and Landscape Research. Available from http://www.wsl.ch/dendro/xylemdb/index.php [Accessed: 15 September 2009].

  • Seiler, J. R., E. C. Jensen & J. A. Peterson. 2008. Yellowroot. VT Tree ID. Virginia Polytechnic Institute and State University. Blacksburg, VA. Available from http://www.cnr.vt.edu/dendro/dendrology/syllabus2/factsheet.cfm?ID=924 [Accessed: 15 September, 2009].

  • Senbeta, F., C. Schmitt, M. Denich, S. Demissew, P. L. G. Velk, H. Preisinger, T. Woldemariam & D. Teketay. 2005. The diversity and distribution of lianas in the Afromontane rain forests of Ethiopia. Diversity and Distributions 11: 443–452.

    Article  Google Scholar 

  • Shen, Y.-F. 1954. Phylogeny and wood anatomy of Nandina. Taiwania 5: 85–92.

    Google Scholar 

  • Sherff, E. 1936. Revision of the genus Coreopsis. Field Museum of Natural History, Chicago, IL.

    Google Scholar 

  • Sinclair, A. & P. Catling. 2001. Cultivating the increasingly popular medicinal plant, goldenseal: Review and update. American Journal of Alternative Agriculture 16: 131–140.

    Article  Google Scholar 

  • Smith, E. B. 1975. Chromosome numbers of North-American Coreopsis with phyletic interpretations. Botanical Gazette 136: 78–86.

    Article  Google Scholar 

  • ———. 1984. Biosystematic study and typification of the Californian Coreopsis (Compositae) sections Tuckermannia, Pugiopappus, and Euleptosyne. SIDA Contributions to Biology 10: 276–289.

    Google Scholar 

  • Sperry, J. S. 2003. Evolution of water transport and xylem structure. International Journal of Plant Sciences 164: S115–S127.

    Article  Google Scholar 

  • ———, U. G. Hacke & J. Pittermann. 2006. Size and function in conifer tracheids and angiosperm vessels. American Journal of Botany 93: 1490–1500.

    Article  Google Scholar 

  • SPSS. 2006. SPSS Base 15 Users Guide. SPSS Inc., Chicago, IL.

    Google Scholar 

  • Stebbins, G. L. 1938. Cytological characteristics associated with the different growth habits in the dicotyledons. American Journal of Botany 25: 189–198.

    Article  Google Scholar 

  • Swearingen, J., A. Reese & R. Lyons. 2006. Fiveleaf Akebia (Akebia quinata). Plant Conservation Alliance, Alien Plant Working Group. Available from http://nps.gov/plants/ALIEN/fact/akqu1.htm [Accessed: October 15, 2008].

  • Swenson, U. & U. Manns. 2003. Phylogeny of Pericallis (Asteraceae): A total evidence approach reappraising the double origin of woodiness. Taxon 52: 533–546.

    Article  Google Scholar 

  • Swofford, D. L. & D. P. Begle. 1993. User manual for PAUP: Phylogenetic Analysis Using Parsimony, Version 3.1. Smithsonian Institution, Washington, DC.

    Google Scholar 

  • Takhtajan, A. 1997. Diversity and classification of flowering plants. Columbia University Press, New York, N.Y.

    Google Scholar 

  • Tamura, M. 1993. Ranunculaceae. In: K. Kubitzki, J. G. Rohwer, & V. Bittrich (eds.), The families and genera of flowering plants II: Flowering plants - dicotyledons. Springer, Berlin.

  • Tani, T., H. Kudoh & N. Kachi. 2001. Responses of photosynthesis and biomass allocation of an understorey herb, Pteridophyllum racemosum, to gradual increases in irradiance. Annals of Botany 88: 393–402.

    Article  Google Scholar 

  • Thorne, R. F. 1969. California islands. Annals of the Missouri Botanical Garden 56: 391–408.

    Article  Google Scholar 

  • Tilman, D. 1988. Plant strategies and the dynamics and structure of plant communities. Princeton University Press, Princeton, NJ.

    Google Scholar 

  • Tippo, O. 1938. Comparative anatomy of the Moraceae and their presumed allies. Botanical Gazette 100: 1–99.

    Article  Google Scholar 

  • Turner, M. & P. Gustafson. 2006. Wildflowers of the Pacific Northwest. Timber Press, Portland, OR.

    Google Scholar 

  • USDA & NRCS. 2009. The PLANTS Database. USDA Natural Resource Conservation Service, National Plant Data Center. Baton Rouge, LA. Available from http://plants.usda.gov [Accessed: 15 September, 2009].

  • Vivar-Evans, S., V. L. Barradas, M. E. Sanchez-Coronado, A. G. de Buen & A. Orozco-Segovia. 2006. Ecophysiology of seed germination of wild Dahlia coccinea (Asteraceae) in a spatially heterogeneous fire-prone habitat. Acta Oecologica 29: 187–195.

    Article  Google Scholar 

  • von Arx, G. & H. Dietz. 2006. Growth rings in the roots of temperate forbs are robust annual markers. Plant Biology 8: 224–233.

    Article  Google Scholar 

  • Wagner, W. H. J. 1969. The construction of a classification. Pp 67–103. In: C. Sibley (ed). Systematic Biology. National Academy of Sciences, Washington, D.C.

    Google Scholar 

  • Wallace, A. R. 1878. Tropical nature and other essays. MacMillan and Company, London.

    Google Scholar 

  • Walton, G. B. & L. Hufford. 1994. Shoot architecture and evolution of Dicentra cucullaria (Papaveraceae, Fumarioideae). International Journal of Plant Sciences 155: 553–568.

    Article  Google Scholar 

  • Wheeler, E. A. & P. Baas. 1991. A survey of the fossil record for dicotyledonous wood and its significance for evolutionary and ecological wood anatomy. IAWA Journal 12: 275–332.

    Google Scholar 

  • Wheeler, J. K., J. S. Sperry, U. G. Hacke & N. Hoang. 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.

    Article  Google Scholar 

  • Woodson, R. E., Jr. 1928. Dysoma: A new species of Berberidaceae. Annals of the Missouri Botanical Garden 15: 335–340.

    Article  Google Scholar 

  • Xiao, M., Q. Li, L. Guo, T. Luo, W. -X. Duan, W. -X. He, L. Wang & F. Chen. 2006. AFLP analysis of genetic diversity of the endangered species Sinopodophyllum hexandrum in the Tibetan region of Sichuan Province, China. Biochemical Genetics 44: 44–57.

    Article  CAS  Google Scholar 

  • Ye, Z.-H. 2002. Vascular tissue differentiation and pattern formation in plants. Annual Review of Plant Biology 53: 183–202.

    Article  CAS  PubMed  Google Scholar 

  • Ying, T.-S., D. E. Boufford & A. R. Brach. 2010. Berberidaceae (Draft). In: Z.-Y. Wu, P.H. Raven, & D.-Y. Hong (eds.), Flora of China: Lentibulariaceae-Dipsacaceae.19: Missouri Botanical Garden Press, St. Louis, MO. Available from http://hua.huh.harvard.edu/china/mss/volume19/Berberidaceae-AGH_final.htm.

Download references

VII. Acknowledgements

We are grateful for the assistance we received while carrying out this research. Pete Diamond (formerly with the NC Zoo), assisted with the collection of Xanthorhiza simplicissima, Holly Forbes (UC Berkeley Botanical Garden), provided specimens of Coreopsis gigantea, and Matina Kalcounis-Rűppell (UNC Greensboro) allowed the collection of Mahonia bealei on her property in Greensboro, NC. We are especially grateful to Sherwin Carlquist for his many comments, and for his encouragement during the research and writing process. Fritz Schweingruber, Frederick Lens, James Mauseth, David Remington, Pieter Baas, John Sperry, Philip Garnock-Jones, Katherine Kron, Norm Douglas, and Jian-Yong Wu all provided data or comments that greatly improved the manuscript. Fritz Schweingruber provided access to unpublished data on wood anatomy of the Brassicaceae, some of which is presented in Table 1. This paper is based, in part, on a Thesis submitted by the first author to the University of North Carolina at Greensboro in partial fulfillment of the requirements for an M.S. degree. We thank David Remington and Dennis LaJeunesse for providing guidance during this process. Funding for the research was provided by grants from the Student Research Support Fund of the Department of Biology, UNCG. All responsibility for the opinions expressed here rests with the authors.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Bruce K. Kirchoff.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dulin, M.W., Kirchoff, B.K. Paedomorphosis, Secondary Woodiness, and Insular Woodiness in Plants. Bot. Rev. 76, 405–490 (2010). https://doi.org/10.1007/s12229-010-9057-5

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12229-010-9057-5

Keywords

Navigation