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Mechanical Architecture and Development in Clematis

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Mechanical Architecture and Development in Clematis Research MechanicalBlackwell Publishing Ltd. architecture and development in Clematis: implications for canalised evolution of growth forms S. Isnard1, T. Speck2 and N. P. Rowe1 1Botanique et Bioinformatique de l’Architecture des Plantes, UMR 5120 CNRS, TA40/PS2, Boulevard de la Lironde, 34398 Montpellier, France; 2Plant Biomechanics Group, Institute for Biology II, Botanical Garden of the Albert-Ludwigs-Universität, Schänzlestrasse 1, D-79104 Freiburg, Germany Summary Author for correspondence: • Mechanical architectures of two Clematis species, the herbaceous perennial S. Isnard Clematis recta and the woody liana, Clematis vitalba, were investigated and + Tel: 33 (0) 467617553 compared with the woody rhizomatous sand dune plant Clematis flammula var. Fax: +33 (0) 467615668 Email: [email protected] maritima. • Bending mechanical properties of stems from various developmental stages were Received: 25 September 2002 compared and related to stem geometry and relative proportions of tissues during Accepted: 28 February 2003 development. doi: 10.1046/j.1469-8137.2003.00771.x • Clematis vitalba and C. flammula var. maritima showed mechanical architectures with reductions in structural Young’s modulus of the stem during ontogeny. Irrever- sible loss of stem rigidity was mediated by disruption, separation and eventual loss of primary phloem fibres via secondary growth of the periderm and cambial activity. Each species showed variations of non-self-supporting mechanical architecture relating to specific habitat preferences. In aerial stems of C. recta the structural Young’s modulus remained approximately constant during ontogeny, a mechanical signal characteristic for semi-self-supporting architectures. •Woody aerial plant stems are extremely rare in the Ranunculaceae and seldom, if ever, show self-supporting characteristics. Growth form evolution in the group may have been canalised by evolution of rhizomatous geophytic growth forms with secondary growth confined to underground stems specialized for water conduction, storage and perennation. Variation of this ground plan includes climbing, straggling or rhizomatous architectures but not self-supporting shrubs or trees with secondary growth generating requisite self-supporting mechanical properties. Certain body plan organisations appear to have inbuilt mechanical constraints which may have profound effects on the subsequent evolution of growth forms. Key words: architecture, biomechanics, canalised evolution, Clematis, growth form. © New Phytologist (2003) 158: 543–559 development and anatomy can be viewed in an evolutionary Introduction context (Rowe & Speck, 2003; Speck et al., 2003). Mechanical properties of plant stems and the changes of these The modification in stems of parameters such as flexural properties during stem development are increasingly being stiffness (EI ) and structural Young’s modulus (Estr) between used to investigate the variation and diversity of plant growth young and old stages of development can distinguish different forms (Speck & Rowe, 1999). Such studies can characterize mechanical architectures such as ‘self-supporting’ and ‘non- and distinguish different growth forms and demonstrate how self-supporting’ plants. In self-supporting plants, the struc- various mechanical strategies are deployed by different plants tural Young’s modulus increases during ontogeny from young (Gartner, 1991a, 1991b). More recently such studies have to old stages and in non-self-supporting plants, structural been combined with phylogenetic studies in which trends Young’s modulus decreases (Speck & Rowe, 1999). This in mechanical properties underlying changes in plant approach has detected a third type of growth form in which © New Phytologist (2003) 158: 543–559 www.newphytologist.com 543 544 Research structural Young’s modulus does not change significantly annual shoots dominated by primary development. Clematis during development of the stem. This has been termed ‘semi- is positioned along with Ranunculus, Trautvettaria and self-supporting’ in which plants simply lean against the sur- Anemone within the Ranunculoideae ( Johansson & Jansen, rounding vegetation. Biomechanical architectures of living 1993; Hoot, 1995; Johansson, 1995; Hoot et al., 1999), plants are investigated by 2-, 3- or 4-point bending tests. which is possibly sister to a second distal group including These methods are now combined with studies, which inves- genera such as Helleborus, Trollius and Caltha. All of these tigate patterns of tissue development from young to old stages genera are predominantly herbaceous or perennial rhizome- and to correlate primary and secondary tissue development forming plants apart from Clematis, which includes perennial with changes in mechanical properties of the stem system. rhizomatous herbs, climbers and some woody species Recent studies have shown that, within each type of described as shrubs or subshrubs. Species of Clematis mechanical architecture, the exact type of signal can vary. described as shrubs include Clematis davidiana, Clematis stans, Such changes can include global values of mechanical para- Clematis addisonii, Clematis integrifolia and Clematis meters as well as the exact timing and trend of change in a heracleifolia (Walters et al., 1989). Inspection of the precise parameter during ontogeny (Speck & Rowe, 1999). For growth forms of the two latter species indicate that the former example, trees and shrubs show two different types of increase is a perennating rhizomatous species with upright, primary in Estr during ontogeny and both have self-supporting growth stems; C. heracleifolia is a low, much branched shrub with forms. In trees an increase in structural Estr is seen throughout flexible aerial axes that barely remains upright for lengths of the entire ontogeny of the plant, albeit only slightly towards more than a metre. Further members of the Ranunculaceae the end of the tree’s growth. In shrubs, Estr levels off although include the genera Aquilegia, Coptis, Isopyrum, Thalictrum stem thickening continues up to the end of growth of the and Xanthorhiza, which form a paraphyletic group, the stem. While secondary growth can play an important role in ‘Thallictroideae’, occurring just above the basal group of changes in stem biomechanics during growth of woody Hydrastis and Glaucidium. These are all perennial herbs with plants, primary differentiation and growth is also important. tuberous, rhizomatous or creeping rhizomatous stems and Young stages of growth of woody plants as well as herbaceous upright annual primary stems. Xanthorhiza is often referred to growth forms lacking secondary growth rely on primary tis- as a woody shrub or subshrub; the single occurring species sues for mechanical support (Niklas, 1990, 1992; Speck & Xanthorhiza simplicissima forms an extensive rhizomatous Vogellehner, 1994; Rowe & Speck, 1997). It is of considerable network producing weakly upright woody stems rarely interest to know what mechanical strategies occur among her- exceeding 60 cm in height. Most members of the Ranun- baceous plants and in what ways these differ from those with culaceae are therefore herbs or tuber/rhizome-forming secondary growth. From an evolutionary perspective, transi- herbs with aerial shoots mostly confined to relatively short- tions between architectures dominated by primary and sec- lived annual stems with primary growth. Secondary growth, ondary growth essentially combine profound changes in body if there is any, is mostly confined to underground organs. The plan organisation with potentially far-reaching effects on the exceptions cited above, may be described as ‘weakly shrubby’ ecology and further evolution of mechanical architectures in view of the fact that the aerial stems are woody, but do not (Niklas, 1997; Bateman et al., 1998; Niklas & Speck, 2001; support strongly self-supporting woody axes above up to a Rowe & Speck, 2003). Are clades that have evolved a lianoid metre in length or height. In the Ranunculaceae, woodiness growth habit capable of returning to a fully self-supporting has been described as secondary ( Judd et al., 2002). habit? Can clades with body plans modified into perennial underground rhizomes and aerial herbaceous axes evolve into Biomechanical approach self-supporting aerial stems with woody axes? Do climbers that have evolved from woody self-supporting ancestors show This study presents new biomechanical data on the archi- different mechanical strategies and properties from those that tecture of two species of Clematis including: Clematis vitalba have evolved from herbaceous or rhizomatous plants? L. and Clematis recta L. and discusses these results in the light of a recent study of Clematis flammula var. maritima L. (Isnard et al., 2003). The study follows previous initial Systematics of the Ranunculaceae and its growth forms reports (Speck, 1991, 1994) in which mechanical bending Clematis is a cosmopolitan genus of the Ranunculaceae tests on C. vitalba and C. recta were used for establishing and showing a range of growth forms mostly confined to per- comparing patterns of mechanical behaviour in non-self- ennial herbs and climbers among its 250 species. Recent supporting and semi-self-supporting plants. phylogenetic analyses indicate that the Ranunculaceae is In this account we compare biomechanical characteristics monophyletic (Hoot, 1995; Hoot et al., 1999) and placed in terms of the overall growth form, and then compare ana- within the Ranunculales among ‘basal tricolpates’. Basal tomical development
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