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Branching Morphology, Vascular Bundle Arrangement and Ontogenetic Development in Leaf Insertion Zones and Ramifications of Three Arborescent Araliaceae Species

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Branching Morphology, Vascular Bundle Arrangement and Ontogenetic Development in Leaf Insertion Zones and Ramifications of Three Arborescent Araliaceae Species Trees DOI 10.1007/s00468-017-1585-8 ORIGINAL ARTICLE Branching morphology, vascular bundle arrangement and ontogenetic development in leaf insertion zones and ramifications of three arborescent Araliaceae species 1,2 3 1,2,4 1,2,4 Katharina Bunk • Siegfried Fink • Thomas Speck • Tom Masselter Received: 24 January 2017 / Accepted: 3 July 2017 Ó The Author(s) 2017. This article is an open access publication Abstract the woody strands in the stem–branch attachment regions. Key message A conspicuous ‘finger-like’ branching Via high-resolution microscopy of serial thin-sections and morphology is described for three arborescent Arali- 3D reconstructions, as well as cryotome sections, aceae species with a focus on the three-dimensional anatomical analysis was carried out of the course and vascular bundle arrangement in leaf insertion and arrangement of vascular bundles through leaf insertions stem–branch attachment regions during ontogenetic and later developing ramifications, including a comparative development. analysis of the different ontogenetic stages. All three spe- Abstract The central aim of this study is to gain a deeper cies investigated present a ‘finger-like’ branching mor- understanding of the structure and development in leaf phology with variations in the number and arrangement of insertions and stem–branch attachments of the arborescent the woody strands. Thin-sectioning reveals a conspicuous Araliaceae species: Schefflera arboricola, Fatsia japonica pattern of leaf trace emergence from the main stem, pro- and Polyscias balfouriana. Therefore, the vascular bundle ceeding into the leaf and the early developing ramifica- arrangement in the leaf insertion zone and ontogenetic tions. Vascular bundle derivatives contribute to the development of the stem–branch attachment after decapi- vascular integration of leaves and axillary buds. The tation were analyzed, with a special focus on their con- described ‘finger-like’ branching morphology in the spicuous ‘finger-like’ branching morphology that, to our investigated Araliaceae species represents a sophisticated knowledge, is unique to the Araliaceae. Decortication of mode of vascular integration in leaf insertion zones and adult ramifications allows for a morphological analysis of developing ramifications. In combination with forthcoming biomechanical experiments, this analysis shall serve as a Communicated by E. Beck. basis for biomimetic translations into textile technology (fiber-reinforced branched composite materials) and civil Electronic supplementary material The online version of this engineering (optimization of branched building structures). article (doi:10.1007/s00468-017-1585-8) contains supplementary material, which is available to authorized users. Keywords Araliaceae Á Branching Á Fatsia japonica Á & Katharina Bunk Polyscias balfouriana Á Schefflera arboricola Á Vascular [email protected] bundles 1 Plant Biomechanics Group, Botanic Garden, University of Freiburg, Scha¨nzlestr. 1, 79104 Freiburg/Breisgau, Germany Introduction 2 Freiburg Center for Interactive Materials and Bioinspired Technologies, University of Freiburg, Georges-Ko¨hler-Allee 105, 79110 Freiburg/Breisgau, Germany The ability to branch is one of the key features in many 3 Chair of Forest Botany, University of Freiburg, Bertoldstr. woody plants, as it enables an optimal arrangement of 17, 79085 Freiburg/Breisgau, Germany photosynthetic tissues and the formation of a complex 4 Competence Network Biomimetics, Scha¨nzlestr. 1, stem and crown. Vascular continuity and mechanical 79104 Freiburg/Breisgau, Germany stability of ramifications have to be ensured in all 123 Trees ontogenetic phases and numerous optimized stem–branch 1983, 1984, 1986a, b; Tomlinson et al. 2005;Schwager attachments have evolved to meet these challenging et al. 2015) and may result in conspicuous branching demands. The analysis of the morphology, anatomy and morphologies, such as in the Araliaceae genus Schefflera biomechanics of botanical ramifications has become of (Tomlinson et al. 2005). In the present study, a special increasing interest in recent years (Mattheck 1991; Niklas focus is laid on the analysis of the branching morphol- 1992; Burgert and Jungnikl 2004; Achim et al. 2006; ogy of Schefflera ramifications which has been described Tomlinson et al. 2005;Mu¨ller et al. 2006; Jungnikl et al. by Tomlinson et al. (2005), as well as two related 2009; Masselter and Speck 2011; Masselter et al. Araliaceae species. Decorticated ramifications display a 2011, 2015, 2016; Theckes et al. 2011;Mu¨ller et al. 2013; ‘finger-like’ progression of woody segments (Fig. 1c–e, Schwager et al. 2013; Haushahn et al. 2014). Compre- h–j, m–o), representing highly lignified vascular bundles, hending the development of botanical ramifications and originally indicating cortical leaf traces (Tomlinson et al. identifying the central concepts of their structure also 2005). These leaf traces are arranged in the same order allow for biomimetic implementations into technical fiber- and position as the later developing woody strands and reinforced materials. form ‘templates’ for their development (Tomlinson et al. A functional understanding of leaf insertion zones and 2005). Tomlinson et al. (2005) have focused on the stem–branch attachments requires the visualization of anatomy of leaf traces and undeveloped axillary buds in the course and arrangement of the continuous vascular Schefflera, and furthermore proposed a conclusive system from the main stem into the leaf, axillary bud schematic ontogenetic scenario of vascular branch and side branches. Conspicuous ramifications with a attachment, via traces of subtending leaves and acces- high potential for biomimetic implementation have been sory bundles. However, time specification and validation found in dicotyledons, such as columnar cacti (Schwager by actual histological samples are lacking. This study et al. 2013), as well as in the monocotyledon genus will address the following questions, which are to be Dracaena (Masselter et al. 2011;Haushahnetal.2014; clarified within the context of leaf insertion vascularity Hesse et al. 2016), in which the visualization of vascular and branch development in Schefflera and related bundle progression was performed via light microscopy Araliaceae genera: (Haushahn et al. 2014) and magnetic resonance imaging 1. Morphological analysis: is the ‘finger-like’ ramifica- (MRI) of the stem–branch attachment region (Masselter tion an exclusive trait of the genus Schefflera or is this et al. 2015, 2016; Hesse et al. 2016). For the first time, morphology also detectable in the species Fatsia MRI imaging allowed analysis of living ramifications japonica and Polyscias balfouriana of the Araliaceae? under load and comparison with the unloaded situation 2. Anatomical analysis: according to which three-dimen- (Masselter et al. 2015, 2016; Hesse et al. 2016). sional pattern are the vascular bundles arranged in the To the best of our knowledge, dicotyledonous leaf region between the main stem, the leaf insertion and insertion regions, ramifications or fiber arrangements the axillary bud, as the origin of developing branches other than those of columnar cacti (Schwager et al. in Schefflera arboricola, F. japonica and P. balfouri- 2013)andOpuntia (Bouakba et al. 2013) have not been ana, 3 weeks after decapitation? investigated in the context of biomimetic applications to 3. Ontogenetic analysis: how are stem–branch attach- fiber technology, excluding research, for example, in the ments developing from leaf insertion regions in S. clothing industry, on branched fibers in so-called ‘plant- arboricola, F. japonica and P. balfouriana after structured textile fabrics’ for optimizing water transport branch development induced via apex decapitation? properties (Fan et al. 2007;Sarkaretal.2009;Chen To what extent can the ontogenetic scheme of branch et al. 2012). Lignified vascular bundles in dicotyledons attachment proposed by Tomlinson et al. (2005)be are mostly arranged in a distinct vascular cylinder from substantiated by these experimental studies? which they proceed into the branch (Shigo 1985;Slater and Harbinson 2010) and are not distributed in a The analysis of ramifications in these three Araliaceae parenchymatous matrix, as for example, shown in Dra- species (Fig. 1c–e, h–j, m–o) and the identification of caena (Haushahn et al. 2014; Hesse et al. 2016;Mas- fundamental functional principles of load-adapted fiber selter et al. 2016). Nevertheless, the morphology and orientation shall also serve for a biomimetic translation of ontogenetic development of a coherent vascular system this conspicuous branching morphology. Our objective is from a main stem into a side axis in dicotyledons is of to implement these functional principles into the develop- high interest in the context of novel structures to be used ment of biomimetic fiber-reinforced plastic (FRP) tubes as in fiber-reinforced materials, as it often involves the reinforcing coatings for branched concrete structures in contribution of various vascular bundle derivatives architecture and constructional engineering (Born et al. (Zimmermann and Tomlinson 1972;Larson2016). 123 Trees Fig. 1 Growth habit and branching morphology of Schefflera japonica. i Top view of decorticated ramification of F. japonica. arboricola, Fatsia japonica and Polyscias balfouriana. a Growth j View of decorticated ramification of F. japonica from underneath habit of S. arboricola. Examined ramification is highlighted with a the branching. Exemplary scars of leaf traces
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