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Fibre Dimorphism: Cell Type Diversification As an Evolutionary Strategy in Angiosperm Woods

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Fibre Dimorphism: Cell Type Diversification As an Evolutionary Strategy in Angiosperm Woods bs_bs_banner Botanical Journal of the Linnean Society, 2014, 174, 44–67. With 9 figures Fibre dimorphism: cell type diversification as an evolutionary strategy in angiosperm woods SHERWIN CARLQUIST* FLS Santa Barbara Botanic Garden, 1212 Mission Canyon Road, Santa Barbara, CA 93105, USA Received 15 May 2013; revised 4 August 2013; accepted for publication 14 August 2013 Dimorphic fibres in angiosperm woods are designated when zones of two different kinds of fibres can be distinguished in transverse sections. The usage of most authors contrasts wider, thinner-walled, shorter (some- times storied) fibres with narrower, thicker-walled fibres that have narrower lumina. The wider fibres can be distinguished in longitudinal sections from axial parenchyma, which usually consists of strands of two or more cells each surrounded by secondary walls (and thus different from septate fibres). This phenomenon occurs in some Araliaceae, Asteraceae, Fabaceae, Myrtales (notably Lythraceae), Sapindales (especially Sapindaceae), Urticales and even some Gnetales. Additional instances can doubtless be found, especially if instances of wide latewood fibres together with narrow earlywood fibres are included. There is little physiological evidence on differential functions of dimorphic fibres, except in Acer, in which hydrolysis of starch in the wide fibres is known to result in transfer of sugar into vessels early in the growing season. Starch storage in axial parenchyma may, in a complementary way, serve for embolism reversal and prevention and thus for maintenance of the water columns. Crystalliferous fibres (Myrtales, Sapindales) can be considered a form of fibre dimorphism that deters predation. Gelatinous fibres, often equated with tension wood, can also be considered as a form of fibre dimorphism. The evolutionary significance of fibre dimorphism is that a few small changes in fibre structure can result in the accomplishment of diversified functions. © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 174, 44–67. ADDITIONAL KEYWORDS: Acer – aerating cells – axial parenchyma – crystalliferous fibres – gelatinous fibres. INTRODUCTION this definition woods in which earlywood fibres corre- spond to the wider fibres, with narrower fibres in The phenomenon of fibre dimorphism was first latewood. A large proportion of instances of fibre described in wood of helianthoid Asteraceae (Carlquist, dimorphism involve living fibres, either septate or 1958), and subsequently cited as a product of imper- nucleate, but without septa. This cursory description forate tracheary element evolution (Carlquist, 1961). does not include the full variety one observes, and the The concept has since been readily accepted, and has present account is designed to characterize fibre been recorded in wood anatomical monographs of dimorphism more fully so that the phenomenon can be families and genera of Myrtales, Sapindales and Urti- noted and mentioned more frequently. cales, as noted in detail below, but is likely to be found In searching for diversity of expressions of fibre more widely. In the usual sense, fibre dimorphism dimorphism, two other manifestations must inevita- consists of coexistence of zones of wide, thin-walled, bly be considered. Crystalliferous fibres are pertinent shorter fibres (usually libriform fibres, occasionally in this respect, and have been described for several fibre-tracheids) and zones of narrower, longer, thicker- families of Myrtales. An expanded consideration of walled fibres. These zones may not correspond at all to crystalliferous fibres and similar crystalliferous fibri- latewood and earlywood. However, one may include in form cells in wood is an additional concern of the present study. Likewise, gelatinous fibres (character- *E-mail: [email protected] istic of tension wood) and similar fibres with 44 © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 174, 44–67 FIBRE DIMORPHISM IN ANGIOSPERM WOOD 45 differentiation between inner- and outer-wall layers of view. When examining a transverse section, in fibriform cells should be included in the concept of however, wide libriform fibres (or fibre-tracheids) may fibre dimorphism. resemble axial parenchyma, and examination of lon- Fibre dimorphism can range from subtle to promi- gitudinal sections is necessary to distinguish between nent as seen in wood sections. To introduce the topic, wide, thin-walled libriform fibres and axial paren- the characteristics that may qualify under the rubric chyma strands. Radial sections are perhaps most of fibre dimorphism are each discussed. This is fol- useful in this respect. Tangential sections, however, lowed by a systematic section, in which genera that are required when one is deciding whether storying exemplify these characteristics are described and occurs in a given wood. Thus, the typical assemblage illustrated in detail. The full extent of fibre dimor- of transverse (cross), tangential and radial sections phism in angiosperm woods cannot be presented at that one commonly sees on permanent slides of woods this point. Wood of only a small fraction of woody is a requisite. Such sections, made with the typical species has been collected to date, and study of all of methods by means of sliding microtome techniques, those collections is not feasible. Before I explore account for the bulk of the collections cited below. angiosperms further for fibre dimorphism, we must be Although sections made from dried wood specimens aware of the range of characteristics that have thus can be entirely satisfactory in many cases, additional far been reported. Most angiosperm woods have important information (e.g. occurrence of nuclei and monomorphic fibres (= monomorphic imperforate tra- starch) can be obtained reliably only from liquid- cheary elements). In certain families, additional preserved material. Comparisons of liquid-preserved examples are likely to be discovered once workers and dried wood specimens of a given species often become familiar with the appearances cited here. show disappearance or alteration of starch during the Some preliminary patterns of systematic occurrence drying process because of hydrolysis and fungal and are evident and can be mentioned, however. Fibre microbial action. For liquid-preserved material in dimorphism in its various manifestations has arisen which thin cell walls are prevalent, the paraffin independently in a number of clades. methods described by Carlquist (1982) have been Fibre dimorphism can be interpreted in terms of followed. wood physiology and mechanics, together with other The term ‘fibre’ is used throughout this paper as a features of any given wood. Fibres can be distin- synonym for ‘imperforate tracheary element’. Most of guished from axial parenchyma in longitudinal sec- the species studied have libriform fibres; a few have tions (in a small number of species, there can be fibre-tracheids, and none was observed to have trac- admixture of the two cell types), and the probable heids. The correlation with libriform fibres is strong, physiological differences between axial parenchyma because nearly all instances of living (including and wide fibres can account for why fibre dimorphism septate) fibres involve libriform fibres. Living fibres should have evolved in a number of woods, rather have contents with potential physiological value and than simply an increase in the amount of axial paren- thereby evolutionary possibilities of more than a chyma. Dimorphism and polymorphism have occurred mechanical nature. Fibre dimorphism in the case of in several cell types. One can point to vessel origin gelatinous fibres (non-lignified fibres), however, from tracheids as a major instance of dimorphism in usually does not involve living fibres. a cell type, resulting in division of labour. Dimor- The collections studied are as follows. Araliaceae: phism in wood cells (vessels, tracheids, fibre- Aralia spinosa L., USw-12014. Asteraceae: Dubautia tracheids) has occurred repeatedly in angiosperm menziesii (A.Gray) D.D.Keck, Carlquist H17 (UC); woods (e.g. coexistence of vasicentric tracheids and D. platyphylla (A.Gray) D.D.Keck, J. W. H. 19188, libriform fibres as a result of tracheid dimorphism, 1948, University of Illinois; D. raillardioides Hillebr., Carlquist, 1988; vessel dimorphism in lianas, Carlquist H16 (UC); Wilkesia gymnoxiphium A.Gray, Carlquist, 1985). Such repatterning by means of cell Carlquist H10 (UC). Burseraceae: Santiria laevigata type diversification represents a salient feature of Blume, Yw-19880. Combretaceae: Combretum eryth- wood evolution, and probably accounts not only for a rophyllum Sond., cultivated at the Vavra Estate of considerable portion of the amazing amount of phyl- (UCLA) C. farinosum Kunth., Henrickson & Christ- etic change that has occurred in angiosperm woods, man 2101 (RSA). Fabaceae: Acacia dealbata Link, but also the physiological success of various clades. cultivated at the Vavra Estate (UCLA); A. urophylla Benth. ex Lindl., Carlquist 5563 (RSA). Fouquie- riaceae: Fouquieria splendens Engelm., stem SJRw- MATERIALS AND METHODS 14358; root Henrickson 21437 (RSA). Moraceae: Fibre dimorphism is conspicuous in wood transverse Maclura pomifera (Rob.) C.K.Schneid., Utrecht sections because wall thickness, lumen diameter and UN-262; Morus rubra L. Ripon W-252. Onagraceae: cell diameter are most easily discerned in this plane Diplandra lopezioides Hook. & Arn., Breedlove 8052 © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 174, 44–67 46 S. CARLQUIST
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