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

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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 (sometimes 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 correspond 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

(DS – CAS); Fuchsia boliviana Carrière, UCBBG phism. I have described here more conspicuous and 49.815; F. macrostemma Ruiz & Pav., UCBBG 49.806; thus easily illustrated instances of fibre dimorphism, Hauya elegans DC. subsp. cornuta (Hemsl.) but there are, naturally, a few transitional cases. The P.H.Raven & Breedlove, Breedlove 6432 (DS – CAS); content of this essay essentially covers types and Pseudolopezia longiflora Rose, Breedlove 8044 (DS – degrees of departure from fibre monomorphy. CAS). Oliniaceae (= Penaeaceae sensu APG III, 2009): Olinia cymosa Thunb., Carlquist 4599 (RSA); Penae- aceae: Penaea cneorum Meerb., Carlquist 4740 (RSA). GELATINOUS FIBRES Punicaceae: Punica granatum L., cultivated at Franc- Gelatinous fibres are usually equated with reaction eschi Park, Santa Barbara, CA. Rutaceae: Evodia wood: in woody angiosperms, reaction wood is consid- cucullata Gillespie, SJRw-28318. Sapindaceae: Allo- ered tension wood. The ‘gelatinous’ secondary wall phyllus cominia (L.) Sw., SJRw-21859; Arytera brack- may contain contractile strands of cellulose in a back- enridgei (A.Gray) Radlk., SJRw-18648; Cupania ground of pectic compounds or other compounds with pseudorhus Rich., SJRw-21855; Guioa subfalcata hydrophilic properties; lignin in lignified fibres has Radlk., SJRw-28232; Paranephelium macrophyllum the effect of providing strength through agglutination King, SJRw-26876. Thymeleaceae: Daphne pseu- of fibrils, whereas gelatinous fibres are capable of domezereum A.Gray, KYOw-6459. Urticaceae: Nerau- shrinkage with dehydration of the pectic background dia melastomatifolia Gaud., USw-15342; Urtica (Du & Yamamoto, 2007; Bowling & Vaughn, 2008). dioica L., Hope Ranch Park, Santa Barbara, CA, We recognize gelatinous fibres in wood because of Carlquist s.n. their wall characteristics: the secondary walls are thick, sometimes almost occluding the lumen MODES OF FIBRE DIMORPHISM (Fig. 1B, nlf). Shrinkage patterns appear in secondary walls in sections that have been dehydrated, as in Delineating the concept of fibre dimorphism depends most permanent slides. Safranin tends to stain ligni- on development of criteria for what we accept as fied fibres more deeply (Fig. 1B). If a counterstain is manifestations. The concern goes beyond nomencla- used, the gelatinous secondary wall tends to absorb ture, because the various kinds of fibre dimorphism the counterstain preferentially, and we see this as represent evolutionary strategies, even though we darker bands of gelatinous fibres in the reaction wood may not be able to say with certainty what some of of various angiosperms (Fig. 6D, E). Little attention those strategies are. I am taking the viewpoint that has been paid to the longevity of gelatinous fibres in we must begin with the premise that any instance of comparison with lignified fibres in angiosperm woods. co-occurrence of more than one type of fibre in sec- Gelatinous fibres may not be entirely equivalent to ondary xylem must be examined as a possible kind of tension wood in angiosperms. The occurrence of fibre dimorphism. gelatinous fibres in wood of relatively non-woody angiosperms such as Onagraceae leads one to suspect MONOMORPHIC FIBRES that the two terms should not be used synonymously (Carlquist, 1977). Gelatinous fibres are usually found In transverse sections, fibres can be distinguished in bands (Fig. 6D, E), but may also be found scattered from axial parenchyma (Fig. 1A, ap) if the fibres are within a matrix of other cells (Figs 1B, 7D). In any thick-walled. If fibres have the same wall thickness as case, no survey of fibre dimorphism would be com- axial parenchyma (e.g. Fig. 1C), one must examine plete without a consideration of gelatinous fibres. longitudinal sections to be sure which cells are in strands and are thus axial parenchyma, and which are undivided cells, as in Figure 1F (in a small number of species, axial parenchyma cells are not LUMEN DIAMETER AND CELL SHAPE subdivided into strands, as discussed below). Fibre The terms wide-lumen fibre and narrow-lumen fibre lengths should be measured in macerations. The are used here. These dimensions can be expressed monomorphic fibres of the root of Fouquieria splend- independently of wall thickness or cell length, but ens (Fig. 1A) contrast with the two kinds of fibres commonly there is some degree of correlation. In (non-lignified fibres, nlf; and lignified fibres, lf – Daphne pseudomezereum (Fig. 1C), the narrower late- which stain more darkly) in the stem. There is no wood fibres differ from the earlywood fibres in cell clear decisive limit separating all instances of mono- diameter and lumen diameter, but all have approxi- morphic fibres from all instances of dimorphic fibres, mately the same wall thickness. In Evodia cucculata because there is natural variability in a cell popula- (Fig. 1D), wider earlywood fibres (above) have both tion. Fibre monomorphism is much more common in wider cell diameter, wider lumina and thinner the world flora than are examples of fibre dimor- walls than earlywood fibres; they resemble axial

Figure 1. Examples of wood features related to fibre dimorphism sensu lato from transverse sections (A–E) and a radial section (F). A–B, Fouquieria splendens. A, root wood; fibres are monomorphic. B, stem wood; non-lignified fibres (gelatinous fibres) are intermixed with lignified fibres. C, Daphne pseodomezereum. Margin of a growth ring; libriform fibres fluctuate in diameter and shape but not wall thickness with respect to position in growth ring. D, Evodia cucullata. Margin of a growth ring. Fibres in latewood are radially narrower and thicker-walled than those in earlywood. E–F, Morus rubra. Libriform fibres are markedly wider in earlywood and resemble parenchyma, but the radial section shows that the wide fibres are not subdivided as parenchyma strands would be. Key: ap, axial parenchyma; ew, earlywood; ewv, earlywood vessel; lf, lignified fibre; lw, latewood; nf, narrow fibres; nlf, non-lignified fibre; nv + vt, narrow vessels + vasicentric tracheids; v, vessel; wf, wider fibres.

© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 174, 44–67 48 S. CARLQUIST parenchyma, but have slightly thinner walls. Axial readily visible. I suspect that figures for fibre length parenchyma occurs in this species in tangential bands in some studies may have been derived from sections, three to six cells wide. because macerations are not specified in the materi- In a wood with growth rings, such as Morus rubra als and methods sections of some papers. (Fig. 1E), the background cells of the earlywood could Even using macerations, results can be inconsist- be either axial parenchyma or wide libriform fibres. ent. Wider fibres tend to be shorter; in Punica L., Longitudinal sections are needed to decide which of ‘fibres around the vessels are wider and shorter than these is present. A radial section of this species other fibres and have rounded ends. Ratio of fibres to (Fig. 1F) reveals that earlywood, wide libriform fibres vessel member length 1.7–1.9:1.’ (Bridgewater & differ markedly from latewood fibres (left). In con- Baas, 1978). The mention of vessel elements, trast, Maclura pomifera (Fig. 9F, G) has wide fibres although incidental, does illustrate that the wider the intermixed with two-celled axial parenchyma strands. cell, the less intrusive and shorter it is as it undergoes Latewood fibres most often appear somewhat flat- growth. If fibres are dimorphic in characteristics as tened in a radial direction; that is, they are wider seen in transverse section, do they form a bimodal tangentially (Fig. 1C, D). Earlywood fibres tend to be curve when fibre lengths are plotted? They do not, for approximately isodiametric as seen in transverse sec- several reasons. First, wider fibres are usually much tions. Baas & Zweypfenning (1979) illustrated the less common than narrower fibres in a wood with rounded shapes of the wider fibres of Lagerstroemia fibre dimorphism. Secondly, fibres of intermediate floribunda Jack, which contrast with the more length are common, so that a curve of fibre lengths angular shapes in the narrower fibres as seen in plotted against fibre diameters tends not to have transverse sections. The wider fibres are associated peaks, but instead to have a broadened summit. with intercellular spaces, lacking between narrower fibres. Fibre dimorphism in Lagerstroemia floribunda is not associated with growth rings. Workers may HOW FIBRES AND AXIAL PARENCHYMA DIFFER ultimately wish to exclude instances of difference in Implicit in the above discussion is that we can always fibre width related to growth rings from the phenom- distinguish between axial parenchyma and fibres in enon of fibre dimorphism, but there are genuine dif- wood, and thereby place axial parenchyma out of ferences between latewood and earlywood fibres, and consideration. Can we? Both cell types are derived in a number of woods, growth rings may be indistinct, from fusiform cambial initials. Differences between so that a distinction between growth-ring-related fibre the two cell types that are commonly cited are as dimorphism and non-growth-ring-related fibre dimor- follows: phism may be difficult or impractical. In any case, the overriding consideration may lie with evolutionary (a) Axial parenchyma is subdivided into strands of interpretations, addressed in the last section of this cells; libriform fibres, even if living, are not. paper, rather than in nomenclatural resolution. Living libriform fibres may be septate, but careful examination shows that cells of axial parenchyma differentiate early in ontogeny, so that each cell in WALL THICKNESS a strand is surrounded by a wall equally thick on One might think that in fibres, if walls are thicker, all sides. Septate fibres have thicker walls, lumina are narrower. However, the features are not so usually secondary, on axial surfaces, with only obviously linked. For example, in Dubautia Gaudich. thin primary walls forming horizontal septa, and Wilkesia A.Gray (Fig. 2), narrower fibres have formed late in ontogeny of the fibre after the walls that are not appreciably thicker than those of secondary walls have been laid down, that sepa- the wider fibres. This applies also in Daphne L. rate the fibre into segments (Fig. 5D, E). In some (Fig. 1C) and Morus L. (Fig. 1E, F). Wall thickness is woods, such as Frankenia L., axial parenchyma greater in narrow-lumen fibres than in wide-lumen cells are never subdivided (Carlquist, 2010). Non- fibres in Paranephelium macrophyllum (Fig. 4G). In subdivided axial parenchyma along with axial comparing fibres within a wood, one should consider parenchyma composed of strands of two cells can cell diameter, lumen diameter and wall thickness be found intermixed in the tangential paren- independently. chyma bands of Erythrina L. and some other Fabaceae. In the Fabaceae, axial parenchyma dis- tributions are distinctive and are not likely to be FIBRE LENGTH mistaken for fibre dimorphism (which does occur Fibre length should be measured on the basis of in some Fabaceae: Fig. 3A–C). macerations. Unfortunately, that is often not done. In (b) Each cell in an axial parenchyma strand is sur- longitudinal sections, tips of fibriform cells are not rounded by its own primary and secondary

Figure 2. Fibre dimorphism in Hawaiian Asteraceae, shown in transverse sections (A, C, E) and tangential sections (B, D, F). Growth rings are not present. A–B, Dubautia raillardioides. Fluctuation in libriform fibre wall thickness, diameter and storying is present, but less conspicuous because of larger cell size. C–D, Dubautia menziesii. Fibre dimorphism is conspicuous because of differences between wide fibres and narrow fibres in wall thickness and diameter. Wider fibres are clearly storied (at right in D), narrower fibres only vaguely so). E–F, Wilkesia gymnoxiphium. Narrower fibres have narrower lumina and greater wall thickness. Wider libriform fibres are easily distinguished from axial parenchyma; the latter is always scantily vasicentric. Key: nf, narrower fibres; r, ray; wf, wider fibres.

Figure 3. Fibre dimorphism in Fabaceae (A–C) and Burseraceae (D–F) as seen in transverse sections (A–E) and a radial section (F). A–B, Acacia urophylla. A, lower power, to show subtle fluctuation in apparent fibre density. B, higher power view to contrast a patch of wider fibres, above, with a patch of narrower fibres, below. C, Acacia dealbata. Earlywood fibres are much wider than latewood fibres; axial parenchyma forms a thin sheath around vessels, seen adjacent to the fibre at bottom. D–F, Santiria laevigata. D, low power view; there are no apparent patches of wider fibres and narrower fibres. Higher power view; between the arrow tips, there are wide fibres adjacent to vessels; axial parenchyma is very sparse in this species, almost absent, and is limited to a cell or two adjacent to vessels. F, arrow indicates wider septate fibre adjacent to vessel; narrower fibres are also septate. Key: ew, earlywood; lw, latewood; nf, narrower fibres; r, ray; v, vessel, wf, wider fibres.

(usually present) wall, and the horizontal walls found in Punica (Fig. 8C, D). Bridgewater & Baas between adjacent cells of an axial parenchyma (1978) provided a scanning electron micrograph of strand are pitted. These characteristics differ crystalliferous fibres in a longitudinal section of from the thin primary walls of septa of fibres. Punica wood, clearly revealing the presence of sec- Those septa stain distinctively and do not show ondary vertical walls. The crystals in this genus are pitting. These distinctions are illustrated in separated by thin walls that can be presumed to be Figures 4D, E, 5E–G and 9B. primary walls, or septa, on the basis of thickness and (c) Axial parenchyma cells frequently have thinner staining. One or two crystals per chamber are char- walls than the fibres they accompany, and, if so, acteristically present (Fig. 8D). Crystalliferous fibres are easy to detect in transverse section. Such in Punica are tapered, like other fibres (Fig. 8C). contrasts are shown in Figure 1A, B and D. The Bridgewater & Baas (1978) stated that crystalliferous section shown in Figure 1C exemplifies an fibres in Punica are shorter than non-crystalliferous instance in which fibres have very thin walls and fibres. cannot readily be distinguished in transverse sec- The categorization of other crystalliferous strands tions from axial parenchyma. In such instances, found in wood may be more elusive than in the longitudinal sections reveal whether these cells Punica example. Olinia Thunb. (Fig. 8A, B), closely are subdivided into strands or not, a contrast that related to Punicaceae, has crystals enclosed in fibri- is usually present. form strands that appear to have primary walls exclu- sively. This is apparently true in other families, such as Sapindaceae (Fig. 4C–E). Because these strands LIVING AND NON-LIVING FIBRES have the same shape and almost the same length as Wolkinger (1970) listed species and genera of woody libriform fibres, they may be termed crystalliferous angiosperms in which various authors have reported strands and cited, along with crystalliferous fibres, as living fibres (including septate fibres). By ‘living an example of fibre dimorphism, although a case fibres’, one connotes fibres in which protoplasts are could be made for terming the crystalliferous strands alive when the fibres have reached their full length, as a form of axial parenchyma. so that in a current year protoplasts and nuclei can be Hauya DC. (Onagraceae) has larger prismatic crys- detected in fibres formed that year provided that tals (Fig. 8E–G). These are located in libriform fibres liquid-preserved material is studied. Not all instances with secondary walls, although the distortion in cell listed by Wolkinger (1970) have fibre dimorphism, but shape due to their inclusion of large styloids masks an appreciable number of them do, for a significant the cell shape. The styloid-containing fibres do taper reason. If fibre dimorphism occurs, there is a division (Fig. 8F, G, tt), indicating this identity. The crystal- of labour between wide and narrow fibres, and that liferous fibres in Hauya are not septate and represent division of labour involves a function reliant on lon- pronounced fibre dimorphism. gevity in the wider fibres, such as starch storage. All instances of septate fibres can be considered as probable instances of living fibres. Septa in fibres do not STORIED FIBRES survive maceration techniques well, but they usually The earliest examples to be cited as illustrating the do survive sectioning techniques. Only liquid- phenomenon of fibre dimorphism were in the woods of preserved materials can reliably document the occur- helianthoid Asteraceae (Carlquist, 1958). Dubautia rence of nuclei in non-septate fibres, however. The spp. with shorter vessel elements (and, thus, with presence of starch in a libriform fibre is to be consid- shorter accompanying libriform fibres), such as ered evidence of living fibre presence in a wood D. menziesii (Fig. 2C, D), tend to show storying more sample. The present listing of living fibres in wood is conspicuously, but storied fibres can be found in all of minimal, and could be expanded greatly by further the Hawaiian madioid Asteraceae (Fig. 2; Carlquist, investigations. 1997, 1998a, b). In these and other helianthoid genera, the shorter fibres are more clearly storied, and longer fibres less conspicuously storied, in agree- CRYSTALLIFEROUS FIBRES ment with the greater intrusiveness (and therefore Crystal occurrence in wood is sometimes not men- greater irregularity in length) of longer, narrower tioned in terms of the cell types in which crystals fibres. Storied wider fibres plus non-storied narrower occur, and probably ray parenchyma and axial fibres were reported by Baas & Zweypfenning (1979) parenchyma are the most common sites of crystal for Lagerstroemia calyculata Kurz (Lythraceae). deposition. There are, however, crystals (generally Bailey (1923) demonstrated that in species with presumed to be calcium oxalate) in cells that must be storied woods, storying increases with increase in termed libriform fibres. A prime example of this is girth of the stem. Thus, species with fibre dimorphism

Figure 4. Fibre dimorphism in transverse sections (A, B, F) and radial sections (C–E, G) of wood of Sapindaceae. A–D, Guioa subfalcata. A, low power, to show contrast between wider fibres (upper left) and narrower fibres (lower right). B, high power, to show location of wider fibres, narrower fibres, axial parenchyma and a crystalliferous strand in relation to a vessel. Axial parenchyma is scanty (three cells visible adjacent to vessel). C, low-power photograph to show axial parenchyma adjacent to vessel and two crystalliferous strands. D, high-power photograph to show features similar to those in C, plus septate wide fibres. E–G, Paranephelium macrophyllum. E, high power, to show wide septate fibres (left), narrow septate fibres (right) and, between them, a crystalliferous strand. F, transverse section showing marked difference between wide, thinner-walled fibres and narrow, thicker-walled fibres. G, radial section showing contrast between narrow fibres (left) and septate wider fibres (right), with some axial parenchyma strands seen in longitudinal section adjacent to a vessel. Key: ap, axial parenchyma; cs, crystalliferous strand; nf, narrower fibres; wf, wider fibres.

Figure 5. Fibre dimorphism in transverse sections (A, C) and radial sections (B, D–G) of Sapindaceae. A–B, Allophyllus cominia. A, margin of growth ring; wider fibres may occur in various places in a growth ring. B, narrow septate fibres in latewood, wider septate fibres in earlywood, an axial parenchyma strand near a vessel. C–F, Cupaniopsis pseudorhus. C, margin of growth ring (latewood at bottom); a notably wide zone of wider fibres adjacent to vessel. D, radial section to show junction between earlywood and latewood. E, higher power of an area shown in D, to illustrate a single strand of axial parenchyma, wider septate fibres and narrower septate fibres. F, wider fibres plus axial parenchyma and a crystalliferous strand. G, Arytera brackenridgei, section to show thin-walled crystalliferous strands plus thick-walled libriform fibres and axial parenchyma. Key: ap, axial parenchyma; cs, crystalliferous strand; ew, earlywood; lw, latewood; nf, narrower fibres; wf, wider fibres.

© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 174, 44–67 54 S. CARLQUIST in which the shorter, wider fibres are storied in wider water conduction. The same phenomenon was stems may not show storying earlier in the develop- described in angiosperms by Ingle & Dadswell (1953) ment of a woody cylinder. for Alstonia scholaris R.Br. and A. spathulata Bl. (photographs reproduced in Carlquist, 1961: 3). The root tracheary elements (best called fibre-tracheids TRANSITIONAL FIBRES because of the presence of bordered pits) differ from The present paper attempts to document instances of those of the stem, which are much more slender, fibre dimorphism. In so doing, it may suggest that thicker-walled and with narrower lumens, providing woods have either monomorphic or dimorphic fibres a marked contrast. Similar contrast between root and and that in the latter case any given fibre can be stem fibre-tracheids (perhaps tracheids) has been placed in one of two categories. As we have seen, in reported for Anaxagorea (Anaxagoreoideae, Annon- some instances (latewood vs. earlywood fibres) there aceae; Chatrou et al., 2012) (Berry, Miller & are varying degrees of differentiation of two fibre Wiedenhoeft, 1999) and Micrandra (Euphorbiaceae) categories. In particular taxonomic groups, incipient (Berry & Wiedenhoeft, 2004). The latter’s photomicro- fibre dimorphism may be present but difficult to docu- graph of a stem wood transverse section of Micrandra ment decisively. The clearest instances of fibre dimor- inundata P.E.Berry & A.Wiedenhoeft illustrates fibre phism have been selected for the present study. dimorphism within the stem, because there is fluc- In Onagraceae, Fuchsia L. has monomorphic fibres, tuation in fibre-tracheid (or tracheid) wall thickness unless one includes the occurrence of gelatinous fibres and lumen diameter. The wide imperforate tracheary as a form of fibre dimorphism (Fig. 6D, E). A fibriform elements of M. inundata are short, with blunt ends, idioblast that contains raphides (Fig. 6F) could be whereas those of the stem are tapered and longer. considered a kind of fibre dimorphism. However, in Naturally, there is no abrupt change from root into Diplandra Hook. & Arn. and Pseudolopezia Rose (also stem in terms of imperforate tracheary elements, and Onagraceae), the axial raphide-containing idioblasts both types may coexist in levels between inundated are thin-walled and subdivided into a pair of cells roots and non-inundated stems. Other genera with (each containing a packet of raphides). In some inundated roots and lower stems from riparian areas Fuchsia spp., raphide-bearing idioblasts are present have been cited by Wiedenhoeft (2001). These genera in the wood, thin-walled and of a fusiform shape, but have the above-mentioned characteristics. shorter than ordinary libriform fibres. Should they be considered an instance of fibre dimorphism? In both Fuchsia and Diplandra (Fig. 7B), there are SYSTEMATIC OCCURRENCES OF FIBRE wide starchy fibres and narrow starchy fibres. There DIMORPHISM are also starch-rich fibres and starch-poor fibres. These variations (which are less likely to be detected Instances of fibre dimorphism cited below are in dried wood samples) can be considered part of a minimal, and many more are likely to be found. Some natural variation pattern rather than production of families have been investigated as exhaustively as two fibre types. In addition, in woods of Diplandra materials permit (e.g. Sapindaceae; Klaassen, 1999), and Pseudolopezia (Fig. 7A–E), there are patches of whereas others have not been studied monographi- lignified fibriform cells and of gelatinous fibres. The cally. In studies that precede the origin of the concept theme of fibre diversification is not vitiated by these of fibre dimorphism, workers were not searching for instances. It is in fact reinforced: uniformity in this phenomenon, although some descriptions clearly expression of cell types is not to be expected. relate to it (e.g. some Urticaceae in Metcalfe & Chalk, 1950). The phenomena of gelatinous fibres and/or tension wood are not included in the listings below. AERATING IMPERFORATE TRACHEARY ELEMENTS There is no point in attempting an exhaustive listing Attention has been directed to the probable function at this time. Only a small fraction of woody angio- of wide-lumen thin-walled tracheids in the roots of sperms are represented in wood collections, so even the conifers Taxodium distichum (L.) Rich. of Cupres- an exhaustive search based on xylarium materials saceae and Dacrydium guillauminii Buchholz and would be incomplete. Podocarpus minor Parl. of Podocarpaceae (Carlquist, The great convenience of xylarium specimens and 1975: 91, 101). These conifers have roots and lower the value of wood collections are unquestionable. Reli- stem portions that are characteristically inundated, ance on wood collections, however, has resulted in a and thereby the lumina of their root tracheids (at lag in our knowledge of living contents of wood least the older ones) potentially provide gas exchange cells, which are best revealed in liquid-preserved pathways between root and stem. The tracheids materials. Such specimens are rarely maintained in formed in the current year probably are active in institutional accumulations, and are mostly studied

Figure 6. Fibre dimorphism in Combretaceae (A–C) and Onagraceae (D–F). A–B, Combretum erythrophyllum. A, transverse section. A zone of wider fibres (left to right, just below centre) next to a zone of narrower fibres (bottom). B, tangential section. Axial parenchyma occurs near vessels; wider fibres, upper right, narrower fibres, lower left. C, C. farinosum, radial section. Between narrow non-septate fibres (left) and septate wider fibres (right) is an axial parenchyma strand, some cells of which contain starch, others a rhomboid crystal each. D, Fuchsia boliviana, transverse section, fibres of various widths, with a band of gelatinous fibres from left to right, centre. E–F, F. macrostemma. E, transverse section, a band of gelatinous fibres from left to right, centre. F, tangential section; a fibriform raphide- containing cell to the right of the ray; axial parenchyma to right of vessel; septate wider fibres at far right. Zonal distinctions are more evident when portions are viewed at lower magnification. Key: ap, axial parenchyma; gf, gelatinous fibres; nf, narrower fibres; r, ray; ra, raphide-containing idioblast; wf, wider fibres.

Figure 7. Wood sections of Onagraceae (A–E) and Penaeaceae (F). A–B, Diplandra lopezioides. A, transverse section, to show various fibre widths; most fibres contain starch. B, tangential section. Most of the starchy fibres are non-septate; vessel is flanked on left and right by azial parenchyma strands. C–E, Pseudolopezia longiflora. C, transverse section; gelatinous fibres in upper half. D, higher power transverse section to show details of starchy fibres, gelatinous fibre and a strand of interxylary phloem. E, tangential section; narower fibres at left, wider fibres in right half of photograph. F, Penaea cneorum. Transverse section; a band of thinner-walled fibre-tracheids from left to right, near centre. Key: gf, gelatinous fibre; ixp, interxylary phloem strand; nf, narrower fibres; nsf, narrower starchy fibres; sf, starchy fibres; v, vessel; wf, wider fibres; wsf, wider starchy fibres.

© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 174, 44–67 FIBRE DIMORPHISM IN ANGIOSPERM WOOD 57 by enterprising wood anatomists who prepare such Mutisieae, with a low percentage (8%), are an early- specimens from field-collected or cultivated plants diverging clade of the family (Funk et al., 2009), and then discard them at the conclusion of an inves- which might be a relevant factor: storying in angio- tigation. The listing of Wolkinger (1970) represents a sperm woods seems likely to be an apomorphy, good beginning in assembling reports of living fibres judging from its rarity in, say, woods with scalariform (including septate fibres), but his review is not likely perforation plates. However, small stem diameter can to be updated or expanded with regularity. also be a factor (Bailey, 1923), and that would explain the low percentages in tribes Calenduleae, Cicho- rieae, Cynareae and Helenieae, which are relatively ASTERALES –ASTERACEAE non-woody. The genus Dubautia was the basis for the initial Fibre dimorphism is related to the living nature of description of the phenomenon of fibre dimorphism fibres, whether septate or otherwise. In Dubautia, (Carlquist, 1958). Fibre dimorphism characterizes the nuclei were observed in libriform fibres in prepara- ‘silversword complex’, Argyroxiphium DC. (Carlquist, tions made from liquid-preserved material of 1997), Dubautia (Carlquist, 1998a) and Wilkesia D. platyphylla. (Carlquist, 1998b). The three species shown in Figure 2 differ in cell size. The relatively large fibres FABALES –FABACEAE of D. raillardioides (Fig. 2A, B) make the patches of Fibre dimorphism seems not to have been reported in wide-lumen fibres less conspicuous. Wide-lumen Fabaceae, although living fibres and storied fibres, fibres occupy the lower left quadrant of Figure 2A and features that sometimes are associated with fibre the central portion of Figure 2B. In the latter, wide- dimorphism, have been (Metcalfe & Chalk, 1950; lumen fibres are vaguely storied. Wolkinger, 1970). There are prominent tangential In D. menziesii, small cell size renders the contrasts bands of thin-walled cells in woods of a number of more obvious. The patch of wide-lumen fibres legumes, such as Erythrina. In that genus, such (Fig. 2C, wf) is easily seen in the transverse section. bands should be interpreted as consisting of axial The wide-lumen fibres in the tangential section of parenchyma, because the cells are so markedly dif- D. menziesii (Fig. 2D, right half of photograph) are ferent from the libriform fibres in that wood. Strands clearly storied, whereas the narrow-lumen fibres (nf) composed of two cells, and similar undivided axially are only vaguely storied. elongate cells in these bands, are another indication In Wilkesia gymnoxiphium (Fig. 2E, F), the narrow- that the bands are composed of parenchyma. lumen fibres (nf, upper half of Fig. 2E) are distin- Excluding examples such as Erythrina from consid- guishable from the narrow-lumen fibres (which are eration, there are clear instances of fibre dimorphism also narrower in cell diameter) at the top of the in the family. Examples from the large genus Acacia photograph. Nearly all of the tangential section s.l. (but see, for example, Kyalangalilwa et al., 2013) portion shown (Fig. 2F) consists of wide-lumen fibres are presented here (Fig. 3A–C); more Acacia spp. with (wf) which are storied, a fact more obvious when a fibre dimorphism are likely to be found. In a low- larger area is viewed. power transverse section (Fig. 3A) of A. urophylla, Axial parenchyma occurs as strands of two to three fibre dimorphism is visible in the form of alternation cells, and is adjacent to vessels (Fig. 2B, right) in of somewhat darker bands and lighter bands. When these genera. This can readily be seen in the silver- examined under higher power, the darker bands sword complex. Tangential sections rather than radial prove to be composed of narrower libriform fibres sections have been illustrated here for Asteraceae (Fig. 3B, nf). The two kinds of areas grade impercep- because storying can only be demonstrated in tangen- tibly into each other. tial sections. Fibre dimorphism in Asteraceae is dis- Acacia urophylla lacks well-defined growth rings. tinctive in that degree of storying is one of the In a species with well-demarcated growth rings, distinctions between wide and narrow fibres. Shorter A. dealbata (Fig. 3C), wide fibres occur in earlywood fibres in Asteraceae also have blunter tips (Fig. 2D), (ew), narrower fibres in latewood (lw). The vessel in whereas longer fibres are more acuminate or acicular, the transverse section of A. dealbata (Fig. 3C, bottom) suggesting a greater degree of intrusive growth. is surrounded by paratracheal axial parenchyma. Storied libriform fibres are common in Asteraceae Various patterns of paratracheal axial parenchyma at large. A survey of woods of the family (Carlquist, are characteristic for Acacia and permit one to dis- 1966) showed that 45% of the family has storied criminate between axial parenchyma and earlywood fibres. The percentage varies greatly depending on fibres as seen in transverse section. In longitudinal the tribe. Tribes with a high degree of storying sections, the distinction is readily made because axial include Astereae (70%) and Senecioneae (62%). Heli- parenchyma consists of strands of more than one cell antheae are intermediate in this respect (29%). each.

Metcalfe & Chalk (1950) cited fibres adjacent to Heimsch (1942), but working with the same collection paratracheal parenchyma as thinner walled and with he did, I have found that P. macrophyllum has indis- intercellular spaces among them as characteristic of tinct growth rings and that wide-lumen fibres occur Mimosoideae. Metcalfe & Chalk (1950) also state that in randomly occurring patches within the wood fibres of Mimosoideae ‘sometimes contain starch’. A (Fig. 4F). systematic search for fibre dimorphism in Fabaceae In Allophyllus cominia and Cupania pseudorhus, would no doubt yield many more examples. In this however, growth rings are present (Fig. 5A,C), Wide connection, Evans, Gasson & Lewis (2006) offered a fibres do occur in earlywood, but in neither of these number of apparent instances. genera is there a steady progression in fibre diameter reduction from earlywood to latewood. In latewood, there may be patches of wider fibres (Fig. 5A, wf). In SAPINDALES –BURSERACEAE Allophyllus, these patches of wider fibriform cells are Santiria laevigata (Fig. 3D–F) would not seem at first septate fibres (Fig. 5B). glance to have fibre dimorphism. However, patches of In Cupania pseudorhus, wide fibres occur around wider fibres are present, mostly near vessels (Fig. 3D, vessels (Fig. 5C, wf), recalling the condition in San- between arrow tips). Axial parenchyma is scarce in tiria Blume (Burseraceae). Vasicentric scanty paren- S. laevigata, often only one or two cells in contact chyma is present, as in Santiria (Fig. 3E). Wider with a vessel as seen in a transverse section. Septa fibres occur at growth ring margins in Cupania pseu- are present both in wider fibres (Fig. 3F, arrow) and dorhus (Fig. 5C, D). Axial parenchyma strands are in narrower fibres of S. laevigata. also present at the juncture of earlywood and latewood (Fig. 5E–G, ap), but axial parenchyma strands are easily distinguishable from wide fibres of the SAPINDALES –SAPINDACEAE earlywood (Fig. 5E,F, wf), which are septate. Narrow Although Heimsch (1942) worked before the develop- fibres are also septate (Fig. 5E, nf). ment of the concept of fibre dimorphism, he accu- In addition to the presence of wide and narrow rately described instances of the phenomenon in fibres in Sapindaceae, strands of crystals are present. Sapindaceae. In Allophyllus Gled., he reported a ten- (Fig. 4C–E). The cells of these strands may have dency for formation of irregular, parenchyma-like primary walls (Fig. 4C, D) or secondary walls bands of septate fibres. These bands of septate fibres (Fig. 4E), both vertical and horizontal, rather than are rounded in transverse section and associated with being septate fibres. Crystals are often encapsulated pronounced intercellular spaces. Similar bands were by secondary wall material (Fig. 4E). In Cupania noted by Heimsch (1942) in Paullinia L. and Serjania pseudorhus, the crystals are all encapsulated Mill. Klaassen (1999) in his monograph of wood (Fig. 5F,G), but the encapsulating material covering anatomy of Sapindacaeae s.s. reported ‘distinct’ fibre each crystal is thin. dimorphism in 17% (13 genera) of the family in the narrow sense [see Buerki et al. (2011) and references SAPINDALES – OTHER FAMILIES therein for discussion of Sapindaceae s.l.]. In Simaroubaceae, there is fibre dimorphism in the In Guioa subfalcata (Fig. 3A–D), the fibres differ genus Alvaradoa Liebm. According to Heimsch with respect to position in growth rings, with wider (1942), ‘the septate fibres occur in bands or patches, lumina in earlywood (Fig. 4A, wf), somewhat nar- in a transverse section, the cells of these groupings rower in latewood. In addition, wider fibres may be have thinner walls, greater diameter, and frequent scattered near vessels and in radial rows (Fig. 4B, intercellular spaces around them.’ Patches of wider wf). Axial parenchyma is scanty (Fig. 4B–D, ap) and fibres can also be found in the wood of Ailanthus strictly vasicentric, so that fibres are readily distin- altissima (Mill.) Swingle. guished from axial parenchyma. In addition, the In Rutaceae, several genera have wider, thinner- fibres are septate (Fig. 4D, wf), whereas axial paren- walled fibres in earlywood combined with narrower, chyma cells are in strands (Fig. 4D, ap). thicker-walled fibres in latewood. Evodia cucculata In Paranephelium macrophyllum (Fig. 4E–G), as (Fig. 1D) is representative of this tendency. Fibre noted by Heimsch (1942), the wide-lumen fibres dimorphism has not previously been reported in almost look like parenchyma, being so different from Rutaceae, but it may be more widely present. I did the narrow fibres. Both narrow and wide fibres are not observe any easily discernible instances of fibre septate (Fig. 4E, G). Axial parenchyma is restricted to dimorphism in an assortment of slides of Anacardi- incomplete vasicentric sheaths usually one cell thick aceae or Hippocastanaceae (= Sapindaceae sensu APG (Fig. 4G), and is in strands and readily distinguished III, 2009) I studied. from the fibres. Wide-lumen fibres were reported to Aceraceae, now placed in Sapindaceae (APG III, be related to growth rings in P. macrophyllum by 2009; Soltis et al., 2011), show marked fibre

© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 174, 44–67 FIBRE DIMORPHISM IN ANGIOSPERM WOOD 59 dimorphism in some species. In a transverse section fresh or ethanol-preserved material of woods of Com- of wood of Acer palmatum Thunb., Heimsch (1942) bretaceae might yield more information about fibre noted ‘bands and areas of thinner-walled fibres which dimorphism in the family. store starch when in the living condition.’ For Acer L. as a whole, he reported that ‘sections prepared by the usual methods, i.e. acid treatment etc., do not display MYRTALES –ONAGRACEAE these areas as distinctly as fresh or dried untreated Fibre dimorphism may exist in more numerous wood.’ This distinctive feature has not been noted by species of this family than indicated below. In a wood several workers interested in the wood physiology of monograph of the family (Carlquist, 1977), a special Acer. Various methods were used by Vasquez-Cooz & search for the phenomenon was not undertaken. Meyer (2008) to demonstrate fibre dimorphism in Gelatinous fibres [shown here for Fuchsia boliviana Acer. (Fig. 6D), F. macrostemma (Fig. 7C) and Pseudolope- zia longiflora (Fig. 7D)] are common in Onagraceae and constitute a form of fibre dimorphism, whether MYRTALES –COMBRETACEAE or not they represent a form of tension wood. The Patches of wide, thick-walled fibres may be found in term gelatinous fibre was also used by Baas & a background of narrow, thick-walled fibres in Com- Zweypfenning (1979) in their survey of the wood of bretum erythrophyllum (Fig. 6A, B). The wide, thin- the myrtalean family Lythraceae. walled fibres are not restricted to earlywood or Wide fibres are frequently septate in Onagraceae, latewood, but occur throughout a growth ring. Wide as seen in Diplandra lopezioides (Figs 6F, 7A, B). A fibres of another species, C. farinosum, are septate distinction between wide starchy fibres and narrow and rich in starch (Fig. 6C, swf), whereas starch is starchy fibres may be seen in D. lopezioides (Fig. 7A, much less abundant in the narrower fibres (Fig. 6C, B). Axial vasicentric parenchyma and parenchyma in nf), which are mostly non-septate. strands of interxylary phloem of Pseudolopezia longi- Fibre dimorphism was not described in the wood flora (Fig. 7C–E) are poor in starch or lacking it monograph of Combretaceae by van Vliet (1979), (Fig. 7C, D), whereas most wide fibres in P. longiflora although he does note ‘considerable variation’ in fibre contain abundant starch (Fig. 7D, sf). wall thickness. van Vliet did, however, present careful Crystalliferous fibres, markedly distorted in shape drawings of the cell types in which crystals occur (van by the presence of large encapsulated styloid crystals, Vliet, 1979, fig. 4). For Combretum fruticosum Stuntz, characterize Hauya (Fig. 8E–G). Thin-walled fibriform he showed a fibre with a secondary wall that con- raphide-bearing cells occur in Fuchsia macrostemma tained druses separated by septa (like that in fig. 4b), (Fig. 6F) and other Onagraceae. Sometimes, like the ‘from juvenile wood’. Such a fibre resembles that libriform fibres, they are septate, with each compart- figured here for Punica (Fig. 8C, D) and can be con- ment containing a packet of raphides. sidered to represent fibre dimorphism. van Vliet also showed (Fig. 4a) ‘clustered and solitary crystals in axial parenchyma’, which is chambered and septate, MYRTALES –PENAEACEAE for C. fruticosum. The co-occurrence of what some Fibre dimorphism has not been previously reported in would call two different cell types in a single wood Penaeaceae. Bands of thin-walled fibres may be found suggests that we can group fibriform crystalliferous occasionally in the wood of Penaea cneorum (Fig. 7F). strands with crystalliferous fibres and consider both of them manifestations of fibre dimorphism. Both of these and ordinary fibres, of course, are derived from MYRTALES –OLINIACEAE AND ALLIED FAMILIES fusiform cambial initials that are presumably Oliniaceae are considered to be close to Penaeaceae uniform. by Schönenberger & Conti (2003), who also recog- van Vliet (1979) depicted axial parenchyma nized Alzateaceae and Rhynchocalycaceae as separate strands, each cell of which is surrounded by a sec- families on the basis of molecular evidence, but Olini- ondary wall and contains a crystal, for wood of Buche- aceae and Rhyncocalycaceae are included in Penae- navia Eichler and Terminalia L. This mode of crystal aceae sensu APG III (2009). Fibre dimorphism is occurrence can be distinguished from fibres and fibri- somewhat evident in Alzateaceae (Baas, 1979), form strands, and is shown here for Combretum fari- Crypteroniaceae (van Vliet, 1974) and Rhynchocaly- nosum (Fig. 6C). The crystal-bearing cells are much caceae (van Vliet, 1974). In Olinia, there are larger than the starch-bearing cells in this paren- crystalliferous strands (Fig. 8A, B) which could be chyma strand. The existence of starch in adjacent considered a form of fibre dimorphism. Both vertical wide septate fibres (Fig. 6C, swf) differs from starch and horizontal walls in the crystalliferous strands are paucity in the narrow fibres (nf) and suggests that primary. Fibres are septate (Fig. 8A, B) in O. cymosa,

Figure 8. Sections of Oliniaceae (= Penaeaceae) (A–B), Punicaceae (C–D) and Onagraceae (E–G) to show modes of crystal occurrence. A–B, Olinia cymosa, radial sections. A, fibriform crystalliferous strand and septate fibres. B, fibriform crystalliferous strand, starch apparent in some of the fibres. C–D, Punica granatum, radial sections. C, septate fibres, tip of two adjacent crystalliferous fibres. D, several adjacent crystalliferous fibres with secondary walls. E–G, Hauya elegans subsp. cornuta, high power photographs to illustrate styloid-containing crystalliferous fibres, much distorted in shape. E, transverse section. F–G, radial sections. F, a large and a smaller styloid, encapsulated together. G, large encapsulated styloid plus small crystal mass. Key: cf, crystalliferous fibres; ec, encapsulated crystal; fcs, fibriform crystalliferous strand; r, ray; se, septum; sef, septate fibres; st, starch; tt, tapering tip of styloid-containing fibre.

© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 174, 44–67 FIBRE DIMORPHISM IN ANGIOSPERM WOOD 61 relatively uniform in wall thickness and diameter, Obetia Gaudich. Apotracheal parenchyma has not and contain starch (Fig. 8B). been reported in Urticaceae except for Obetia. In Urtica L. (Fig. 9C–E), there are strands of thin- walled wide fibres. These occur chiefly in axial zones MYRTALES –PUNICACEAE free from vessels. The areas that contain vessels are Bridgewater & Baas (1978) reported for one collection often arranged in radial strips (Metcalfe & Chalk, of Punica that fibres near vessels are wider and 1950, fig. 299G). The pattern termed ‘vessel restric- shorter than those located distally. They considered tion patterns’ (Carlquist & Zona, 1988; Carlquist, the occurrence of crystalliferous fibres in Punica to 2009) characterizes transverse sections of U. dioica L. represent an instance of fibre dimorphism, and stated Although Metcalfe & Chalk (1950) termed the thin- that crystalliferous fibres are shorter than fibres that walled fibres in Urtica ‘parenchyma’, these zones lack lack crystals. Their descriptions of crystalliferous subdivision into strands, whereas vasicentric paren- fibres correspond to the illustrations offered here chyma, present in Urtica as in other Urticaceae, is (Fig. 8C, D). subdivided into strands (Fig. 9E). Bands or strands of thin-walled fibres have been reported (as ‘parenchyma’) in Laportea Gaudich. MYRTALES –LYTHRACEAE (Dendrocnide Miq.), Myriocarpa Benth., Touchardia Fibre dimorphism has been reported in some, but Gaudich. and Urera Gaudich. (Metcalfe & Chalk, not all genera of Lythraceae, (Baas & Zweypfenning, 1950). Chalk & Chattaway (1937) cited thin-walled 1979; Baas, 1986; Graham et al., 1986). Baas & fibres in Myriocarpa in their monograph of woods Zweypfenning used the term ‘fibre dimorphism’ and with ‘included phloem’, although their drawing and assigned instances of wider and/or thinner-walled text clearly indicated that, in fact, no phloem had fibres along with narrower, thicker-walled fibres to been detected in the secondary xylem of Myriocarpa. fibre dimorphism and offered a page of convincing photomicrographs of the phenomenon in Lagerstro- emia L. They also recognized that occurrence of crys- URTICALES –MORACEAE talliferous fibres in Lythraceae may be considered an Tippo (1938) did not recognize fibre dimorphism in his expression of fibre dimorphism. monograph of woods of Moraceae, perhaps because the concept had not yet been originated. One can find, however, marked disparity in fibre dimensions and MYRTALES –MELASTOMATACEAE wall thickness between earlywood and latewood in Studies by van Vliet (1981) and ter Welle & Moraceae with growth rings, as noted earlier (Fig. 1E, Koek-Noorman (1979, 1981) demonstrated the exist- F). Similar disparity occurs in Maclura pomifera ence of fibre dimorphism under the term ‘pseudo- (Fig. 9F, G). In latewood, vessels are embedded in parenchyma’. ter Welle & Koek-Noorman (1981) strands of axial parenchyma (nv + ap). In earlywood claimed that in no genus do the bands of ‘pseudo- (Fig. 9F, top; Fig. 9G, left), there are wide vessels parenchyma’ coexist with axial parenchyma except for (containing tyloses) with wide fibres and axial paren- Huilaea Wurdack. The possibility that there may be chyma (as judged by subdivision of the cells into intermediacy between ‘pseudoparenchyma’ and true strands of two cells each). The non-subdivided fibres axial parenchyma in Miconia Ruiz & Pav. is consid- could conceivably be regarded as a kind of axial ered by ter Welle & Koek-Noorman (1978). parenchyma, but in that case, one would have to say that earlywood in M. pomifera lacks fibres entirely, whereas earlywood in Morus has fibres as the back- URTICALES –URTICACEAE ground cell type. The vessel-containing bands in Fibre dimorphism was reported in wood of various Maclura alternate with bands of narrow fibres Urticaceae by Bonsen & ter Welle (1984). Typical of (Fig. 9F, G, nf). The possibility of a situation in which the woodier Urticaceae is the wood of Neraudia wide fibres and axial parenchyma coexist within a Gaudich. (Fig. 9A, B). It shows bands of thinner- given wood and form a continuum or transition has walled fibres alternating with bands of thicker-walled been entertained by ter Welle & Koek-Noorman fibres. The differences between the two types of libri- (1979) for Miconia (Melastomataceae). form fibres are evident when one surveys a transverse section and notices differences in staining (Fig. 9A). In a radial section of Neraudia (Fig. 9B), axial paren- OTHER EUDICOT FAMILIES chyma is limited to a few vasicentric strands. Bands Occurrences of fibre dimorphism are likely to be found such as those in Neraudia are probably equivalent to in a number of families in which the phenomenon has the bands figured by Metcalfe & Chalk (1950) for not been reported. For example, in wood of Aralia

Figure 9. Fibre dimorphism in Urticaceae (A–E) and Moraceae (F–G). A–B, Neraudia melastomatifolia. A, transverse section. Alternating bands of wider and narrower fibres. B, radial section; axial parenchyma scanty, vasicentric; fibres are septate. C–E, Urtica dioica. C, transverse section. In radial vessel-free bands, there are zones of thinner-walled fibres and of narrow thicker-walled fibres. D–E, tangential sections. D, an area that contains wider fibres and a ray; E, an area that contains narrower fibres plus a vessel with adjacent axial parenchyma. F–G, Maclura pomifera. F, transverse section. Latewood contains narrow vessels with axial parenchyma; earlywood contains wider fibres mixed with axial parenchyma. Narrow fibres are also present. G, radial section; to the right of the wider earlywood vessel are wider fibres mixed with two-celled axial parenchyma strands. Centre and right of photograph consist of narrow vessels embedded in axial parenchyma plus, at right, narrow latewood fibres. Key: ap, axial parenchyma; nf, narrower fibres; tf, thinner-walled fibres; v, vessel; wf, wider fibres.

© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 174, 44–67 FIBRE DIMORPHISM IN ANGIOSPERM WOOD 63 spinosa (Araliaceae), I found wide fibres in earlywood had vestigially bordered (‘inconspicuous’) pits. Fami- and narrow fibres in latewood, but, in addition, radial lies with libriform fibres or fibre-tracheids tending rows of wide fibres occur among narrow fibres, much towards libriform fibres are not randomly distributed like the condition illustrated for Guioa subfalcata. in angiosperm clades. All of the families considered Fibre dimorphism could be claimed for Melianthus L. above occur in the listing of families with libriform (Melianthaceae), Stylobasium Desf. (Surianaceae), fibres (Carlquist, 2001: 133–134). several genera of Thymelaeaceae (Daphne L. is illus- The wood of Gnetales is pertinent to the topic of trated in Fig. 1C) and Viviania Cav., a genus now fibre dimorphism. Esau (1965: 240) figured cell types placed in Geraniaceae (e.g. Soltis et al., 2011). Whether in wood of Ephedra L. and recognized tracheids, these claims are credited or not depends on whether nucleated fibre-tracheids and fibriform nucleated one considers occurrence of appreciably wider, thinner- ‘axial parenchyma’ cells. One can indeed find these walled fibres in earlywood (with opposite conditions in three cell types in wood of Ephedra, but one should latewood) to represent this phenomenon or not. Wood probably revise this terminology so as to recognize of stems of Alstonia R.Br. (Apocynaceae) (Ingle & tracheids, longer, narrower fibre-tracheids with bor- Dadswell, 1953; photographs reproduced in Carlquist, dered pits and shorter, wider fibre-tracheids with pits 1961) and Micrandra (Euphorbiaceae) shows dimor- simple (at least on some facets), True strands of axial phism in tracheary elements by virtue of fluctuating parenchyma are indeed present in a few Ephedra spp. diameter and wall thickness of imperforate tracheary (Carlquist, 1992: fig. 31). In Gnetum L., axial paren- elements. In these two instances, the imperforate chyma strands rich in starch are common, in addition tracheary elements should probably be termed fibre- to starch-rich septate fibres (with simple to vestigially tracheids. The distinctive nature of root wood and its bordered pits) and tracheids (Carlquist, 1996a: fig. 13; imperforate tracheary elements with respect to the 1996b).One can make a case for fibre dimorphism in ecology of these species (both represent trees in inun- Gnetales, a possibility that should be more thor- dated river margins) has been noted above. Instances oughly explored. of fibre dimorphism undoubtedly occur in many more families FUNCTIONAL SIGNIFICANCE OF LIVING FIBRES IN RELATION TO FIBRE DIMORPHISM

EVOLUTIONARY SIGNIFICANCE OF FIBRE Holbrook, Zwieniecki & Melcher (2002) made a com- pelling case for axial parenchyma as a source of ions DIMORPHISM and presumably sugars that can reverse embolisms SYSTEMATIC IMPLICATIONS and otherwise control the conductive process in angio- Instances of fibre dimorphism are not randomly dis- sperms. Parenchyma cells adjacent to vessels and tributed among woody angiosperm clades. Most tracheids in monocots may have much the same func- examples are linked to families in which living fibres tion (Carlquist, 2012a). The distinctive patterns of (either septate or nucleated) are present. In turn, axial parenchyma distribution in angiosperm woods longevity of fibres is related to pitting. By far the are highly suggestive, although we only have experi- majority of living fibres, as listed by Wolkinger (1970), mental data to a limited extent at present. are instances of libriform fibres with simple pits. A The concept that living fibres store starch has been relevant finding is that of Tippo (1938), who found 44 noted repeatedly (e.g. Wolkinger, 1970). We ordinar- genera of Moraceae and allies to have septate fibres; ily think of starch storage as a prerequisite for of these, only eight had vestigial borders (fibre- flowering or flushes of growth, or mechanisms for tracheids) and the 36 remaining genera had libriform perennation that permit a plant to survive dry or fibres. This is one of many families that could be cited cold seasons. However, osmotic regulation of sap flow as showing that a shift away from a conductive func- by means of mobilization of starches into sugars may tion by imperforate tracheary elements is accompa- be more important in Acer, in which fibre dimor- nied by a change from bordered pits to simple pits or phism is concerned. Gregory (1978) noted that pits with only the most vestigial borders. Not starch-bearing fibres are adjacent to vessels in Acer, included in the count for libriform fibres in Moraceae whereas fibres distal to vessels are starch-poor. are genera in which fibres are living but not septate. Heimsch (1942) also noted bands of starch-rich Although change from fibre-tracheids to libriform fibres (which are also thinner-walled and shorter) in fibres does not by itself result in fibre dimorphism, the wood of Acer. The work of Sauter, Iten & it is a sort of preceding event in the majority of Zimmermann (1973) confirmed that change of instances. None of the families with fibre dimorphism starches in these fibres to sugar and transfer of the in the senses included here had tracheids (with fully sugars into vessels produces an osmotic change in bordered pits), and only a few (such as Penaeaceae) vessel sap that jump-starts sap flow just before

© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 174, 44–67 64 S. CARLQUIST leafing-out occurs, pulling water from thawing soil enon that is closely allied to crystalliferous fibres. A into the conductive system of a tree. number of occurrences in mimosoids (Evans et al., Living fibres are certainly common outside the 2006) are worthy of further study. One should be genera that have been shown to have fibre dimor- careful to distinguish between axial parenchyma phism. Genera such as Hedera L. (Araliaceae) or strands that contain crystals and fibriform strands Bursera Jacq. ex L. (Burseraceae) have monomorphic that contain crystals, wherever possible. fibres, but they are in families in which fibre dimorphism also occurs. Why do those particular genera lack fibre dimorphism? There can be various reasons. GELATINOUS FIBRES Perhaps the semi-succulent habit of Bursera and the On one level, this is the most obvious instance of fibre non-tree habit of Hedera changes the selective value dimorphism. On another, workers may resist inclu- of axial cells away from thick-walled fibres. Bursera sion of gelatinous fibres in this category because it stems presumably store water to a greater degree has not been explicitly done before, but surely gelati- than other Burseraceae. Hedera may store starch for nous fibres represent a distinctive type of fibre. flushes of growth and flowering. We have little knowl- Gelatinous fibres feature a coil-like deposition of cel- edge of the functioning of living fibres in angiosperm lulose microfibrils. These coils can contract because woods at large; ecology and habit may point the way they are not cemented together by lignin, but occur in to valuable experiments. One salient feature in this a matrix of pectic compounds and other hygrophilic regard is the coexistence of living fibres and axial molecules (Du & Yamamoto, 2007; Bowling & parenchyma in so many woods. Do these two systems Vaughn, 2008). Gelatinous fibres and sclereids occur serve different purposes? Does axial parenchyma in various tissues of Gnetales other than wood where serve more for maintaining water columns on an they have no function like that in reaction wood. Such immediate basis, whereas living fibres (which so fre- gelatinous walls might even serve for water storage, a quently contain starch) serve for major growth events possibility suggested by the marked shrinkage of or flowering and fruiting events? gelatinous wall layers when such cells are subjected The above considerations pertain to the content of to dehydration (Carlquist, 2012c). The massive zones wider fibres, but fibre dimorphism by definition of phloem fibres in Welwitschia Hook.f. are notable in implies that the narrower, thicker-walled, longer this regard (Carlquist, 2012c). They are interpretable fibres have a different function. Mechanical strength as an herbivore-deterrent mechanism, but if that seems the obvious explanation, although experimen- were the selective factor, one might expect lignified tal demonstration of the selective value of the thick- walls instead of gelatinous walls. The possibility that walled fibres would perhaps be difficult. Indirect gelatinous fibres may store water and play roles in evidence by means of observations that show varia- accordance with that has been raised (Sonsin et al., tion in location of thick-walled fibres and their abun- 2012; Whinder et al., 2013). dance with relation to habit, positioning and growth events of a woody species could be an excellent starting-place and foundation. Fibre dimorphism GROWTH-RING-RELATED FIBRE DIMORPHISM offers the great advantage of being able to vary posi- Why are fibres wider and shorter in earlywood of tioning and abundance of fibres on an ongoing basis. Morus, but longer and narrower in latewood? This pattern can be found in many woody angiosperms other than Morus. In interpreting this pattern, CRYSTALLIFEROUS FIBRES conifer woods are relevant. In conifers with growth As discussed above, crystal-bearing septate fibres rings, earlywood has wide-lumen tracheids with thin in Hauya (Onagraceae), Lawsonia L. (Lythraceae), walls, whereas latewood has narrow-lumen thick- Punica (Punicaceae) and Rhynchocalyx (Rhyncho- walled tracheids. There is a transition from early- calycaceae/Penaeaceae) are indubitable instances of wood to latewood in these respects. The increased fibre dimorphism. There may be a number of other hydraulic capacity of earlywood tracheids, with large, cases of crystalliferous fibres that qualify, but have numerous bordered pits on radial walls can be readily not yet been described in detail. The literature on claimed, but what is the value of the latewood trac- wood anatomy tends to mention crystals and location, heids? One can say that, by inference, they offer a but often omits details about the walls of the cells mechanical strength that compensates for poorer that contain the crystals. We should probably include mechanical strength of earlywood tracheids. However, crystalliferous strands similar to libriform fibres in in this connection, one should keep in mind that there length but with primary walls as instances of fibre are conifers such as some Araucariaceae and Podo- dimorphism. These instances (notable in such fami- carpaceae that have little or no growth ring activity, lies as Sapindaceae: Klaassen, 1999) seem a phenom- especially in the species that grow closer to the

Equator (Greguss, 1955). Both mechanical and is no sharp root/stem difference in distribution of hydraulic functions may be served equally in trac- aerating imperforate tracheary elements; there is a heids of such species, but most conifer species have transition between wide-lumen elements and thicker- more marked growth rings in which latewood acts to walled narrow-lumen elements in stem wood, propor- promote mechanical strength (and provides tracheids tions depending on the level. Presumably the most quite unlikely to embolize), whereas earlywood pro- recently formed fibre-tracheids could contain water, vides tracheids with maximal flow characteristics. but they would be air-filled in older wood. These facts Note that most conifers have at least a few strands of are in accordance with the aerating function of wide- axial parenchyma, usually with vestigially bordered lumen thin-walled tracheids in the conifers Taxodium pits (Greguss, 1955). Axial parenchyma is more distichum (Cupressaceae) and Dacrydium guillaumi- common in Cupressaceae than in Pinaceae. nii and Podocarpus minor (Podocarpaceae) (Carlquist, 1975: 91, 101), as noted above.

ADMIXTURE OF WIDE FIBRES AND AXIAL PARENCHYMA EVOLUTIONARY SIGNIFICANCE This condition, noted for Maclura pomifera (Moraceae), needs explanation: why are the two cell Fibre dimorphism is important because it is one of a types, similar except for the occurrence of strands of series of evolutionary pathways that make wood two cells in the case of parenchyma, intermixed in anatomy such an intricate field, difficult to visualize earlywood? Similar questions apply to the instance in its entirety (Carlquist, 2012b). Fibre dimorphism is mentioned for Miconia [Melastomataceae (ter Welle & undoubtedly a series of apomorphies, because the Koek-Noorman, 1979)]. There seems to be a sharp several clades in which it is found are well separated delimitation between libriform fibres and gelatinous from each other by groups in which fibre dimorphism fibres: where they co-occur in wood, transitional cells is absent. Also (except in the case of gelatinous fibres), are infrequent. Intermediacy between fibres and axial fibre dimorphism characterizes a small number of parenchyma is a genuine possibility, however. One species. Formation of two kinds of living fibres so as can make a case for recognition of axial parenchyma to perform two different functions is plausible, and that is never subdivided into strands in some genera the function of wide fibres and axial parenchyma may with short fusiform cambial initials, like Frankenia overlap little in woods where these two cell types (Carlquist, 2010), and probably some other genera. co-occur (the distribution of the two cell types with How different are axial parenchyma and living fibres? relation to each other is suggestive of this). They seem quite well differentiated in many of the Development of fibre dimorphism, like the evolu- instances presented in the present essay. In this tion of other distinctive structural modes in wood, regard, instances of imperceptible incipient fibre may not be highly complex genomically: it may reflect dimorphism are to be expected, and may be difficult to small alterations in gene regulation. Ultimately, we recognize. The more recognizable the differences, will want to know the genomic origin of fibre dimor- however, the more likely that functional differences phism. Meanwhile, the systematic distribution of between wide and narrow fibres are being served. fibre dimorphism, the appearances that this phenomenon takes, and the physiological and mechanical functions that are taking place in these cells offer AERATING MECHANISMS many possibilities for study. Although perhaps of minor importance in the world flora at large, the imperforate tracheary elements in ACKNOWLEDGEMENTS wood of roots of characteristically inundated trees have a distinctive morphology that has not received Extensive collections are required for a study that sufficient mention. These tracheary elements are surveys a phenomenon in wood of angiosperms at more often fibre-tracheids or tracheids than libriform large. Particular individuals have been especially fibres in the genera studied thus far. The occurrence helpful. Peter Raven provided collections of liquid- of wide (sometimes even radially widened), thin- preserved Onagraceae. Dr Robert Ornduff invited me walled imperforate tracheary elements in root wood of to collect wood samples from the University of Cali- unrelated genera of angiosperms (Alstonia, Apocyn- fornia Botanic Garden, Berkeley, following a freeze aceae; Anaxagorea, Annonaceae; Micrandra, Euphor- that killed many specimens of Fuchsia. Dr Charles biaceae; and other genera cited by Wiedenhoeft, 2001) Heimsch gave me microscope slides of sapindalean serves to validate this interpretation. The large pit woods that he had used in his doctoral work. Samples areas on imperforate tracheary elements in root wood from the Forest Products Laboratory, Madison, Wis- may serve for passage of gases rather than water in consin, were furnished by Dr Regis Miller. Fieldwork much of the mature root wood of these genera. There that resulted in collection of samples involved in this

© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 174, 44–67 66 S. CARLQUIST study was funded by the National Science Founda- Carlquist S. 1982. The use of ethylene diamine in softening tion, the American Philosophical Society and the hard plant structures for paraffin sectioning. Stain Technol- Simon Guggenheim Foundation. Reviews by Peter E. ogy 57: 311–317. Gasson and Alex C. Wiedenhoeft provided helpful Carlquist S. 1985. Observations on functional wood histology improvements to the manuscript. of vines and lianas: vessel dimorphism, tracheids, vasicentric tracheids, narrow vessels, and parenchyma. Aliso 11: 139–157. REFERENCES Carlquist S. 1988. Tracheid dimorphism: a new pathway in evolution of imperforate tracheary elements. Aliso 12: 103– APG III. 2009. An update of the Angiosperm Phylogeny 118. Group classification for the orders and families of flowering Carlquist S. 1992. Wood, bark, and pith anatomy of the Old plants: APG III. Botanical Journal of the Linnean Society World species of Ephedra and summary for the genus. Aliso 161: 105–121. 13: 255–295. Baas P. 1979. The anatomy of Alzatea Ruiz & Pav. (Myrtales). Carlquist S. 1996a. Wood, bark, and stem anatomy of Acta Botanical Neerlandica 28: 156–158. Gnetales: a summary. International Journal of Plant Sci- Baas P. 1986. Wood anatomy of Lythraceae – additional ences 157 (Suppl): S58–S76. genera (Capuronia, Galpinia, Haitia, Orias, and Pleu- Carlquist S. 1996b. Wood and bark anatomy of lianoid Indo- rophora. Annals of the Missouri Botanical Garden 73: 810– malesian and Asiatic species of Gnetum. Botanical Journal 819. of the Linnean Society 121: 1–24. Baas P, Zweypfenning RCVJ. 1979. Wood anatomy of the Carlquist S. 1997. Wood anatomy of Argyroxiphium (Aster- Lythraceae. Acta Botanica Neerlandica 28: 117–155. aceae): adaptive radiation and ecological correlations. Bailey IW. 1923. The cambium and its derivative tissues. IV. Journal of the Torrey Botanical Society 124: 1–10. Increase in girth of the cambium. American Journal of Carlquist S. 1998a. Wood anatomy of Dubautia (Asteraceae: Botany 10: 499–509. Madiinae) in relation to adaptive radiation. Pacifc Science Berry PE, Miller RB, Wiedenhoeft AC. 1999. A new 52: 345–368. lightweight-wooded species of Anaxagorea (Annonaceae) Carlquist S. 1998b. Wood anatomy of Wilkesia (Asteraceae) from flooded black-water shrublands of southern Venezuela. with relation to systematics, organography, and habit. Systematic Botany 24: 506–511. Journal of the Torrey Botanical Society 125: 261–267. Berry PE, Wiedenhoeft AC. 2004. Micrandra inundata,a Carlquist S. 2001. Comparative wood anatomy, 2nd edn. new species with unusual wood anatomy from black-water Berlin: Springer Verlag. river banks in southern Venezuela. Systematic Botany 29: Carlquist S. 2009. Non-random vessel distribution in woods: 125–132. patterns, modes, diversity, correlations. Aliso 27: 39–58. Bonsen KJ, ter Welle BJH. 1984. Systematic wood anatomy Carlquist S. 2010. Caryophyllales: a key group for under- and affinities of the Urticaceae. Botanisches Jarhrbücher standing wood anatomy character states and their evolu- Systematik 105: 49–71. tion. Botanical Journal of the Linnean Society 164: 342–393. Bowling AJ, Vaughn KC. 2008. Imunocytochemical charac- Carlquist S. 2012a. Monocot xylem revisited: new informa- terization of tension wood: gelatinous fibers contain more tion, new paradigms. Botanical Review 78: 87–153. than just cellulose. American Journal of Botany 95: 655– Carlquist S. 2012b. How wood evolves: a new synthesis. 663. Botany 90: 901–940. Bridgewater SD, Baas P. 1978. Wood anatomy of the Puni- Carlquist S. 2012c. Wood anatomy of Gnetales in a func- caceae. IAWA Bulletin 1978/1: 3–6. tional, ecological, and evolutionary context. Aliso 30: 33–47. Buerki S, Lowry II PP, Andriambololonera S, Phillipson Carlquist S, Zona S. 1988. Wood anatomy of Papaveraceae, PB, Vary L, Callmander MW. 2011. How to kill two with comments on vessel restriction patterns. IAWA Bulle- genera with one tree: clarifying generic circumscriptions in tin, New Series 9: 253–267. an endemic Malagasy clade of Sapindaceae. Botanical Chalk L, Chattaway MM. 1937. Identification of woods with Journal of the Linnean Society 165: 223–234. included phloem. Tropical Woods 50: 1–31. Carlquist S. 1958. Wood anatomy of Heliantheae (Composi- Chatrou LW, Pirie MD, Erkens RHJ, Couvreur TLP, tae). Tropical Woods 108: 1–30. Neubig KM, Abbott JR, Mols JB, Maas JW, Saunders Carlquist S. 1961. Comparative plant anatomy. New York: RMK, Chase MW. 2012. A new subfamilial and tribal Holt, Rinehart & Winston. classification of the pantropical flowering plant family Carlquist S. 1966. Wood anatomy of Compositae: a summary, Annonaceae informed by molecular phylogenetics. Botanical with factors controlling wood evolution. Aliso 6: 25–44. Journal of the Linnean Society 169: 5–40. Carlquist S. 1975. Ecological strategies of xylem evolution. Du S, Yamamoto F. 2007. An overview of the biology of Berkeley: University of California Press. reaction wood formation. Journal of Integrative Biology 49: Carlquist S. 1977. Wood anatomy of Onagraceae, with notes 131–143. on alternative modes of photosynthate movement in dicoty- Esau K. 1965. Plant anatomy, 2nd edn. New York: Wiley. ledon woods. Annals of the Missouri Botanical Garden 62: Evans A, Gasson P, Lewis GP. 2006. The wood anatomy of 386–424. the Mimosoideae. IAWA Journal, Supplement 5: 1–117.

Funk VA, Susanna A, Stuessy TF, Bayer RJ, eds. 2009. Soltis DE, Smith SA, Cellinese N, Wurdack KJ, Tank DC, Systematics, evolution, and biogeography of Compositae. Brockington SJ, Refulio-Rodriguez NF, Walker JB, Vienna: International Association of Plant Taxonomy. Moore MJ, Carlsward BS, Bell CD, Latvis M, Graham SA, Tobe H, Baas P, Raven PH. 1986. Koehneria, Crawley S, Black C, Diouf D, Xi Z, Rushworth CA, a new genus of Lythraceae from Madagascar. Annals of the Gitzendanner MA, Sytsma KJ, Qiu YL, Hilu KW, Davis Missouri Botanical Garden 73: 788–809. CC, Sanderson MJ, Beaman RS, Olmstead RG, Judd Gregory RA. 1978. Living elements of the conducting sec- WS, Donoghue MJ, Soltis PS. 2011. Angiosperm phylog- ondary xylem of sugar maple (Acer saccharum Marsh). eny: 17 genes, 640 taxa. American Journal of Botany 98: IAWA Bulletin 4: 65–69. 704–730. Greguss P. 1955. Identification of living gymnosperms on the Sonsin JO, Gasson PE, Barros CF, Marcati CR. 2012. A basis of xylotomy. Budapest: Akademiai Kiado. comparison of the wood antomy of eleven species from two Heimsch C. 1942. Comparative anatomy of the secondary cerrado habitats (cerrado s.s. and adjacent gallery forest). xylem in the ‘Gruinales’ and ‘Terebinthales’ of Wettstein Botanical Journal of the Linnean Society 170: 257–276. with reference to taxonomic groupings. Lilloa 8: 83–198. Tippo O. 1938. The comparative wood anatomy of Moraceae Holbrook NM, Zwieniecki M, Melcher PJ. 2002. The and their presumed allies. Botanical Gazette 100: 1–99. dynamics of ‘dead wood’ maintenance of water transport Vasquez-Cooz I, Meyer RW. 2008. Fundamental differences through plant stems. Integrative and Comparative Biology between two fiber types in Acer. IAWA Journal 29: 129–141. 42: 492–496. van Vliet GJCM. 1974. Wood anatomy of Crypteroniaceae Ingle HD, Dadswell HE. 1953. The anatomy of the timbers sensu lato. Journal of Microscopy 104: 65–82. of the south-west Pacific area. II. Apocynaceae and Annon- van Vliet GJCM. 1979. Wood anatomy of the Combretaceae. aceae. Australian Journal of Botany 1: 1–26. Blumea 25: 141–223. Klaassen R. 1999. Wood anatomy of the Sapindaceae. IAWA van Vliet GJCM. 1981. Wood anatomy of the Palaeotropical Journal, supplement 2: 1–214. Melastomataceae. Blumea 27: 395–462. Kyalangalilwa B, Boatwright JS, Daru BH, Maurin O, ter Welle BJH, Koek-Noorman J. 1979. On fibres, paren- van der Bank M. 2013. Phylogenetic position and revised chyma, and intermediate forms in the genus Miconia. Acta classification of Acacia s.l. (Fabaceae: Mimosoideae) in Botanica Neerlandica 27: 1–9. Africa, including new combinations in Vachellia and Sen- ter Welle BJH, Koek-Noorman J. 1981. Wood anatomy of egalia. Botanical Journal of the Linnean Society 172: 500– Neotropical Melastomataceae. Blumea 27: 335–394. 523. Whinder F, Clark KI, Warwick NWM, Gasson PE. 2013. Metcalfe CR, Chalk L. 1950. Anatomy of the dicotyledons. Structural diversity of the wood of temperate species of Oxford: Clarendon Press. Acacia s.s. (Leguminosae: Mimosoideae). Australian Sauter JJ, Iten WI, Zimmermann MH. 1973. Studies on Journal of Botany 61: 281–301. the release of sugar into the vessels of the sugar maple (Acer Wiedenhoeft AC. 2001. Preliminary wood anatomical char- saccharum). Canadian Journal of Botany 51: 1–8. acterization of some lightweight-wooded species growing in a Schönenberger J, Conti E. 2003. Molecular phylogeny and seasonally inundated Venezuelan igapo. Master’s thesis, floral evolution of Penaeaceae, Oliniaceae, Rhynchocaly- University of Wisconsin-Madison. caceae, and Alzateaceae (Myrtales). American Journal of Wolkinger F. 1970. Das Vorkommen lebender Holzfasern in Botany 90: 293–309. Sträuchern und Bäumen. Phyton (Austria) 14: 55–67.